Abstract
The present study was conducted to identify the novel QTLs controlling salinity and sodicity tolerance using indica MAGIC rice population. Phenotyping was carried out in salinity (EC ~ 10 dS/m) and sodicity (pH ~ 9.8) at the seedling stage. Among 391 lines, 43 and 98 lines were found tolerant and moderately tolerant to salinity. For sodicity condition, 2 and 45 lines were showed tolerance and moderately tolerance at seedling stage. MAGIC population was genotyped with the help of genotyping by sequencing (GBS) and filtered 27041SNPs were used for genome wide marker trait association studies. With respect to salinity tolerance, 25 SNPs were distributed on chromosomes 1, 5, 11 and 12, whereas 18 SNPs were mapped on chromosomes 6, 4 and 11 with LOD value of > 3.25 to sodicity tolerance in rice. The candidate gene analysis detected twelve causal genes including SKC1 gene at Saltol region for salinity and six associated genes for sodic stress tolerance. The significant haplotypes responsible for core histone protein coding gene (LOC_Os12g25120) and three uncharacterized protein coding genes (LOC_Os01g20710, LOC_Os01g20870 and LOC_Os12g22020) were identified under saline stress. Likewise, five significant haplotypes coding for ribose 5-phosphate isomerise (LOC_Os04g24140), aspartyl protease (LOC_Os06g15760), aluminum-activated malate transporter (LOC_Os06g15779), OsFBX421-Fbox domain containing protein (LOC_Os11g32940) and one uncharacterized protein (LOC_Os11g32930) were detected for sodic stress tolerance. The identified novel SNPs could be the potential candidates for functional characterization. These candidate genes aid to further understanding of genetic mechanism on salinity and sodicity stress tolerance in rice. The tolerant line could be used in future breeding programme to enhance the salinity and sodicity tolerance in rice.
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References
Alam R, Sazzadur Rahman M, Seraj Z, Thomson M, Ismail A, Tumimbang-Raiz E, Gregorio G (2011) Investigation of seedling-stage salinity tolerance QTLs using backcross lines derived from Oryzasativa L. Pokkali. Plant Breed 130(4):430–437
Ali S, Gautam R, Mahajan R, Krishnamurthy S, Sharma S, Singh R et al (2013) Stress indices and selectable traits in SALTOL QTL introgressed rice genotypes for reproductive stage tolerance to sodicity and salinity stresses. Field Crop Res 154:65–73
Arshadullah M., Rasheed, M. and Zaidi.S.A.R. (2011) Salt tolerance of different rice cultivars for their salt tolerance under salt-affected soils.International Research Journal of Agricultural Science and Soil Science 1:183–184.
Babu N, Krishnan S, Vinod K, Krishnamurthy S, Singh V, Singh M et al. (2017) Marker Aided Incorporation of Saltol, a Major QTL Associated with Seedling Stage Salt Tolerance, into Oryzasativa ‘Pusa Basmati 1121’. Frontiers in Plant Science 8.
Bandillo N, Raghavan C, Muyco P, Sevilla M, Lobina I, Dilla-Ermita C et al (2013) Multi-parent advanced generation inter-cross (MAGIC) populations in rice: progress and potential for genetics research and breeding. Rice 6:11
Bhandari A, Jayaswal P, Yadav N, Singh R, Singh Y, Singh B et al. (2019) Genomics-assisted backcross breeding for infusing climate resilience in high-yielding green revolution varieties of rice. Indian Journal of Genetics and Plant Breeding (The) 79.
Biatczyk J, Lechowski Z, Libik A (1994) Growth of tomato seedlings under different HCO-3concentration in the medium. J Plant Nutr 17:801–816
Bonilla P, Mackell D, Deal K, Gregorio G (2002) RFLP and SSLP mapping of salinity tolerance genes in chromosome 1 of rice (Oryzasativa L.) using recombinant inbred lines. Philippine Agricultural Scientist 65(1):68–76
Bradbury P, Zhang Z, Kroon D, Casstevens T, Ramdoss Y, Buckler E (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635
Brautigan D, Rengasamy P, Chittleborough D (2012) Aluminium speciation and phytotoxicity in alkaline soils. Plant Soil 360:187–196
Cao J (2012) The pectin Lyases in arabidopsis thaliana: evolution, selection and expression profiles. PLoS ONE 7(10):e46944. https://doi.org/10.1371/journal.pone.0046944
Cavanagh C, Morell M, Mackay I, Powell W (2008) From mutations to MAGIC: resources for gene discovery, validation and delivery in crop plants. Curr Opin Plant Biol 11:215–221
Chapagain S, Park YC, Jang CS (2017) Functional diversity of RING E3 ligases of major cereal crops in response to abiotic stresses. J Crop Sci Biotech 20(5):351–357
Chini A, Grant J, Seki M et al (2004) Drought tolerance established by enhanced expression of CC-NBS-LRR gene ADR1 requires salicylic acid, EDS1, and ABI1. Plant J 38:810–822
Claes B, Dekeyser R, Villarroel R, den Bulcke M, Bauw G, Montagu M et al (1990) Characterization of a rice gene showing organ-specific expression in response to salt stress and drought. Plant Cell 2:19
Darvasi A, Soller M (1995) Advanced intercross lines, an experimental population for fine genetic mapping. Genetics 141:1199–1207
Delhaize E, Ryan PR, Hebb DM, Yamamoto Y, Sasaki T, Matsumoto H (2004) Engineering high-level aluminum tolerance in barley with the ALMT1 gene. Proc Natl Acad Sci USA 101:15249–15254
Dixit S, Swamy B, Vikram P, Ahmed H, Sta Cruz M, Amante M et al (2012) Fine mapping of QTLs for rice grain yield under drought reveals sub-QTLs conferring a response to variable drought severities. Theor Appl Genet 125:155–169
Elshire R, Glaubitz J, Sun Q, Poland J, Kawamoto K, Buckler ES et al (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6:19379
FAO (2013) Global cereals forecast to increase by 7 percent in 2013. http://wwwfao.org/asiapacific/rap/home/news/detail/en/?newsuid=180032.
Fujita M, Fujita Y, Noutoshi Y et al (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. CurrOpin Plant Biol 9:436–442
Ganie SA, Karmakar J, Roychowdhury R, Mondal TK, Dey N (2014) Assessment of genetic diversity in salt-tolerant rice and its wild relatives for ten SSR loci and one allele mining primer of salT gene located on 1st chromosome. Plant Syst Evol 300:1741–1747
Geetha S, Vasuki A, Selvam P, Saraswathi R, Krishnamurthy S, Palanichamy M et al (2017) Development of sodicity tolerant rice varieties through marker assisted backcross breeding. Electron J Plant Breed 8:1013
Głowacki S, Macioszek VK, Kononowicz AK (2011) R proteins as fundamentals of plant innate immunity. Cell MolBiolLett 16:1–24
Gregorio GB (1997) Tagging salinity tolerance genes in rice using amplified fragment length polymorphism (AFLP). Ph.D Thesis, University of the Philippines Los Banõs, Laguna
Guo R, Zhao J, Wang XX et al (2015) Constitutive expression of a grape aspartic protease gene in transgenic arabidopsis confers osmotic stress tolerance. Plant Cell Tissue Organ Cult 121:275–287
Heenan D, Lewin L, McCaffery D (1988) Salinity tolerance in rice varieties at different growth stages. Animal Product Science 28:343–349
Hoekenga O, Maron L, Pineros M, Cancado G, Shaff J, Kobayashi Y et al (2006) AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminium tolerance in Arabidopsis. Proc Natl Acad Sci 103:9738–9743
Huang X, Huang X, Wei X, Sang T, Zhao Q, Feng Q, Zhao Y et al (2010) Genome-wide association studies of 14 agronomic traits in rice landraces. Nat Genet 42:961–967
Huang X, Zhao Y, Wei X, Li C, Wang A, Zhao Q et al (2011) Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nat Genet 44:32–39
Inoue H, Hayashi N, Matsushita A et al (2013) Blast resistance of CC-NBS-LRR protein Pb1 is mediated by WRKY45 through protein-protein interaction. ProcNatlAcadSci USA 110:9577–9582. https://doi.org/10.1073/pnas.1222155110
Jain M, Nijhawan A, Rita-Arora R et al (2007) F-Box proteins in rice. Genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress. Plant Physiol 143(4):1467–1483
Jaiswal S, Gautam R, Singh R, Krishnamurthy S, Ali S, Sakthivel K et al (2019) Harmonizing technological advances in phenomics and genomics for enhanced salt tolerance in rice from a practical Perspective. Rice 12:89. https://doi.org/10.1186/s12284-019-0347-1
Jansen R, Jannink J, Beavis W (2003) Mapping quantitative trait loci in plant breeding populations. Crop Sci 43:829–834
Jin H, Plaha P, Park J, Hong C, Lee I, Yang Z et al (2006) Comparative EST profiles of leaf and root of Leymuschinensis, a xerophilous grass adapted to high pH sodic soil. Plant Sci 170:1081–1086
Kim Y, Tsuda K, Igarashi D et al (2014) Signaling mechanisms underlying the robustness and tunability of the plant immune network. Cell Host Microbe 15:84–94
Korte A, Farlow A (2013) The advantages and limitations of trait analysis with GWAS: a review. Plant Methods 9:1
Krishnamurthy S, Sharma S, Sharma D, Singh Y, Mishra V et al (2016a) Analysis of stability and G × E interaction of rice genotypes across saline and alkaline environments in India. Cereal Res Commun 44:349–360
Krishnamurthy S, Gautam R, Sharma P, Sharma D (2016b) Effect of different salt stresses on agro-morphological traits and utilisation of salt stress indices for reproductive stage salt tolerance in rice. Field Crop Res 190:26–33
Krishnamurthy S, Pundir P, Warriach A, Rathor S, Lokeshkumar B, Singh N et al (2021) IntrogressedSaltol QTL lines improve the salinity tolerance in rice at seedling stage. Front Plant Sci 11:833
Krishnamurthy S, Sharma P, Sharma D, Ravikiran K, Singh Y, Mishra V, et al (2017) Identification of mega-environments and rice genotypes for general and specific adaptation to saline and alkaline stresses in India. Sci Rep 7
Kumar V, Singh A, Mithra S, Krishnamurthy S, Parida S, Jain S et al (2015) Genome-wide association mapping of salinity tolerance in rice (Oryzasativa). DNA Res 22:133–145
Lang N, Yanagihara S, Buu BC (2000) Quantitative trait loci for salt tolerance in rice via molecular markers. Omonrice 8:37–48
De Leon TB, Steven Linscombe S, Subudhi PK (2016) Molecular dissection of seedling salinity tolerance in rice (Oryzasativa L) using a high-density GBS-Based SNP linkage map. Rice 9(1):52
Li H, Yan S, Zhao L et al (2014) Histone acetylation associated up-regulation of the cell wall related genes is involved in salt stress induced maize root swelling. BMC Plant Biol 14:105
Li W, Pang S, Lu Z et al (2020) Function and mechanism of WRKY transcription factors in abiotic stress responses of plants. Plants (basel) 9(11):1515
Liu S, Gao H, Wu X, Fang Q, Chen L, Zhao F et al (2016) Isolation and characterization of an aluminium-resistant mutant in rice. Rice 9(1):60
Mackay I, Powell W (2007) Methods for linkage disequilibrium mapping in crops. Trends Plant Sci 12(5):7–63
Mazumder A, Rohilla M, Bisht D, Krishnamurthy S, Barman M, Sarma R et al (2020) Identification and mapping of quantitative trait loci (QTL) and epistatic QTL for salinity tolerance at seedling stage in traditional aromatic short grain rice landrace Kolajoha (Oryzasativa L.) of Assam, India. Euphytica 216:75
McWilliam JR (1986) The national and international importance of drought and salinity effects on agricultural production. Funct Plant Biol 13:1–13
Millar A, Rathjen A, Cooper D (2007) Genetic variation for subsoil toxicities in high pH soils. In: Buck HT, Nisi JE, Salomön N (eds) Wheat production in stressed environments. Springer, pp 395–401
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681
Negrao S, Courtois B, Ahmadi N, Abreu I, SaiboNand OMM (2011) Recent updates on salinity stress in rice: from physiological to molecular responses. Crit Rev Plant Sci 30:329–377
Pan Y, Chen L, Yang X, et al (2020) Mapping quantitative trait loci for cold tolerance in rice under germination stage by whole genome resequencing and analysis of candidate genes. Guangxi Academy AgriSci https://orcid.org/0000-0003-0782-6158
Pandit A, Rai V, Bal S, Sinha S, Kumar V, Chauhan M et al (2010) Combining QTL mapping and transcriptome profiling of bulked RILs for identification of functional polymorphism for salt tolerance genes in rice (Oryzasativa L.). Mol Genet Genomics 284:121–136
Ponce K, Zhang Y, Guo L et al (2020) Genome-wide association study of grain size traits in indica rice multiparent advanced generation Intercross (MAGIC) population. Front Plant Sci. https://doi.org/10.3389/fpls.2020.00395
Pundir P, Sharma P, Krishnamurthy S, Devi A, Warraich A, Sharma A (2016) Utilization of salt stress indices and genetic variability in F2 population (PS5×CSR10) of rice for salinity tolerance at reproductive stage. J Soil Salin Water Quality 8:14–24
Raghavan C, Mauleon R, Lacorte V, Jubay M, Zaw H, Bonifacio J, Singh RK, Huang BE, Leung H (2017) Approaches in characterizing genetic structure and mapping in a rice multiparental population. G3: Genes Genomes Genetics 7(6):1721–1730. https://doi.org/10.1534/g3.117.042101
Ren Z, Gao J, Li L, Cai X, Huang W, Chao D et al (2005) A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat Genet 37:1141–1146
Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn SJ, Ryan PR, Matsumoto H (2004) A wheat gene encoding an aluminum-activated malate transporter. Plant J 37:645–653. https://doi.org/10.1111/j.1365-313X.2003.01991.x
Singh R, Flowers T (2010) The physiology and molecular biology of the effects of salinity on rice. In: Pessarakli M (ed) Handbook of plant and crop stress. Handbook of Plant and Crop Stress, 3rd edn. Taylor and Francis, Florida, pp 901–942
Singh R, Redoña E, Refuerzo L (2010) Varietal improvement for abiotic stress tolerance in crop plants, special reference to salinity in rice. In: Pareek A, Sopory SK, Bohnert HJ, Govindjee (eds) Abiotic stress adaptation in plants, physiological, molecular and genomic foundation. Springer, New York, pp 387–415
Singh Y, Singh D, Sharma S, Krishnamurthy S (2013) Evaluation of rice genotypes for yield, physiological and biological traits in sodic soil. J Soil Salin Water Quality 5:40–49
Singh Y, Singh D, Krishnamurthy S (2014) Grouping of advanced rice breeding lines based on grain yield and Na: K ratio under alkaline conditions. J Soil Salin Water Quality. 6:21–27
Singh R, Singh Y, Xalaxo S, Verulkar S, Yadav N, Singh S et al (2016) From QTL to variety-harnessing the benefits of QTLs for drought, flood and salt tolerance in mega rice varieties of India through a multi-institutional network. Plant Sci 242:278–287
Storey J, Tibshirani R (2003) Statistical significance for genome wide studies. Proc Natl Acad Sci 100:9440–9445
Tack J, Singh R, Nalley L, Viraktamath B, Krishnamurthy S, Lyman N et al (2015) High vapor pressure deficit drives salt-stress-induced rice yield losses in India. Glob Change Biol 21:1668–1678
Thomson M, De Ocampo M, Egdane J, Rahman M, Sajise A, Adorada D et al (2010) Characterizing the Saltol quantitative trait locus for salinity tolerance in rice. Rice 3:148–160
Tiwari S, Krishnamurthy S, Kumar V, Singh B, Rao A, Mithra S et al (2016) Mapping QTLs for salt tolerance in rice (Oryzasativa L.) by bulked segregant analysis of recombinant inbred lines using 50K SNP Chip. PLoS ONE 11:e0153610
Tuan V, Fukuta Y, Mand Ban T (2000) Mapping quantitative trait loci for salinity tolerance in rice. Omonrice 8:27–35
Turner S (2014) qqman: an R package for visualizing GWAS results using Q-Q and manhattan plots. bioRxiv. https://doi.org/10.1101/005165
Visscher P, Brown M, McCarthy M, Yang J (2012) Five years of GWAS discovery. Am J Human Genet 90:7–24
Warraich A, Krishnamurthy S, Sooch B, Vinaykumar N, Dushyanthkumar B, Bose J et al (2020) Rice GWAS reveals key genomic regions essential for salinity tolerance at reproductive stage. Acta Physiol Plant 42:134
Xiong Y, DeFraia C, Williams D, Zhang X, Mou Z (2009) Deficiency in a cytosolic ribose-5-phosphate isomerase causes chloroplast dysfunction, late flowering and premature cell death in Arabidopsis. Physiol Plant 137:249–263
Yadav A, Kumar A, Grover N, Ellur R, Krishnan S, Bollinedi H et al (2020) Marker aided introgression of “Saltol”, a major QTL for seedling stage salinity tolerance into an elite Basmati rice variety “Pusa Basmati 1509.” Sci Rep 10(1):13877
Yoshida S, Forno D, Cock J, Gomez K (1976) Laboratory manual for physiological studies of rice. IRRI, Las Banos
Zeng L, Shannon MC (2000a) Salinity effects on seedling growth and yield components of rice. Crop Sci 40:996–1003
Zeng L, Shannon MC (2000b) Effects of salinity on grain yield and yield components of rice at different seeding densities. Agron J 92:418–423
Zhang Z, Ersoz E, Lai C, Todhunter R, Tiwari H, Gore M et al (2010) Mixed linear model approach adapted for genome-wide association studies. Nat Genet 42:355–360
Zhang Y, Zhao J, Li Y et al (2010) Transcriptome analysis highlights defense and signaling pathways mediated by rice pi21 gene with partial resistance to magnaportheoryzae. Front Plant Sci 7:1834
Acknowledgements
We thank Indian Council of Agricultural Research (ICAR), India and International Rice Research Institute (IRRI), Philippines for funding and sparing breeding materials, the GWAS, MAGIC team at IRRI for sparing GBS data and advice in data analysis and Central Soil Salinity Research Institute Karnal (PME Cell reference no Research Article/95/2019).
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SLK, PCS, RKS, HL design the experiment, edit the manuscript, SLK, ASW conducted experiments, draft the manuscript and analyze the data, DD, SR NMV, ASW, BML performed the analysis of data, wrote and revised the manuscript.
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Krishnamurthy, S.L., Sharma, P.C., Dewan, D. et al. Genome wide association study of MAGIC population reveals a novel QTL for salinity and sodicity tolerance in rice. Physiol Mol Biol Plants 28, 819–835 (2022). https://doi.org/10.1007/s12298-022-01174-8
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DOI: https://doi.org/10.1007/s12298-022-01174-8