wheat research paper 2020

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• Published: 23 September 2019

Improving grain yield, stress resilience and quality of bread wheat using large-scale genomics

• Philomin Juliana 1 ,
• Jesse Poland   ORCID: orcid.org/0000-0002-7856-1399 2 ,
• Julio Huerta-Espino 3 ,
• Sandesh Shrestha 2 ,
• José Crossa   ORCID: orcid.org/0000-0001-9429-5855 1 ,
• Leonardo Crespo-Herrera 1 ,
• Fernando Henrique Toledo 1 ,
• Velu Govindan 1 ,
• Suchismita Mondal   ORCID: orcid.org/0000-0002-8582-8899 1 ,
• Uttam Kumar 4 ,
• Sridhar Bhavani 1 ,
• Pawan K. Singh 1 ,
• Mandeep S. Randhawa 5 ,
• Xinyao He 1 ,
• Carlos Guzman 1 , 6 ,
• Susanne Dreisigacker   ORCID: orcid.org/0000-0002-3546-5989 1 ,
• Matthew N. Rouse 7 ,
• Yue Jin 7 ,
• Paulino Pérez-Rodríguez 8 ,
• Osval A. Montesinos-López 9 ,
• Daljit Singh 2 ,
• Mohammad Mokhlesur Rahman   ORCID: orcid.org/0000-0003-1831-3198 2 , 10 ,
• Felix Marza 11 &
• Ravi Prakash Singh   ORCID: orcid.org/0000-0002-4676-5071 1  

Nature Genetics volume  51 ,  pages 1530–1539 ( 2019 ) Cite this article

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• Genome-wide association studies
• Plant breeding

Bread wheat improvement using genomic tools is essential for accelerating trait genetic gains. Here we report the genomic predictabilities of 35 key traits and demonstrate the potential of genomic selection for wheat end-use quality. We also performed a large genome-wide association study that identified several significant marker–trait associations for 50 traits evaluated in South Asia, Africa and the Americas. Furthermore, we built a reference wheat genotype–phenotype map, explored allele frequency dynamics over time and fingerprinted 44,624 wheat lines for trait-associated markers, generating over 7.6 million data points, which together will provide a valuable resource to the wheat community for enhancing productivity and stress resilience.

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Data availability.

The phenotyping data for the lines used in this study are available in Supplementary Data 1 . The marker P values, additive effects and percentage variation explained by each marker are available in Supplementary Table 2 . The genomic fingerprints of 44,624 wheat lines for 195 trait-associated markers are available in Supplementary Table 4a–d . The raw genotyping data for the lines are available in FigShare ( https://doi.org/10.6084/m9.figshare.8940257.v1 ).

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Acknowledgements

This research was supported by the Feed the Future project through the US Agency for International Development (USAID), under the terms of contract no. AID-OAA-A-13-00051 (J.P. and R.P.S.). The opinions expressed herein are those of the authors and do not necessarily reflect the views of the USAID. We thank the innovation laboratory at Kansas State University, the CGIAR Research Program on Wheat, the Indian Council of Agricultural Research (ICAR), the Australian Centre for International Agricultural Research (ACIAR), several national partners (Afghanistan, Bangladesh, Canada, Egypt, India, Morocco, Pakistan and Sudan) and field technicians for their support in generating the genotyping and phenotyping data.

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Authors and affiliations.

International Maize And Wheat Improvement Center (CIMMYT), Texcoco, Mexico

Philomin Juliana, José Crossa, Leonardo Crespo-Herrera, Fernando Henrique Toledo, Velu Govindan, Suchismita Mondal, Sridhar Bhavani, Pawan K. Singh, Xinyao He, Carlos Guzman, Susanne Dreisigacker & Ravi Prakash Singh

Wheat Genetics Resource Center, Department of Plant Pathology, Kansas State University, Manhattan, KS, USA

Jesse Poland, Sandesh Shrestha, Daljit Singh & Mohammad Mokhlesur Rahman

Campo Experimental Valle de Mexico, Instituto Nacional de Investigaciones Forestales, Agricolas y Pecuarias (INIFAP), Chapingo, Mexico

Julio Huerta-Espino

Borlaug Institute for South Asia (BISA), New Delhi, India

Uttam Kumar

International Maize and Wheat Improvement Center (CIMMYT), Nairobi, Kenya

Mandeep S. Randhawa

Departamento de Genética, Escuela Técnica Superior de Ingeniería Agronómica y de Montes, Campus de Rabanales, Universidad de Córdoba, Cordoba, Spain

Carlos Guzman

United States Department of Agriculture, Agricultural Research Service (USDA-ARS), Cereal Disease Laboratory and Department of Plant Pathology, University of Minnesota, St Paul, MN, USA

Matthew N. Rouse & Yue Jin

Colegio de Post graduados, Montecillos, Mexico

Paulino Pérez-Rodríguez

Facultad de Telematica, Universidad de Colima, Colima, Mexico

Osval A. Montesinos-López

Regional Agricultural Research Station, Bangladesh Agricultural Research Institute (BARI), Jamalpur, Bangladesh

Mohammad Mokhlesur Rahman

Instituto Nacional de Innovación Agropecuaria y Forestal (INIAF), La Paz, Bolivia

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Contributions

P.J. drafted the manuscript and performed the analyses. R.P.S., J.P., J.H.-E. and J.C. planned the study and supervised the analysis. F.H.T., P.P.-R. and O.A.M.-L. performed some of the analyses. L.C.-H., V.G., S.M., U.K., S.B., P.K.S., M.S.R., X.H., C.G., M.N.R., Y.J., D.S., M.M.R. and F.M. generated the phenotyping data. S.D. performed the DNA extraction and S.S. called the marker polymorphisms.

Corresponding author

Correspondence to Ravi Prakash Singh .

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Supplementary information

Supplementary information.

Supplementary Figs. 1–6

Reporting Summary

Supplementary tables.

Supplementary Tables 1–7

Supplementary Data 1

Phenotyping data for the lines in the YT, EYTs, SABWYTs, IBWSNs, SRRSNs and ESWYTs

Supplementary Data 2

Manhattan plots of the absolute marker effects for all the traits estimated using Bayes B approach in the combined EYT panel of 3,485 lines and the genomic prediction accuracies within and across panels using the Bayes B approach

Supplementary Data 3

Chromosome-wise linkage disequilibrium between the significant markers, shown by the marker R 2 vales (the correlation between the alleles at two loci) and the P values for the test of linkage disequilibrium using a two-sided Fisher’s exact test

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Juliana, P., Poland, J., Huerta-Espino, J. et al. Improving grain yield, stress resilience and quality of bread wheat using large-scale genomics. Nat Genet 51 , 1530–1539 (2019). https://doi.org/10.1038/s41588-019-0496-6

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DOI : https://doi.org/10.1038/s41588-019-0496-6

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Meeting the challenges facing wheat production: the strategic research agenda of the global wheat initiative.

1. Introduction

2. background, 2.1. why wheat, 2.2. impact of climate change, 2.3. the wheat initiative, 2.4. global wheat research, 3. existing strategic research agenda—work in progress.

3.1. Objective 1: To Increase Yield Potential

3.2. objective 2: to protect ‘on farm’ yield, 3.3. objective 3: ensuring the supply of high-quality safe wheat, 3.4. objective 4: enabling technologies and the sharing of resources, 3.5. objective 5: germplasm accessibility, 3.6. objective 6: knowledge exchange, education and training, 4. major issues and challenges facing wheat production and research, 4.1. inconsistencies in regulatory environment, 4.2. access to staff with the necessary skills in both new and old technologies, 4.3. data access and standards, 4.4. support for multinational research and public–private partnerships, 5. research priorities, 5.1. strengthen existing research activities, 5.2. enhance agronomy in its broadest definition (crop production and soil management), 5.3. increase genetic diversity.

• A broad series of activities can be undertaken to address this research priority:
• Revise and update the Global Wheat Conservation Strategy prepared in 2007 [ 26 ].
• Encourage the large-scale genotyping and phenotypic characterisation of germplasm held in the major genebanks.
• Advocate for the free and open exchange of germplasm and associated data.
• Encourage the utilisation of existing specialist germplasm collections collated by EWGs and share the outcomes: ◦ Tetraploid collections developed by the Durum EWG ▪ Durum elite and landrace collection in conjunction with a tetraploid core collection (GDP: Global Durum wheat Panel) capturing about 80% of the AABB haplotypes [ 27 ] of the collection (TGC: Tetraploid wheat Global Collection) described in [ 28 ]. ◦ Heat and drought tolerant germplasm collections developed by HeDWIC. ◦ Wheat quality assessment panels developed by the Quality EWG.
• Support research aimed at the enhanced utilisation of unadapted germplasm: ◦ Development of introgression populations. ◦ Re-domestication. ◦ Exploration of novel germplasm evaluation strategies. ◦ Development of efficient methods for gene editing.

5.4. Understanding Root and Soil Biology

• Continuing improvement of root phenotyping techniques, particularly in the field.
• Expand information of soil–microbe–plant interactions.
• Integration of data and information on roots and the microbiome in the analysis of wheat production with the full cropping system. It will also be important to emphasise the differences between low and high input systems and organic farming.

6. Wheat Initiative Structure and Organisation

6.1. develop educational and training programs.

• Ensure the full and rapid implementation of the postgraduate and ECR plan for involvement in the EWGs.
• Establish an exchange program that provides partial funding for students to work in other laboratories.
• Encourage EWGs to deliver training workshops and courses, and link to existing options offered by other organisations, such as universities, CIMMYT and ICARDA.
• Develop an online Wheat Initiative seminar program.
• Develop mentoring programs to support students and link to industry.

6.2. The Wheat Initiative as an Advocacy and Lobby Organisation

• Produce public explanatory documents and videos covering the Wheat Initiative activities, major topics and issues affecting wheat production, such as the role of germplasm exchange, gene editing, hybrid wheat, and crop protection.
• Participate in relevant G20 workshops and meetings and develop links to government agencies and international organisations.
• Advocate and lobby for the support of transnational research.
• Develop links to the wheat grower and processing industry organisations.
• Promote wheat resources such as WheatIS and WheatVIVO.

6.3. Expand Engagement

• The Institutions’ Coordination Committee has established a sub-committee to work through the options to build membership.
• Develop and distribute documentation explaining the value to industry from joining the WI—Industry.
• Increase industry participation in WI activities, particularly in training and mentorship: a component would be to identify platforms and capabilities that could be used by industry.
• Identify and target government and institutional organisations in major wheat producing and wheat-importing countries to seek greater engagement in the WI.
• Target early career researchers in under-represented countries to encourage the membership of EWGs. In addition, provide support to allow key people from these regions to participate in WI activities.

6.4. Supporting Multinational Research

• Stage 1 —Coordination across existing research to capture synergies, prevent duplication and identify gaps—low incremental costs but a proactive coordination is instrumental and essential.
• Stage 2 —Project alignment and leverage of existing investments: initially focus on the twinning of existing projects or building on a call(s) for proposals by one or more national funders joining (e.g., recent AAFC (Canada)/BBSRC (UK) IWYP-aligned call-linked consecutive calls for proposals in each country).
• Stage 3 —Scaling-up joint investment: under the key areas of interest to all funders, funding can be allocated to a common/centrally managed pot/program or managed nationally by a lead funder, still aligned under a broad umbrella theme.

7. Conclusions

• Boost research and technology delivery capabilities by investing in staff and student training and encourage and support the exchange of personnel between research organisations and building research infrastructure. This can be achieved if national research programmes place priority on activities with strong international linkages. Financial or organisational support from national agencies to research groups seeking participation in international partnerships would be beneficial.
• Provide support, both financial and organisational, to international activities aiming to facilitate the exchange of resources, particularly germplasm, and support the evaluation and delivery of research outcomes.
• Actively participate in Wheat Initiative research alliances that gather the capabilities and resources targeting global research challenges. These include the work of the Expert Working Groups and the three current alliances: The International Wheat Yield Partnership (boosting wheat yield potential), the Alliance for Wheat Adaptation to Heat and Drought (producing heat- and drought-tolerant germplasm) and the Wheat Initiative Crop Health Alliance (diagnosis and monitoring of wheat diseases).

Author Contributions

Data availability statement, acknowledgments, conflicts of interest, abbreviations.

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Langridge, P.; Alaux, M.; Almeida, N.F.; Ammar, K.; Baum, M.; Bekkaoui, F.; Bentley, A.R.; Beres, B.L.; Berger, B.; Braun, H.-J.; et al. Meeting the Challenges Facing Wheat Production: The Strategic Research Agenda of the Global Wheat Initiative. Agronomy 2022 , 12 , 2767. https://doi.org/10.3390/agronomy12112767

Langridge P, Alaux M, Almeida NF, Ammar K, Baum M, Bekkaoui F, Bentley AR, Beres BL, Berger B, Braun H-J, et al. Meeting the Challenges Facing Wheat Production: The Strategic Research Agenda of the Global Wheat Initiative. Agronomy . 2022; 12(11):2767. https://doi.org/10.3390/agronomy12112767

Langridge, Peter, Michael Alaux, Nuno Felipe Almeida, Karim Ammar, Michael Baum, Faouzi Bekkaoui, Alison R. Bentley, Brian L. Beres, Bettina Berger, Hans-Joachim Braun, and et al. 2022. "Meeting the Challenges Facing Wheat Production: The Strategic Research Agenda of the Global Wheat Initiative" Agronomy 12, no. 11: 2767. https://doi.org/10.3390/agronomy12112767

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REVIEW article

Salinity stress in wheat ( triticum aestivum l.) in the changing climate: adaptation and management strategies.

• 1 Department of Agronomy, Faculty of Agriculture, University of Kafrelsheikh, Kafr El-Shaikh, Egypt
• 2 Department of Field Crops, Faculty of Agriculture, Siirt University, Siirt, Turkey
• 3 Department of Agronomy, Hajee Mohammad Danesh Science and Technology University, Dinajpur, Bangladesh
• 4 Department of Botany and Plant Physiology, Faculty of Agrobiology, Food, and Natural Resources, Czech University of Life Sciences Prague, Prague, Czechia
• 5 College of Agronomy, Sichuan Agricultural University, Chengdu, China
• 6 Principal Scientist (Agronomy), Punjab Agricultural University, Regional Research Station, Faridkot, India
• 7 Department of Genetics and Plant Breeding, Bangladesh Agricultural University, Mymensingh, Bangladesh
• 8 Department of Agronomy, Bangladesh Wheat and Maize Research Institute, Dinajpur, Bangladesh
• 9 College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, China
• 10 Plant Physiology Division, Nuclear Institute of Agriculture (NIA), Tandojam, Pakistan
• 11 Department of Agronomy, Faculty of Agriculture, University of Poonch Rawalakot (AJK), Rawalakot, Pakistan
• 12 Department of Agricultural Biology, Faculty of Agriculture, University of Ruhuna, Matara, Sri Lanka
• 13 ICAR-Indian Grassland and Fodder Research Institute, Jhansi, India
• 14 International Rice Research Institute, Bangladesh Office, Dhaka, Bangladesh
• 15 Department of Botanical and Environmental Sciences, Guru Nanak Dev University, Amritsar, India
• 16 College of Agriculture, Bahauddin Zakariya University, Bahadur Sub-Campus Layyah-Pakistan, Layyah, Pakistan
• 17 Department of Plant Physiology, Slovak University of Agriculture, Nitra, Slovakia
• 18 Institute of Crop Science and Resource Conservation (INRES), Crop Science Group, University of Bonn, Bonn, Germany
• 19 Faculty of Science, Plant Breeding Institute, Sydney Institute of Agriculture, School of Life and Environmental Sciences, University of Sydney, Sydney, NSW, Australia
• 20 College of Resources and Environmental Sciences, China Agricultural University, Beijing, China

Wheat constitutes pivotal position for ensuring food and nutritional security; however, rapidly rising soil and water salinity pose a serious threat to its production globally. Salinity stress negatively affects the growth and development of wheat leading to diminished grain yield and quality. Wheat plants utilize a range of physiological biochemical and molecular mechanisms to adapt under salinity stress at the cell, tissue as well as whole plant levels to optimize the growth, and yield by off-setting the adverse effects of saline environment. Recently, various adaptation and management strategies have been developed to reduce the deleterious effects of salinity stress to maximize the production and nutritional quality of wheat. This review emphasizes and synthesizes the deleterious effects of salinity stress on wheat yield and quality along with highlighting the adaptation and mitigation strategies for sustainable wheat production to ensure food security of skyrocketing population under changing climate.

Introduction

Recently, climate change and global warming have directly affected the crops yield and quality by intensifying the frequency and extent of numerous stresses. Wheat, rice, and maize are the most important staple crops globally and contribute a significant part of daily calories and protein intake ( Kizilgeci et al., 2021 ). Among these major cereals, wheat is ranked at the first position due to its domestication and contribution as the primary staple food crop globally ( Iqbal et al., 2021 ). Currently, it is dominating the most of arable land (38.8%), with relatively higher grain protein (12–15%) than other cereals, but the productivity remains low [ Food and Agriculture Organization (FAO) of the United Nations, 2016 ]. It can further decrease owing to climate change that has given to rise a variety of abiotic stresses. Various climate models projected that wheat production could decrease by 6% due to stressful environments ( Asseng et al., 2015 ).

Salt stress affects 20% of global cultivable land and is increasing continuously owing to the change in climate and anthropogenic activities ( Arora, 2019 ). Environmental stress including salinity can cause about 50% of production losses ( Acquaah, 2007 ). Furthermore, the continuous increase in the human population put pressure on global food security as the world's food supply needs to be increased by up to 70% by 2050 ( FAO, 2009 ). Wheat ( Triticum aestivum ) is considered the most significant grain crop among all the cereals and ranked 1st globally among grain-producing crops, especially for human consumption ( Giraldo et al., 2019 ). About 36% of the world's population is dependent on wheat as a staple food. About 20% of calories and 55% of carbohydrates are being provided by wheat across the globe. Both growth and yield of wheat are negatively influenced by salinity ( Royo and Abió, 2003 ). Salinity stress causes osmotic stress and ion toxicity, through increasing the assimilation of Na + ion and decreasing the Na + /K + ratio due to lower osmotic potential within the plant roots. Further, these ionic imbalance affects the uptake, and transport of other important essential ions in target cells and hamper the crucial plant processes and functions ( Arif et al., 2020 ). Salinity impairs the seedling establishment, stunted plant growth, poor reproductive development, and ultimately declines the crop yield ( Turan et al., 2009 ). Salinity also alters the ultrastructural cell components, disturbs the photosynthesis machinery, damages the membranous structure, increases the reactive oxygen species production, reduces the enzymatic activity, which limit the growth and yield of crops ( Hasanuzzaman et al., 2014 ). Tolerancey of plants to salinity is a polygenic character that is governed by many genetic factors ( Arzani and Ashraf, 2016 ). Crop growth is improved under salinity by the increase in K + , elimination of Na + or by optimizing the ratio of both Na + and K + ions, improving transpiration efficiency, regulation of osmotic potential, and by the antioxidant, immune system of plants ( Rahman et al., 2005 ).

Among various field crops, generally, wheat is more sensitive to salinity that hampers the growth and development of plant, leads to low productivity or even complete crop failure under extreme severity of salinity. The knowledge of stress tolerance in plants regarding the physiological basis is important for selection and breeding programs ( Chaves et al., 2003 ). Thus, understanding of morphoanatomical, physiological, biochemical, and molecular mechanisms of wheat responses to salinity stress at each phase of growth is essential to improve breeding techniques and to develop salt-tolerant varieties with genetic modifications. The recent findings indicate that change in leaf and stem anatomical features in different genotypes of wheat are crucial traits to adaptation under salinity stress ( Nassar et al., 2020 ). The research on the physiological changes that occur during leaf senescence due to some stresses has been primarily focused on the loss of photosynthetic pigments, protein degradation, and re-absorption of mineral nutrients ( Zheng et al., 2008 ). At the same time accumulation of secondary metabolites (anthocyanins, flavones, phenolics, and specific phenolic acids) often occurs in plants subjected to stresses including various elicitors or signal molecules ( Sytar et al., 2018 ). It was demonstrated that pigmented wheat genotypes with high anthocyanin content can maintain significantly higher dry matter production under salt stress conditions ( Mbarki et al., 2018 ), which shown the role of phenolic compounds in salinity tolerance together with new breaded pigmented wheat genotypes.

Determination of physiological traits related to stress tolerance could be used as a selection criterion to enhance wheat adaptation to stress conditions. According to the previous investigations, there is a link between different physiological responses of crops to stress and their tolerance mechanisms, such as high relative water content and water potential ( Datta et al., 2011 ). Moreover, it has been observed that anthesis and grain filling period are very sensitive stages under multiple environmental stresses including salinity and have been identified as major constraints to wheat production worldwide ( Ghosh et al., 2016 ). Therefore, it is crucial to understand the effects of salt stress on wheat yield improvement while maintaining superior productivity and adopting mitigation strategies toward the long-term goal of sustainable food security. This study aimed to synthesize salinity effects on wheat germination, seedling growth, reproductive development, grain yield, and quality. Additionally, deleterious effects of salinity in relations to nutrient imbalance and water relations have been objectively described. Moreover, integrated approach for salinity mitigation through osmoprotectants, plant hormones, mineral nutrients, and signaling molecules has been elucidated.

The current review overviews the adverse effects of salinity stress on wheat and its adaptation and mitigation strategies for the sustainability of wheat productivity under the changing climate.

Adverse Effects of Salinity Stress on Wheat

Most of the agricultural lands, which are affected by different degrees of salinity, are located in semi-arid or arid regions ( Liu et al., 2020 ). Huang et al. (2019) concluded that the damage of crops is mostly intensified by the synchronized action of xerothermic aspects, such as aridity and high temperature. Salinity is the most adversely affecting factor on productivity and quality of wheat through altering the physiological as well as biochemical activities in plants. Generation of ROS due to Na + toxicity, which damage biomolecules (e.g., lipids, proteins, and nucleic acids) ( Apel and Hirt, 2004 ) on the cellular level and alters redox homeostasis, is a common phenomenon under salt stress ( Kundu et al., 2018 ). However, salt impacted soils are difficult to remediate due to the circumstances outlined by Arzani and Ashraf (2016) . First, Na + and Cl − ions are highly mobile in soils. Second, it is often an expensive and short-term solution for the chronic problem. Third, soil salinity has a dynamic nature and spatial variation in salinity is generated by the interactions among different variables of edaphic effects (soil pH, bulk density, permeability, topography, geohydrology, water table depth, and groundwater salt content), geographic factors (elevation, slope, and aspect), agronomic practices (irrigation, drainage, tillage, crop rotation, and fertilization), and climatic effects (temperature, humidity precipitation, wind, and evaporation) ( Bui, 2013 ). Therefore, the integrated agronomical, physiological, and soil management approaches and targeting multiple traits at the same time are a crucial step to achieve salinity tolerance. Therefore, it is important to substitute Na + with the Ca 2+ followed by removal/leaching of salts derived by the reaction of the amendment from sodic soil for sustainable crop production ( Sorour et al., 2019 ).

Salinity delays the onset of seedlings germination, decreases the seedling growth and the dispersion of germination events, seedling metabolism, causing a reduction in plant growth and crop productivity ( El Sabagh et al., 2019a , b , c , 2020 ). One important approach is to develop an understanding of the plant response toward salinity stress. The response of plants to salinity can be described in two subsequent phases ( Arzani and Ashraf, 2016 ), during the first phase, salinity causes osmotic stress because of a decrease in the soil water potential ( James et al., 2006 ). The second phase develops within a few days or weeks (depend on the severity of salinity) and accumulates Na + ions in different plant tissues, causing reduced yield and even plant death ( Munns and Tester, 2008 ). Under salinity, Na + is the principle of toxic ion imposing both osmotic stress and ionic toxicity ( Munns and Tester, 2008 ). Salinity also negatively affects wheat phenological developments such as leaf number, leaf expansion rate, and root/shoot ratio ( El-Hendawy et al., 2005 ), and biomass production ( Sorour et al., 2019 ). The saline environment disturbs plant water relations including relative water content, leaf water potential, water uptake, transpiration rate, water retention, and water use efficiency ( Nishida et al., 2009 ).

Salinity adversely affects the growth and yield of crop plants by decreasing the availability of soil moisture, and due to the toxicity effects of sodium and chloride ions at high concentrations to the plant ( Munns and Tester, 2008 ). Salinity stress accelerates all phenological phases of wheat ( Grieve et al., 1994 ), reduces the number of fertile tillers ( Abbas et al., 2013 ), decreases the number of spikelet number spike −1 ( Frank et al., 1987 ), kernel weight ( Abbas et al., 2013 ), and affects grain yield adversely ( Sorour et al., 2019 ). For instance, yield losses up to 45% have been recorded in salt-stressed wheat ( Ali et al., 2009 ). Hasan et al. (2015) observed that saline stress (15 dSm −1 ) significantly decreases grains per spike, 1,000-grain weight, and seed yield in tolerant and sensitive wheat cultivars. The effect of salinity stress on root activity, germination, morphological traits, crucial plant processes, yield, and yield attributes in wheat are illustrated in Figure 1 .

Figure 1 . Illustrates the effects of salinity stress on different growth stages and crucial plant processes.

Germination and Plant Growth

Soil salinity is the second major factor responsible for land degradation after soil erosion, causing a decline in agricultural economic outputs for 10,000 years ( Shahid et al., 2018 ). Poor salinity management can cause soil sodicity of farming soils, where sodium (Na) binds to negatively charged clay, causing clay swelling and dispersal, subsequently decreasing the crop yield. Higher levels of salinity confiscate 1.5 million hectares of land globally every year, and hence ~50% of cultivable land could be deteriorated by the mid of 21st century. During salinity, the exaggeration of most plants is apparent in the early stages, especially during seedling establishment, as it is the most responsive and critical stage that is reported to be strongly associated with successful germination and seedling development. Various factors hamper the crop yield under salinity stress, but osmotic stress, ionic imbalance, and oxidative stress are the major ones among them. In brief, the osmotic stress leads to a higher accumulation of salts in cell sap and tissues which become observable as leaf burn and wilting. These symptoms are reported to be associated directly with the accumulation of Na + and Cl − . Thus, this ionic imbalance causes disequilibrium of nutrients that declines germination, and adversely affects the subsequent metabolic processes ( Hussain et al., 2019 ). Furthermore, the oxidative stress exerted via accelerated ROS generation induces lipid peroxidation, disrupt nucleic acids that ultimately decreases the consistency and overall yield of the affected seed ( Dehnavi et al., 2020 ; Kumari and Kaur, 2020 ).

Germination is a dynamic and critical phase in the lifecycle of a plant that pledges via the imbibition of water ( Kumari and Kaur, 2018 ). It is a triphasic process, and during phase 1, the seeds absorb water, followed by the second phase, i.e. , the “ plateau phase” (stable water content), and characterized by test rupturing. In the third phase, endosperm ruptures and radicle protrusion take place, and it is also referred to as the post-germination phase ( Chamorro et al., 2017 ). In 2007, Läuchli and Grattan proposed a general scheme for depicting the relationship of germination percentage with the time of germination under low, moderate, and high salinity levels ( Figure 2 ).

Figure 2 . Association between germination rate and exposure duration after sowing at different salinity levels (low, moderate, and high) (Source: Läuchli and Grattan, 2007 ).

Salinity inhibits seed germination by either exerting osmotic stress that thwarts water uptake or causes ionic toxicity. These consequences collectively inhibit cell division and expansion, as well as modulates the activity of some key enzymes, thus lastly reduces the seed reserves utilization ( El-Hendawy et al., 2019 ). Thus, it can be said that salinity negatively affected the process of germination by altering the normal germination mechanism that resulted in reduced growth and development, ultimately declined the economic yield. Moreover, the increased incidence of salt stress in the arable land indicates that there is an urgent need for a deeper understanding of the mechanisms for plant tolerance to preserve crop productivity through the optimal regulation of growing conditions of cereal crops. There is dire need to develop strategies such seed priming with natural or synthetic growth regulators etc. for boosting cereals germination in saline environment, otherwise significant decline in germination could lead food crisis in future.

Adverse Effects of Salinity Stress on Morphological Processes of Plants

Soil salinity detrimentally affects the various morphological characteristics of wheat plants including seedling growth, plant height, shoot, and root length, the number of roots, leaves, leaf area, fresh and dry weight, root/shoot ratio, and chlorophyll content. Ahmad et al. (2013a) observed that the early maturity of wheat due to salinity stress reduced the crop height and leaf area and found that plumule length was the most sensitive during early growth stages. Bacilio et al. (2004) found that root colonization pattern, leaf expansion, and flag leaf area in wheat was significantly lower under salinity stress. Furthermore, the number of leaves plant −1 and leaf size, along with leaf longevity, were shriveled because of salinity stress ( El-Hendawy et al., 2009 ). Otu et al. (2018) reported that wheat facing salinity stress exhibited reduced stem length, stem weight, and shoot dry matter. Such detrimental effects of salinity stress on the dry weight of shoot may be due to the direct impact on photosynthesis ( Parida et al., 2005 ). Maas (1990) stated that the salinity changes the final size of a spike and a significant reduction occurs in spike length and number, and grains spike −1 . Shafi et al. (2010) found that salinity stress inhibited the shoot and root dry weight, number of root tips (lateral roots), total root length, average root diameter, and total root volume. The root is the first important organ, and a well-developed root system can contribute advantages to wheat plant to maintain plant growth for the period of early growth phases, and extracts water and micro-nutrients through the soil ( Egamberdieva, 2009 ). The production of the well-developed root system under stress conditions is vital for above-ground biomass production ( Iqbal et al., 2018 ). Saboora et al. (2006) observed that the root development inclined severely due to salinity stress in wheat besides reduced root length as well as area. Ammonium inhibits the root growth of many plants, including wheat, whereas NaCl stimulates the accumulation of ammonium in roots which restrains the root growth. New cultivars having improved agro-morphological traits and potential to ameliorate the adverse effect of salinity must be developed through a targeted breeding program.

Adverse Effects of Salinity Stress at the Reproductive Stage on Plant Growth and Yield

Several earlier studies illustrated that the reproductive phase of any crop is the most sensitive stage to the abiotic stresses, including salinity ( Ehtaiwesh and Rashed, 2020 ), and cause massive yield penalty in important crops, including wheat ( Kalhoro et al., 2016 ). However, it is well-postulated that salinity influences plant growth and yield attributes primarily due to ion toxicity and osmotic stress. Although, the intrinsic pathways and molecular mechanisms are so far not clear. Salt stress influences cell ion homeostasis by altering ion balance, such as increased Na + and a simultaneous decreased Ca 2+ and K + content. A recent study suggested that the class I high-affinity K + transporter (HKT) family is involved in the exclusion of Na + from leaf blades at the reproductive stage, and this significantly influences sodium ion homeostasis under salinity stress ( Suzuki et al., 2016 ). Likewise, the grain dry matter and K + /Na + ratio showed a significant correlation and regulated the grain filling rate and duration under salt stress ( Poustini and Siosemardeh, 2004 ). Similarly, an isotopic study (δ 13 C, δ 18 O, and δ 15 N) in wheat crop under different salinity regimes depicted that nitrogen metabolism and stomatal limitations at the anthesis stage are among the major cause of biomass reduction ( Yousfi et al., 2013 ). Furthermore, transcriptomics study in wheat (Arg cultivar) genotype revealed that 109 genes are unique in treated plants, which are mainly associated with transcription factors gene (late embryogenic abundant [ LEA ] protein, dehydrin, MYB , and ERF ), ion transporter ( SOS1 ), antioxidant defense (peroxidase, glutathione S -transferase, GST) and secondary metabolites (caffeic acid 3-O-methyltransferases), and have a role in the regulation of ion homeostasis, cell redox balance, and oxidative stress ( Amirbakhtiar et al., 2019 ).

Besides ionic imbalance, salinity stress influences available soil water, tissue water content, water use efficiency, water potential, transpiration rate, rooting depth, root respiration, root biomass, root hydraulic conductance, cell turgidity, and osmolytes accumulations ( Zheng et al., 2008 ). Besides, it also reduces the photosynthetic rate, biomass accumulation, and source-sink activity, which hastens the reproductive organ's senescence and negatively affects the yield response factors ( Khataar et al., 2018 ). Similarly, at the reproductive phase, alteration in water potential reduces the cell elongation, flag leaf thickness, vascular tissue thickness, mesophyll, and epidermal cell size, which are responsible for the reduction of flag leaf turgidity and leaf area, assimilates synthesis, and finally yield potential ( Farouk, 2011 ).

Although, Ashraf and Ashraf (2016) suggested that these physiological and biochemical trait alterations are stage-specific and attribute to final yield potential. For example, salinity at different stages such as anthesis, early booting, and mid grain filling causes a reduction of grain yield by 39.1, 24.3, and 13.4%, respectively. Salt stress caused the acceleration of shoot apex development but decreased the number of spikelet primordia and also resulted in early terminal spikelet stage and anthesis. This decreased the number of spikes and kernels per spikes, which ultimately reduced the yield potential in wheat ( Maas and Grieve, 1990 ). Likewise, use of 200 mM NaCl stress at pre-anthesis and post-anthesis stage caused reduction in aboveground biomass, ears plant −1 , ear weight, number of grains plant −1 , C, N, and C/N ratio in grains, and carbon use efficiency at both stages, although the reductions were higher due to imposition of stress at both stages as compared to single-stage ( Eroglu et al., 2020 ). It has also been observed that the unavailability of sufficient photo-assimilates during the reproductive stage is the leading cause for losing yield potential in wheat, and this might be due to the changes in gene expression caused by salt stress during the pre-anthesis and grain filling stage. For example, alteration of sucrose 1-fructosyltransferase, sucrose: fructan6-fructosyltransferase, and fructanexohydrolase hampers the fructan accumulation, and remobilization of carbohydrate to grains ( Sharbatkhari et al., 2016 ). Similarly, yield component traits such as spike length, spike weight, filled spikelet plant −1 , total spikelet plant −1 , and test weight were reduced to 8, 3, 37, 20, and 10%, respectively under stress condition, and resulted in 16% low total grain weight plant −1 ( Tareq et al., 2011 ). Further, losses of grain weight under saline stress occurs due to pollen sterility, less production of assimilates, and reduced partitioning toward economic parts (grains) of plants. Likewise, the study on 151 synthetic wheat-breeding lines suggested that salt stress to be associated with Na + toxicity, which reduced the total kernel weight, and starch content by 20 and 6%, respectively ( Dadshani et al., 2019 ).

In spite of these changes, salinity stress has substantial impacts on grain quality traits. For example, the use of 200 mM of NaCl in wheat (cv. Shatabdi) showed an increase in Na + , K + , and Ca +2 content in grains by 155, 10, and 20%, respectively under stress ( Tareq et al., 2011 ). Similarly, the use 0.75% NaCl salt increased the contents of high molecular weight glutenin subunit, glutenin macro-polymers (36.14%), and amino acids and improved wheat quality at certain levels but reduce grain yield ( Zhang et al., 2016 ). Similarly, Nadeem et al. (2020) reported that salinity negatively influenced the yield (grain length, test weight, and grain yield), nutritional quality traits (moisture, fat, ash, fiber, and gluten content), and mineral nutrient content (K, Ca, Fe, P, Zn, and Mg) in wheat crop. Therefore, it can be concluded that salinity stress is a major factor for limiting yield and yield quality traits, and it affects the reproductive phage severely by altering ion homeostasis, water status, and assimilate partitioning.

Adverse Effects of Salinity on Grain Quality

Soil salinity imparts detrimental impacts on vital metabolic, biochemical, and physiological processes occurring within the plants leading to the deterioration of grain quality. The extent of changes in grain quality caused by salinity depends on the sternness of the stress. From physiological perspectives, grain quality is affected owing to the accumulation of salts in the root zone leading to osmotic stress induction, which vigorously disrupted cell ion homeostasis. Salt exposure causes osmotic stress at the beginning, while subsequently, ion toxicity hampers growth, grain development, and quality, especially if the exposure periods get prolonged. The deterioration of grain quality of cereals has also been explained in agronomic perspectives as well. The reduction in the capability of roots for water uptake owing to osmotic stress contributes to growth inhibition, declined crop productivity, and inferior grain quality ( Netondo et al., 2004 ). Thus, grain quality is drastically affected by the devastating effects of osmotic stress, while the subsequent slower ion toxicity phase is even more detrimental.

Winter wheat constitutes a vital source of carbohydrates and protein for humans across the globe ( Siddiqui et al., 2019 ). There have been significant achievements pertaining to boost wheat yield over the decades. However, the demand for higher-quality grain has also increased with the improvement in human lifestyle ( Park et al., 2009 ). Plant variety, in conjunction with the prevalent environment, has also been reported to determine the wheat quality to a certain extent ( Sairam et al., 2002 ). Previously, most researchers focused on the impacts of salinity on wheat grain yield ( Zheng et al., 2009 ), but little is known about the relationships between salt-tolerance and grain quality. There are diverse effects of salinity levels on the grain quality of cereals. It has been inferred that salinity levels, especially beyond 150 mM of NaCl, significantly reduced the grain yield, whereby grain quality deterioration remained significant at 100 mM ( Farooq and Azam, 2005 ). There is a varying impact of salinity on the nutritional value of grains depending upon the plant growth stage at which stress occurs. Breeding approaches to improve grain yield, especially in the salt-tolerant varieties have negatively affected the grain quality as these traits are often inversely related.

As far as grain quality of cereals under abiotic stresses especially salinity is concerned, there have been relatively limited investigations. Protein, fat, and fibers contents in grain decreased significantly due to salinity. In response to imposed salinity, protein content improved in the sensitive wheat genotypes, while it decreased in tolerant genotypes. The ash and beta-carotene contents were enhanced, while the gluten index got declined considerably ( Katerji et al., 2005 ). At the same time, Maqsood et al. (2008) inferred that the decrease in protein and fiber contents of cereals was due to the accumulation of salts in the root zone, which deteriorated the grain quality. Additionally, higher concentration of Na + in the external environment interferes with the absorption of nitrogen, which leads to lower protein content in wheat grains. Thus, the nutritional imbalance is reported to be the major factor behind the deteriorated grain quality of wheat under salt stress. Furthermore, salt stress interfered with prime processes, including photosynthesis, energy production, lipid metabolism, and protein synthesis. Lastly, salinity reduced phosphorus (P) concentration in plant shoots, which interfered with grain development and nutritional quality. Optimization of P foliar doses might be developed as a potent approach to alleviate the salinity effects on grain size and weights which are the vital yield attributes of cereals.

Protein Content

Protein content is the most important indicator of wheat grain quality and hence it governs and determines the end-use quality. The grain quality of wheat, especially the quality of protein as well as its quantity, is vital for dough properties and the bread-making quality of wheat flour. Under the saline condition, the protein quantity is increased, but the protein quality is decreased in wheat and triticale. The protein content is controlled by the genetic makeup of a particular cultivar or line, environmental factors, especially temperature and soil fertility status predominantly concerning N concentration in soil solution. It is significantly affected by environmental factors and their interactions. Positive correlations between environmental factors and wheat grain protein content have been reported during grain filling ( Huebner et al., 1997 ). Protein content, along with composition, significantly modifies wheat flour quality for bread-making ( Branlard et al., 2001 ). Nevertheless, the high protein content of the wheat grain is privileged because flour protein content has a linear relationship with bread-making quality ( Schofield, 1994 ). Conversely, protein quality signifies the quality of bread-making. It has been established that the composition of grain protein primarily depends on wheat genotypes; however, environmental factors and their association significantly affect protein composition ( Zhu and Khan, 2001 ). Among environmental factors, soil fertility status, especially nitrogen concentration, temperature, and moisture, influence cereals grain protein content ( Rao et al., 1993 ). Environmental stresses also impart their influence on milling-quality as indicated by test weight. Test weight is a highly heritable character and has a direct relationship with grain quality, which can find its use for early selection of wheat lines in breeding programs ( Troccoli et al., 2000 ). The crude protein content of cereal declined from 17.21 to 8.51% under salt stress ( Fernandez-Figares et al., 2000 ). Similarly, Darvey et al. (2000) recorded a higher reduction of protein content in wheat compared to triticale. Contrarily, Francois et al. (1986) observed the increment of protein content in durum wheat under salt stress. Environmental factors, especially heat and salt-stressed to promote leaf senescence at grain filling, which promotes protein deposition over accumulation of starch in the grain. It is due to the fact of carbohydrate synthesis, as well as translocation to the grain, is highly prone to adverse and harsh growing conditions compared to protein synthesis and translocation ( Fernandez-Figares et al., 2000 ). Furthermore, it is also established a fact that the protein and starch deposition rate and duration in the cereals grain are entirely independent events, which are influenced and governed by a group of environmental factors ( Jenner et al., 1991 ). Likewise, starch deposition seemingly remains more sensitive under salt stress for shortening of grain filling period in comparison to the deposition of protein. Moreover, optimum environmental factors cause a delay in leaf senescence, which promote nitrogen absorption from the soil and subsequently translocate it to leaves. In this way, a higher grain yield with lower protein content is produced by wheat. The existence of a negative relationship between protein content and grain yield has been reported in wheat, barley, and triticale (manmade cereal developed by crossing wheat and rye) crops ( Garcia del Moral et al., 1995 ). In response to imposed salinity, photosynthetic rate declines as feedback response due to several internal changes leading to higher demand for assimilates; triggering the rate of carbohydrate accumulation and cause a delay in leaf senescence and consequently promoting the onset of Rubisco hydrolysis. The net result is limited N availability, which tends to remobilize toward the grains. Moreover, salinity exposure results in rapid degradation of the RuBisCo enzyme, leading to the higher redistribution of N to the developing grains ( Fernandez-Figares et al., 2000 ).

Gluten Content

The proteins for gluten storage are divided into gliadins (confers extensibility) and glutenins (causes elasticity). Similar to the protein content of the wheat grain, salinity tends to boost wet and dry gluten content in salt-tolerant wheat cultivars, while the opposite has been observed for salt-sensitive cultivars ( Khan et al., 2008 ). Regarding the salt stress effect on the gluten content of wheat grains, it multiplied with increasing salt content in the soil ( Shen et al., 2007 ). In contrast, Kahrizi and Sedghi (2013) inferred that salinity has a very minute impact on the gluten content of cereals grains, while Houshmand et al. (2014) observed that abiotic stresses (salt and drought) result in a significant increment of wet and dry gluten contents. Zheng et al. (2009) also found that the gluten content of wheat cultivars has a direct relationship with the salt concentration of soil. There is a dire need to conduct further in-depth studies to determine the impact of salinity levels on gluten concentration and composition in wheat grain under varying pedo-environmental conditions.

Ash Content

The Ash content of wheat grain represents the mineral constituents of grain. In comparison to saline conditions, optimal growing conditions give rise to the higher ash content of whole-grain owing to improved minerals uptake from the soil solution ( Troccoli et al., 2000 ). Contrarily, Katerji et al. (2005) found an inverse relationship between salinity and ash content of durum wheat. Likewise, Francois et al. (1986) reported that soil salinity reduces ash content of durum as well as semi-dwarf bread wheat; thus, it may be inferred that there are disturbing effects of soil salinity pertaining to the minerals uptake, translocation as well as accumulation processes which result in a severe decline of ash content in wheat grain. Reddy et al. (2003) examined that salinity significantly reduced the grain yield as well as quality along with crop residue quality. Francois et al. (1986) concluded that soil salinity reduced the ash content and improved the flour color as well as protein content. Katerji et al. (2005) reported that excessive salt decreases ash content of wheat, and in this way, wheat grain quality gets improved. Moreover, the direct relationship between water use efficiency (WUE) and ash content of wheat grain can be a useful indicator to select wheat varieties having superior WUE under saline conditions.

Carbohydrate Content

Carbohydrate content is an important indicator of wheat grain quality, which is influenced by salinity stress, especially when wheat plants are exposed to saline environment at the grain filling stage. The synthesis and translocation of carbohydrates are more sensitive to suboptimal growing conditions compared to protein production ( Rao et al., 1993 ). Salinity stress at the post-anthesis stage seriously shortens the accumulation duration of storage proteins leading to modification in gliadins and glutenins accumulation pathways. Moreover, the disruption effects of salinity on photosynthesis rate reduces carbohydrates synthesis at the vegetative growth stage, while it also disrupts or halts the translocation of carbohydrates toward grains at the initiation of grain filling stage, and thus it results in a significant reduction of carbohydrates concentration in wheat grain ( Fernandez-Figares et al., 2000 ).

Beta-Carotene Content

There are rare research investigations that have focused on wheat grain quality, especially beta-carotene content under salinity stress. The beta-carotene contents varied significantly in salt-tolerant and sensitive cultivars of durum wheat under saline conditions. The beta-carotene content of grains recorded a sharp decline in wheat cultivars under salt stress environments ( Katerji et al., 2005 ). Likewise, Francois et al. (1986) reported that both beta-carotene and ash content witnessed a sharp decline owing to salinity. Future studies need to explore the detrimental effect of saline environment on carotene contents with respect to interactive effect of varying genotypes, agro-environmental factors and agronomic management practices along with frequency and intensity of salinity.

Salinity and Nutrient Imbalance

One of the adverse effects of a saline environment, especially high salt concentration in soil solution, causes a severe reduction in the uptake of nutrients and water. Resultantly, osmotic stress intensifies ion toxicity, imbalance of nutrients under water-deficit conditions. Salinity leads to injury of photo-synthetically active leaves by causing chlorosis and triggering leaf senescence in cereals ( Hanin et al., 2016 ). Ion imbalance is one of the most severe impacts caused by a saline environment dominated by NaCl presence, while numerous other ions also multiply the severity of the stress. The combinations of ions in the saline environment determine the types of nutrients which become either deficient or excessive ( Hawkins and Lewis, 1993 ). The underlying mechanism of ionic imbalance has recently been elaborated. Under low-moderate salinity, the nutrient imbalance is prevented by salt ions transportation, which occurs within the vacuole that tends to off-set the ion flux into the cell from the plasma membrane ( Blumwald et al., 2000 ). When the influx rate is higher, ionic homeostasis in cells gets compromised, and anions (Cl − ) and cations (Na + , Mg 2+ , Ca 2+ ) accumulate in the plasmatic compartments (cytosol, matrix, and stroma) of the cell instead of the vacuole, which results in nutrient imbalance especially K and P. To avoid ion imbalance in the short term, accumulation of ions in the apoplast continues, and resultantly no transportation of ions from the apoplast to the symplast occurs. Such ion accumulation in apoplast is usually regarded as the causal mechanism behind salinity-induced ionic imbalance ( Speer and Kaiser, 1991 ). Accumulation of salt in the leaf apoplast disrupts cell water relations leading to wilting ( Flowers et al., 1991 ).

Inorganic ions often perform to be competitive enzyme inhibitors, which host ionic substrates but also interfere with protein surface charges besides destabilizing molecular level interactions. The nutrient imbalance under saline conditions leads Na + to substitute K + from the essential binding sites. In biochemistry, the typical instances for K + dependency are ribosomes and pyruvate kinase. It has been reported that K + presence in optimal concentration boosts pyruvate kinase activity (Vmax) as much as 400 times ( Oria-Hernández et al., 2005 ), while K + substitution by Na + causes inhibition up to 92%. In addition, peptidyl transferase activity in eukaryotic ribosomes gets regulated by K + concentration and might reach upto 20 s −1 under optimal conditions ( Ioannou and Coutsogeorgopoulos, 1997 ). However, metabolic imbalances occur in the case of drop-in K + concentration and an increase in Na + concentration, and such ionic imbalance leads to the initiation of numerous inhibitory processes that cause redox and energy metabolism.

Under normalized conditions, nutrient ion net fluxes of different cereals (maize, wheat, and barley) and legumes such as broad beans get adjusted in accordance with cellular requirements and crop development phases, leading to the establishment of ionic homeostasis ( Niu et al., 1995 ). However, salinity severely disturbs ionic harmony as excessive salt ions (e.g., Na + , Cl − or Mg 2+ and SO 4 2 - ) accumulation alters the composition of the soil solution. Excessive accumulation of the Na + cation disturbs uptake of many cationic nutrients such as K + ( Wakeel et al., 2011 ) or Ca 2+ ( Gardner, 2016 ); resulting in nutrient imbalance. For instance, excessive Na + induces Ca 2+ deficiency having an appearance like lesions on aerial plant parts along with a reduction in leaf blade dry weight ( Maas and Grieve, 1990 ). Furthermore, Na + induces K + uptake reduction leading to declined shoot growth. In contrast, Cl − presence in excessive concentration leads to impairment of nutrient uptake by disturbing anions uptake ( Geilfus, 2018a , b ). The uptake and anion-anion interactions are antagonistic in nature as the Cl − concentration multiplies by many folds in the soil solution under NaCl salt stress. It has been established that Cl − is greatly mobile in the soil, and negatively charged kaolin and clay minerals significantly repel Cl − leading to its accumulation in the soil macro-pores and soil solution ( Thomas and Swoboda, 1970 ). On the other hand, cations, including Na + , get absorbed in very minute concentration by the negatively charged soil surface under the soil environment ( Borggaard, 1984 ). Moreover, antagonism has been reported among Cl − and nitrate (NO 3 − ) when external Cl − concentrations become too higher ( Abdelgadir et al., 2005 ), which causes a reduction in the growth and yield of wheat ( Hu and Schmidhalter, 1998 ). However, this has not been similar for corn crop ( Hütsch et al., 2016 ). Interestingly, severe competition for anion-anion uptake has also been described for Cl − and phosphate (PO 4 3− ). In addition to cereals, such competition has also been reported for tomatoes as well as rose plants ( Massa et al., 2009 ).

Under NaCl salinity, it seems that Cl − tends to hinder the growth and development of crops by inducing the deficiency of phosphorous and sulfur through inhibiting PO 4 3− and SO 4 2− uptake. However, facts remain that generalizable conclusions may not be drawn from the published research and relevant findings. For concise conclusiveness, it becomes pertinent to distinguish between Cl − and counter-cations effect under saline environment. There is a dire need to perform further experiments regarding the behavior of membrane-impermeable counter-cations of a specific salt. Besides, the underlying molecular mechanism of nutrient-nutrient antagonistic uptake remains unclear. However, one of the possible justifications can be attributed to antagonistic competition for a binding site at transport proteins of salts ions. Another justification can be leaking of Cl − from protein pores, which quantitatively displace PO 4 3− or SO 4 2− leading to a sharp decline in their take up. Both above-stated scenarios rely on transmembrane pores, physicochemical attributes such as their charge and size. For instance, hydrated Cl − ion radius is similar to SO 4 2− . It seems that under salinity stress, glycophytic crops did not encounter the necessity to escape Na + and Cl − uptake during the breeding and evolution process, which hampered the development of adaptive mechanism at the transporter site for differentiating among the requisite nutrients and undesired ions of salts. Thus, it might be inferred that two pronged strategy encompassing reduction in the uptake of salt ions and their replacement in the soil solution as well as plant need further investigations to cope with the serious challenge of salinity and impart sustainability to cereals production.

Water Relation to Salinity Stress

Wheat plants exposed to salt stress change their environmental condition. The capability of plants to tolerate salt is determined by several biochemical ways that facilitate the acquisition or maintenance of water relations, ionic homeostasis, and protect chloroplast functioning. In agriculture, salinity has been the most distressing abiotic stress having pronounced damaging effect on physiological, morphological, and biochemical characteristics of the crop plants, including uptake of water and nutrients, germination, growth, photosynthesis, enzyme actions, and yield ( Cisse et al., 2019 ). Plant water status is hard to measure as it keeps on changing every minute-to-minute. Since stomatal conductance on which it is entirely dependent in the short term ( Gil-Muñoz et al., 2020 ), and psychometric or pressure chamber measurements are often tricky to deliver accurate values ( El-Hendawy et al., 2005 ). In areas where the rainfall is low and the salt remains in the subsoil, increased salt tolerance would allow plants to extract more water ( Munns et al., 2006 ). Mostly wheat productivity is reduced when water stress occurs at heading time, and the reduction is severe when it occurs after anthesis ( Barutcular et al., 2016a , b ).

Accessibility of water in plants is a crucial factor for all physiological and metabolic processes of plants ( Sreenivasulu et al., 2007 ). The higher concentration of salts causes osmotic stress to plants, which results in low water potential in wheat crop ( Qamar et al., 2020 ). The rate at which new leaves are produced depends basically on the water potential of the soil water, in the same way as for a drought-stressed plant. According to the previous investigations, there is a link between the different physiological reaction of crops to stress and their tolerance mechanisms, viz. high relative water content and water potential ( Datta et al., 2011 ). Singh et al. (2015) reported that salinity prevents seed germination by either exerting osmotic stress that thwarts uptake of water. Such stresses cooperatively inhibit cell expansion and division, as well as modulates the activity of some key enzymes, thus reduces the seed reserves utilization ( El-Hendawy et al., 2019 ).

Water potential of plants at reproductive phases also reduces the cell extension, vascular tissue thickness, flag leaf thickness, mesophyll, and epidermal cell size, which are responsible for the reduction of flag leaf turgidity, flag leaf area, assimilates synthesis, and yield potential ( Nassar et al., 2020 ). Zhang S. et al. (2016) reported that relative water content (RWC) declined by 3.5 and 6.7%, compared to their controls in the salt-tolerant, and salt-sensitive cultivars, respectively, after 6 d of 100 mM NaCl exposure. Further research resulted in a significant reduction in water use efficiency (WUE) of both tolerant and sensitive cultivars under saline field conditions ( Gil-Muñoz et al., 2020 ). The ratio of water content decreased in the root but increased in shoot and spike of other cultivars of wheat ( Tammam et al., 2008 ). Moreover, a direct relationship between WUE and an ash content of wheat grain can be a useful indicator to select wheat varieties having superior WUE under salinity ( Zhang et al., 2020 ).

Consequently, from these findings, we conclude that salinity stress is a major factor for limiting yield and grain quality traits, and it affects the reproductive phase severely by altering ionic homeostasis, water status, and assimilate partitioning. Foliar application of antioxidants and growth regulators that maintain an appropriate water level in the leaves to facilitate adjustment of osmotic and stomatal activity ( Arshad et al., 2020 ). The introduction of deep-rooted crop species is necessary to lower the water table, but salt tolerance will be required not only for the “de-watering” species but also for the annual crops that follow, as salt will be left in the soil when the water table is lowered.

Approaches to Improve Salt Stress Tolerance in Wheat

Improving the crop performance by conventional breeding methods, introducing gene markers, and selection of genetically modified genotypes are the basic approaches to produce tolerance against salinity stress in plants ( Hasanuzzaman et al., 2011 ). In recent year development of transgenics (transfer of genes from tolerant sources) are a promising approach to developing stress-tolerant varieties. Several transgenics are also developed in wheat crop to ameliorate the adverse effects of salinity. Table 1 represents the transgenic developed in wheat crop using the osmoprotectant, ion transporters genes and their source and influenced traits to make salinity tolerant wheat.

Table 1 . Highlights the some transgenic developed in wheat crop and influenced traits for salinity tolerance.

Salt Tolerance Through Osmoprotectants

Various mechanisms are adopted by plants under salinity stress at the organism and tissue level to avoid adverse effects of salinity. Plants produce osmolytes and some beneficial solutes that prevent them from the impact of salinity stress by maintaining osmotic and ionic balance ( Ashraf and Foolad, 2007 ). These compatible solutes and osmoprotectants are uncharged, less toxic soluble organic solutes that provide a -optimal environment to plants under salt stress. Proline, glycine betaine, salicylic acid (SA), and sugar alcohols like trehalose, sorbitol, and mannitol are examples of osmolytes. Membrane stabilization, protein synthesis, and maintenance of osmotic pressure are the important functions performed by these osmolytes and exogenous application of these compounds are helpful for improving salt tolerance in wheat. Plant's exposure to salt stress improves their ability to synthesize osmolytes like glycine betaine, sugar alcohols, and sorbitol that helps them to survive under salinity ( Chen and Jiang, 2010 ). The use of osmolytes was found very vital against salt tolerance induction ( Alam et al., 2014 ). Application of trehalose (10 mM) reduces H 2 O 2 level, lipid peroxidation, free amino acids, proline and LOX enzyme activity, while improves photosynthetic pigments, accumulation of organic solutes and elevating the expression of AOX, NHX1, SOS1 to ion homeostasis under salinity stress ( Alla et al., 2019 ). Further, seed priming and foliar application with plant growth regulators (PGRs), inorganic and organic ion found effective in salinity tolerance as they improve osmolytes production and strength the antioxidant system of plants ( Wajid et al., 2019 ). Recently, the metabolic engineering of osmoprotectants elucidates the mechanisms of salinity tolerance in crops. Further, they also suggested that engineering of these metabolic compounds open a way for understanding the complex nature of salt stress and its relation with other crucial plant processes ( Alzahrani, 2021 ). However, thorough investigations are needed to identify crop-specific osmoprotectants, their dose optimization for exogenous application, time of foliar sprays and stage of crops.

Salinity Tolerance Through Plant Hormones

Salt stress tolerance and plant growth regulation are associated with the biosynthesis of a variety of compounds in minute concentrations, which are termed asplant hormones ( Ryu and Cho, 2015 ). Salt stress was mitigated by several types of plant growth hormones, abscisic acid (ABA), auxins (AUX), cytokinin (CK), and ethylene (ET). Auxin is an important growth regulator that enhances seedling establishment, shoot dry weight, and also balanced the ionic pressure in plants under salinity stress ( Iqbal and Ashraf, 2007 ). Primed seeds with growth regulator auxin mitigated the salinity by improving the hormone balance, nutrients uptake leading to better yield and productivity of both salt resistant and susceptible genotypes. Crop growth rate, leaf area index, photosynthetic efficiency, grain yield, and its quality were improved by seed priming with gibberellic acid (GA) ( Shaddad et al., 2013 ). Foliar applied -GA also enhances salinity tolerance by increasing seedling establishment, plant productivity, and antioxidant enzymatic efficiency under salt stress ( Tabatabaei, 2013 ). Salinity stress could be mitigated by priming with cytokinin that improved seedling establishment, tillers formation, and grain weight under salt-affected soils ( Iqbal et al., 2006 ).

Plant Nutrients

The availability of nutrients is also responsible for mitigating the salt stress effect by various physiochemical and biological mechanisms. Foliar application of potassium improves photosynthesizing efficiency, antioxidant enzymatic efficiency, potassium intake by plants, and sodium absorption and salt stress environments ( El-Lethy et al., 2013 ). Sodium absorption, leaf area index, and biological yield were found to be improved under stressed environments by external application of phosphorous ( Khan et al., 2013 ). Calcium sulfate is also an important nutrient that alleviates the ill effect of salt stress by improving the intake of calcium and potassium and improves crop growth in salinity stress ( Zaman et al., 2005 ). The application of calcium nitrate decreased the peroxidation of lipids and excretion of electrolytes that enhanced the salt tolerance in plants ( Tian et al., 2015 ). Recently the application of inorganic nutrients (Si, K, Zn), organic extract (moringa leaf extract, biochar), as seed or foliar treatments improve the salinity stress tolerance ( Jan et al., 2017 ). Likewise, the application of nanoparticles (Zn, Si) ( Mushtaq et al., 2017 ) showed promising results. Although, the molecular understanding regarding the application of different nutrients and transporters response can accelerate the salinity stress tolerance program in plants.

Salt Tolerance Through Various Signaling Molecules

Various signaling molecules can crosstalk with phytohormones and antioxidants within the plants that help plants to survive under salt stress. Nitric oxide (NO) is the most widely used signaling molecule to mitigate various abiotic stresses, particularly salt stress. It has interaction with other molecules by several pathways due to its signaling role besides improved crop productivity under salt-stressed environments ( Hasanuzzaman et al., 2013 ). A valuable improvement was noticed in the wheat seedling establishment by exogenous application of NO under salt stress. Other than the NO, hydrogen sulfide (H 2 S), H 2 O 2 , and ROS have a significant role in salinity stress tolerance ( Khan et al., 2017 ). These compounds have crucial roles in the regulation of salinity stress tolerance via ion, hormonal, and redox homeostasis in salt-affected cells and reduce the drastic effect by strengthening the antioxidant defense ( Bhuyan et al., 2020 ). Moreover, these compounds have the ability to crosstalk with other signaling compounds and plant growth regulators such as melatonin, ET, ABA, and salicylic acid ( Kolbert et al., 2019 ). Although, the last few years study of gas transmitters (gaseous signaling molecules) under plant abiotic stresses opens gate for further understanding the abiotic stress signaling mechanisms in depth. However, depth study at molecular level still required to complete understanding of abiotic stresses signaling mechanisms.

Use of Plant Growth Hormones in Mitigating Salinity-Induced Damages

Salt stress adversely affects plant growth and related metabolites, and consequently reduces crop yield ( Islam et al., 2011 ). The reduction of plant growth and alteration of related metabolites is evident due to the decline of natural growth hormones in plant tissues ( Yurekli et al., 2004 ). Wang et al. (2001) stated that salinity stress decreased the indole-3-acetic acid (IAA) and salicylic acid (SA), whereas increased the abscisic acid (ABA) and jasmonic acid (JA). Exogenous application of hormones, i.e., plant growth regulators (PGRs), ameliorated the negative effect of salt-induced stress and enhanced the crop yield. PGRs under the saline environment can alleviate the adverse effects of salt stress by enhancing the germination and seedling growth of wheat ( Samad and Karmoker, 2012 ).

Gibberellic Acid (GA 3 )

Gibberellic acid improved the growth criteria, photosynthetic pigments, and consequently the crop yield of wheat cultivars due to better osmoregulation resulting in increased water flow and water status using the organic solutes (saccharides and proteins), which in turn increased the photosynthetic area and yield ( Shaddad et al., 2013 ). Under saline stress conditions, GA 3 stimulated the growth of wheat ( Afzal et al., 2005 ), maize ( Hassanein et al., 2009 ), and sorghum ( Azooz et al., 2004 ). At the same time, GA 3 modulation could support abiotic stress tolerance in wheat crop ( Abhinandan et al., 2018 ). GA 3 signaling mechanism involved in various developmental and abiotic stress conditions is mediated through an important GA 3 signaling molecule called DELLA protein. DELLA protein regulates a complex network of transcription factors and genes ( Schwechheimer, 2012 ). GA 3 signaling has shown the targeted deterioration of a group of GA 3 -response through transcriptional repressors ( Golldack et al., 2014 ). Such signal pathway has observed to be dominant to the success of wheat crop seedlings in the Mediterranean soil under water deficit conditions ( Amram et al., 2015 ). It was found that the endogenous level of GA 3 is inhibited under drought and salt stress ( Llanes et al., 2016 ). Uses of GA-inhibiting compounds drought-stressed plants alleviate the negative effects of stress and increase bio weight and yield ( Plaza-Wüthrich et al., 2016 ). It has been also found that GA and auxin (IAA) treatment in wheat reduces the negative effects of ethylene and regulate salinity tolerance in wheat crop ( Abd El-Samad, 2013 ).

Abscisic Acid (ABA)

Abscisic acid has been found to be the main regulator of abiotic stress tolerance in wheat via regulation of protein kinases activities, which is important for phosphorylation processes ( Umezawa et al., 2009 ). The contribution of Snf1-related protein kinases (SnRKs) has been studied extensively in Arabidopsis. Some studies of SnRKs in wheat has shown the presence of other SnRK2 homologs that appear to play a role in ABA-mediated abiotic stress signaling ( Mao et al., 2010 ). The expression of wheat SnRK homologs is stimulated by salt stress, cold stress, drought (induced by PEG), and the application of exogenous ABA ( Tian et al., 2013 ). Likewise, Dong et al. (2013) reported that 12-oxo-phytodienoic acid reductases (OPRs) gene associated with the synthesis of ABA and promotion of ABA-dependent and ROS related stress signaling mechanisms and confer salinity tolerance in wheat. Recently, an ABA functional analog B2 has been shown a positive response under salinity stress by enhancing the expression of ABA-responsive genes and antioxidant activity ( Duan, 2020 ). Moreover, ABA is a crucial stress hormone that regulates the multiple abiotic stresses in the plant including salinity via crosstalk with other signaling molecules and PGRs. To date, numerous genes/transcription factor are identified (TaASN1, TabHLH1) ( Yang et al., 2016 ), which associated with ABA signaling and stress tolerance.

Auxin and Cytokinin

The exogenous application of auxins, cytokinins mitigate the adverse effects of salt stress and consequently improved seed germination and growth ( Naidu, 2001 ; Khan et al., 2004 ). Auxin and targeted cytokinin signaling is observed to be suppressed during abiotic stress signaling in wheat plants ( Abhinandan et al., 2018 ). Furthermore, the cytokinin and auxin pathways regulate a plethora of developmental processes through their dynamic and complementary actions and their ability to crosstalk support as perfect candidates for mediating stress-adaptation responses ( Bielach et al., 2017 ). Tryptophan derivative auxin is mostly present in the form of indole-3-acetic acid (IAA), and it was decreased in the leaves of wheat under the cold or frost stress ( Kosová et al., 2012 ). It was shown that the cold-sensitive wheat variety was characterized by a high concentration of auxin followed by an acclimatization period connected with reduced fitness. The cytokinin level is reduced early in cold-tolerant wheat varieties as compared to the cold-sensitive ones ( Kosová et al., 2012 ). The imposition of drought and salt stress during the reproductive stages of wheat has been shown to reduce the grain filling, which allied with reduced auxin concentration ( Abid et al., 2017 ). Nishiyama et al. (2011) observed that drought stress decreased the cytokinin biosynthetic enzymes along with suppressed positive cytokinin signaling components, which might improve the drought-tolerance of wheat plants. The reproductive phase of wheat is more sensitive to stress, and the imposition of drought stress at this stage reduced grain filling, which is linked with low levels of auxin and cytokinin, while external cytokinin application rescued this problem ( Abid et al., 2017 ). It has been reported that cytokinin increases the activities of antioxidant enzymes catalase (CAT) and ascorbate peroxidase (APX), prevent cellular damage by ROSs, and shore up antioxidant molecules, xanthophyll ( Wilkinson et al., 2012 ).

Salicylic Acid

The application of salicylic acid (SA) mitigates the harmful effect of abiotic stresses ( Abhinandan et al., 2018 ). External application of SA in wheat has been shown to be a signaling molecule to stimulate the internal radical detoxification system ( Noreen et al., 2017 ; Fardus et al., 2018 ). Exogenous application of SA in wheat supports antioxidants production via utilizing ROS to be a second messenger ( Agarwal et al., 2005a , b ). Such responses can reduce oxidative damage under drought, heat, and saline conditions ( Fardus et al., 2018 ). Salicylic acid also induces the accumulation of auxin and ABA, which provides tolerance against salinity stress ( Shakirova et al., 2003 ). Likewise, the seed priming with SA, ABA and ascorbic acid improved the seedling performance by enhancing seedling fresh weight, length, and decrease electrolyte leakage. Although, the authors suggested that the priming with ABA is not so effective ( Afzal et al., 2006 ).

The promotion of abiotic stress tolerance in wheat has been shown by ethylene inhibitors ( Abhinandan et al., 2018 ). Ethylene modulates salinity stress responses largely via maintaining the homeostasis of Na+/K+, nutrients, and ROS by inducing antioxidant defense in addition to elevating the assimilation of nitrates and sulfates. Moreover, a cross-talk of ethylene signaling with other phytohormones has also been observed, which collectively regulate the salinity stress responses in plants ( Riyazuddin et al., 2020 ). Ethylene participation in the later phase of plant growth and development relates to leaf abscission, ripening of fruit, maturation of seeds, and plant drying ( Wilkinson et al., 2012 ). It was shown the role of glycine betaine (GB) and ethylene in salt tolerance variation of different wheat cultivars. The salt-tolerant cultivar exhibited GB content, which was found correlative with ethylene ( Khan et al., 2012 ).

The activation and expression of some ethylene-responsive factors, proteins like TaERF1 and TaERF3, which support resistance to multiple stresses, can be induced by the perception of abscisic acid or ethylene ( Rong et al., 2014 ). The study with isolation and molecular characterization of TdERF1, an ERF gene from durum wheat (Triticum turgidum L. subsp. durum) different varieties showed that TdERF1 gene may provide a discriminating marker between tolerant and sensitive wheat varieties ( Makhloufi et al., 2014 ). The severity as well as stress period dictates the level of ethylene evolution and its response levels.

Salt stress declines the metabolic activity of plant cells, which inevitably reflects the inhibition of plant growth ( Çiçek and Çakirlar, 2002 ). Application of ethephon and zeatin reverse the growth-inhibiting effect of salt stress and increase the shoot and root growth of wheat ( Egamberdieva, 2009 ). Gul et al. (2000) stated that the plant growth stimulating compounds such zeatin, and ethephon alleviate the negative effect of salt stress and increase the germination and growth of Ceratoideslanata, Halogetonglomeratus ( Khan et al., 2004 ).

Brassinosteroids (BRs)

The application of brassinosteroids (BRs) exogenously increases plant tolerance against abiotic stress ( Abhinandan et al., 2018 ). Though the effect of BRs on growth and development of wheat has been studied extensively but has not been much studied at the molecular level. Although a detailed study regarding the BR receptor and other signaling components has been performed in the case of Arabidopsis , there are only limited studies of BRI1 orthologs availability in other taxa. Navarro et al. (2015) reported the presence of a single copy of BRI1 ( TaBRI1 ) in each of three wheat genomes on the long arm of chromosome 3 with in silico analysis. It is very difficult to prove directly that BRs can improve abiotic stress tolerance due to lacking in vivo genetic data. But the exogenous application of BRsis significantly able to improve abiotic stress tolerance in wheat crop. The growing of wheat seedlings under 0.4 μM 24-epibrassinolide treatment has shown high levels of cytokinin in roots and shoots as compared to control plants ( Yuldashev et al., 2012 ). The BRs acts as a defense agent under cadmium (Cd), lead (Pb), and salinity stress-induced Triticum aestivum . Wheat plants grown in cadmium and saline conditions normally have decreased photosynthetic activity and growth, but simulated antioxidant enzymatic activity and increased Pro concentration ( Hayat et al., 2014 ). The manipulation with strigolactone, which is engaged in symbiotic relations in the rhizosphere, provides new ways for generating stress tolerant wheat germplasm ( Abhinandan et al., 2018 ). Plants treated with synthetic SL analog GR24 exogenously under drought stress conditions significantly increased the thousand-grain weight as compare to non-treated drought-stressed two winter wheat cultivars ( Sedaghat et al., 2017 ). Future research need to focus the vital role of synthetic and natural hormones for alleviating salinity stress as various hormones hold potential to modulate and regulate vital metabolic processes under stressful environment.

Plant Growth-Promoting Bacteria (PGPB)

Plant growth-promoting bacteria directly or indirectly enhanced the growth of plants ( Ahmad et al., 2013b ). It has been reported by Kotuby-Amazher et al. (2000) that beneficial microorganisms could reduce salt stress by ~50% in wheat. PGPB produce some beneficial compounds like indole acetic acid, siderophore, HCN, etc., solubilize minerals and break down organic matters for easy uptake by plants, fix atmospheric nitrogen, and produce siderophores that enhance the bioavailability of iron, and synthesize phytohormones such as cytokinin's, auxins and gibberellins which have beneficial roles in various stages of plant growth ( Richardson and Simpson, 2011 ). PGPB also decreases or inhibits the detrimental effects of pathogenic organisms by enhancing the host resistance to pathogenic organisms ( Van Loon, 2007 ). Orhan (2016) reported that halotolerant and halophilic bacterial strains significantly increased the root and shoot length, and total fresh weight of wheat under severe salt stress (200 mM NaCl). IAA is declined due to the negative effect of salt stress ( Wang et al., 2001 ), and bacterial strains P. aureantiaca TSAU22, P. extremorientalis TSAU6, and P. extremorientalis TSAU20 produce IAA, which alleviate the reductive effect of salt stress and increase the germination percentage (up to 79%) of wheat ( Egamberdieva, 2009 ).

The cross talks of signaling molecules with other PGRs compounds in wheat crop under salinity are highlighted in Table 2 . In this table different signaling molecules and PGRs are participating in common signaling pathways and regulates the multiple stresses tolerance.

Table 2 . Highlights the crosstalk between plant growth regulators and signaling compounds to ameliorate the salinity stress in wheat crop.

Antioxidant Defense in Response to Salinity-Induced Oxidative Stress

Salinity stress hampers the antioxidant strength via altering antioxidant enzyme activity viz. biosynthesis of ascorbate peroxidase (APX), sodium dismutase (SOD), and glutathione reductase (GR), and non-enzyme antioxidant (ascorbic acid, glycine betaine, and proline). These changes in antioxidants cause the accumulation of harmful ROS, malondialdehyde (MDA), and elevation of lipid peroxidation, ion leakage, membrane stability, and ultimately weakening of antioxidant system ( Sairam et al., 2002 ).

Oxidative stress is caused by production and accumulation of ROS in cells and tissues owing to irregularities in the electron transport chain (ETC) that cause lipid peroxidation, protein oxidation, nucleic acid damage, enzyme inhibition, activation of programmed cell death pathway, and ultimately causing cell death ( Hossain et al., 2021 ). In the biological system, the plants can generally detoxify these reactive products. Under normal growth conditions of the plant, toxic oxygen metabolites are produced in low volume, and there is desired balance between production and ROS quenching; however, this balance may be disturbed by several adverse conditions, including salinity stress. The common ROS are superoxide radicals (O 2 ∙−), hydrogen peroxide (H 2 O 2 ), hydroxyl radicals (∙OH), and singlet oxygen ( 1 O 2 ) ( Navarro-Yepes et al., 2014 ). All ROS are extremely deleterious to plants at higher concentration. To understand salt adaptation strategies of plants, it is an important task of plant biologists to find out suitable mechanisms for developing salt-tolerant wheat that can produce sufficient yield under stress ( Kaur et al., 2017 ). Priming and exogenous use of different eco-friendly compounds had been exploited to tolerate the salt stress-induced oxidative stress in different crops, including wheat ( Kaur et al., 2017 ).

Several antioxidants have been exploited in recent years, which have a beneficial effect against oxidative stress, and to avoid oxidative damage higher plants usually raise the concentration of the endogenous antioxidant system comprising of enzymatic and non-enzymatic components to scavenge ROS ( Sharma et al., 2012 ). In-plant cells, specific ROS producing, and scavenging systems have been established in different organelles viz., mitochondria, chloroplast, and peroxisomes etc. The enzymatic components of the antioxidative defense system (ADS) are comprised of several antioxidant enzymes like superoxide dismutase (SOD), catalase (CAT), peroxidase (POX), guaiacol peroxidase (GPX), ascorbate peroxidase (APX), monodehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR), and glutathione reductase (GR) ( Hossain et al., 2021 ). The non-enzymic components of the ADS include the major cellular redox buffers, ascorbate (AsA) and glutathione (GSH), as well as tocopherol, carotenoids, and phenolic compounds ( Mandhania et al., 2006 ). They interact with numerous cellular components and, in addition to crucial roles in defense and as enzyme cofactors ( Rakhmankulova et al., 2015 ). Ascorbate has remained the most abundant, low molecular weight antioxidant playing a vital role in defense against oxidative stress caused by increased ROS level by scavenging O 2 - and H 2 O 2 ( Karuppanapandian et al., 2011 ). Mandhania et al. (2006) found the NaCl induced enhancement of peroxidase activity in salinized cells of wheat by decomposition of H 2 O 2 generated by antioxidant SOD. Catalase is another enzyme involved in H 2 O 2 detoxification and its conversion into water and oxygen. Similar results were also found by Sairam et al. (2002) , who reported enhancement in CAT activity in both salt-sensitive as well as salt-tolerant wheat cultivars. Mandhania et al. (2006) also reported that stimulation of APX and GR activity under salt stress was much higher in the salt-tolerant cultivar. Kaur et al. (2017) found that exogenous application of phenolic acids (caffeic and sinapic acids) upregulated the stressed shoots of a salt-tolerant wheat cultivar by increasing the activity of CAT and peroxidase. In comparison to stress plants, without the application of phenolic acids, APX activity was upregulated in stressed seedlings, and GB was increased in the stressed roots. Phenolic acids being major non-enzymatic components of the defense system can be used to enhance endogenous levels of these antioxidants in wheat seedlings grown under salt stress conditions. In contrast, wheat crop crucial plant processes are affected by the salinity stress. Therefore, soil and agronomical (drainage system management, leaching of salt, nutrient managements), physiological (osmotic adjustment, seed priming, improve photosynthesis efficiency, and water relation), biochemical (redox, ion, and hormonal homeostasis), and molecular (development of transgenic, genetical engineering, identification of gene) are the crucial step in wheat salinity stress tolerant program ( Figure 3 ).

Figure 3 . Illustrate the integrated approaches (physiological, biochemical and molecular) of salinity stress tolerance in wheat crop.

Conclusions

Among abiotic stresses, salinity stress especially in the arid and semi-arid regions of the world is one of has emerged as one of the most important threats to the sustainability of wheat production. It reduces germination, seedling growth as well as reproductive growth by disrupting numerous vital physiological and metabolic processes which lead to sharp decline in yield and quality depending on frequency and extent of saline environment. Although salinity tolerant plants employ several physiological and biochemical mechanisms to adapt under salinity stress, there is a lack of robust salinity tolerant wheat cultivars globally. Therefore, plant physiologists, breeders, and agronomists need to develop an integrated and sustainable strategy to enhance salt tolerance in wheat. Among these mitigation strategies, soil management practices, crop establishment, as well as the foliar application of antioxidants and growth regulators through maintaining an appropriate water level in the leaves to facilitate adjustment of osmotic and stomatal performance could be explored further to mitigate the adverse effect of salinity on wheat yield and grain quality. However, breeding strategies especially gene pyramiding should be undertaken to develop salt-tolerant varieties by exploring halotolerant gene homologs from wheat germplasm. However, an integrated approach involving soil and agronomic practices (drainage system management, salt leaching, nutrients managements for salt ions replacement), physiological strategies (osmotic adjustment, seed priming, improve photosynthesis efficiency, and water relation), biochemical (redox, ion, and hormonal homeostasis), and molecular tools (development of transgenic, genetic engineering, identification of gene, genes insertion, editing, or slicing) needs to be developed to ameliorate salinity effects and boost cereal production on sustainable basis.

Author Contributions

All authors listed have made a substantial, direct and intellectual contribution to the work, and approved it for publication.

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Keywords: salinity stress, antioxidant defense, wheat, stress tolerance, physiological and biochemical mechanisms

Citation: EL Sabagh A, Islam MS, Skalicky M, Ali Raza M, Singh K, Anwar Hossain M, Hossain A, Mahboob W, Iqbal MA, Ratnasekera D, Singhal RK, Ahmed S, Kumari A, Wasaya A, Sytar O, Brestic M, ÇIG F, Erman M, Habib Ur Rahman M, Ullah N and Arshad A (2021) Salinity Stress in Wheat ( Triticum aestivum L.) in the Changing Climate: Adaptation and Management Strategies. Front. Agron. 3:661932. doi: 10.3389/fagro.2021.661932

Received: 31 January 2021; Accepted: 27 May 2021; Published: 08 July 2021.

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Copyright © 2021 EL Sabagh, Islam, Skalicky, Ali Raza, Singh, Anwar Hossain, Hossain, Mahboob, Iqbal, Ratnasekera, Singhal, Ahmed, Kumari, Wasaya, Sytar, Brestic, ÇIG, Erman, Habib Ur Rahman, Ullah and Arshad. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY) . The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Ayman EL Sabagh, ayman.elsabagh@agr.kfs.edu.eg

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Nazia nahid.

• Department of Bioinformatics and Biotechnology, GC University–Faisalabad, Pakistan

Parwsha Zaib

Tayyaba shaheen *, kanval shaukat.

• Department of Botany, University of Balochistan, Pakistan

Akmaral U. Issayeva

• M. Auezov South Kazakhstan University, Kazakhstan

Mahmood-ur-Rahman Ansari *

*Address all correspondence to: [email protected] and [email protected]

1. Introduction

Wheat ( Triticum aestivum ) is known as one of the most important cereal crops and is extensively grown worldwide [ 1 ]. Wheat contributes to 50% and 30% of the global grain trade and production respectively [ 2 ]. Wheat is also known as a staple food in more than 40 countries of the world. Wheat provides 82% of basic calories and 85% of proteins to the world population [ 3 , 4 ]. Wheat-based food is rich in fiber contents than meat-based food. Dough produced from bread wheat flour has different viscoelastic properties than other cereals. It is considered a higher fiber food. Therefore, its positive effects on controlling cholesterol, glucose, and intestinal functions in the body were observed [ 5 ]. Primarily, wheat is being used to make Chapatti (Bread) but it also contributes to other bakery products. Wheat utility and high nutritional value made it the staple food for more than 1/3rd population of the world. Wheat grain is separated from the chaff and stalks after the harvesting of wheat. Stalks of wheat are further used in animal bedding and construction material. Globally, the need for wheat production is enhancing even in countries having unfavorable climates for its production. Global climate changes are badly affecting the production of wheat and it raised the concern for food security.

It is estimated that annual cereal production should be increased by 1 billion tons to feed the expected population of 9.1 billion by 2050 [ 1 ]. The current scenario demands an increase in crop productivity to meet the increased requirements of food supply [ 6 ]. Wheat is grown in tropical and subtropical regions which experiences a lot of stress. These stresses result in a reduction of yield [ 7 ]. Major environmental stresses include cold, salinity, heat, and drought which are drastically affecting its yield. However, water and heat are considered as the key environmental stresses which caused in reduction of the wheat yield globally [ 8 , 9 ]. So, genetic improvements related to yield and stress tolerance are mandatory to enhance the production of wheat [ 10 , 11 ].

2. Genetically modified wheat plants

Genetically modified wheat plants have been produced by the use of bacteria. Wheat plants were inoculated with the plant-growth-promoting bacteria (PGPB) which resulted in the higher expression of abiotic stress (mainly drought and salinity) tolerant genes [ 12 ]. PGPB inoculated wheat cultivars also showed the higher expression of genes encoding antioxidant-enzymes, such as catalase (CAT), peroxidase , ascorbate peroxidase (APX), and glutathione peroxidase (GPX). So, it was concluded that PGPB used in wheat plants resulted in increased tolerance to abiotic stresses [ 12 ]. Cold shock proteins increase the survival of bacteria in severe environmental conditions. CspA and CspB genes from bacteria were transformed into wheat. Transgenic wheat plants expressing SeCspA and SeCspB were observed to have decreased water loss rate, increased proline and chlorophyll contents under salinity, and less water-stress conditions [ 13 ]. It was further investigated that SeCsp transgenic wheat plants resulted in enhanced weight and yield of grain than the control plants. SeCspA transgenic wheat plants were observed to have an improved water-stress tolerance than the control plants ( Table 1 , [ 13 ]).

Development of transgenic wheat having various traits/phenotypes.

Gluten is a protein comprised of gliadins found in wheat. Gluten is the main cause of coeliac disease in individuals. Bread-making quality of wheat is determined by the gluten proteins. Wheat varieties with less gliadin contents were produced using gene-editing technologies and RNAi (RNA interference). Wheat lines lacking immunogenic gluten were produced. Low immunogenic gluten and more nutritional values were added in one wheat line named E82. A better microbiota profile (protection microorganisms available in the gut) was observed in the NCWS patients using the bread made with E82 [ 28 ]. Plant cuticle has a positive role in the protection of plant against biotic and abiotic stresses. Wheat plants transformed with TaSHN1 resulted in increased water-stress tolerance by reducing the leaf stomatal density and changing the composition of the cuticle [ 29 ].

3. Biotic stress tolerance in wheat

Wheat is considered an excessive contributor toward the human calorie intake [ 30 ]. Pests and pathogens cause yield losses in wheat up to 21.5% of the total losses and could be reached to 28.1% [ 31 ]. Wheat is affected by the fungal disease, powdery mildew caused by Blumeria graminis f. sp. tritici (Bgt). Powdery mildew is a damaging disease that resulted in greater loss of wheat [ 32 ]. Broad-spectrum resistant genes (BSR) are considered to have the most significant role to control powdery mildew. CMPG1-V gene was cloned from the Hynaldia villosa and it was observed that higher expression of CMPG1-V gene resulted in the Broad-spectrum resistance against powdery mildew [ 33 , 34 ]. Barley chi26 gene could also be used to enhance the resistance against powdery mildew and rust through genetic modification [ 35 ]. Some epigenetic regulators were determined to have a role in wheat powdery mildew resistance. TaHDT701 is a histone deacetylase that was found as a negative regulator of wheat defense against powdery mildew. TaHDT701 was observed to be associated with the one repeat protein (TaHOS15) and RPD3 type histone deacetylase TaHDA6. Knockdown of this histone deacetylase complex ( TaHDT701 , TaHDA6 , TaHOS15 ) in wheat resulted in increased powdery mildew tolerance [ 36 ].

Fusarium graminearum is a plant fungal pathogen that causes a devastating disease called Fusarium head blight in wheat. It results in the reduction of wheat production. Genetic techniques were used to increase the FHB (Fusarium head blight) resistance in wheat. Transgenic wheat plants expressing barley class II chitinase gene 2 were observed to have a higher resistance against Fusarium graminearum [ 37 ]. Lr10 and Lr21 were cloned and transformed into wheat. The transgenic plants were reported to be resistant to leaf rust disease. Evolution and diversification of HIPPs (heavy metal-associated isoprenylated plant proteins) genes were studied in Triticeae [ 38 ]. HIPPs genes of Hynaldia villosa were cloned through homology-based cloning. Transgenic wheat having HIPP1-V was developed and the role of HIPP1-V in cadmium stress was characterized. It was observed that higher expression of this gene resulted in increased tolerance to cadmium stress. Therefore, HIPP1-V could be used to increase the tolerance in wheat against cadmium [ 39 ].

4. Abiotic stress tolerance in wheat

Grain number, weight, and size are greatly reduced under the negative effects of environmental stresses. However, the timing, duration, and intensity of stress determine the severity of the negative effects [ 40 , 41 ]. Wheat is a major source of protein and calories for the human diet. High temperature is badly affecting the yield of wheat which is a main concern worldwide. Drought and heat stresses are the two main abiotic stresses which are playing a greater role in the reduction of wheat yield. Reduction in starch contents, photosynthetic activity, grain number, and chlorophyll contents in the endosperm is caused due to rise in temperature. Heat stress results in the accumulation of reactive oxygen species (ROS) which is the main reason for higher oxidative damage to the plant. Heat stress also results in the variation of wheat biochemistry, morphology, and physiology. Tolerance, avoidance, and escape are known as the three major mechanisms that support the plant to grow in a heat-stress environment. Major heat tolerance mechanisms in wheat are known as stay green, heat shock proteins, and antioxidant defense [ 42 ]. Protein synthesis and folding were observed to be interrupted during heat stress. Heat stress also resulted in the production of several stress agents badly affecting transcription, translation, and DNA replication in plants [ 43 ]. Plants speed up the production of heat shock proteins as a defense mechanism [ 44 ]. Higher activity of antioxidants, such as peroxidases, catalase, and superoxide dismutase, was observed under heat stress. Wheat cultivar showing greater tolerance to heat stress was observed to have higher activity of catalase, ascorbate peroxidase, and S-transferase [ 45 ].

Salt stress greatly affects the growth of wheat plants. Salinity stress has a higher impact on the morphology and physiology of wheat plants. Plants having less tolerance to salinity are not suitable for cropping. Potassium transporter ( HKT ) genes have a greater role in achieving salinity tolerance in wheat. Sodium (Na + ) exclusion through HKT genes is a major mechanism in wheat to have a salinity tolerance. OsMYBSs and AtAB14 are the transcription factors having a role in regulating HKT genes, which are considered as the candidate targets for increasing salinity tolerance in wheat [ 46 ]. Wheat transformed with a mutated transcription factor, HaHB4 showed higher water-use efficiency and was more yielding under drought stress [ 26 ]. Transgenic wheat expressing GmDREB1 gene from soybean was also observed to have higher drought tolerance under water-stress conditions [ 47 ]. DREB1A gene from Arabidopsis thaliana was introduced to bread wheat and increased tolerance against water stress in the transgenic wheat was observed. Bread wheat under drought stress was observed to have a higher level of WRKY proteins [ 48 ]. Higher expression of AtHDG11 gene in transgenic wheat resulted in increased water-stress tolerance during drought-stress conditions. Enhanced TaNAC69 expression in root and leaf of wheat during drought stress was observed [ 49 ]. Researchers are working to develop transgenic wheat having various traits/phenotypes by using advanced approaches of biotechnology for the last several decades ( Table 1 ). Numbers of transgenic wheat cultivars are being grown in the fields and several more are under trial.

5. CRISPR/Cas9 system in wheat

Gliadins and glutenins are known as the gluten proteins and ingestion of these proteins from barley, rye, and wheat could cause the disease called coeliac disease in humans. The only remedy is to develop gluten-free food. Transgenic wheat which retains baking quality and is safe for coeliac could not be produced using conventional methods because of the complexity of the wheat genome. Coeliac disease (CD) is activated by the immunogenic isotopes mainly gliadins. Gliadin families were downregulated by the use of RNA interference. CRISPR/Cas9 is a targeted gene manipulation tool considered to have a potential role in genetic modification ( Table 2 , [ 60 , 61 ]). CRISPR/Cas9 system was recently used for gene editing of gliadins. Offsprings with deleted, edited, or silenced gliadins were produced by CRISPR/Cas9. They helped to decrease the exposure of the patient to the CD epitopes [ 62 ]. This technology has been used to develop wheat cultivars having gluten genes with inactivated CD epitopes [ 62 , 63 ].

Genome edited wheat developed by CRISPR/Cas9 system.

CRISPR/Cas9 system and TALENS (transcription activator-like effector nuclease) were used in the bread wheat to generate the mutations in three homoeoalleles that encode MLO locus proteins against mildew. Mutations in all three TaMLO were generated by using TALENS which resulted in resistance against powdery mildew. The MLO homoeoalleles ( TaMLOA1 , TaMLOB1, and TaMLOD1 ) of bread wheat contributed to the mildew infection. Mutation of MLO alleles resulted in powdery mildew tolerance in wheat [ 50 ]. Genome editing was reported in which pds (phytoene desaturase) and inox (inositol oxygenase) genes in the cell suspension-culture of wheat were targeted. It was demonstrated that the genome-editing technique could also be applied in the cell suspension of wheat [ 64 ]. Very recently, various research groups are involved to develop transgenic wheat by using genome-editing technology. Some of the experiments are listed in Table 2 .

6. Wheat computational analysis

A comprehensive resource for wheat reference genome was developed by International Wheat Genome Sequencing Consortium. The URGI portal ( https://wheat-urgi.versailles.inra.fr/ ) was developed for the breeders and researchers to access the genome sequence data of bread-wheat. InterMine tools, genome browser, and BLAST were established for the exploration of genome sequences together with the additional linked datasets, including gene expression, physical maps, and sequence variation. Portal provided the higher browser and search features that facilitated the use of the latest genomic resources required for the upgradation of wheat [ 65 ].

DNA binding with one finger (Dof) transcription factors is known to have an important role in abiotic stress tolerance as well as the growth of plants. Ninety-six TaDof members of the gene family have been studied using computational approaches. By qPCR analysis, it was revealed that TaDof genes were upregulated under heavy metal and heat stress in wheat. Consequently, it could be concluded that detection of amino acid sites, genome-wide analysis, and identification of the Dof transcription factor family could provide us the new insight into the function, structure, and evolution of the Dof gene family [ 66 ].

Acknowledgments

This work was supported by funds from the Higher Education Commission of Pakistan.

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Measuring the Effects of Climate Change on Wheat Production: Evidence from Northern China

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The data will be available on request.

The current study examines the long-run effects of climatic factors on wheat production in China’s top three wheat-producing provinces (Hebei, Henan, and Shandong). The data set consists of observations from 1992 to 2020 on which several techniques, namely, fully modified OLS (FMOLS), dynamic OLS (DOLS), and canonical co-integrating regression (CCR) estimators, and Granger causality, are applied. The results reveal that climatic factors, such as temperature and rainfall, negatively influenced wheat production in Henan Province. This means that Henan Province is more vulnerable to climate change. In contrast, it is observed that climatic conditions (via temperature and rainfall) positively contributed to wheat production in Hebei Province. Moreover, temperature negatively influenced wheat production in Shandong Province, while rainfall contributed positively to wheat production. Further, the results of Granger causality reveal that climatic factors and other determinants significantly influenced wheat production in the selected provinces.

1. Introduction

China cultivates only eight percent of the world’s arable land to feed eighteen percent of the global population. It is expected that China’s population will peak around 2030 [ 1 ]; hence, the food security problem in China has always been a concern. In the “Outline of the 14th Five-Year Plan for National Economic and Social Development of the People’s Republic of China and the Long-term Goals in 2035,” the Chinese government, for the first time, incorporated the food security strategy into the planning system and set the goal of ensuring that grain output will remain stable at over 650 million tons over the 14th Five-Year Plan period. Climate has a strong influence on food production. Climate change and more frequent bad weather events around the world exacerbate the insecurity of China’s grain production [ 2 , 3 ]. As a result, understanding the impact of climate change on China’s grain crop productivity and devising countermeasures to implement China’s food security strategy are critical.

The impact of climate change on grain crop production has both advantages and disadvantages. Nevertheless, the disadvantages outweigh the advantages overall, and different climate variables have different impacts on different crops and regions [ 4 , 5 , 6 ]. In recent years, the increased heat caused by climate change has been conducive to expanding the grain sown area and producing more grain [ 7 ]. Increasing rainfall and CO 2 concentrations are beneficial for crop production to some extent, but high temperatures may negate this effect in some areas [ 8 , 9 ]. Similarly, climate change had a negative impact on grain production by expanding pest and disease occurrence areas, shortening crop growth cycles, and increasing the frequency of extreme weather events [ 10 , 11 ].

The global climatic variations are a sensitive topic being discussed in China. According to the National Meteorological Administration, China’s temperature has increased by 0.3 °C every 10 years (higher than the global average during the same period), and its annual precipitation has increased by 5.1 mm every 10 years between 1961 and 2020 [ 12 ]. Climate change is causing a “double increase in water and heat.” By evaluating the expected impact of global warming on the yields of China’s main crops (wheat, rice, and corn), it was discovered that the crop yield effect emanating from climate change is primarily due to an increase in air temperature [ 13 ]. Grain production has been impacted by significant deviations in China’s agricultural climate resources. The regional space of grain production is also changing, with the emphasis shifting to the main production areas in the north [ 14 ]. Researchers incorporate technological progress factors into the research system of food production under climate change [ 15 , 16 , 17 , 18 ]. Food security is a technical issue in terms of production mode, and the level of technology determines the ability to ensure food security. As a result, technological advancement can be used as an effective tool for grain production to cope with climate change [ 19 , 20 ].

Many studies have found that technological progress significantly impacts grain production, which is primarily reflected in the two factors listed below. First, technological advancement has improved the crops’ ability to withstand disasters. The advancement of bio-pesticides due to technological advancement has increased the agricultural departments’ ability to prevent and control major agricultural pests and diseases while causing less environmental impact [ 21 , 22 ]. Simultaneously, the monitoring technology system of major sudden agricultural meteorological disasters constructed by the agricultural sector is also conducive to the agricultural sector’s better response to extreme weather events [ 23 ]. Second, technological advancement is a driving force in changing the mode of production. Modern agricultural mechanization can promote rapid agricultural production growth while producing good environmental results [ 24 , 25 ]. Fertilizer use can improve crop yield, but excessive use reduces crop yield [ 26 ]. Improved seed varieties, fertilizers, pesticides, technical equipment, and infrastructure are used as proxies for technological progress in agricultural production [ 18 , 27 , 28 , 29 ]. Hence, this study also considers fertilizer use a proxy for technological advancement, as it is a crucial factor in crop production.

Wheat is China’s second most important food crop, after rice, and its planting area accounts for 22~30% of the total cultivated land [ 30 ]. Winter wheat is the predominant crop in China, accounting for more than 90 percent of the total output [ 31 ]. The regions of China that produce winter wheat can be divided into Southern and Northern cultivation areas. The northern winter wheat producing region is the most concentrated wheat growing and consuming region in China, and its sown area and wheat output account for around two-thirds of the country. In recent years, the top three provinces in northern China for winter wheat production were Henan, Shandong, and Hebei. Henan Province has an alternating temperate monsoon and subtropical climate, whereas Shandong and Hebei Provinces have a temperate monsoon climate. Figure 1 and Figure 2 show their geographical location, wheat yield, temperature, and rainfall.

The distribution of wheat production (10,000 tons) in Hebei, Henan, and Shandong Provinces.

The distribution of temperature (°C) and rainfall (mm) in Hebei, Henan, and Shandong Provinces.

Previous studies in various parts of the world have extensively documented the impact of changing climate on wheat crop yield. Most existing research on China discussed the relationship between the two at the national and regional levels [ 31 , 32 , 33 ] or only focused on a specific province, such as Henan Province, which has the highest wheat yield [ 30 , 34 ]. However, climate change causes food production variability in regions with varying climate resources. The current paper assesses the long-term effects of changing climate on wheat production in the top three provinces in northern China to further analyze the heterogeneous influence of changing climate on wheat production, propose targeted measures to deal with climate change for the main grain-producing areas in China, and contribute to China’s food security strategy. Figure 3 shows the dynamic nexus between climatic factors, other determinants, and wheat production.

The study’s conceptual framework.

2. Literature Review

Wheat may be one of the crops most susceptible to the effects of climate change, but its substantial impact on crop production is profound. Numerous research works have investigated the impacts of climate change on wheat development and harvest in major wheat-producing regions in Asia, Europe, and northern Africa. However, it is important to note that varied temperature conditions and precipitation patterns affect wheat growth and yield differently in different regions.

Several researchers, for example, Zhai et al. [ 18 ], Abbas [ 27 ], Gul et al. [ 28 ], Ali et al. [ 35 ], and Warsame et al. [ 36 ], have explored the short-term and long-term climate change effects on food crop production by applying the autoregressive distributed lag (ARDL) methodology and reported mix outcomes related to climate variables. While, a study by You et al. [ 37 ] revealed that climate warming lowered wheat yield growth, a 1 °C rise in wheat growing temperature reduced wheat production by 3–10% in China. However, the findings of Zhai et al. [ 18 ] from 1970 to 2014 in China evaluated that temperature did not significantly influence the amount of wheat produced per unit of land in the short run and long run, while farm mechanization and fertilizer usage increased wheat output in the long run.

More recently, the research by Gul et al. [ 5 ] from 1985 to 2016 in Pakistan established the long-term link between climate variables and main food crop production. The findings showed that temperature negatively affects key food crop production, while rainfall improves food production. Similarly, the study of Chandio et al. [ 38 ] from 1977 to 2014 in Pakistan revealed that climate change and CO 2 have a detrimental short- and long-term influence on grain productivity, reducing cereal production and causing food security issues in the country.

Another similar study by Warsame et al. [ 39 ] for the period of 1980–2017 in Somalia examined the effects of climate change along with political instability on the productivity of sorghum by using various estimation techniques (i.e., FMOLS, DOLS, and CCR). The findings revealed that political instability and temperature significantly declined the productivity of sorghum, while rainfall and cultivated area enhanced the production in the long term. The long-term findings are also verified by the CCR approach. In the case of India, Bhardwaj et al. [ 40 ] reported that climate variables negatively contributed to wheat and paddy production; moreover, excessive rainfall had a detrimental influence on wheat and rice yields.

In the case of Ghana, Ntiamoah et al. [ 41 ] used a novel dynamic simulated autoregressive distributed lag (ARDL) model to examine the impact of CO 2 emissions, rainfall, credit supply, and fertilizer on the productivity of maize and soybean, covering the period from 1990 to 2020. The findings revealed that CO 2 emissions, as well as rainfall, have a significant and positive impact on crop production, while the supply of credit and fertilizer negatively influenced maize production. In the context of Asia, Ozdemir [ 42 ] studied the effects of climate change on agricultural output by using various estimation techniques (i.e., PMG and CCEMG). The outcomes showed that temperature and CO 2 affected agricultural output negatively and significantly in the long term, while precipitation improved productivity. In addition, other factors, such as power consumption for agricultural machinery and fertilizer, significantly enhanced agricultural output in the same period.

According to research by Akhtar and Masud [ 4 ] on the influence of climatic factors on rice and cereal production from the period 1985–2016, it was found that temperature and energy usage severely influence rice and vegetable output, although their effect on cereal productivity is minor. However, CO 2 emissions negatively influenced coffee production, and the temperature, energy use, and fossil fuel usage induced climate change, which had a negative impact on Malaysian agriculture. The empirical study of Kumar et al. [ 43 ] in selected lower-middle-income nations from 1971 to 2016 assessed the climate change–cereal crops production association. The authors’ findings revealed that rising temperatures diminish crop productivity. Rainfall and CO 2 emissions boosted crop yields, and a bidirectional causation between grain output, temperature, and CO 2 emissions was discovered. Rainfall and temperature affect grain production uni-directionally and might threaten the food security of the rural populations.

In particular, a study in China by Pickson et al. [ 44 ] from 1998 to 2017 examined the effects of climate change on rice cultivation. The findings showed that the climate variable, such as the temperature, adversely influences rice cultivation, while average rainfall influences the rice output but is insignificant. The farmed area positively affected short-term crop output. At the same time, fertilizer use had little effect and bidirectional causation between rice production and the cultivated area. Similarly, the investigation of Pickson et al. [ 6 ] in China over the period 1990Q1–2013Q4 found that the average temperature and its variability associated with cereal production were negative but significant in the long run. Additionally, rainfall variability and cereal production linkage showed no significant effect in the long run, but two variables (CO 2 and temperature variability) had a negatively significant association in the short run.

Likewise, Pickson et al. [ 45 ] investigated the impact of global warming on the main food crops (i.e., rice and maize) production in the case of China over the periods 1978Q1–2015Q4. The outcomes revealed a significantly positive trend in average temperature and seasonal temperature increases during the spring, summer, and fall with the insignificant change in the monthly, seasonal, and annual precipitation. The impact of temperature decreases maize and rice production at higher quantiles.

Due to the diverse time scales, geographic locations, and techniques, the following research work has not yet formed consistent findings on climate change’s influence on wheat growth and yield. These research works failed to combine the climatic conditions and agricultural progress elements into crop yield–climate functions to investigate their influence, and the long-run impacts on wheat must be studied. In this work, we employed the FMOLS method to assess the long-run climate variations’ influence on wheat yield in the northern region of China. The findings of the FMOLS approach are verified by the DOLS and CCR estimators.

3. Materials and Methods

The present study intends to investigate the long-run impact of temperature, rainfall, fertilizer usage, power usage, farming area, and labor on wheat production in the context of top 3 wheat-producing provinces of northern China. Wheat production is used as the dependent variable, and it is measured in 10,000 tons, while climatic factors, namely, temperature measured in degrees Celsius, rainfall measured in millimeters, fertilizer usage measured in 10,000 tons, power consumption measured in 1000 kWh, the cultivated area measured in 1000 hectares, and labor measured in 10,000 people, are used as the independent variables. The data were extracted from the China Rural Statistical Yearbook ( https://data.cnki.net/Yearbook/Navi?type=type&code=A# (accessed on 1 June 2022)) and the National Weather Science Data Center ( http://data.cma.cn/ (accessed on 1 June 2022)).

3.2. Econometric Modeling

This study examines the long-run impact and the causal relationship between temperature, rainfall, fertilizer usage, power consumption, cultivated area, labor, and wheat production in the selected provinces of China. Several investigation tests were carried out to achieve the research objective, including the co-integration test, FMOLS, DOLS, and CCR estimators, and the Granger causality test. The basic model is constructed as shown below:

The logarithmic arrangement of Equation (1) can be developed as follows:

where WP indicates wheat production, TEMP denotes average annual temperature, RF represents average annual rainfall, FER indicates fertilizer usage, PC shows the power consumption, WA stands for wheat cultivated area, LF indicates rural labor force.

3.3. FMOLS Long-Run Estimator

This paper uses the fully modified OLS (FMOLS) proposed by Phillips and Hansen [ 46 ] to estimate the co-integration coefficient. Based on the OLS, this method uses the semi-parametric two-stage estimation method to correct the equalization error and the explained variable, which can effectively eliminate the endogeneity caused by the co-integration relationship and the sequence correlation of error terms, thus obtaining the consistent estimator of co-integration parameter estimator and the asymptotic normal distribution of FMOLS estimator. Suppose the model is

Let μ t ′ = μ 1 t ′ + μ 2 t ′ . First, perform OLS estimation on Equation (3) to obtain the θ ^ and μ t ^ of OLS estimators. Second, estimate the long-term variance of μ t . Let Ω and ∆ represent long-term variance and one-sided long-term variance, respectively, and the estimates are shown in Formulae (5) and (6).

By adjusting the endogeneity, we can obtain Equation (7).

By adjusting the sequence correlation, we can obtain Equation (8).

The final FMOLS estimator is obtained as shown in Equation (9).

Furthermore, we use the dynamic OLS (DOLS) proposed by Stock and Watson [ 47 ] and the canonical co-integrating regressions (CCR) proposed by Park [ 48 ] to verify the robustness of FMOLS estimation results. The DOLS estimation model contains the lag term of explanatory variables, and the standard deviation of its estimator has a normal asymptotic distribution, which is also better than the OLS estimation [ 40 ]. The idea of the CCR model is the same as the FMOLS model, but the difference is that it transforms the data stationarity to obtain the least-square estimation and then eliminates the dependency between the co-integration equation and the random correction equation of the explanatory variables.

4. Results and Discussion

We use the FMOLS, DOLS, and CCR estimators to examine the long-term influence of temperature, rainfall, fertilizer use, power consumption, wheat farming area, and labor on wheat production in the selected three provinces of China. Table 1 reports the statistical summary of the dependent and independent variables for the Hebei, Henan, and Shandong Provinces. The J-B test confirms that all the studied variables are normally distributed. Figure 4 shows the trend of wheat production and climatic factors in the selected provinces of China.

Trend of wheat production, temperature, and rainfall in Hebei, Henan, and Shandong Provinces of China.

Statistical summary for Hebei, Henan, and Shandong Provinces.

Note: LWP, LTEMP, LRF, LFER, LPC, LWA, LLF signify the natural log of wheat production, average annual temperature, average annual rainfall, fertilizer usage, power consumption, wheat cultivated area, and rural labor force, while J-B denotes the Jarque–Bera test.

The outcomes of the correlation matrix for Hebei, Henan, and Shandong Provinces are presented in Table 2 . The findings for Hebei Province reveal that temperature, rainfall, fertilizer usage, power consumption, and labor are significantly and positively associated with wheat production, while the cultivated area is negatively associated. Further, the findings for Henan Province show that all the studied variables are significantly linked with wheat production, except rainfall. In addition, the outcomes for Shandong Province indicate that temperature, cultivated area, and labor are significant and interrelated with wheat production, whereas fertilizer is negatively associated.

Results of the correlation matrix for Hebei, Henan, and Shandong Provinces.

Note: *** p value < 0.01, ** p value < 0.05, and * p value < 0.1.

We employ the Johansen and Juselius co-integration procedure to explore the long-term association between the explained variables, such as wheat production and its explanatory variables. We test the research hypothesis, as the null hypothesis states that the explained variables, wheat production and its explanatory variables, are not co-integrated in the long term. In contrast, the alternative hypothesis mentions that the considered variables are co-integrated in the long term. To reach a decision about the hypothesis, we use the Trace t-statistic test, and the findings for Hebei, Henan, and Shandong Provinces are reported in Table 3 . The findings reveal that wheat production, temperature, rainfall, fertilizer usage, power consumption, cultivated area, and labor force are co-integrated in the long term in China’s selected wheat-producing provinces.

Co-integration outcomes for Hebei, Henan, and Shandong Provinces.

Note: TS indicates the trace statistic, * signifies rejection of the hypothesis at the 0.05 level.

Table 4 reports the estimated results of long-term effect of climate variables and other control variables on wheat yield in Hebei, Henan, and Shandong Provinces, respectively.

Results of FMOLS estimator for top three provinces in northern China.

In the case of Hebei Province, the climate variables (i.e., temperature and rainfall) have a positive, significant impact on wheat production. This means the climate conditions are more favorable for wheat cultivation in Hebei Province. Specific to the North China Plain, where this study area is located, some research evidence shows that in the north of this plain, the impact of rainfall on wheat production is positive, while in the south of this plain, the impact of rainfall turns negative [ 49 ]. Similarly, for temperature, the increase in temperature increases the winter wheat yield in the northern part of the North China Plain but decreases the wheat yield produced in winter in the south of the North China Plain [ 50 ]. The top three wheat-producing provinces are selected for this investigation. Hebei, Shandong, and Henan Provinces are distributed in the North China Plain. The three provinces’ yearly mean temperature and yearly mean precipitation are ranked from low to high in Hebei, Shandong, and Henan (see Figure 2 ). The temperature and rainfall in Hebei Province are low, and the impacts of temperature and precipitation on wheat yield are positive.

Further results reveal that fertilizer use, cultivated area, and labor force also have a positive, significant influence on wheat production. The long-run coefficients of fertilizer use, cultivated area, and labor force indicate that a 1% increase in fertilizer treatment use, cultivated area, and labor force wheat production improved by 0.17%, 0.58%, and 1.36%, respectively.

In the case of Henan Province, the climatic factors (i.e., temperature and rainfall) and wheat production relationship was significant and negative. This means that climatic factors severely impact wheat production in Henan Province. The long-run coefficient of both climate variables, temperature and rainfall, indicates that with a 1% increase in both climate variables (i.e., temperature and rainfall), wheat production decreases by 0.51%, and 0.05%. Geng et al. [ 51 ] reported that high temperatures will be detrimental to wheat production by shortening the growth cycle of the wheat crop. Further, Song et al. [ 33 ] stated that excessive rainfall causes excessive water accumulation, which will aggravate the wet damage of wheat and negatively affect wheat production.

Moreover, the results show that fertilizer usage also significantly negatively impacts wheat production. The long-term coefficient of fertilizer usage reveals that if a farmer overuses the fertilizer by 1%, wheat production declines by 0.61%. Fertilization can not only supplement the nutrients needed by wheat but also improve the utilization rate of water, thus increasing the yield of wheat [ 52 , 53 ]. However, unreasonable and excessive use of chemical fertilizers will cause soil degradation and adversely affect wheat yield. This shows that the rational use of chemical fertilizers is very important for wheat production, and Henan Province should pay more attention to improving chemical fertilizer use efficiency.

In contrast, these variables (power usage, wheat farming area, and labor force) and the wheat production relationship were significant and positive. The long-run coefficient of power usage, wheat farming area, and labor force reveals that a 1% increase in power usage, wheat farming area, and labor force increases wheat production by 0.48%, 2.98%, and 0.21%, respectively.

In the case of Shandong Province, the climate variables, temperature, and wheat production displayed a diverse relationship. At the same time, rainfall had a significant and positive influence, suggesting that with a 1% increase in temperature and rainfall, wheat production decreased by 0.07% and improved by 0.08%. The heterogeneous effect of the climate variables on regional wheat yield is verified by some existing studies. For example, the evidence from Mexico and China verified that the sensitivity of wheat yield to climate variables is uneven in space [ 54 , 55 ]. Tao et al. [ 56 ] studied climate change’s influence on wheat productivity and found the prospective consequences of climate change on winter wheat output in northern China under 10 climatic scenarios and concluded that environmental variability might enhance wheat yield by 37.7% (18.6%), 67.8% (23.1%), and 87.2% (34.4%), with (without) CO 2 fertilization effects in the 2020s, 2050s, and 2080s, respectively, in the future. The temperature and rainfall in Shandong Province are in the middle of the three provinces, and the impact of temperature on wheat yield is negative, but the impact of rainfall is positive. In Henan Province, it is observed that the temperature is higher, and the rainfall is higher; the influence of temperature and rainfall on wheat is negative. Moreover, the results show that these variables (fertilizer use, cultivated area, and labor force) and wheat production association was significant and positive, suggesting that a 1% increase in fertilizer usage, cultivated area, and labor force enhanced wheat production by 0.29%, 1.16%, and 0.23%, respectively.

This study applied the DOLS and CCR long-run estimators as a robust check approach for the FMOLS findings. Table 5 shows that climate variables positively affect wheat production in the context of Hebei Province. The estimated coefficients of DOLS and CCR are consistent with the findings of the FMOLS model. Likewise, in Henan Province’s case, climatic factors negatively influence wheat production. These outcomes are also consistent with the outcomes of the FMOLS model. In addition, climatic factors, such as temperature, only have a negative impact on wheat production. Meanwhile, rainfall has a significant and positive linkage with wheat production. Hence, the results of both techniques, such as DOLS and CCR, are similar to the results of the FMOLS method.

Robustness check.

Although the long-run impact of the variables concerned was explored through the FMOLS, DOLS, and CCR estimators, the causal connection between the underlying variables is still in question. Therefore, we further apply the Granger causality method. The findings for Hebei, Henan, and Shandong Provinces are presented in Table 6 . A bidirectional causality between precipitation and fertilizer usage with wheat production in the context of Hebei Province can be observed. This means that rainfall and fertilizer usage significantly contributed to Hebei Province’s wheat production.

Granger causality test outcomes for Hebei, Henan, and Shandong Provinces.

Note: ⇏   indicates “does not cause Granger”, *** p value < 0.01, ** p value < 0.05, and * p value < 0.1.

Further, the results only discover a unidirectional causality association between wheat production and temperature. In the context of Henan Province, it is revealed that a unidirectional causality association runs from precipitation and fertilizer usage to wheat production. In contrast, a bidirectional causality exists between power consumption and wheat production. This depicts that climate change factors, such as rainfall, and other inputs also positively influence wheat production. In addition, a bidirectional causality is established between the farming area and wheat production, while a unidirectional causality is detected from precipitation and labor to wheat production. These results imply that the cultivated area, rainfall, and labor significantly improve wheat production in the context of Shandong Province.

5. Conclusions

The current study assesses the climate variables’ long-run impact on wheat production in China’s top three wheat-producing provinces. The other important factors considered in this paper include fertilizer usage, cultivated area, power consumption, and labor. The data set consists of observations from 1992 to 2020 on which several time-series techniques, namely, the DOLS, FMOLS, CCR, and Granger causality, were applied. Based on the estimations, the findings revealed that wheat production is negatively affected by climate change in Henan Province. In contrast, climate change is more favorable for wheat production in Hebei Province.

On the other hand, temperature negatively influenced wheat production but was not significant, while rainfall significantly contributed positively to wheat production in Shandong Province. Further findings showed that fertilizer usage, cultivated area, and labor positively and significantly improved wheat production in Hebei and Shandong Provinces. In contrast, power usage, wheat farming area, and labor force significantly and positively enhanced wheat production in Henan Province. In addition, the findings of the Granger causality test reported a bidirectional causality between rainfall and fertilizer use with wheat production in Hebei Province, while a unidirectional causality connection was revealed between wheat production and temperature. In the context of Henan Province, it was discovered that a unidirectional causality link was observed from rainfall and fertilizer use to wheat production. In contrast, a bidirectional causality existed between power consumption and wheat production. Moreover, a bidirectional causality was established between the cultivated area and wheat production, while a unidirectional causality was detected from the rainfall and labor to wheat production in Shandong Province.

Based on the estimated outcomes, the current paper offers several policy implications:

With both advantages and disadvantages, China’s wheat production is affected by global warming. To mitigate the effects of a changing climate on China’s wheat yield, it is vital to increase the adaptability of wheat production. First, modify wheat’s sowing date and area in a reasonable manner. Adjust the sowing date of crops, rationally plan the planting areas, fully utilize the additional heat resources brought about by climate change, decrease the impact of meteorological disasters, and increase the stability of wheat production based on the climatic conditions of various regions.

Second, agricultural technology advancement will continue to be important in ensuring wheat yield stability. On the one hand, the Chinese government must prioritize research and develop seed resources resistant to extreme weather conditions. It is crucial to develop and store wheat germplasm resources that can respond to adverse weather conditions, given the prevalence of extreme weather events (high-temperature resistance, waterlogging resistance, low-temperature resistance, etc.). On the other hand, it is essential to continue using advanced agricultural technologies to produce wheat. For instance, more fertilizer use techniques should be implemented to increase the input effectiveness of chemical fertilizers and ensure the sustainability of agricultural production.

Furthermore, there are regional differences in wheat planting varieties and methods in China, making it difficult to continuously improve wheat production levels by relying solely on a single technology. As a result, it is necessary to promote improved varieties in conjunction with good methods, agricultural machinery, and agronomy, as well as to further tap the potential of science and technology to increase production.

Funding Statement

This research was funded by the National Social Science Fund of China (Grant number: 19CSH029).

Author Contributions

Conceptualization, A.A.C. and H.Z.; methodology, A.A.C.; software, A.A.C. and Y.T.; validation, G.R.S.; formal analysis, A.A.C. and Y.T.; investigation, A.A.C. and Y.T.; resources, H.Z.; data curation, Y.T.; writing—original draft preparation, A.A.C. and Y.T.; writing—review and editing, M.A.T. and G.R.S.; visualization, H.Z.; supervision, A.A.C.; project administration, H.Z.; funding acquisition, H.Z. All authors have read and agreed to the published version of the manuscript.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Data availability statement, conflicts of interest.

The authors declare no conflict of interest.

Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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Wheat improvement in India: present status, emerging challenges and future prospects

• Original Paper
• Published: 04 April 2007
• Volume 157 , pages 431–446, ( 2007 )

Cite this article

• A. K. Joshi 1 ,
• B. Mishra 2 ,
• R. Chatrath 2 ,
• G. Ortiz Ferrara 3 &
• Ravi P. Singh 4  

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India is the second largest producer of wheat in the world, with production hovering around 68–75 million tons for past few years. The latest estimated demand for wheat production for the year 2020 is approximately 87.5 million tons, or about 13 million tons more than the record production of 75 million tons harvested in crop season 1999–2000. Since 2000, India has struggled to match that record production figure and thus faces a critical challenge in maintaining food security in the face of its growing population. The current major challenges facing future wheat production in India are increasing heat stress; dwindling water supplies for irrigation; a growing threat of new virulence of diseases such as wheat rusts (yellow, brown, and black) and leaf blight; continuous adoption of rice-wheat systems on around 11 million hectares; changes in urbanization patterns, and demand for better quality wheat. In addition, the threat posed by the new stem rust race Ug99 can not be underestimated. The wide gap (around 2.5 t/ha) between the potential and harvested yield in the eastern Gangetic Plains also cries out for solutions. Addressing issues related to different stresses will require harnessing genes discovered in landraces and wild relatives following conventional as well as non-conventional approaches. For effective technology delivery in areas that suffer from poor linkages with farmers, participatory research needs to be strengthened. The future germplasm requirements from a dependable collaborator such as CIMMYT are largely being dictated by the above factors.

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Wheat Improvement

Global Crop Improvement Networks to Bridge Technology Gaps

Abbreviations.

Eastern Gangetic Plains

Eastern Gangetic Plains Yield Trial

Eastern Gangetic Plains Screening Nursery

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Department of Genetics and Plant Breeding, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi, 221005, India

A. K. Joshi

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Joshi, A.K., Mishra, B., Chatrath, R. et al. Wheat improvement in India: present status, emerging challenges and future prospects. Euphytica 157 , 431–446 (2007). https://doi.org/10.1007/s10681-007-9385-7

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Received : 12 September 2006

Accepted : 20 February 2007

Published : 04 April 2007

Issue Date : October 2007

DOI : https://doi.org/10.1007/s10681-007-9385-7

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