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Haplotype distribution and association of candidate genes with salt tolerance in Indian wild rice germplasm

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The association of natural genetic variations of salt-responsive candidate genes belonging to different gene families with salt-tolerance phenotype and their haplotype variation in different geographic regions.

Abstract

Soil salinity covers a large part of the arable land of the world and is a major factor for yield losses in salt-sensitive crops, such as rice. Different gene families that respond to salinity have been identified in rice, but limited success has been achieved in developing salt-tolerant cultivars. Therefore, 21 salt stress-responsive candidate genes belonging to different gene families were re-sequenced to analyse their genetic variation and association with salt tolerance. The average single nucleotide polymorphism (SNP) density was 16 SNPs per kbp amongst these genes. The identified nucleotide and haplotype diversity showed comparatively higher genetic variation in the transporter family genes. Linkage disequilibrium (LD) analysis showed significant associations of SNPs in BADH2, HsfC1B, MIPS1, MIPS2, MYB2, NHX1, NHX2, NHX3, P5CS1, P5CS2, PIP1, SIK1, SOS1, and SOS2 genes with the salt-tolerant phenotype. A combined analysis of SNPs in the 21 candidate genes and eight other HKT transporter genes produced two separate clusters of tolerant genotypes, carrying unique SNPs in the ion transporter and osmoticum-related genes. Haplotype network analysis showed all the major and few minor alleles distributed over distant geographic regions. Minor haplotypes may be recently evolved alleles which migrated to distant geographic regions and may represent recent expansion of Indian wild rice. The analysis of genetic variation in different gene families identified the relationship between adaptive variations and functional significance of the genes. Introgression of the identified alleles from wild relatives may enhance the salt tolerance and consequently rice production in the salinity-affected areas.

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References

  • Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signalling. Plant Cell 15:63–78

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  CAS  PubMed  Google Scholar 

  • Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635

    Article  CAS  PubMed  Google Scholar 

  • Brar D, Khush G (2003) Utilization of wild species of genus Oryza in rice improvement. Science Publishers, Enfield

    Google Scholar 

  • Chen S, Yang Y, Shi W et al (2008) Badh2, encoding betaine aldehyde dehydrogenase, inhibits the biosynthesis of 2-acetyl-1-pyrroline, a major component in rice fragrance. Plant Cell 20:1850–1861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Das-Chatterjee A, Goswami L, Maitra S, Dastidar KG, Ray S, Majumder AL (2006) Introgression of a novel salt-tolerant l-myo-inositol 1-phosphate synthase from Porteresia coarctata (Roxb.) Tateoka (PcINO1) confers salt tolerance to evolutionary diverse organisms. FEBS Lett 580:3980–3988

    Article  CAS  PubMed  Google Scholar 

  • Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors Trends. Plant Sci 5:199–206

    Article  CAS  Google Scholar 

  • FAO, UN (2009) How to feed the world in 2050. In: High-Level Expert Forum, Rome

  • Fukuda A, Nakamura A, Hara N, Toki S, Tanaka Y (2011) Molecular and functional analyses of rice NHX-type Na+/H+ antiporter genes. Planta 233:175–188

    Article  CAS  PubMed  Google Scholar 

  • Ghomi K, Rabiei B, Sabouri H, Sabouri A (2013) Mapping QTLs for traits related to salinity tolerance at seedling stage of rice (Oryza sativa L.): an agrigenomics study of an Iranian rice population. OMICS 17:242–251

    Article  CAS  PubMed  Google Scholar 

  • Gouiaa S, Khoudi H, Leidi EO, Pardo JM, Masmoudi K (2012) Expression of wheat Na+/H+ antiporter TNHXS1 and H+-pyrophosphatase TVP1 genes in tobacco from a bicistronic transcriptional unit improves salt tolerance. Plant Mol Biol 79(1–2):137–155

    Article  CAS  PubMed  Google Scholar 

  • Gregorio GB, Senadhira D, Mendoza RD (1997) Screening rice for salinity tolerance. International Rice Research Institute discussion paper series, Metro Manila

    Google Scholar 

  • Hall T (2011) BioEdit: an important software for molecular biology. GERF Bull Biosci 2:60–61

    Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acid Res 27:297–300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horie T, Costa A, Kim TH et al (2007) Rice OsHKT2; 1 transporter mediates large Na+ influx component into K+-starved roots for growth. EMBO J 26:3003–3014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hur J, Jung K-H, Lee C-H, An G (2004) Stress-inducible OsP5CS2 gene is essential for salt and cold tolerance in rice. Plant Sci 167:417–426

    Article  CAS  Google Scholar 

  • Jacobs M, Angenon G, Hermans C, Thu TT, Roosens NH (2003) Proline accumulation and Δ 1-pyrroline-5-carboxylate synthetase gene properties in three rice cultivars differing in salinity and drought tolerance. Plant Sci 165:1059–1068

    Article  Google Scholar 

  • Khush GS, Ling K (1974) Inheritance of resistance to grassy stunt virus and its vector in rice. J Hered 65:135–136

    Google Scholar 

  • Kumar K, Kumar M, Kim S-R, Ryu H, Cho Y-G (2013) Insights into genomics of salt stress response in rice. Rice 6:27

    Article  PubMed  PubMed Central  Google Scholar 

  • Kurokawa Y, Noda T, Yamagata Y et al (2016) Construction of a versatile SNP array for pyramiding useful genes of rice. Plant Sci 242:131–139

    Article  CAS  PubMed  Google Scholar 

  • Lestari P, Lee G, Ham T-H et al (2011) Single nucleotide polymorphisms and haplotype diversity in rice sucrose synthase 3. J Hered 102:735–746

    Article  CAS  PubMed  Google Scholar 

  • Li R, Li L, Wei S et al. (2010) The evaluation and utilization of new genes for brown planthopper resistance in common wild rice (Oryza rufipogon Griff.). Mol Entomol 1:1–7

    Google Scholar 

  • Liu C, Fukumoto T, Matsumoto T et al (2013) Aquaporin OsPIP1; 1 promotes rice salt resistance and seed germination. Plant Physiol Biochem 63:151–158

    Article  CAS  PubMed  Google Scholar 

  • Liu C, Mao B, Ou S et al (2014) OsbZIP71, a bZIP transcription factor, confers salinity and drought tolerance in rice. Plant Mol Biol 84:19–36

    Article  CAS  PubMed  Google Scholar 

  • Londo JP, Chiang Y-C, Hung K-H, Chiang T-Y, Schaal BA (2006) Phylogeography of Asian wild rice, Oryza rufipogon, reveals multiple independent domestications of cultivated rice, Oryza sativa. Proc Natl Acad Sci USA 103:9578–9583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maclean J, Hardy B, Hettel G (2013) Introduction and setting. Rice Almanac: source book for one of the most important economic activities on earth, 4th edn. GRiSP, IRRI, USA, pp 1–14

    Google Scholar 

  • Martinez-Atienza J, Jiang X, Garciadeblas B, Mendoza I, Zhu J (2007) Conservation of the SOS pathway for salt-tolerance in rice. Plant Physiol 143:1001–1012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McNally KL, Childs KL, Bohnert R et al (2009) Genomewide SNP variation reveals relationships among landraces and modern varieties of rice. Proc Natl Acad Sci USA 106:12273–12278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mercer J (2010) Disaster risk reduction or climate change adaptation: are we reinventing the wheel? J Int Dev 22:247–264

    Article  Google Scholar 

  • Mishra S, Singh B, Panda K et al (2016) Association of SNP haplotypes of HKT family genes with salt tolerance in Indian wild rice germplasm. Rice 9:1

    Article  Google Scholar 

  • Murray M, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nuclic Acid Res 8:4321–4326

    Article  CAS  Google Scholar 

  • Nakamura T, Yokota S, Muramoto Y, Tsutsui K, Oguri Y, Fukui K, Takabe T (1997) Expression of a betaine aldehyde dehydrogenase gene in rice, a glycinebetaine nonaccumulator, and possible localization of its protein in peroxisomes. Plant J 11:1115–1120

    Article  CAS  PubMed  Google Scholar 

  • Negrão S, Cecília Almadanim M, Pires IS et al (2013) New allelic variants found in key rice salt-tolerance genes: an association study. Plant Biotechnol J 11:87–100

    Article  PubMed  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Ohta M, Guo Y, Halfter U, Zhu J-K (2003) A novel domain in the protein kinase SOS2 mediates interaction with the protein phosphatase 2C ABI2. Proc Natl Acad Sci USA 100:11771–11776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ouyang SQ, Liu YF, Liu P et al (2010) Receptor-like kinase OsSIK1 improves drought and salt stress tolerance in rice (Oryza sativa) plants. Plant J 62:316–329

    Article  CAS  PubMed  Google Scholar 

  • Platten JD, Egdane JA, Ismail AM (2013) Salinity tolerance, Na + exclusion and allele mining of HKT1; 5 in Oryza sativa and O. glaberrima: many sources, many genes, one mechanism? BMC Plant Biol 13:1

    Article  Google Scholar 

  • Ren Z-H, Gao J-P, Li L-G et al (2005) A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat Genet 37:1141–1146

    Article  CAS  PubMed  Google Scholar 

  • Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP (2011) Integrative genomics viewer. Nat Biotechnol 29:24–26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  CAS  PubMed  Google Scholar 

  • Schmidt R, Schippers JH, Welker A, Mieulet D, Guiderdoni E, Mueller-Roeber B (2012) Transcription factor OsHsfC1b regulates salt tolerance and development in Oryza sativa ssp. Japonica. AoB Plants 2012:pls011

    Article  PubMed  PubMed Central  Google Scholar 

  • Sengupta S, Patra B, Ray S, Majumder AL (2008) Inositol methyl transferase from a halophytic wild rice, Porteresia coarctata Roxb. (Tateoka): regulation of pinitol synthesis under abiotic stress. Plant Cell Environ 31:1442–1459

    Article  CAS  PubMed  Google Scholar 

  • Serrano R, Rodriguez-Navarro A (2001) Ion homeostasis during salt stress in plants. Curr Opin Cell Biol 13:399–404

    Article  CAS  PubMed  Google Scholar 

  • Shaw RG, Etterson JR (2012) Rapid climate change and the rate of adaptation: insight from experimental quantitative genetics. New Phytol 195:752–765

    Article  PubMed  Google Scholar 

  • Singh B, Bohra A, Mishra S, Joshi R, Pandey S (2015a) Embracing new-generation ‘omics’ tools to improve drought tolerance in cereal and food-legume crops. Biol Plant 59:413–428

    Article  CAS  Google Scholar 

  • Singh BP, Jayaswal PK, Singh B et al (2015b) Natural allelic diversity in OsDREB1F gene in the Indian wild rice germplasm led to ascertain its association with drought tolerance. Plant Cell Rep 34:993–1004

    Article  CAS  PubMed  Google Scholar 

  • Singh BP, Singh B, Kumar V, Singh PK, Jayaswal PK, Mishra S, Singh NK (2015c) Haplotype diversity and association analysis of SNAC1 gene in wild rice germplasm. Indian J Genet Pl Br 75(2):157–166

    Article  CAS  Google Scholar 

  • Singh R, Singh Y, Xalaxo S, Verulkar S et al (2015d) 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

    Article  PubMed  Google Scholar 

  • Singh N, Jayaswal PK, Panda K, Mandal P et al (2015e) Single-copy gene based 50 K SNP chip for genetic studies and molecular breeding in rice. Sci Rep 5:11600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singla-Pareek SL, Yadav SK, Pareek A, Reddy M, Sopory S (2008) Enhancing salt tolerance in a crop plant by overexpression of glyoxalase II. Transgenic Res 17:171–180

    Article  CAS  PubMed  Google Scholar 

  • Stern DL, Orgogozo V (2008) The loci of evolution: how predictable is genetic evolution? Evolution 62:2155–2177

    Article  PubMed  PubMed Central  Google Scholar 

  • Storz JF, Wheat CW (2010) Integrating evolutionary and functional approaches to infer adaptation at specific loci. Evolution 64:2489–2509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acid Res 22:4673–4680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thorvaldsdóttir H, Robinson JT, Mesirov JP (2013) Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 14:178–192

    Article  PubMed  Google Scholar 

  • Turral H, Burke J, Faures JM (2011) Climate change, water and food security. FAO

  • Watterson G (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:256–276

    Article  CAS  PubMed  Google Scholar 

  • Watterson G, Guess H (1977) Is the most frequent allele the oldest? Theor Popul Biol 11:141–160

    Article  CAS  PubMed  Google Scholar 

  • Xiang Y, Tang N, Du H, Ye H, Xiong L (2008) Characterization of OsbZIP23 as a key player of the basic leucine zipper transcription factor family for conferring abscisic acid sensitivity and salinity and drought tolerance in rice. Plant Physiol 148:1938–1952

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu X, Liu X, Ge S et al (2012) Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes. Nat Biotechnol 30:105–111

    Article  CAS  Google Scholar 

  • Yang A, Dai X, Zhang W-H (2012) A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J Exp Bot 63:err431

    Google Scholar 

  • Yuan S-C, Zhang Z-G, He H-H, Zen H-L, Lu K-Y, Lian J-H, Wang B-X (1993) Two photoperiodic-reactions in photoperiod-sensitive genic male-sterile rice. Crop Sci 33:651–660

    Article  Google Scholar 

  • Zhu J-K (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The financial assistance from the Indian Council of Agricultural Research through National Professor B. P. Pal Chair project is gratefully acknowledged. We are thankful to the National Bureau of Plant Genetic Resources, New Delhi, India for providing seeds of 58 wild rice accessions.

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Correspondence to Nagendra Kumar Singh.

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Communicated by M. Prasad.

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Mishra, S., Singh, B., Misra, P. et al. Haplotype distribution and association of candidate genes with salt tolerance in Indian wild rice germplasm. Plant Cell Rep 35, 2295–2308 (2016). https://doi.org/10.1007/s00299-016-2035-6

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  • DOI: https://doi.org/10.1007/s00299-016-2035-6

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