Molecular Genetics and Genomics

, Volume 289, Issue 3, pp 333–343 | Cite as

QTL mapping and development of candidate gene-derived DNA markers associated with seedling cold tolerance in rice (Oryza sativa L.)

  • Suk-Man Kim
  • Jung-Pil Suh
  • Chung-Koon Lee
  • Jeong-Heui Lee
  • Yeong-Gyu Kim
  • Kshirod Kumar Jena
Original Paper

Abstract

Cold stress at the seedling stage is a major threat to rice production. Cold tolerance is controlled by complex genetic factors. We used an F7 recombinant inbred line (RIL) population of 123 individuals derived from a cross of the cold-tolerant japonica cultivar Jinbu and the cold-susceptible indica cultivar BR29 for QTL mapping. Phenotypic evaluation of the parents and RILs in an 18/8 °C (day/night) cold stress regime revealed continuous variation for cold tolerance. Six QTLs including two on chromosome 1 and one each on chromosomes 2, 4, 10, and 11 for seedling cold tolerance were identified with phenotypic variation (R 2) ranging from 6.1 to 16.5 %. The QTL combinations (qSCT1 and qSCT11) were detected in all stable cold-tolerant RIL groups, which explained the critical threshold of 27.1 % for the R 2 value determining cold tolerance at the seedling stage. Two QTLs (qSCT1 and qSCT11) on chromosomes 1 and 11, respectively, were fine mapped. The markers In1-c3, derived from the open reading frame (ORF) LOC_Os01g69910 encoding calmodulin-binding transcription activator (CAMTA), and In11-d1, derived from ORF LOC_Os11g37720 (Duf6 gene), co-segregated with seedling cold tolerance. The result may provide useful information on seedling cold tolerance mechanism and provide DNA markers for a marker-assisted breeding program to improve seedling cold tolerance in indica rice varieties.

Keywords

Rice Seedling cold tolerance QTL Candidate genes DNA marker 

Abbreviations

AFGP

Antifreeze glycoprotein

BAC

Bacterial artificial chromosome

CAMTA

Calmodulin-binding transcription activator

CBF

C-repeat binding factor

CBS

Cystathionine β-synthase

CDS

Cold damage score

CIM

Composite interval mapping

CT

Cold treatment

GST

Glutathione S-transferase

InDel

Insertion–deletion polymorphisms

LOD

Logarithm of odds

R2

Phenotypic variance

LTH

Lijianxintuanheigu

ORF

Open reading frame

QTL

Quantitative trait loci

RIL

Recombinant inbred line

RP

Recovery period

SPV

Sum of phenotypic variation

SSR

Simple sequence repeat

Notes

Acknowledgments

This research was supported in part by a grant to the Temperate Rice Research Consortium (TRRC) and Agenda Program (Code No. PJ0068272011) of the Rural Development Administration, Republic of Korea. We thank Dr. Benildo De Los Reyes, University of Maine, Orono, Maine, USA for a critical review and suggestions to improve the manuscript. We thank Bill Hardy, senior science editor of IRRI, for editing the manuscript.

References

  1. Andaya VC, Mackill DJ (2003) Mapping of QTLs associated with cold tolerance during the vegetative stage in rice. J Exp Bot 54:2579–2585PubMedCrossRefGoogle Scholar
  2. Andaya VC, Tai TH (2006) Fine mapping of the qCTS12 locus, a major QTL for seedling cold tolerance in rice. Theor Appl Genet 113:467–475PubMedCrossRefGoogle Scholar
  3. Andaya VC, Tai TH (2007) Fine mapping of the qCTS4 locus associated with seedling cold tolerance in rice (Oryza sativa L.). Mol Breed 20:349–358CrossRefGoogle Scholar
  4. Baek KH, Skinner DZ (2003) Alteration of antioxidant enzyme gene expression during cold acclimation of near-isogenic wheat lines. Plant Sci 165:1221–1227CrossRefGoogle Scholar
  5. Churchill GA, Doerge RW (1994) Empirical threshold value for quantitative trait mapping. Genetics 138:963–971PubMedCentralPubMedGoogle Scholar
  6. De los Reyes BG, Morsy M, Gibbons J, Varma TS, Antoine W, McGrath JM, Halgren R, Redus M (2003) A snapshot of the low temperature stress transcriptome of developing rice seedlings (Oryza sativa L.) via ESTs from a subtracted cDNA library. Theor Appl Genet 107:1071–1082PubMedCrossRefGoogle Scholar
  7. Dingkuhn M, De Datta SK, Pamplona R, Javellana C, Schnier HF (1992) Effect of late-season N-fertilization on photosynthesis and the yield of transplanted and direct-seeded tropical flooded rice I. Growth dynamics. Field Crops Res 28:235–249CrossRefGoogle Scholar
  8. Doherty CJ, Van Buskirk HA, Myers SJ, Thomashow MF (2009) Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance. Plant Cell 21:972–984PubMedCentralPubMedCrossRefGoogle Scholar
  9. 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 108:794–799PubMedCrossRefGoogle Scholar
  10. Griffith M, Lumb C, Wiseman SB, Wisniewski M, Johnson RW, Marangoni AG (2005) Antifreeze proteins modify the freezing process in planta. Plant Physiol 138(1):330–340PubMedCentralPubMedCrossRefGoogle Scholar
  11. Han LZ, Qiao YL, Cao GL, Zhang YY, An YP, Ye JD, Koh HJ (2007) QTL analysis of cold tolerance during early growth period for rice. Rice Sci 11(5–6):245–250Google Scholar
  12. Jiang L, Xun MM, Wang JK, Wan JM (2008) QTL analysis of cold tolerance at seedling stage in rice (Oryza sativa L.) using recombination inbred lines. J Cereal Sci 48:173–179CrossRefGoogle Scholar
  13. Kaneda C, Beachell HM (1973) Response of indica-japonica rice hybrids to low temperatures. SABRAO J 6:17–32Google Scholar
  14. Kanneganti V, Gupta AK (2008) Over-expression of OsiSAP8, a member of stress associated protein (SAP) gene family of rice confers tolerance to salt, drought and cold stress in transgenic tobacco and rice. Plant Mol Biol 66:445–462PubMedCrossRefGoogle Scholar
  15. Kim S, An CS, Hong YN, Lee KW (2004) Cold-inducible transcription factor, CaCBF, is associated with a homeodomain leucine zipper protein in hot pepper (Capsicum annuum L.). Mol Cells 18:300–308PubMedGoogle Scholar
  16. Koseki M, Kitazawa N, Yonebayashi S, Maehara Y, Wang ZX, Minobe Y (2010) Identification and fine mapping of a major quantitative trait locus originating from wild rice, controlling cold tolerance at the seedling stage. Mol Genet Genomics 284:45–54PubMedCrossRefGoogle Scholar
  17. Kushwaha HR, Singh AK, Sopory SK, Singla-Pareek SL, Pareek A (2009) Genome wide expression analysis of CBS domain containing proteins in Arabidopsis thaliana (L.) Heynh and Oryza sativa L. reveals their developmental and stress regulation. BMC Genomics 10:200PubMedCentralPubMedCrossRefGoogle Scholar
  18. Lander ES, Green P, Abrahamson H, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181PubMedCrossRefGoogle Scholar
  19. Lou Q, Chen L, Sun Z, Xing Y, Li J, Xu X, Mei H, Luo L (2007) A major QTL associated with cold tolerance at seedling stage in rice (Oryza sativa L.). Euphytica 158:87–97CrossRefGoogle Scholar
  20. McCouch SR, Teytelman L, Xu Y, Lobos KB, Clare K, Walton M, Fu B, Maghirang R, Li Z, Xing Y, Zhang Q, Kono I, Yano M, Fjellstrom R, DeClerck G, Schneider D, Cartinhour S, Ware D, Stein L (2002) Development and mapping of 2240 new SSR markers for rice (Oryza sativa L.). DNA Res 9:199–207PubMedCrossRefGoogle Scholar
  21. Miura K, Lin SY, Yano M, Nagamine T (2001) Mapping quantitative trait loci controlling low temperature germinability in rice (Oryza sativa L.). Breed Sci 51:293–299CrossRefGoogle Scholar
  22. Morsy MR, Abeer M, Almutairi AM, Gibbons J, Yun SJ, Benildo DR (2005) The OsLti6 genes encoding low-molecular-weight membrane proteins are differentially expressed in rice cultivars with contrasting sensitivity to low temperature. Gene 344:171–180PubMedCrossRefGoogle Scholar
  23. Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucl Acids Res 8:4321–4325PubMedCentralPubMedCrossRefGoogle Scholar
  24. Nakagahra M, Okuno K, Vaughan D (1997) Rice genetic resources: history, conservation, investigative characterization and use in Japan. Plant Mol Biol 35:69–77PubMedCrossRefGoogle Scholar
  25. Park MR, Yun KY, Mohanty B, Herath V, Xu F, Wijaya E, Bajic VB, Yun SJ, De los Reyes BG (2010) Supra-optimal expression of the cold-regulated OsMyb4 transcription factor in transgenic rice changes the complexity of transcriptional network with major effects on stress tolerance and panicle development. Plant Cell Environ 33:2209–2230PubMedCrossRefGoogle Scholar
  26. Pasquali G, Biricolti S, Locatelli F, Baldoni E, Mattana M (2008) Osmyb4 expression improves adaptive responses to drought and cold stress in transgenic apples. Plant Cell Rep 27:1677–1686PubMedCrossRefGoogle Scholar
  27. Peterson ML, Jones DB, Rutger JN (1978) Cool temperature screening of rice lines for seedling Vigor. IlRiso 27:269–274Google Scholar
  28. Qian Q, Zeng D, He P, Zheng X, Chen Y, Zhu L (2000) QTL analysis of the rice seedling cold tolerance in a double haploid population derived from anther culture of a hybrid between indica and japonica rice. Chin Sci Bull 45:448–453CrossRefGoogle Scholar
  29. Qin F, Sakuma Y, Li J, Liu Q, LI YQ, Shinozaki k, Yamaguchi SK (2004) Cloning and functional analysis of a novel DREB1/CBF transcription factor involved in cold-responsive gene expression in Zea mays L. Plant Cell Physiol 45:1042–1052PubMedCrossRefGoogle Scholar
  30. Reyes LC (2009) Grappling with cold. Rice Today 9:20–23Google Scholar
  31. Rozen S, Skaletsky H (2000) Primer 3 on the WWW for general users and for biologist programmers. Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, pp 365–386Google Scholar
  32. Saito K, Hayano-Saito Y, Kuroki M, Sato Y (2010) Map-based cloning of the rice cold tolerance gene Ctb1. Plant Sci 179:97–102CrossRefGoogle Scholar
  33. Shen YJ, Jiang H, Jin JP, Zhang ZB, Biao XB, He YY, Wang G, Wang C, Qian L, Li X, Yu QB, Liu HJ, Chen DH, Gao JH, Huang H, Shi TL, Yang ZN (2004) Development of genome wide DNA polymorphism database for map-based cloning of rice genes. Plant Physiol 135:1198–1205PubMedCentralPubMedCrossRefGoogle Scholar
  34. Suh JP, Jeung JU, Lee JI, Choi YH, Yea JD, Virk PS, Mackill DJ, Jena KK (2010) Identification and analysis of QTLs controlling cold tolerance at the reproductive stage and validation of effective QTLs in cold-tolerant genotypes of rice (Oryza sativa L.). Theor Appl Genet 120:985–995PubMedCrossRefGoogle Scholar
  35. Suh JP, Lee CK, Lee JH, Kim JJ, Kim SM, Cho YC, Park SH, Shin JC, Kim YG, Jena KK (2012) Identification of quantitative trait loci for seedling cold tolerance using RILs derived from a cross between japonica and tropical japonica rice cultivars. Euphytica 184:101–108CrossRefGoogle Scholar
  36. Takesawa T, Ito M, Kanzaki H, Kameya N, Nakamura I (2002) Over-expression of ζ-glutathione S-transferase in transgenic rice enhances germination and growth at low temperature. Mol Breed 9:93–101CrossRefGoogle Scholar
  37. Wang S, Basten CJ, Zeng ZB (2007) Windows QTL cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, NC. http://statgen.ncsu.edu/qtlcart/WQTLCart.htm
  38. Yoo KS, Ok SH, Jeong BC, Jung KW, Cui MH, Hyoung S, Lee MR, Song HK, Shin JS (2011) Single cystathionine β-synthase domain-containing proteins modulate development by regulating the thioredoxin system in Arabidopsis. Plant Cell 23:3577–3594PubMedCentralPubMedCrossRefGoogle Scholar
  39. Yoshida R, Kanno A, Sato T, Kameya T (1996) Cool temperature induced chlorosis in rice plant. Plant Physiol 110:997–1005PubMedCentralPubMedCrossRefGoogle Scholar
  40. Zhang ZH, Su L, Li W, Chen W, Zhu YG (2005) A major QTL conferring cold tolerance at the early seedling stage using recombinant inbred lines of rice (Oryza sativa L.). Plant Sci 168:527–534CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Suk-Man Kim
    • 1
    • 2
  • Jung-Pil Suh
    • 3
  • Chung-Koon Lee
    • 3
  • Jeong-Heui Lee
    • 3
  • Yeong-Gyu Kim
    • 3
  • Kshirod Kumar Jena
    • 1
  1. 1.Plant Breeding, Genetics, and Biotechnology DivisionInternational Rice Research InstituteMetro ManilaPhilippines
  2. 2.C/o IRRI-Korea OfficeNational Institute of Crop Science, Rural Development AdministrationSuwonRepublic of Korea
  3. 3.Rice Research DivisionNational Institute of Crop Science, Rural Development AdministrationSuwonRepublic of Korea

Personalised recommendations