Skip to main content
Log in

Development of low-temperature germinability markers for evaluation of rice (Oryza sativa L.) germplasm

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

Low-temperature germinability (LTG) is an important trait for breeding of varieties for use in direct-seeding rice production systems. Although rice (Oryza sativa L.) is generally sensitive to low temperatures, genetic variation for LTG exists and several quantitative trait loci (QTLs) have been reported. Most notably, the gene underlying the major effect QTL qLTG3-1 has been cloned and implicated in tissue weakening. The objective of this study was to develop molecular markers for use in selecting rice germplasm with enhanced LTG. A panel of japonica rice accessions (n = 180) from temperate regions in Asia was evaluated for LTG and genotyped with markers from qLTG3-1 and regions previously reported to harbor other LTG QTLs. In addition to the germplasm evaluation using these markers, an association analysis was conducted using SNP data generated by reduced representation sequencing of the panel. Eight SNP markers were found to be significantly associated with LTG using general and mixed linear models. Two of these markers were in close proximity (~35 kb) to each other on chromosome 4 in a region previously linked to LTG in rice. The identification of several markers strongly associated with LTG in locations not previously reported provides a foundation for further genetic dissection of this complex trait.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Andaya VC, Mackill DJ (2003) Mapping of QTLs associated with cold tolerance during the vegetative stage in rice. J Exp Bot 54:2579–2585

    Article  CAS  PubMed  Google Scholar 

  • Arai-Kichise Y, Shiwa Y, Ebana K, Shibata-Hatta M, Yoshikawa H, Yano M, Wakasa K (2014) Genome-wide DNA polymorphisms in seven rice cultivars of temperate and tropical japonica groups. PLoS One 9:e86312

    Article  PubMed Central  PubMed  Google Scholar 

  • Challam C, Kharshing GA, Yumnam JS, Rai M, Tyagi W (2013) Association of qLTG3-1 with germination stage cold tolerance in diverse rice germplasm from the Indian subcontinent. Plant Genet Resour-C 11:206–211

    Article  CAS  Google Scholar 

  • Chen L, Lou QJ, Sun ZX, Xing YZ, Yu XQ, Luo LJ (2006) QTL mapping of low temperature on germination rate of rice. Rice Sci 13:93–98

    Google Scholar 

  • Chen H, He H, Zou Y, Chen W, Yu R, Liu X, Yang Y, Gao YM, Xu JL, Fan LM, Li Y, Li ZK, Deng XW (2011) Development and application of a set of breeder-friendly SNP markers for genetic analyses and molecular breeding of rice (Oryza sativa L.). Theor Appl Genet 123:869–879

    Article  PubMed  Google Scholar 

  • Courtois B, Audebert A, Dardou A, Roques S, Ghneim-Herrera T, Droc G, Frouin J, Rouan L, Gozé E, Kilian A, Ahmadi N, Dingkuhn M (2013) Genome-wide association mapping of root traits in a japonica rice panel. PLoS One 8:e78037

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cui KH, Peng SB, Xing YZ, Xu CG, Yu SB, Zhang Q (2002) Molecular dissection of seedling-vigor and associated physiological traits in rice. Theor Appl Genet 105:745–753

    Article  CAS  PubMed  Google Scholar 

  • Fujino K, Sekiguchi H (2011) Origins of functional nucleotide polymorphisms in a major quantitative trait locus, qLTG3-1, controlling low-temperature germinability in rice. Plant Mol Biol 75:1–10

    Article  CAS  PubMed  Google Scholar 

  • Fujino K, Sekiguchi H, Sato T, Kiuchi H, Nonoue Y, Takeuchi Y, Ando T, Lin SY, Yano M (2004) Mapping of quantitative trait loci controlling low-temperature germinability in rice (Oryza sativa L.). Theor Appl Genet 108:794–799

    Article  CAS  PubMed  Google Scholar 

  • Fujino K, Sekiguchi H, Matsuda Y, Sugimoto K, Ono K, Yano M (2008) Molecular identification of a major quantitative trait locus, qLTG3-1, controlling low-temperature germinability in rice. Proc Natl Acad Sci USA 105:12623–12628

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Han LZ, Zhang YY, Qiao YL, Cao GL, Zhang SY, Kim JH, Koh HJ (2006) Genetic and QTL analysis for low-temperature vigor of germination in rice. Acta Genet Sin 33:998–1006

    Article  CAS  PubMed  Google Scholar 

  • Henry IM, Nagalakshmi U, Lieberman M, Ngo KJ, Krasileva KV, Vasquez-Gross H, Akhunova A, Akhunov E, Dubcovsky J, Tai TH, Comai L (2014) Efficient genome-wide detection and cataloging of EMS-induced mutations using exome capture and next-generation sequencing. Plant Cell 26:1382–1397

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Huang X, Wei X, Sang T, Zhao Q, Feng Q, Zhao Y, Li C, Zhu C, Lu T, Zhang Z, Li M, Fan D, Guo Y, Wang A, Wang L, Deng L, Li W, Lu Y, Weng Q, Liu K, Huang T, Zhou T, Jing Y, Li W, Lin Z, Buckler ES, Qian Q, Zhang Q, Li J, Han B (2010) Genome-wide association studies of 14 agronomic traits in rice landraces. Nat Genet 42:961–967

    Article  CAS  PubMed  Google Scholar 

  • Ji SL, Jiang L, Wang YH, Liu SJ, Liu X, Zhai HQ, Atsushi Y, Wan JM (2008) QTL and epistasis for low temperature germinability in rice. Acta Agron Sin 34:551–556

    Article  CAS  Google Scholar 

  • Ji SL, Jiang L, Wang YH, Zhang WW, Liu X, Liu SJ, Chen LM, Zhai HQ, Wan JM (2009) Quantitative trait loci mapping and stability for low temperature germination ability of rice. Plant Breed 128:387–392

    Article  Google Scholar 

  • Jiang L, Liu SJ, Hou MY, Tang JY, Chen LM, Zhai HQ, Wan JM (2006) Analysis of QTLs for seed low temperature germinability and anoxia germinability in rice (Oryza sativa L.). Field Crops Res 98:68–75

    Article  Google Scholar 

  • Kharabian-Masouleh A, Waters DLE, Reinke RF, Ward R, Henry RJ (2012) SNP in starch biosynthesis genes associated with nutritional and functional properties of rice. Sci Rep 2:557. doi:10.1038/srep00557

    Article  PubMed Central  PubMed  Google Scholar 

  • Kim SI, Tai TH (2013) Identification of SNPs in closely related temperate japonica rice cultivars using restriction enzyme-phased sequencing. PLoS One. doi:10.1371/journal.pone.0060176

    Google Scholar 

  • Ko JC, Baek MK, Kim WJ, Shon JY, Ha KY, Kang HJ, Shin MS, Ko JK (2011) Analysis of low temperature germination ratio in rice cultivars for breeding of direct seeding variety. Korean J Intl Agric 23:89–94

    Google Scholar 

  • Kotaka S, Abe N (1988) The varietal difference of germinability at low-temperature in rice varieties and the testing method for the percentage establishment of seedlings. J Agric Sci Tokyo 43:165–168

    Google Scholar 

  • Kumar V, Ladha JK (2011) Direct seeding of rice: recent developments and future research needs. In: Sparks DL (ed) Advances in agronomy 111. Academic Press, London, pp 297–413

    Chapter  Google Scholar 

  • Larsson SJ, Lipka AE, Buckler ES (2013) Lessons from Dwarf8 on the strengths and weaknesses of structured association mapping. PLoS Genet 9:e1003246

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079

    Article  PubMed Central  PubMed  Google Scholar 

  • Li LF, Liu X, Xie K, Wang YH, Liu F, Lin QY, Wang WY, Yang CY, Lu BY, Liu SJ, Chen LM, Jiang L, Wan JM (2013) qLTG-9, a stable quantitative trait locus for low-temperature germination in rice (Oryza sativa L.). Theor Appl Genet 126:2313–2322

    Article  CAS  PubMed  Google Scholar 

  • Mammadov J, Aggarwal R, Buyyarapu R, Kumpatla S (2012) SNP markers and their impact on plant breeding. Int J Plant Genomics 2012:728398

    Article  PubMed Central  PubMed  Google Scholar 

  • Monson-Miller J, Sanchez-Mendez DC, Fass J, Henry IM, Tai TH, Comai L (2012) Reference genome-independent assessment of mutation density using restriction enzyme-phased sequencing. BMC Genomics 13:72

  • Miura K, Lin SY, Yano M, Nagamine T (2001) Mapping quantitative trait loci controlling low temperature germinability in rice (Oryza sativa L.). Breed Sci 51:293–299

    Article  CAS  Google Scholar 

  • Nandi S, Subudhi PK, Senadhira D, Manigbas NL, Sen-Mandi S, Huang N (1997) Mapping QTLs for submergence tolerance in rice by AFLP analysis and selective genotyping. Mol Gen Genet 255:1–8

    Article  CAS  PubMed  Google Scholar 

  • Narayanan NN, Baisakh N, Oliva NP, VeraCruz CM, Gnanamanickam SS, Datta K, Datta SK (2004) Molecular breeding: marker-assisted selection combined with biolistic transformation for blast and bacterial blight resistance in Indica rice (cv. CO39). Mol Breed 14:61–71

    Article  CAS  Google Scholar 

  • Niedziela A, Bednarek PT, Cichy H, Budzianowski G, Kilian A, Anioł A (2012) Aluminum tolerance association mapping in triticale. BMC Genom 13:67

    Article  CAS  Google Scholar 

  • Nordborg M, Weigel D (2008) Next-generation genetics in plants. Nature 456:720–723

    Article  CAS  PubMed  Google Scholar 

  • Park IK, Oh CS, Kim DM, Yeo SM, Ahn SN (2013) QTL mapping for cold tolerance at the seedling stage using introgression lines derived from an intersubspecific cross in rice. Plant Breed Biotech 1:1–8

    Article  Google Scholar 

  • Pereira da Cruz R, Milach SCK, Federizzi LC (2006) Inheritance of rice cold tolerance at the germination stage. Genet Mol Biol 29:314–320

    Article  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

  • Rao AN, Johnson DE, Sivaprasad B, Ladha JK, Mortimer AM (2007) Weed management in direct-seeded rice. Adv Agron 93:153–255

    Article  CAS  Google Scholar 

  • RDA (2012) Standard protocol of research method and analysis. Rural Development Administration, Suwon, p 322

    Google Scholar 

  • Septiningsih E, Ignacio JIC, Sendon PMD, Sanchez DL, Ismail A, Mackill DJ (2013) QTL mapping and confirmation for tolerance of anaerobic conditions during germination derived from the rice landrace Ma-Zhan Red. Theor Appl Genet 126:1357–1366

    Article  PubMed  Google Scholar 

  • Sipaseuth Basnayake J, Fukai S, Farrell TC, Senthonghae M, Sengkeo Phamixay S, Linquist B, Chanphengsay M (2007) Opportunities to increasing dry season rice productivity in low temperature affected areas. Field Crops Res 102:87–97

    Article  Google Scholar 

  • Takahashi N (1997) Inheritance of seed germination and dormancy. In: Matsuo T, Futsuhara Y, Kikuchi F, Yamaguchi H (eds) The science of the rice plant. Food and Agriculture Policy Research Center, Tokyo, pp 348–359

    Google Scholar 

  • Teng S, Zeng DL, Qian Q, Kunihifo Y, Huang DN, Zhu LH (2001) QTL analysis of rice low temperature germinability. Chin Sci Bull 46:1800–1803

    Article  Google Scholar 

  • Wang ZF, Wang JF, Wang FH, Bao YM, Wu YY, Zhang HS (2009) Genetic control of germination ability under cold stress in rice. Rice Sci 16:173–180

    Article  Google Scholar 

  • Wang ZF, Wang FH, Zhou R, Wang JF, Zhang HS (2011) Identification of quantitative trait loci for cold tolerance during the germination and seedling stages in rice (Oryza sativa L.). Euphytica 181:405–413

    Article  Google Scholar 

  • Xu X, Liu X, Ge S, Jensen D, Hu F, Li X, Dong Y, Gutenkunst RN, Fang L, Huang L, Li J, He W, Zhang G, Zheng X, Zhang F, Li Y, Yu C, Kristiansen K, Zhang X, Wang J, Wright M, McCouch S, Nielsen R, Wang J, Wang W (2011) Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes. Nat Biotechnol 30:105–111

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Rural Development Administration (RDA) of the Republic of Korea through the RDA/USDA-ARS Virtual Laboratory program (D.Y.H. and T.H.T.) and by the “Research Program for Agricultural Science & Technology Development (Project No. PJ008368 and PJ010871)” of the National Academy of Agricultural Science, RDA (D.Y.H). Additional support was provided by USDA-ARS CRIS Project 5306-21000-021-00D (T.H.T.). This work used the Vincent J. Coates Genomics Sequencing Laboratory at UC Berkeley, supported by NIH S10 Instrumentation Grants S10RR029668 and S10RR027303.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Thomas H. Tai.

Additional information

Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture. USDA is an equal opportunity provider and employer.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 1273 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hyun, D.Y., Lee, G.A., Kang, M.J. et al. Development of low-temperature germinability markers for evaluation of rice (Oryza sativa L.) germplasm. Mol Breeding 35, 104 (2015). https://doi.org/10.1007/s11032-015-0298-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11032-015-0298-1

Keywords

Navigation