, 215:193 | Cite as

QTL analysis of main agronomic traits in rice under low temperature stress

  • Jianghong Tang
  • Xiaoding Ma
  • Di Cui
  • Bing Han
  • Leiyue Geng
  • Zhengwu Zhao
  • Yafei Li
  • Longzhi HanEmail author


To identify cold tolerance at the reproductive stage in rice (Oryza sativa L.), the cold susceptible accession, IAPAR-9 (tropical japonica) was crossed with the cold tolerant accessions Akihikari and Liaoyan241 (temperate japonica) to construct two recombinant inbred lines (RIL) to detected QTLs related to cold-tolerance of rice through analyze phenotypic variation. The two RILs and their parents were experimentally grown in natural conditions and cold water irrigation at one site, Gongzhuling Jilin (China), and at natural low temperature in another site, Kunming Yunnan (China). We measured plant height, panicle length, number of panicles per plant, grain number per panicle, seed setting rate and panicle exsertion of parents and RIL populations in the maturation stage. In the three treatment environments, the traits of the two RILs showed normal distributions, and both exhibited transgressive segregation. Low temperature stress had greater influence on number of panicles per plant and grain number per panicle and lower influence on plant height and panicle length. Seventeen quantitative trait locus (QTLs) were detected, distributed on chromosomes 1, 3-6, 8, 11 and 12. Among these, four QTLs had values of phenotypic variance explained that were greater than 10%. There were two QTLs, qPN12-2E2 and qPN12-2E3, detected in the IAPAR-9/Akihikari RIL population in same region under cold water irrigation condition in Gongzhuling Jilin and natural low temperature in Kunming Yunnan. Major regions related to cold tolerance QTLs in these two populations was on chromosome 12 from RM511 to RM3739. The cold tolerance allele was from the Akihikari and Liaoyan241 in the respective populations for both QTL regions.


Rice Low temperature stress Agronomic traits Quantitative trait locus 



This work was supported by the National Key Research and Development Program of China (2016YFD0100101, 2016YFD0100301), the National Natural Science Fundation of China (31671664), the National Science and Technology Support Program of China (2015BAD01B01-1), CAAS Science and Technology Innovation Program, National Infrastructure for Crop Germplasm Resources (NICGR2017-01), Protective Program of Crop Germplasm of China (2017NWB036-01, 2017NWB036-12-2).

Supplementary material

10681_2019_2507_MOESM1_ESM.xls (47 kb)
Supplementary material 1 (XLS 47 kb)
10681_2019_2507_MOESM2_ESM.xls (25 kb)
Supplementary material 2 (XLS 25 kb)
10681_2019_2507_MOESM3_ESM.xls (25 kb)
Supplementary material 3 (XLS 25 kb)


  1. Cao YQ, Luo J, Xin KY, Xue Y, Ma LM, Fang P (2017) Chilling injury of rice flowering and its impact on yield in liangshan prefecture of Sichuan Province. Guizhou Agric Sci 45(11):18–22 (in Chinese) Google Scholar
  2. Dai LY, Ye CR, Yu TQ, Xu FR (2002) Studies on cold tolerance of rice, Oryza sativa L. I. Description on types of cold injury and classifications of evaluation methods on cold tolerance in rice. Southwest China J Agric Sci 15(1):41–45 (in Chinese) Google Scholar
  3. Feng XY, Guo ChM, Chen CS, Liu S (2013) Spatial-temporal variation of sterile-type chilling damages at rice booting stage in Northeast China in last 50 years based on meteorological model. Chin J Agrometeorol 34(4):462–467 (in Chinese) Google Scholar
  4. Guo LB, Luo LJ, Xing YZ, Xu CG, Mei HW, Wang YP, Zhong DB, Qian Q, Ying CS, Shi CH (2003) Dissection of QTLs in two years for important agronomic traits in rice (Oryza sativa L.). Chin J Rice Sci 17(3):211–218 (in Chinese) Google Scholar
  5. Han LZ, Kou HJ, Piao ZZ (2002) Status and prospects of genetic and QTLs analysis for cold tolerance in rice. Chinese J Rice Sci 16(2):193–198 (in Chinese) Google Scholar
  6. Han LZ, Yuan DL, Xuan YS, Piao ZZ, Koh HJ (2004) Genetic analysis of cold water response on several agronomic traits of rice. Chin J Rice Sci 18(1):23–28 (in Chinese) Google Scholar
  7. Han LZ, Qiao YL, Zhang YY, Cao GL, Yea JD, Koh HJ (2005) Identification of QTLs for cold tolerance at booting stage in rice. Acta Agron Sin 31(5):653–657 (in Chinese) Google Scholar
  8. Han LZ, Qiao YL, Zhang SY, Zhang YY, Cao GL, Kim JH, Lee K, Koh HJ (2007) Identification of quantitative trait loci for cold response of seedling vigor traits in rice. J Genet Genom 34(3):239–246CrossRefGoogle Scholar
  9. Hou MY, Wang CM, Jiang L, Wan JM, Hideshi Y, Atsushi Y (2004) Inheritance and QTL mapping of low temperature germinability in rice (Oryza sativa L.). Acta Genet Sin 31(7):701–706PubMedPubMedCentralGoogle Scholar
  10. Jena KK, Kim SM, Suh JP, Yang CI, Kim YG (2012) Identification of cold-tolerant breeding lines by quantitative trait loci associated with cold tolerance in rice. Crop Sci 52(2):517–523CrossRefGoogle Scholar
  11. Ji SL, Jiang L, Wang YH, Liu SJ, Liu X, Zhai HQ, Yoshimura A, Wan JM (2008) QTL and epistasis for low temperature germinability in rice. Acta Agronom Sin 34(4):551–556 (in Chinese) Google Scholar
  12. Jian SR (2011) QTL mapping for controlling seeding cold tolerance in Dongxiang wild rice (Oryza rufipogon Griff.). Dissertation, Jiangxi Normal University (in Chinese)Google Scholar
  13. Kuroki M, Saito K, Matsuba S, Yokogami N, Shimizu H, Ando I, Sato Y (2007) A quantitative trait locus for cold tolerance at the booting stage on rice chromosome 8. Theor Appl Genet 115:593–600PubMedCrossRefPubMedCentralGoogle Scholar
  14. Li JL, Pan YH, Guo HF, Zhou L, Yang S, Zhang ZY, Yang JZ, Zhang HL, Li JJ, Zeng YW, Li ZC (2018) Fine mapping of QTL qCTB10-2 that confers cold tolerance at the booting stage in rice. Theor Appl Genet 131(1):157–166PubMedCrossRefPubMedCentralGoogle Scholar
  15. Liang YT, Meng LJ, Lin XY, Cui YR, Pang YL, Xu JL, Li ZK (2018) QTL and QTL networks for cold tolerance at the reproductive stage detected using selective introgression in rice. PLoS ONE 13(9):e0200846PubMedPubMedCentralCrossRefGoogle Scholar
  16. Liu X, Gong YJ, Dong YJ, Lin DZ (2009) Study on fine mapping of a major QTL for cold tolerance at seedling stage of rice. Chin Agric Sci Bull 25(22):62–66 (in Chinese) Google Scholar
  17. Luo XD, Zhao J, Dai LF, Zhang FT, Zhou Y, Wan Y, Xie JK (2016) Linkage map construction and QTL mapping for cold tolerance in Oryza rufipogon Griff. at early seedling stage. J Integr Agric 15:60345–60347Google Scholar
  18. Luo XD, Liu J, Zhao J, Dai LF, Chen YI, Zhang L, Zhang FT, Hu BI, Xie JK (2018) Rapid mapping of candidate genes for coId toIerance in Oryza rufipogon Griff. by QTL-seq of seedIings. J Integr Agric 17(2):265–275CrossRefGoogle Scholar
  19. Lv Y, Guo ZL, Li XK, Ye HY, Li XH, Xiong LZ (2016) New insights into the genetic basis of natural chilling and cold shock tolerance in rice by genome-wide association analysis. Plant Cell Environ 39:556–570PubMedCrossRefPubMedCentralGoogle Scholar
  20. Malosetti M, Ribaut JM, Vargas M, Crossa J, Vaneeuwijk FA (2008) A multi-trait multi-environment QTL mixed model with an application to drought and nitrogen stress trials in maize (Zea mays L.). Euphytica 161(1/2):241–257CrossRefGoogle Scholar
  21. Mao DH, Yu L, Chen DZ, Li LY, Zhu YX, Xiao YQ, Zhang DC, Chen CY (2015) Multiple cold resistance loci confer the high cold tolerance adaptation of Dongxiang wild rice (Oryza rufipogon) to its high-latitude habitat. Theor Appl Genet 128(7):1359–1371PubMedCrossRefPubMedCentralGoogle Scholar
  22. Messmer R, Fracheboud Y, Banziger M, Vargas M, Stamp P, Ribaut JM (2009) Drought stress and tropical maize: QTL-by-environment interactions and stability of QTLs across environments for yield components and secondary traits. Theor Appl Genet 119(5):913–930PubMedCrossRefPubMedCentralGoogle Scholar
  23. Pan YH, Zhang HL, Zhang DL, Li JJ, Xiong HY, Yu JP, Li JL, Rashid M, Li GL, Ma XD, Cao GL, Han LZ, Li ZC (2015) Genetic analysis of cold tolerance at the germination and booting stages in rice by association mapping. PLoS ONE 10(3):e0120590PubMedPubMedCentralCrossRefGoogle Scholar
  24. Saito K, Hayano-Saito Y, Kuroki M, Sato Y (2010) Map-based cloning of the rice cold tolerance gene Ctb1. Plant Sci 179(1):97–102CrossRefGoogle Scholar
  25. Sales E, Viruel J, Domingo C, MarqueÂs L (2017) Genome wide association analysis of cold tolerance at germination in temperate japonica rice (Oryza sativa L.) varieties. PLoS ONE 12(8):e0183416PubMedPubMedCentralCrossRefGoogle Scholar
  26. Schläppi MR, Jackson AK, Eizenga GC, Wang AJ, Chu CC, Shi Y, Shimoyama N, Boykin DL (2017) Assessment of five chilling tolerance traits and GWAS mapping in rice using the USDA Mini-Core collection. Front Plant Sci 8:957–969PubMedPubMedCentralCrossRefGoogle Scholar
  27. Shakiba E, Edwards JD, Jodari F, Duke SE, Baldo AM, Korniliev P, McCouch SR, Eizenga GC (2017) Genetic architecture of cold tolerance in rice (Oryza sativa) determined through high resolution genome-wide analysis. PLoS ONE 12(3):e0172133PubMedPubMedCentralCrossRefGoogle Scholar
  28. Shinada H, Iwata N, Sato T, Fujino K (2013) Genetical and morphological characterization of cold tolerance at fertilization stage in rice. Breed Sci 63:197–204PubMedPubMedCentralCrossRefGoogle Scholar
  29. Song T, Gao Y, Zhang MK, Wang HY (2016) Research status of rice chilling injury. Mod Agric Sci Technol 14:56–57 (in Chinese) Google Scholar
  30. Spitzer M, Wildenhain J, Rappsilber J, Tyers M (2014) Box-PlotR: a web tool for generation of box plots. Nat Methods 11(2):121–122PubMedPubMedCentralCrossRefGoogle Scholar
  31. Sun GY (2015). Association analysis of rice cold tolerance at early growing stage with SSR markers of Japonica rice in cold region. Dissertation, Northeast Agricultural University (in Chinese) Google Scholar
  32. Wu XL, Yu L, Luo Y, Yang TM, Xu M (2017) Analysis of characteristics of low temperature chilling injury in critical rice growing period in Anhui Province. Jiangsu Agric Sci 45(6):68–71 (in Chinese) Google Scholar
  33. Xiong ZM, Min SK, Wang GL, Cheng SH, Cao LY (1990) Genetic analysis of cold tolerance at the seeding stage of early rice (O. satica L. subsp. indica). Chin J Rice Sci 4(2):75–78 (in Chinese) Google Scholar
  34. Xu FR, Yu TQ, Tang CF, Xin-xiang A, Fan CZ, Hu YL, Zhang DY, Dong C, Dai LY (2008) Low-temperature response to major agronomic traits by using Recombinant Inbred Line (RIL) populations derived from Towada/Kunmingxiaobaigu. Sci Agric Sin 41(11):3437–3447 (in Chinese) Google Scholar
  35. Yang TF (2016) Identification and pyramiding of QTLs for cold tolerance by use of single segment substitution lines in rice (Oryza sativa L.). Dissertation, South China Agricultural University (in Chinese) Google Scholar
  36. Yang TF, Zhang SH, Zhao JL, Huang ZH, Zhang GQ, Liu B (2015) Meta-analysis of QTLs underlying cold tolerance in rice (Oryza sativa L.). Mol Plant Breed 13(1):1–15Google Scholar
  37. Yin SH, Xu JL, Zhu LQ (2016) Temporal and spatial variation of chilling injury at rice heading-filling stage and its influence on rice yield in Jiangsu Province in recent 30 years. Acta Agric Jiangxi 28(5):7–13 (in Chinese) Google Scholar
  38. Zeng YW, Yang SM, Cui H, Yang XJ, Xu LM, Du J, Pu XY, Li ZC, Cheng ZQ, Huang XQ (2009) QTLs of cold tolerance-related traits at the booting stage for NIL-RILs in rice revealed by SSR. Genes Genom 31(2):143–154CrossRefGoogle Scholar
  39. Zhang MY, Zou DT (2012) Association analysis of rice cold tolerance at tillering stage with SSR markers in Japonica cultivars in Northeast China. Chin J Rice Sci 26(4):423–430 (in Chinese) Google Scholar
  40. Zhang FF, Zhang EL, Tang CF, Dong C, Jin HZ, Chen D, Xin-xiang A, Lu DY, Xu FR (2015) QTL analysis of cold tolerance-related agronomic traits in rice across different environment. Mol Plant Breed 13(10):2174–2184 (in Chinese) Google Scholar
  41. Zhang ZY, Li JJ, Pan YH, Li JL, Zhou L, Shi HL, Zeng YW, Guo HF, Yang SM, Zheng WW et al (2017) Natural variation in CTB4a enhances rice adaptation to cold habitats. Nat Commun 8:14788–14800PubMedPubMedCentralCrossRefGoogle Scholar
  42. Zhang MC, Ye J, Xu Q, Feng Y, Yuan XP, Yu HY, Wang YP, Wei XH, Yang YL (2018) Genome-wide association study of cold tolerance of Chinese indica rice varieties at the bud burst stage. Plant Cell Rep 37(3):529–539PubMedCrossRefPubMedCentralGoogle Scholar
  43. Zhou L, Zeng Y, Zheng WW, Tang B, Yang SM, Zhang HL, Li JJ, Li ZC (2010) Fine mapping a QTL qCTB7 for cold tolerance at the booting stage on rice chromosome 7 using a near-isogenic line. Theor Appl Genet 121(5):895–905PubMedCrossRefPubMedCentralGoogle Scholar
  44. Zhu YJ, Chen K, Mi XF, Chen TX, Ali J, Ye GY, Xu JL, Li ZK (2015) Identification and fine mapping of a stably expressed QTL for cold tolerance at the booting stage using an interconnected breeding population in rice. PLoS ONE 10(12):e0145704PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Jianghong Tang
    • 1
    • 2
  • Xiaoding Ma
    • 1
  • Di Cui
    • 1
  • Bing Han
    • 1
  • Leiyue Geng
    • 1
  • Zhengwu Zhao
    • 2
  • Yafei Li
    • 3
  • Longzhi Han
    • 1
    Email author
  1. 1.Institute of Crop SciencesChinese Academy of Agricultural SciencesBeijingChina
  2. 2.Chongqing Engineering Research Center of Specialty Crop ResourceChongqing Normal UniversityChongqingChina
  3. 3.Institute of Genetics and Developmental BiologyChinese Academy of SciencesBeijingChina

Personalised recommendations