Abstract
Background and aims
India is one of the countries being projected as the salinization hotspots in the near future. To identify novel donors imparting salt tolerance, barley mini-core collection comprising 107 Hordeum vulgare germplasm and 3 wild accessions from the Indian National Genebank were evaluated under salt stress.
Methods
Barley accessions were screened under salt stress (200 mM NaCl) at early growth and the adult plant stage based on morpho-physiological traits including salt uptake parameters. Further, the possible role of candidate gene Hordeum vulgare root abundant factor (HvRAF) was studied by deciphering allelic variation and expression analysis in selected salt tolerant and susceptible accessions.
Results
Analysis of variance revealed a significant effect of salinity on all traits and elucidated profound genotypic variation. Salinity caused a drastic reduction in growth and severely affected ion homeostasis resulting in decline in grain yield by 65.35% compared to control. Accessions EC0578359, EC0578251, IC0547723, EC0123148, EC0299361, EC0177250 and IC0247671 were identified as the most promising salt-tolerant genotypes. Further investigation of allelic variation in HvRAF revealed a total of 26 SNPs, of which 10 were non-synonymous, 8 were synonymous and 5 were conserved. Haplotype variant analysis indicated two major haplotypic groups (Hap 1 and Hap 2) for HvRAF, of which the Hap 2 was found to be more prevalent than Hap 1.
Conclusions
Salt-tolerant phenotype exhibited the physiological basis of tolerance and upregulated expression of HvRAF, although none of the identified Hap groups could be associated with salt tolerance suggesting the governance of trait by multiple loci.
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Data availability
The original contributions presented in the study are included in the article/supplementary information. The full-length HvRAF gene sequences from barley germplasm accessions were submitted to NCBI (https://www.ncbi.nlm.nih.gov/nucleotide/) under GenBank ids: OR077393, OR077394, OR077395, OR077396, OR077397, OR077398, OR077399, OR0773400, OR0773401, OR0773402, OR0773403, and OR0773404 and are also included in the manuscript under supplementary information (Table S7). Further enquiries may be directed to the corresponding author.
References
Abrar MM, Saqib M, Abbas G, Atiq-ur-Rahman M, Mustafa A, Shah SAA et al (2020) Evaluating the contribution of growth, physiological, and ionic components towards salinity and drought stress tolerance in Jatropha curcas. Plants 9(11):1574. https://doi.org/10.3390/plants9111574
Adolf VI, Jacobsen SE, Shabala S (2013) Salt tolerance mechanisms in quinoa (Chenopodium quinoa Wild.). Environ Exp Bot 92(1–2):43–54. https://doi.org/10.1016/j.envexpbot.2012.07.004
Ahmadi J, Pour-Aboughadareh A, Ourang SF, Khalili P, Poczai P (2020) Unraveling salinity stress responses in ancestral and neglected wheat species at early growth stage: A baseline for utilization in future wheat improvement programs. Physiol Mol Biol Plants 26(3):537–549. https://doi.org/10.1007/s12298-020-00768-4
Akhter MS, Noreen S, Mahmood S, Athar HR, Ashraf M, Alsahli AA et al (2021) Influence of salinity stress on PSII in barley (Hordeum vulgare L.) genotypes, probed by chlorophyll-a fluorescence. J King Saud Univ Sci 33(1):101239. https://doi.org/10.1016/j.jksus.2020.101239
Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24(12):1337–1344. https://doi.org/10.1046/j.1365-3040.2001.00778.x
Ali RM, Abbas HM (2003) Response of salt stressed barley seedlings to phenylurea. Plant Soil Environ 49(4):158–162. https://doi.org/10.17221/4107-PSE
Amna, Ali B, Azeem MA, Qayyum A, Mustafa G, Ahmad MA et al (2021) Bio-fabricated silver nanoparticles: A sustainable approach for augmentation of plant growth and pathogen control. In: Faizan M, Hayat S, Yu F (eds) Sustainable Agriculture Reviews 53, Springer, Cham. https://doi.org/10.1007/978-3-030-86876-5_14
Aravind J, Kaur V, Wankhede DP, Nanjundan J 2020. EvaluateCore: Quality evaluation of core collections. R package version 0.1.1. Available online at: https://aravindj.github.io/EvaluateCore/https://CRAN.R-project.org/package=EvaluateCore
Arif Y, Singh P, Siddiqui H, Bajguz A, Hayat S (2020) Salinity induced physiological and biochemical changes in plants: An omic approach towards salt stress tolerance. Plant Physiol Biochem 156:64–77. https://doi.org/10.1016/j.plaphy.2020.08.042
Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Aust J Biol Sci 15:413–428. https://doi.org/10.1071/BI9620413
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207. https://doi.org/10.1007/BF00018060
Brown AHD (1989) Core collections: A practical approach to genetic resources management. Genome 31:818–824. https://doi.org/10.1139/g89-144
Chaurasia S, Kumar A, Singh AK (2022) Comprehensive evaluation of morpho-physiological and ionic traits in wheat (Triticum aestivum L.) genotypes under salinity stress. Agriculture 12(11):1765. https://doi.org/10.3390/agriculture12111765
Chinnusamy V, Jagendorf A, Zhu JK (2005) Understanding and improving salt tolerance in plants. Crop Sci 45(2):437–448. https://doi.org/10.2135/cropsci2005.0437
Dawson IK, Russell J, Powell W, Steffenson B, Thomas WTB, Waugh R (2015) Barley: a translational model for adaptation to climate change. New Phytol 206(3):913–931. https://doi.org/10.1111/nph.13266
De Dorlodot S, Forster B, Pagès L, Price A, Tuberosa R, Draye X (2007) Root system architecture: Opportunities and constraints for genetic improvement of crops. Trends Plant Sci 12(10):474–481. https://doi.org/10.1016/j.tplants.2007.08.012
De Beukelaer H, Davenport GF (2018) Corehunter: Multi-Purpose Core Subset Selection. R package version 3.2.1. Available online at: https://CRAN.Rproject.org/package=corehunter
De Beukelaer H, Davenport GF, Fack V (2018) Core Hunter 3: flexible core subset selection. BMC Bioinform 19:203. https://doi.org/10.1186/s12859-018-2209-z
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15
Ebrahim F, Arzani A, Rahimmalek M, Sun D, Peng J (2019) Salinity tolerance of wild barley Hordeum vulgare ssp. spontaneum. Plant Breed 139(2):304–316. https://doi.org/10.1111/pbr.12770
ElBasyoni I, Saadalla M, Baenziger S, Bockelman H, Morsy S (2017) Cell membrane stability and association mapping for drought and heat tolerance in a worldwide wheat collection. Sustainability 9(9):1–16. https://doi.org/10.3390/su9091606
FAO (2023) Global map of salt affected soils version 1.0. https://www.fao.org/soils-portal/data-hub/soil-maps-and-databases/global-map-of-salt-affected-soils/en/ Accessed February 2023
Fischer R, Maurer R (1978) Drought resistance in spring wheat cultivars. I. Grain yield response. Aust J Agic Res 29:897–912. https://doi.org/10.1071/AR9780897
Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179(4):945–963. https://doi.org/10.1111/j.1469-8137.2008.02531.x
Gürel F, Öztürk ZN, Uçarlı C, Rosellini D (2016) Barley genes as tools to confer abiotic stress tolerance in crops. Front Plant Sci 7:1137. https://doi.org/10.3389/fpls.2016.01137
Gutterson N, Reuber TL (2004) Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol 7(4):465–471. https://doi.org/10.1016/j.pbi.2004.04.007
Hammer O, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):1–9. http://palaeo-electronica.org/2001_1/past/issue1_01.htm
Hasegawa PM (2013) Sodium (Na+) homeostasis and salt tolerance of plants. Environ Exp Bot 92:19–31. https://doi.org/10.1016/j.envexpbot.2013.03.001
Hassani A, Azapagic A, Shokri N (2021) Global predictions of primary soil salinization under changing climate in the 21st century. Nat Commun 12(1):6663. https://doi.org/10.1038/s41467-021-26907-3
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125(1):189–198. https://doi.org/10.1016/0003-9861(68)90654-1
Hemantaranjan A, Bhanu AN, Singh MN, Yadav DK, Patel PK, Singh R et al (2014) Heat stress responses and thermotolerance. Adv Plants Agric Res 1(3):62–70. https://doi.org/10.15406/apar.2014.01.00012
Hiscox JD, Israelstam GF (1979) A method for extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57(12):1332–1334. https://doi.org/10.1139/b79-163
Hoagland DR, Arnon DI (1950) The water culture method for growing plants without soil. Circ Calif Agricl Exp Stn 347:32. http://hdl.handle.net/2027/uc2.ark:/13960/t51g1sb8j
Hossain MS (2019) Present scenario of global salt affected soils, its management and importance of salinity research. Int Res J Biol Sci 1(1):1–3
Ibrahim AMH, Quick JS (2001) Heritability of heat tolerance in winter and spring wheat. Crop Sci 41(5):1401–1405. https://doi.org/10.2135/cropsci2001.4151401x
Jamshidi A, Javanmard HR (2018) Evaluation of barley (Hordeum vulgare L.) genotypes for salinity tolerance under field conditions using the stress indices. Ain Shams Eng J 9(4):2093–2099. https://doi.org/10.1016/j.asej.2017.02.006
Javed MM, Al-Doss AA, Tahir MU, Khan MA, El-Hendawy S (2022) Assessing the suitability of selection approaches and genetic diversity analysis for early detection of salt tolerance of barley genotypes. Agronomy 12(12):3217. https://doi.org/10.3390/agronomy12123217
Jung J, Won SY, Suh SC, Kim H, Wing R, Jeong Y et al (2007) The barley ERF-type transcription factor HvRAF confers enhanced pathogen resistance and salt tolerance in Arabidopsis. Planta 225(3):575–588. https://doi.org/10.1007/s00425-006-0373-2
Kaur V, Kumari J, Manju, Jacob SR, Panwar BS (2018) Genetic diversity of indigenous and exotic germplasm of barley (Hordeum vulgare L.) and identification of trait specific superior accessions. Wheat Barley Res 10(3):190–197. https://doi.org/10.25174/2249-4065/2018/83620
Kaur V, Aravind J, Manju, Jacob SR, Kumari J, Panwar BS et al (2022) Phenotypic characterization, genetic diversity assessment in 6,778 accessions of barley (Hordeum vulgare L. ssp. vulgare) germplasm conserved in National Genebank of India and development of a core set. Front Plant Sci 13:771920. https://doi.org/10.3389/fpls.2022.771920
Kaur V, Yadav SK, Wankhede DP, Pulivendula P, Kumar A, Chinnusamy V (2020) Cloning and characterization of a gene encoding MIZ1, a domain of unknown function protein and its role in salt and drought stress in rice. Protoplasma 257(2):475–487. https://doi.org/10.1007/s00709-019-01452-5
Kishore N, Kumar V, Verma RPS (2016) Barley. In: Singh M, Kumar S (eds) Broadening the genetic base of grain cereals. Springer, India, pp 89–125
Kumar A, Mann A, Kumar A, Devi S, Sharma PC (2018) Potential and role of halophyte crops in saline environments. In: Gupta SK, Goyal MR, Singh A (eds) Engineering practices for management of soil salinity. Apple Academic Press Inc, Canada, pp 329–365
Lee JH, Hong JP, Oh SK, Lee S, Choi D, Kim WT (2004) The ethylene-responsive factor like protein 1 (CaERFLP1) of hot pepper (Capsicum annuum L.) interacts in vitro with both GCC and DRE/CRT sequences with different binding affinities: possible biological roles of CaERFLP1 in response to pathogen infection and high salinity conditions in transgenic tobacco plants. Plant Mol Biol 55(1):61–81. https://doi.org/10.1007/s11103-004-0417-6
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C (T)) method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Lynch JP (2007) Roots of the second green revolution. Aust J Bot 55(5):493–512. https://doi.org/10.1071/BT06118
Ma J, Saleem MH, Yasin G, Mumtaz S, Qureshi FF, Ali B et al (2022) Individual and combinatorial effects of SNP and NaHS on morpho-physio-biochemical attributes and phytoextraction of chromium through Cr-stressed spinach (Spinacia oleracea L.). Front Plant Sci 13:973740. https://doi.org/10.3389/fpls.2022.973740
Mahajan RK, Sapra RL, Srivastava U, Singh M, Sharma GD (2000) Minimal descriptors (for characterization and evaluation) of agri-horticultural crops (Part I). National Bureau of Plant Genetic Resources, New Delhi.
Manju YSK, Wankhede DP, Saroha A, Jacob SR, Pandey R et al (2023) Screening of barley germplasm for drought tolerance based on root architecture, agronomic traits and identification of novel allelic variants of HVA1. J Agron Crop Sci 209(5):705–723. https://doi.org/10.1111/jac.12650
Manju, Kaur V, Sharma K, Kumar A (2019a) Identification of promising sources for drought tolerance in cultivated and wild species germplasm of barley based on root architecture. J Environ Biol 40(3):309–315. https://doi.org/10.22438/jeb/40/3/MRN-995
Manju KV, Sharma K, Jacob SR (2019b) Assessment of genetic diversity in cultivated and wild species germplasm of barley based on morpho-agronomical and root architecture traits. Indian J Plant Genet Resour 32(3):360–367. https://doi.org/10.5958/0976-1926.2019.00039.1
Mwando E, Angessa TT, Han Y, Li C (2020) Salinity tolerance in barley during germination- homologs and potential genes. J Zhejiang Univ Sci B 21(2):93–121. https://doi.org/10.1631/jzus.b1900400
Odong TL, Jansen J, van Eeuwijk FA, van Hintum TJL (2013) Quality of core collections for effective utilisation of genetic resources review, discussion and interpretation. Theor App Genet 126(2):289–305. https://doi.org/10.1007/s00122-012-1971-y
Pour-Aboughadareh A, Sanjani S, Nikkhah-Chamanabad H, Mehrvar MR, Asadi A, Amini A (2021) Identification of salt-tolerant barley genotypes using multiple-traits index and yield performance at the early growth and maturity stages. Bull Natl Res Cent 45:117. https://doi.org/10.1186/s42269-021-00576-0
Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38(8):904–909. https://doi.org/10.1038/ng1847
Rajeswari S, Sood N, Swarup TG, Subramanian R (2019) Assessing salt-stress tolerance in barley. Univ Sci 24(1):91–109. https://doi.org/10.11144/javeriana.sc24-1.asst
Rangani J, Parida AK, Panda A, Kumari A (2016) Coordinated changes in anti-oxidative enzymes protect the photosynthetic machinery from salinity induced oxidative damage and confer salt tolerance in an extreme halophyte Salvadora persica L. Front Plant Sci 7:50. https://doi.org/10.3389/fpls.2016.00050
Rasel M, Tahjib-Ul-Arif M, Hossain MA, Hassan L, Farzana S, Brestic M (2020) Screening of salt-tolerant rice landraces by seedling stage phenotyping and dissecting biochemical determinants of tolerance mechanism. J Plant Growth Regul 40:1853–1868. https://doi.org/10.1007/s00344-020-10235-9
Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophy Res Commun 290(3):998–1009. https://doi.org/10.1006/bbrc.2001.6299
Serraj R, Krishnamurthy L, Kashiwagi J, Kumar J, Chandra S, Crouch JH (2004) Variation in root traits of chickpea (Cicer arietinum L.) grown under terminal drought. Field Crops Res 88(2–3):115–127. https://doi.org/10.1016/j.fcr.2003.12.001
Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W et al (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539. https://doi.org/10.1038/msb.2011.75
Tao R, Ding J, Li C, Zhu X, Guo W, Zhu M (2021) Evaluating and screening of agro-physiological indices for salinity stress tolerance in wheat at the seedling stage. Front Plant Sci 12:646175. https://doi.org/10.3389/fpls.2021.646175
Tavakkoli E, Rengasamy P, McDonald GK (2011) The response of barley to salinity stress differs between hydroponic and soil system. Funct Plant Biol 37(7):621–633. https://doi.org/10.1071/FP09202
Tuberosa R, Sanguineti MC, Landi P, Giuliani MM, Salvi S, Conti S (2002) Identification of QTLs for root characteristics in maize grown in hydroponics and analysis of their overlap with QTLs for grain yield in the field at two water regimes. Plant Mol Biol 48(5):697–712. https://doi.org/10.1023/a:1014897607670
UN (2023) Sustainable consumption and production. https://sdgs.un.org/goals/goal12. Accessed 13 May 2023
United Nations Department of Economic and Social Affairs, Population Division (2022) World PopulationProspects 2022: Summary of Results. UN DESA/POP/2022/TR/NO. 3.
Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M et al (2012) Primer 3-new capabilities and interfaces. Nucleic Acids Res 40(15):e115. https://doi.org/10.1093/nar/gks596
Wild A (2003) Soils, land and food: Managing the land during the twenty-first century. Cambridge University Press, Cambridge, UK, p 256
Yi SY, Kim JH, Joung YH, Lee S, Kim WT, Yu SH et al (2004) The pepper transcription factor CaPF1 confers pathogen and freezing tolerance in Arabidopsis. Plant Physiol 136(1):2862–2874. https://doi.org/10.1104/pp.104.042903
Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6(5):441–445. https://doi.org/10.1016/s1369-5266(03)00085-2
Acknowledgements
The authors acknowledge funding and research facilities available at the Indian Council of Agricultural Research-National Bureau of Plant Genetic Resources (ICAR-NBPGR), New Delhi, India. The authors are thankful to Dr. Gyanendra Pratap Singh, (Director, ICAR-NBPGR) for the research facilities and facilitation. The contributions of several scientists and technicians in the exploration and conservation of barley genetic resources over time at ICAR-NBPGR are greatly acknowledged.
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Authors acknowledge the funding support received from ICAR for the Institutional research project (PGR/GEV-BUR-DEL-01.01). The study has not received any funding support from external funding agencies.
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S: Investigation, data curation, writing original draft; VK: Conceptualization, resources, supervision, writing, review and editing; SKY: Investigation, formal analysis and writing original draft; SSA: Conceptualization, Supervision, JA: Resources, formal analysis; SRJ: Resources; RKG: review and resources.
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Sonia, Kaur, V., Yadav, S.K. et al. Development and evaluation of barley mini-core collection for salinity tolerance and identification of novel haplotypic variants for HvRAF. Plant Soil 497, 317–337 (2024). https://doi.org/10.1007/s11104-023-06397-6
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DOI: https://doi.org/10.1007/s11104-023-06397-6