Skip to main content
SpringerLink
Log in

Elucidating the genetic architecture controlling antioxidant status and ionic balance in barley under salt stress

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Key Message

Association genetic analysis empowered us to identify candidate genes underlying natural variation of morpho-physiological, antioxidants, and grain yield-related traits in barley. Novel intriguing genomic regions were identified and dissected.

Abstract

Salinity stress is one of the abiotic stresses that influence the morpho-physiological, antioxidants, and yield-related traits in crop plants. The plants of a core set of 138 diverse barley accessions were analyzed after exposure to salt stress under field conditions during the reproductive phase. A genome-wide association scan (GWAS) was then conducted using 19,276 single nucleotide polymorphisms (SNPs) to uncover the genetic basis of morpho-physiological and grain-related traits. A wide range of responses to salt stress by the accessions was explored in the current study. GWAS detected 263 significantly associated SNPs with the antioxidants, K+/Na+ content ratio, and agronomic traits. Five genomic regions harbored interesting putative candidate genes within LD ± 1.2 Mbp. Choromosome 2H harbored many candidate genes associated with the antioxidants ascorbic acid (AsA) and glutathione (GSH), such as superoxide dismutase (SOD), ascorbate peroxidase (APX), and glutathione reductase (GR), under salt stress. Markedly, an A:C SNP at 153,773,211 bp on chromosome 7H is located inside the gene HORVU.MOREX.r3.7HG0676830 (153,772,300–153,774,057 bp) that was annotated as l-gulonolactone oxidase, regulating the natural variation of SOD_S and APX_S. The allelic variation at this SNP reveals a negative selection of accessions carrying the C allele, predominantly found in six-rowed spring landraces originating from Far-, Near-East, and central Asia carrying photoperiod sensitive alleles having lower activity of enzymatic antioxidants. The SNP-trait associations detected in the current study constitute a benchmark for developing molecular selection tools for antioxidant compound selection in barley.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

Enquiries about data availability should be directed to the authors.

References

  • Aebi H (1984) Catalase in vitro. Method Enzymol 105:121–126

    Article  CAS  Google Scholar 

  • Ahanger MA, Mir RA, Alyemeni MN, Ahmad P (2020) Combined effects of brassinosteroid and kinetin mitigates salinity stress in tomato through the modulation of antioxidant and osmolyte metabolism. Plant Physiol Biochem 147:31–42

    Article  CAS  PubMed  Google Scholar 

  • Ahmad P, Sarwat M, Sharma S (2008) Reactive oxygen species, antioxidants and signaling in plants. J Plant Biol 51:167–173

    Article  CAS  Google Scholar 

  • Akladious SA, Hanafy RS (2018) Alleviation of oxidative effects of salt stress in white lupine (Lupinus termis L.) plants by foliar treatment with l-arginine. J Anim Plant Sci 28:165–176

    CAS  Google Scholar 

  • Allaire J (2012) RStudio: integrated development environment for R. Boston, MA. 770(394):165–171

  • Alqudah AM, Samarah NH, Mullen RE (2011) Drought stress effect on crop pollination, seed set, yield and quality, pp 193–213

  • Alqudah AM, Sallam A, Stephen Baenziger P, Borner A (2020) GWAS: fast-forwarding gene identification and characterization in temperate cereals: lessons from barley—a review. J Adv Res 22:119–135

    Article  PubMed  Google Scholar 

  • Angessa TT, Zhang XQ, Zhou G, Broughton S, Zhang W, Li C (2017) Early growth stages salinity stress tolerance in CM72 x Gairdner doubled haploid barley population. PLoS One 12:e0179715

    Article  PubMed  PubMed Central  Google Scholar 

  • Ashraf M (2009) Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnol Adv 27:84–93

    Article  CAS  PubMed  Google Scholar 

  • Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48

  • Blaha G, Stelzl U, Spahn CM, Agrawal RK, Frank J, Nierhaus KH (2000) Preparation of functional ribosomal complexes and effect of buffer conditions on tRNA positions observed by cryoelectron microscopy. Methods Enzymol 317:292–309

    Article  CAS  PubMed  Google Scholar 

  • Carlberg I, Mannervik B (1985) Glutathione reductase. In: Glutamate, glutamine, glutathione, and related compounds. Academic Press, London, pp 484–490

  • Chen Z, Zhou M, Newman IA, Mendham NJ, Zhang G, Shabala S (2007) Potassium and sodium relations in salinised barley tissues as a basis of differential salt tolerance. Funct Plant Biol 34:150–162

    Article  CAS  PubMed  Google Scholar 

  • Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19:371–379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Kok L, Maas F, Godeke J, Haaksma A, Kuiper P (1986) Glutathione, a tripeptide which may function as a temporary storage compound of excessive reduced sulphur in H2S fumigated spinach plants. In: Fundamental, ecological and agricultural aspects of nitrogen metabolism in higher plants. Springer, Berlin, pp 203–206

  • De Storme N, Geelen D (2014) The impact of environmental stress on male reproductive development in plants: biological processes and molecular mechanisms. Plant Cell Environ 37:1–18

    Article  PubMed  Google Scholar 

  • Dhindsa RS, Matowe W (1981) Drought tolerance in two mosses: correlated with enzymatic defence against lipid peroxidation. J Exp Bot 32:79–91

    Article  CAS  Google Scholar 

  • Fernandez GC (1992) Effective selection criteria for assessing plant stress tolerance. In: Proceeding of the international symposium on adaptation of vegetables and other food crops in temperature and water stress, Aug 13–16, Shanhua, Taiwan, 1992, pp 257–270

  • Flowers TJ, Gaur PM, Gowda CL, Krishnamurthy L, Samineni S, Siddique KH, Turner NC, Vadez V, Varshney RK, Colmer TD (2010) Salt sensitivity in chickpea. Plant Cell Environ 33:490–509

    Article  CAS  PubMed  Google Scholar 

  • Fu Y, Cheng M, Li M, Guo X, Wu Y, Wang J (2020) Identification and characterization of PLATZ transcription factors in wheat. Int J Mol Sci 21:8934

    Article  CAS  PubMed Central  Google Scholar 

  • Garratt LC, Janagoudar BS, Lowe KC, Anthony P, Power JB, Davey MR (2002) Salinity tolerance and antioxidant status in cotton cultures. Free Radic Biol Med 33:502–511

    Article  CAS  PubMed  Google Scholar 

  • Hanin M, Ebel C, Ngom M, Laplaze L, Masmoudi K (2016) New insights on plant salt tolerance mechanisms and their potential use for breeding. Front Plant Sci 7:1787

    Article  PubMed  PubMed Central  Google Scholar 

  • Hazzouri KM, Khraiwesh B, Amiri KMA, Pauli D, Blake T, Shahid M, Mullath SK, Nelson D, Mansour AL, Salehi-Ashtiani K, Purugganan M, Masmoudi K (2018) Mapping of HKT1;5 gene in barley using GWAS approach and its implication in salt tolerance mechanism. Front Plant Sci 9:156

    Article  PubMed  PubMed Central  Google Scholar 

  • Hemavathi UCP, Akula N, Young KE, Chun SC, Kim DH, Park SW (2010) Enhanced ascorbic acid accumulation in transgenic potato confers tolerance to various abiotic stresses. Biotechnol Lett 32:321–330

    Article  CAS  PubMed  Google Scholar 

  • Hernández JA, Jiménez A, Mullineaux P, Sevilia F (2001) Tolerance of pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defences. Plant Cell Environ 23:853–862

    Article  Google Scholar 

  • Hou B, Lim EK, Higgins GS, Bowles DJ (2004) N-glucosylation of cytokinins by glycosyltransferases of Arabidopsis thaliana. J Biol Chem 279:47822–47832

    Article  CAS  PubMed  Google Scholar 

  • Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P (2008) Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinform 2008:420747

    Article  Google Scholar 

  • Hwang JE, Lim CJ, Chen H, Je J, Song C, Lim CO (2012) Overexpression of Arabidopsis dehydration-responsive element-binding protein 2C confers tolerance to oxidative stress. Mol Cells 33:135–140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ishikawa T, Shabala S (2019) Control of xylem Na(+) loading and transport to the shoot in rice and barley as a determinant of differential salinity stress tolerance. Physiol Plant 165:619–631

    Article  CAS  PubMed  Google Scholar 

  • Lairson LL, Henrissat B, Davies GJ, Withers SG (2008) Glycosyltransferases: structures, functions, and mechanisms. Annu Rev Biochem 77:521–555

    Article  CAS  PubMed  Google Scholar 

  • Li YJ, Wang B, Dong RR, Hou BK (2015) AtUGT76C2, an Arabidopsis cytokinin glycosyltransferase is involved in drought stress adaptation. Plant Sci 236:157–167

    Article  CAS  PubMed  Google Scholar 

  • Lipka AE, Tian F, Wang Q, Peiffer J, Li M, Bradbury PJ, Gore MA, Buckler ES, Zhang Z (2012) GAPIT: genome association and prediction integrated tool. Bioinformatics 28:2397–2399

    Article  CAS  PubMed  Google Scholar 

  • Liu JM, Zhao JY, Lu PP, Chen M, Guo CH, Xu ZS, Ma YZ (2016a) The E-subgroup pentatricopeptide repeat protein family in Arabidopsis thaliana and confirmation of the responsiveness PPR96 to abiotic stresses. Front Plant Sci 7:1825

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu X, Huang M, Fan B, Buckler ES, Zhang Z (2016b) Iterative usage of fixed and random effect models for powerful and efficient genome-wide association studies. PLoS Genet 12:e1005767

    Article  PubMed  PubMed Central  Google Scholar 

  • Maldonado-Calderon MT, Sepulveda-Garcia E, Rocha-Sosa M (2012) Characterization of novel F-box proteins in plants induced by biotic and abiotic stress. Plant Sci 185–186:208–217

    Article  PubMed  Google Scholar 

  • Malekzadeh K, Niazi A, Shahriari-Ahmadi F, Mirshamsi-Kakhaki A, Zare-Mehrjerdi M (2015) The responses of L-gulonolactone oxidase and HKT2;1 genes in Aeluropus littoralis’ shoots under high concentration of sodium chloride. J Plant Mol Breed 3:28–35

    Google Scholar 

  • Mascher M, Wicker T, Jenkins J, Plott C, Lux T, Koh CS, Ens J, Gundlach H, Boston LB, Tulpova Z, Holden S, Hernandez-Pinzon I, Scholz U, Mayer KFX, Spannagl M, Pozniak CJ, Sharpe AG, Simkova H, Moscou MJ, Grimwood J, Schmutz J, Stein N (2021) Long-read sequence assembly: a technical evaluation in barley. Plant Cell 33:1888–1906

    Article  PubMed  PubMed Central  Google Scholar 

  • Milner SG, Jost M, Taketa S, Mazon ER, Himmelbach A, Oppermann M, Weise S, Knupffer H, Basterrechea M, Konig P, Schuler D, Sharma R, Pasam RK, Rutten T, Guo G, Xu D, Zhang J, Herren G, Muller T, Krattinger SG, Keller B, Jiang Y, Gonzalez MY, Zhao Y, Habekuss A, Farber S, Ordon F, Lange M, Borner A, Graner A, Reif JC, Scholz U, Mascher M, Stein N (2019) Genebank genomics highlights the diversity of a global barley collection. Nat Genet 51:319–326

    Article  CAS  PubMed  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  CAS  PubMed  Google Scholar 

  • Munns R, James RA, Lauchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57:1025–1043

    Article  CAS  PubMed  Google Scholar 

  • Mwando E, Han Y, Angessa TT, Zhou G, Hill CB, Zhang XQ, Li C (2020) Genome-wide association study of salinity tolerance during germination in barley (Hordeum vulgare L.). Front Plant Sci 11:118

    Article  PubMed  PubMed Central  Google Scholar 

  • Mwando E, Han Y, Angessa T, Zhang X-Q, Li C (2021) Fine-mapping and characterisation of genes on barley (Hordeum vulgare) chromosome 2H for salinity stress tolerance during germination. Crop J. https://doi.org/10.1016/j.cj.2021.10.008

  • Nakano Y, Asada K (1980) Spinach-chloroplasts scavenge hydrogen-peroxide on illumination. Plant Cell Physiol 21:1295–1307

    Article  CAS  Google Scholar 

  • Panta S, Flowers T, Lane P, Doyle R, Haros G, Shabala S (2014) Halophyte agriculture: success stories. Environ Exp Bot 107:71–83

    Article  Google Scholar 

  • Ramachandra Reddy A, Chaitanya KV, Vivekanandan M (2004) Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 161:1189–1202

    Article  PubMed  Google Scholar 

  • Rivandi J, Miyazaki J, Hrmova M, Pallotta M, Tester M, Collins NC (2011) A SOS3 homologue maps to HvNax4, a barley locus controlling an environmentally sensitive Na+ exclusion trait. J Exp Bot 62:1201–1216

    Article  CAS  PubMed  Google Scholar 

  • Robles P, Quesada V (2019) Transcriptional and post-transcriptional regulation of organellar gene expression (OGE) and its roles in plant salt tolerance. Int J Mol Sci 20:1056

    Article  CAS  PubMed Central  Google Scholar 

  • Saade S, Brien C, Pailles Y, Berger B, Shahid M, Russell J, Waugh R, Negrao S, Tester M (2020) Dissecting new genetic components of salinity tolerance in two-row spring barley at the vegetative and reproductive stages. PLoS One 15:e0236037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sarker U, Oba S (2020a) Phenolic profiles and antioxidant activities in selected drought-tolerant leafy vegetable amaranth. Sci Rep 10:18287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sarker U, Oba S (2020b) The response of salinity stress-induced A. tricolor to growth, anatomy, physiology, non-enzymatic and enzymatic antioxidants. Front Plant Sci 11:559876

    Article  PubMed  PubMed Central  Google Scholar 

  • Sayed MA, Nassar SM, Moustafa ES, Said MT, Borner A, Hamada A (2021) Genetic mapping reveals novel exotic and elite QTL alleles for salinity tolerance in barley. Agronomy 11:1774

    Article  CAS  Google Scholar 

  • Shavrukov Y, Gupta NK, Miyazaki J, Baho MN, Chalmers KJ, Tester M, Langridge P, Collins NC (2010) HvNax3—a locus controlling shoot sodium exclusion derived from wild barley (Hordeum vulgare ssp. spontaneum). Funct Integr Genom 10:277–291

    Article  CAS  Google Scholar 

  • Shrivastava P, Kumar R (2014) Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J Biol Sci 22:123–131

    Article  PubMed  PubMed Central  Google Scholar 

  • Siringam K, Juntawong N, Cha-um S, Kirdmanee C (2011) Salt stress induced ion accumulation, ion homeostasis, membrane injury and sugar contents in salt-sensitive rice (Oryza sativa L. spp. indica) roots under isoosmotic conditions. Afr J Biotechnol 10:1340–1346

    CAS  Google Scholar 

  • So H-A, Choi SJ, Chung E, Lee J-H (2015) Molecular characterization of stress-inducible PLATZ gene from soybean (Glycine max L.). Plant Omics J 8:479–484

  • Temel A, Gozukirmizi N (2015) Physiological and molecular changes in barley and wheat under salinity. Appl Biochem Biotechnol 175:2950–2960

    Article  CAS  PubMed  Google Scholar 

  • Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thabet SG, Alqudah AM (2019) Crops and drought. eLS 1–8. https://doi.org/10.1002/9780470015902.a0025265

  • Thabet SG, Moursi YS, Karam MA, Borner A, Alqudah AM (2020) Natural variation uncovers candidate genes for barley spikelet number and grain yield under drought stress. Genes (basel) 11:533

    Article  CAS  Google Scholar 

  • Thabet SG, Alomari DZ, Alqudah AM (2021a) Exploring natural diversity reveals alleles to enhance antioxidant system in barley under salt stress. Plant Physiol Biochem 166:789–798

    Article  CAS  PubMed  Google Scholar 

  • Thabet SG, Moursi YS, Sallam A, Karam MA, Alqudah AM (2021b) Genetic associations uncover candidate SNP markers and genes associated with salt tolerance at the seedling stage in barley. Environ Exp Bot 188:104499

    Article  CAS  Google Scholar 

  • Thabet SG, Sallam A, Moursi YS, Karam MA, Alqudah AM (2021c) Genetic factors controlling nTiO2 nanoparticles stress tolerance in barley (Hordeum vulgare) during seed germination and seedling development. Funct Plant Biol 48:1288–1301

    Article  CAS  PubMed  Google Scholar 

  • Thabet SG, Alomari DZ, Brinch-Pedersen H, Alqudah AM (2022) Genetic analysis toward more nutritious barley grains for a food secure world. Bot Stud 63:6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei T, Simko V (2017) corrplot: Visualization of a correlation matrix. R package version 084 230:11

  • Westerman RL (1990) Soil testing and plant analysis. Soil Science Society of America, Madison, pp 534–587

  • Xu Z-Y, Lee KH, Dong T, Jeong JC, Jin JB, Kanno Y, Kim DH, Kim SY, Seo M, Bressan RA, Yun D-J, Hwang I (2012) A vacuolar β-glucosidase homolog that possesses glucose-conjugated abscisic acid hydrolyzing activity plays an important role in osmotic stress responses in Arabidopsis. Plant Cell 24:2184–2199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xue DW, Huang YZ, Zhang XQ, Wei K, Westcott S, Li CD, Chen MC, Zhang GP, Lance R (2009) Identification of QTLs associated with salinity tolerance at late growth stage in barley. Euphytica 169:187–196

    Article  Google Scholar 

  • Xue W, Yan J, Zhao G, Jiang Y, Cheng J, Cattivelli L, Tondelli A (2017) A major QTL on chromosome 7HS controls the response of barley seedling to salt stress in the Nure × Tremois population. BMC Genet 18:79

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang Z, Yang X, Dong S, Ge Y, Zhang X, Zhao X, Han N (2020) Overexpression of beta-Ketoacyl-CoA synthase from Vitis vinifera L. improves salt tolerance in Arabidopsis thaliana. Front Plant Sci 11:564385

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu J, Zhao W, Tong W, He Q, Yoon MY, Li FP, Choi B, Heo EB, Kim KW, Park YJ (2018) A genome-wide association study reveals candidate genes related to salt tolerance in rice (Oryza sativa) at the germination stage. Int J Mol Sci 19:3145

    Article  PubMed Central  Google Scholar 

  • Zhang Y, Xu WY, Li ZH, Deng XW, Wu WH, Xue YB (2008) F-box protein DOR functions as a novel inhibitory factor for abscisic acid-induced stomatal closure under drought stress in Arabidopsis. Plant Physiol 148:2121–2133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou SM, Kong XZ, Kang HH, Sun XD, Wang W (2015) The involvement of wheat F-box protein gene TaFBA1 in the oxidative stress tolerance of plants. PLoS One 10:e0122117

    Article  PubMed  PubMed Central  Google Scholar 

  • Zsigmond L, Szepesi A, Tari I, Rigo G, Kiraly A, Szabados L (2012) Overexpression of the mitochondrial PPR40 gene improves salt tolerance in Arabidopsis. Plant Sci 182:87–93

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This study was funded by Novo Nordisk Fonden (NNF20OC0064295, NNF19OC0056580).

Author information

Authors and Affiliations

  1. Department of Botany, Faculty of Science, Fayoum University, 63514, Fayoum, Egypt

    Samar G. Thabet

  2. Department of Agroecology, Aarhus University, Flakkebjerg, Forsøgsvej 1, 4200, Slagelse, Denmark

    Dalia Z. Alomari, Henrik Brinch-Pedersen & Ahmad M. Alqudah

  3. Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), OT Gatersleben, Corrensstr 3, 06466, Seeland, Germany

    Andreas Börner

Authors
  1. Samar G. Thabet
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dalia Z. Alomari
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andreas Börner
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Henrik Brinch-Pedersen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ahmad M. Alqudah
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SGT and AMA designed the experiment; SGT performed the experiments; AMA and SGT analyzed data; SGT wrote the first draft of the paper; SGT, DZA, AB, HBP, and AMA; Wrote and edit the paper. SGT, DZA, AB, HBP, and AMA conceived the idea and participated in the interpretation of the results. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Ahmad M. Alqudah.

Ethics declarations

Conflict of interest

The authors have not disclosed any competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 135 kb)

Supplementary file2 (PPTX 7174 kb)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Thabet, S.G., Alomari, D.Z., Börner, A. et al. Elucidating the genetic architecture controlling antioxidant status and ionic balance in barley under salt stress. Plant Mol Biol 110, 287–300 (2022). https://doi.org/10.1007/s11103-022-01302-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-022-01302-8

Keywords

Search

Navigation