, 214:13 | Cite as

Identification of QTLs controlling low-temperature germinability and cold tolerance at the seedling stage in rice (Oryza Sativa L.)

  • L. M. Yang
  • H. L. Liu
  • L. Lei
  • H. W. Zhao
  • J. G. Wang
  • N. Li
  • J. Sun
  • H. L. Zheng
  • D. T. Zou


Both low-temperature germinability (LTG) and cold tolerance at the seedling stage (CTS) are important traits for rice. In this study, a rice population of recombinant inbred lines (RILs), derived from the backcross population of a cross between Dongnong422 and Kongyu131, was developed to detect quantitative trait loci (QTL) affecting LTG and CTS by using seed of different storage times. Correlation analysis indicated that there was no significant relationship between LTG and CTS, suggesting that cold tolerance might be genetic differences for LTG and CTS. In total, Twelve and twenty-three major QTLs were detected for LTG and CTS, respectively, which could explain greater than 10% of the phenotypical variation. Eight (qCG12-1, qGI12-1, qGV9-1, qMLIT12-1, qPV6-1, qMDG12-1, qLDWcold10-1, qLFWcold10-1) significant QTLs were mapped for different storage time, it concluded that such QTLs were not affected by environment (storage time) and were closely related QTLs to cold tolerance. One or more QTLs were identified for each trait with some of these QTLs co-locating, qMLIT7-1, qCG7-1, and qGI7-1 for LTG, qLFWcold10-1, and qLDWcold10-1 for CTS with contributions over 15% were mapped common marker interval, respectively, co-location of QTLs for different traits can be an indication that a locus has pleiotropic effects on multiple traits due to a common mechanistic basis. Two lines, RIL128 and RIL73, might be valuable to improve the LTG and CTS through a combination of crosses. The identified QTLs might be applicable to improve the rice cold tolerance by the marker-assisted selection approach.


Rice Storage time Low-temperature germinability Cold tolerance of seedling Quantitative trait loci 



This work was supported by the major science and technology fund bidding project in Heilongjiang province (GA14B102-02).

Supplementary material

10681_2017_2092_MOESM1_ESM.pdf (208 kb)
Supplementary material 1 (PDF 208 kb)
10681_2017_2092_MOESM2_ESM.xlsx (59 kb)
Supplementary material 2 (XLSX 59 kb)


  1. Alonso-Blanco C, Aarts MG, Bentsink L, Keurentjes JJ, Reymond M, Vreugdenhil D, Koornneef M (2009) What has natural variation taught us about plant development, physiology, and adaptation? Plant Cell 21(7):1877–1896CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alvarez R, Valbuena L, Calvo L (2007) Effect of high temperatures on seed germination and seedling survival in three pine species (Pinus pinaster, P. sylvestris and P. nigra). Int J Wildland Fire 16(1):63–70CrossRefGoogle Scholar
  3. Andaya V, Mackill D (2003a) Mapping of QTLs associated with cold tolerance during the vegetative stage in rice. J Exp Bot 54(392):2579–2585CrossRefPubMedGoogle Scholar
  4. Andaya V, Mackill D (2003b) QTLs conferring cold tolerance at the booting stage of rice using recombinant inbred lines from a japonica × indica cross. Theor Appl Genet 106(6):1084–1090CrossRefPubMedGoogle Scholar
  5. Bettey M, Finch-Savage W, King GJ, Lynn J (2000) Quantitative genetic analysis of seed vigour and pre-emergence seedling growth traits in Brassica oleracea. New Phytol 148(2):277–286CrossRefGoogle Scholar
  6. Bewley JD, Bradford K, Hilhorst H (2012) Seeds: physiology of development, germination and dormancy. Seed Sci Res 23(4):289Google Scholar
  7. Blum A, Ebercon A (1981) Cell membrane stability as a measure of drought and heat tolerance in wheat. Crop Sci 21(1):43CrossRefGoogle Scholar
  8. Cheng LR, Wang JM, Uzokwe V, Meng LJ, Yun W, Yong S, Zhu LH, Xu JL, Li ZK (2012) Genetic analysis of cold tolerance at seedling stage and heat tolerance at anthesis in rice (Oryza sativa L.). J Integr Agric 11(3):359–367CrossRefGoogle Scholar
  9. Chung G (1979) The rice cold tolerance program in Korea. In: Report of a Rice Cold Tolerance Workshop. IRRI, Manila, pp 7–20Google Scholar
  10. Clerkx EJ, El-Lithy ME, Vierling E, Ruys GJ, Blankestijn-De Vries H, Groot SP, Vreugdenhil D, Koornneef M (2004) Analysis of natural allelic variation of Arabidopsis seed germination and seed longevity traits between the accessions Landsberg erecta and Shakdara, using a new recombinant inbred line population. Plant Physiol 135(1):432–443CrossRefPubMedPubMedCentralGoogle Scholar
  11. Cui K, Peng S, Xing Y, Xu C, Yu S, Zhang Q (2002) Molecular dissection of seedling-vigor and associated physiological traits in rice. Theor Appl Genet 105(5):745–753CrossRefPubMedGoogle Scholar
  12. Das D, Satapathy SS, Buragohain AK, Ray SK (2006) Mapping QTLs underlying seedling vigour traits in rice (Oryza sativa L.). Curr Sci 90(1):25Google Scholar
  13. Dias PMB, Brunel-Muguet S, Dürr C, Huguet T, Demilly D, Wagner M-H, Teulat-Merah B (2011) QTL analysis of seed germination and pre-emergence growth at extreme temperatures in Medicago truncatula. Theor Appl Genet 122(2):429–444CrossRefPubMedGoogle Scholar
  14. Edelstein M, Kigel J, Nerson H (1991) Relationships among germination, emergence and seedling development of muskmelon at low temperature. Sci Hortic 47(1):51–58CrossRefGoogle Scholar
  15. Foolad M, Lin G (2001) Genetic analysis of cold tolerance during vegetative growth in tomato, Lycopersicon esculentum Mill Euphytica 122(1):105–111CrossRefGoogle Scholar
  16. Fujino K, Sekiguchi H, Sato T, Kiuchi H, Nonoue Y, Takeuchi Y, Ando T, Lin S, Yano M (2004) Mapping of quantitative trait loci controlling low-temperature germinability in rice (Oryza sativa L.). Theor Appl Genet 108(5):794–799CrossRefPubMedGoogle Scholar
  17. Ghassemi-Golezani K, Khomari S, Dalil B, Hosseinzadeh-Mahootchy A, Chadordooz-Jeddi A (2010) Effects of seed aging on field performance of winter oilseed rape. J Food Agric Environ 8(1):175–178Google Scholar
  18. Han L-Z, Zhang Y-Y, Qiao Y-L, Cao G-L, Zhang S-Y, Kim J-H, Koh H-J (2006) Genetic and QTL analysis for low-temperature vigor of germination in rice. Acta Genet Sin 33(11):998–1006Google Scholar
  19. Han L, Qiao Y, Zhang S, Zhang Y, Cao G, Kim J, Lee K, Koh H (2007) Identification of quantitative trait loci for cold response of seedling vigor traits in rice. J Genet Genom 34(3):239–246CrossRefGoogle Scholar
  20. Ikehashi H (1973) Studies on the environmental and varietal differences of germination habits in rice seeds with special reference to plant breeding. J Cent Agric Exp Stan 19:1–60Google Scholar
  21. Ji S, Jiang L, Wang Y, Zhang W, Liu X, Liu S, Chen L, Zhai H, Wan J (2009) Quantitative trait loci mapping and stability for low temperature germination ability of rice. Plant Breed 128(4):387–392CrossRefGoogle Scholar
  22. Jiang L, Hou MY, Wang CM, Wan JM (2004) Quantitative trait loci and epistatic analysis of seed anoxia germinability in rice (Oryza sativa). Rice Sci 11:238–244Google Scholar
  23. Jiang L, Liu S, Hou M, Tang J, Chen L, Zhai H, Wan J (2006) Analysis of QTLs for seed low temperature germinability and anoxia germinability in rice (Oryza sativa L.). Field crops Res 98(1):68–75CrossRefGoogle Scholar
  24. Jiang N, Shi S, Shi H, Khanzada H, Wassan GM, Zhu C, Peng X, Yu Q, Chen X, He X, Fu J, Hu L, Xu J, Ouyang L, Sun X, Zhou D, He H, Bian J (2017) Mapping QTL for seed germinability under low temperature using a new high-density genetic map of rice. Front Plant Sci. Google Scholar
  25. Kim SM, Suh JP, Lee CK, Lee JH, Kim YG, Jena KK (2014) QTL mapping and development of candidate gene-derived DNA markers associated with seedling cold tolerance in rice (Oryza sativa L.). Mol Genet Genom 289(3):333–343CrossRefGoogle Scholar
  26. Landjeva S, Lohwasser U, Börner A (2010) Genetic mapping within the wheat D genome reveals QTL for germination, seed vigour and longevity, and early seedling growth. Euphytica 171(1):129CrossRefGoogle Scholar
  27. Larsen RJ, Marx ML (1985) An introduction to probability and its applications. Prentice Hall, New York 15 (214):404–411Google Scholar
  28. Lee J, Kwon SW (2015) Analysis of quantitative trait loci associated with seed germination and coleoptile length under low temperature condition. J Crop Sci Biotechnol 18(4):273–278CrossRefGoogle Scholar
  29. Li CC, Rutger J (1980) Inheritance of cool-temperature seedling vigor in rice and its relationship with other agronomic characters. Crop Sci 20(3):295–298CrossRefGoogle Scholar
  30. Li H, Zhang Q, Liu A, Zou J, Chen Z (1996) A genetic analysis of low-temperature-sensitive sterility in indica-japonica rice hybrids. Plant Breed 115(5):305–309CrossRefGoogle Scholar
  31. Li H, Wang J, Liu A, Liu K, Zhang Q, Zou J (1997) Genetic basis of low-temperature-sensitive sterility in indica-japonica hybrids of rice as determined by RFLP analysis. Theor Appl Genet 95(7):1092–1097CrossRefGoogle Scholar
  32. Liu F, Xu W, Song Q, Tan L, Liu J, Zhu Z, Fu Y, Su Z, Sun C (2013) Microarray-assisted fine-mapping of quantitative trait loci for cold tolerance in rice. Mol Plant 6(3):757–767CrossRefPubMedGoogle Scholar
  33. 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(1–2):87–94CrossRefGoogle Scholar
  34. Ma Y, Dai X, Xu Y, Luo W, Zheng X, Zeng D, Pan Y, Lin X, Liu H, Zhang D (2015) COLD1 confers chilling tolerance in rice. Cell 160(6):1209–1221CrossRefPubMedGoogle Scholar
  35. Miura K, Lin S, Yano M, Nagamine T (2001) Mapping quantitative trait loci controlling low temperature germinability in rice (Oryza sativa L.). Breed Sci 51(4):293–299CrossRefGoogle Scholar
  36. Miura K, Lin S, Yano M, Nagamine T (2002) Mapping quantitative trait loci controlling seed longevity in rice (Oryza sativa L.). Theor Appl Genet 104(6–7):981–986PubMedGoogle Scholar
  37. Nagel M, Börner A (2010) The longevity of crop seeds stored under ambient conditions. Seed Sci Res 20(1):1CrossRefGoogle Scholar
  38. Narayanan NN, Baisakh N, Oliva NP, Casiana MV, Samuel SG, Karabi D, Swapan KD (2014) Molecular breeding: marker-assisted selection combined with biolistic transformation for blast and bacterial blight resistance in Indica rice (cv. CO39). Mol Breed 14(1):61–71CrossRefGoogle Scholar
  39. Nguyen TP, Keizer P, van Eeuwijk F, Smeekens S, Bentsink L (2012) Natural variation for seed longevity and seed dormancy are negatively correlated in Arabidopsis. Plant Physiol 160(4):2083–2092CrossRefPubMedPubMedCentralGoogle Scholar
  40. Niu Y, Xu Y, Liu XF, Yang SX, Wei SP, Xie FT, Zhang YM (2013) Association mapping for seed size and shape traits in soybean cultivars. Mol Breed 31(4):785–794CrossRefGoogle Scholar
  41. Nonogaki H, Bassel GW, Bewley JD (2010) Germination—still a mystery. Plant Sci 179(6):574–581CrossRefGoogle Scholar
  42. Nykiforuk CL, Johnson-Flanagan AM (1999) Storage reserve mobilization during low temperature germination and early seedling growth in Brassica napus. Plant Physiol Biochem 37(12):939–947CrossRefGoogle Scholar
  43. Pandit E, Tasleem S, Barik SR, Mohanty DP, Nayak DK, Mohanty SP, Dsa S, Pradhan SK (2017) Genome-wide association mapping reveals multiple QTLS governing tolerance response for seedling stage chilling stress in indica rice. Front Plant Sci. PubMedPubMedCentralGoogle Scholar
  44. Paterson AH, Lin YR, Li Z, Schertz KF (1995) Convergent domestication of cereal crops by independent mutations at corresponding genetic loci. Science 269(5231):1714CrossRefPubMedGoogle Scholar
  45. Pelgas B, Bousquet J, Meirmans PG, Ritland K, Isabel N (2011) QTL mapping in white spruce: gene maps and genomic regions underlying adaptive traits across pedigrees, years and environments. BMC Genom 12(1):145CrossRefGoogle Scholar
  46. Rajjou L, Duval M, Gallardo K, Catusse J, Bally J, Job C, Job D (2012) Seed germination and vigor. Annu Rev Plant Biol 63(3):507–533CrossRefPubMedGoogle Scholar
  47. Redona E, Mackill D (1996) Mapping quantitative trait loci for seedling vigor in rice using RFLPs. Theor Appl Genet 92(3–4):395–402CrossRefPubMedGoogle Scholar
  48. Teng S, Zeng D, Qian Q, Kunihifo Y, Huang D, Zhu L (2001) QTL analysis of rice low temperature germinability. Chin Sci Bull 46(21):1800–1803 (in Chinese) CrossRefGoogle Scholar
  49. Trachsel S, Messmer R, Stamp P, Ruta N, Hund A (2010) QTLs for early vigor of tropical maize. Mol Breed 25(1):91–103CrossRefGoogle Scholar
  50. Verma S, Xalxo M, Saxena R, Verulkar S (2014) Identification of QTLs for cold tolerance at seedling stage in rice (Oryza sativa L.). Indian. J Genet 74(1):86–89Google Scholar
  51. Voorrips R (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93(1):77–78CrossRefPubMedGoogle Scholar
  52. 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(3):173–180CrossRefGoogle Scholar
  53. Wang Z, Wang F, Zhou R, Wang J, Zhang H (2011a) Identification of quantitative trait loci for cold tolerance during the germination and seedling stages in rice (Oryza sativa L.). Euphytica 181(3):405–413CrossRefGoogle Scholar
  54. Wang Z, Wang J, Bao Y, Wu Y, Zhang H (2011b) Quantitative trait loci controlling rice seed germination under salt stress. Euphytica 178(3):297–307CrossRefGoogle Scholar
  55. Xiao N, Huang WN, Zhang XX, Gao Y, Li AH, Dai Y, Yu L, Liu GQ, Pan CH, Li YH (2014) Fine mapping of qRC10-2, a quantitative trait locus for cold tolerance of rice roots at seedling and mature stages. PLoS ONE 9(5):e96046CrossRefPubMedPubMedCentralGoogle Scholar
  56. Yang Z, Huang D, Tang W, Zheng Y, Liang K, Cutler AJ, Wu W (2013) Mapping of quantitative trait loci underlying cold tolerance in rice seedlings via high-throughput sequencing of pooled extremes. PLoS ONE 8(7):e68433CrossRefPubMedPubMedCentralGoogle Scholar
  57. Yang LM, Zhao HW, Wang JG, Liu HL, Sun J, Guo LY (2017) Zou DT Genomic dissection of rice yield traits under low temperature across multi-environments. Euphytica 213(7):134CrossRefGoogle Scholar
  58. Zhang ZH, Qu XS, Wan S, Chen LH, Zhu YG (2005a) Comparison of QTL controlling seedling vigour under different temperature conditions using recombinant inbred lines in rice (Oryza sativa). Ann Bot 95(3):423–429CrossRefPubMedGoogle Scholar
  59. Zhang ZH, Su L, Wei L, Chen W, Zhu YG (2005b) A major QTL conferring cold tolerance at the early seedling stage using recombinant inbred lines of rice (Oryza sativa L.). Plant Sci 168(2):527–534CrossRefGoogle Scholar
  60. Zhang ZH, Yu SB, Yu T, Huang Z, Zhu YG (2005c) Mapping quantitative trait loci (QTLs) for seedling-vigor using recombinant inbred lines of rice (Oryza sativa L.). Field Crops Res 91(2–3):161–170CrossRefGoogle Scholar
  61. Zhang S, Zheng J, Liu B, Peng S, Leung H, Zhao J, Wang X, Yang T, Huang Z (2014) Identification of QTLs for cold tolerance at seedling stage in rice (Oryza sativa L.) using two distinct methods of cold treatment. Euphytica 195(1):95–104CrossRefGoogle Scholar
  62. Zhang AP, Liu CL, Chen G, Kai H, Yang G, Tian P, Peng YL, Zhang B, Ruan BP, Jiang HZ, Guo LB, Qian Q, Gao ZY (2017) Genetic analysis for rice seedling vigor and fine mapping of a major qtlqssl1b for seedling shoot length. Breed Sci 67(3):307–315CrossRefPubMedPubMedCentralGoogle Scholar
  63. Zhao JL, Zhang S, Dong JF, Yang TF, Mao XX, Liu Q, Wang XF, Liu B (2017) A novel functional gene associated with cold tolerance at the seedling stage in rice. Plant Biotechnol J 15(9):1141CrossRefPubMedPubMedCentralGoogle Scholar
  64. Zhou L, Wang JK, Yi Q, Wang YZ, Zhu YG, Zhang ZH (2007) Quantitative trait loci for seedling vigor in rice under field conditions. Field Crops Res 100(2–3):294–301CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2017

Authors and Affiliations

  1. 1.College of AgricultureNortheast Agricultural UniversityHarbinPeople’s Republic of China

Personalised recommendations