Theoretical and Applied Genetics

, Volume 131, Issue 1, pp 157–166 | Cite as

Fine mapping of QTL qCTB10-2 that confers cold tolerance at the booting stage in rice

  • Jilong Li
  • Yinghua Pan
  • Haifeng Guo
  • Lei Zhou
  • Shuming Yang
  • Zhanying Zhang
  • Jiazhen Yang
  • Hongliang Zhang
  • Jinjie Li
  • Yawen Zeng
  • Zichao Li
Original Article

Abstract

Key message

The QTL qCTB10 - 2 controlling cold tolerance at the booting stage in rice was delimited to a 132.5 kb region containing 17 candidate genes and 4 genes were cold-inducible.

Abstract

Low temperature at the booting stage is a major abiotic stress-limiting rice production. Although some QTL for cold tolerance in rice have been reported, fine mapping of those QTL effective at the booting stage is few. Here, the near-isogenic line ZL31-2, selected from a BC7F2 population derived from a cross between cold-tolerant variety Kunmingxiaobaigu (KMXBG) and the cold-sensitive variety Towada, was used to map a QTL on chromosome 10 for cold tolerance at the booting stage. Using BC7F3 and BC7F4 populations, we firstly confirmed qCTB10-2 and gained confidence that it could be fine mapped. QTL qCTB10-2 explained 13.9 and 15.9% of the phenotypic variances in those two generations, respectively. Using homozygous recombinants screened from larger BC7F4 and BC7F5 populations, qCTB10-2 was delimited to a 132.5 kb region between markers RM25121 and MM0568. 17 putative predicted genes were located in the region and only 5 were predicted to encode expressed proteins. Expression patterns of these five genes demonstrated that, except for constant expression of LOC_Os10g11820, LOC_Os10g11730, LOC_Os10g11770, and LOC_Os10g11810 were highly induced by cold stress in ZL31-2 compared to Towada, while LOC_Os10g11750 showed little difference. Our results provide a basis for identifying the genes underlying qCTB10-2 and indicate that markers linked to the qCTB10-2 locus can be used to improve the cold tolerance of rice at the booting stage by marker-assisted selection.

Notes

Acknowledgements

We thank Robert A McIntosh (University of Sydney) for critical reading and suggested revisions to the manuscript. This work was supported by grants from Ministry of Science and Technology of China (2016YFD0100101, 2015BAD02B01 and 2013BAD01B02-15), National Natural Science Foundation of China (31471456, 31671649).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interests.

Supplementary material

122_2017_2992_MOESM1_ESM.docx (19 kb)
Supplementary material 1 (DOCX 19 kb)

References

  1. Abe N, Kotaka S, Toriyama K, Kobayashi M (1989) Development of the rice “Norin-PL 8” with high tolerance to cool temperature at the booting stage. Research Bulletin of the Hokkaido National Agricultural Experiment Station (Japan)Google Scholar
  2. Andaya V, Mackill D (2003) QTLs conferring cold tolerance at the booting stage of rice using recombinant inbred lines from a japonica × indica cross. Theor Appl Genet 106:1084–1090CrossRefPubMedGoogle Scholar
  3. Cui D, Xu CY, Tang CF, Yang CG, Yu TQ, Xin-Xiang A, Cao GL, Xu FR, Zhang JG, Han LZ (2013) Genetic structure and association mapping of cold tolerance in improved japonica rice germplasm at the booting stage. Euphytica 193:369–382CrossRefGoogle Scholar
  4. Dai LY, Lin XH, Ye CR, Ise K, Saito K, Kato A, Xu FR, Yu TQ, Zhang DP (2004) Identification of quantitative trait loci controlling cold tolerance at the reproductive stage in Yunnan landrace of rice, Kunmingxiaobaigu. Breed Sci 54:253–258CrossRefGoogle Scholar
  5. Dorweiler J, Stec A, Kermicle J, Doebley J (1993) Teosinte glume architecture 1: a genetic locus controlling a key step in maize evolution. Science 262:233CrossRefPubMedGoogle Scholar
  6. Endo T, Chiba B, Wagatsuma K, Saeki K, Ando T, Shomura A, Mizubayashi T, Ueda T, Yamamoto T, Nishio T (2016) Detection of QTLs for cold tolerance of rice cultivar ‘Kuchum’ and effect of QTL pyramiding. Theor Appl Genet 129:631–640CrossRefPubMedGoogle Scholar
  7. Guo L, Yang HB, Zhang XY, Yang SH (2013) Lipid transfer protein 3 as a target of MYB96 mediates freezing and drought stress in Arabidopsis. J Exp Bot 64:1755–1767CrossRefPubMedPubMedCentralGoogle Scholar
  8. Hayase H, Satake T, Nishiyama I, Ito N (1969) Male sterility caused by cooling treatment at the meiotic stage in rice plants: III. Male abnormalities at anthesis. Proc Crop Sci Soc Jpn 39:60–64Google Scholar
  9. Kader J-C (1996) Lipid-transfer proteins in plants. Annu Rev Plant Biol 47:627–654CrossRefGoogle Scholar
  10. Khare N, Goyary D, Singh NK, Shah P, Rathore M, Anandhan S, Sharma D, Arif M, Ahmed Z (2010) Transgenic tomato cv. Pusa Uphar expressing a bacterial mannitol-1-phosphate dehydrogenase gene confers abiotic stress tolerance. Plant Cell Tissue Organ Cult 103:267–277CrossRefGoogle Scholar
  11. Kim Y-H, Bae JM, Huh G-H (2010) Transcriptional regulation of the cinnamyl alcohol dehydrogenase gene from sweetpotato in response to plant developmental stage and environmental stress. Plant Cell Rep 29:779–791CrossRefPubMedPubMedCentralGoogle Scholar
  12. 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 115:593–600CrossRefPubMedGoogle Scholar
  13. 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 126:2313–2322CrossRefPubMedGoogle Scholar
  14. Liu ZX, Deng HB (2009) Development of genetic and QTLs analysis for cold tolerance in rice. Chin Agric Sci Bull 16:013Google Scholar
  15. Pan YH, Zhang HL, Zhang DL, Li JJ, Xiong HY, Yu JP, Li JL, Rashid MAR, 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:e0120590CrossRefPubMedPubMedCentralGoogle Scholar
  16. Panaud O, Chen X, McCouch SR (1996) Development of microsatellite markers and characterization of simple sequence length polymorphism (SSLP) in rice (Oryza sativa L.). Mol Gen Genet 252:597–607PubMedGoogle Scholar
  17. Qin XY, Liu Y, Mao SJ, Li TB, Wu HK, Chu CC, Wang YP (2011) Genetic transformation of lipid transfer protein encoding gene in Phalaenopsis amabilis to enhance cold resistance. Euphytica 177:33–43CrossRefGoogle Scholar
  18. Rogers SO, Bendich AJ (1989) Extraction of DNA from plant tissues. Plant molecular biology manual. Springer, New York, pp 73–83CrossRefGoogle Scholar
  19. Saito K, Miura K, Nagano K, Hayano-Saito Y, Araki H, Kato A (2001) Identification of two closely linked quantitative trait loci for cold tolerance on chromosome 4 of rice and their association with anther length. Theor Appl Genet 103:862–868CrossRefGoogle Scholar
  20. Saito K, Hayano-Saito Y, Maruyama-Funatsuki W, Sato Y, Kato A (2004) Physical mapping and putative candidate gene identification of a quantitative trait locus Ctb1 for cold tolerance at the booting stage of rice. Theor Appl Genet 109:515–522CrossRefPubMedGoogle Scholar
  21. 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
  22. Sasaki T, Matsunaga K (1985) Inheritance and improvement of cold tolerance at booting stage in rice. I. Cold tolerance of rice cultivars; Yoneshiro, Todorokiwase and Koshihikari. Jpn J Breed 35:320–321Google Scholar
  23. Satake T, Hayase H (1970) Male sterility caused by cooling treatment at the young microspore stage in rice plants. V. Estimations of pollen developmental stage and the most sensitive stage to coolness. Proc Crop Sci Soc Jpn 39:468–473CrossRefGoogle Scholar
  24. 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:e0172133CrossRefPubMedPubMedCentralGoogle Scholar
  25. Shinada H, Iwata N, Sato T, Fujino K (2013) Genetical and morphological characterization of cold tolerance at fertilization stage in rice. Breed Sci 63:197–204CrossRefPubMedPubMedCentralGoogle Scholar
  26. Shirasawa S, Endo T, Nakagomi K, Yamaguchi M, Nishio T (2012) Delimitation of a QTL region controlling cold tolerance at booting stage of a cultivar, ‘Lijiangxintuanheigu’, in rice, Oryza sativa L. Theor Appl Genet 124:937–946CrossRefPubMedGoogle Scholar
  27. Suh J, Jeung J, Lee J, Choi Y, Yea J, Virk P, Mackill D, Jena K (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 120:985–995CrossRefPubMedGoogle Scholar
  28. Takeuchi Y, Hayasaka H, Chiba B, Tanaka I, Shimano T, Yamagishi M, Nagano K, Sasaki T, Yano M (2001) Mapping quantitative trait loci controlling cool-temperature tolerance at booting stage in temperate japonica rice. Breed Sci 51:191–197CrossRefGoogle Scholar
  29. Wang JK, Li HH, Zhang LY, Meng L (2012) QTL IciMapping version 3.2. The Quantitative Genetics Group Institute of Crop Science Chinese Academy of Agricultural Sciences (CAAS) BeijingGoogle Scholar
  30. Xiao N, Huang WN, Li AH, Gao Y, Li YH, Pan CH, Ji HJ, Zhang XX, Dai Y, Dai ZY (2015) Fine mapping of the qLOP2 and qPSR2-1 loci associated with chilling stress tolerance of wild rice seedlings. Theor Appl Genet 128:173–185CrossRefPubMedGoogle Scholar
  31. Xu LM, Zhou L, Zeng YW, Wang FM, Zhang HL, Shen SQ, Li ZC (2008) Identification and mapping of quantitative trait loci for cold tolerance at the booting stage in a japonica rice near-isogenic line. Plant Sci 174:340–347CrossRefGoogle Scholar
  32. Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L, Fuse T, Baba T, Yamamoto K, Umehara Y, Nagamura Y (2000) Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12:2473–2483CrossRefPubMedPubMedCentralGoogle Scholar
  33. Ye C, Fukai S, Godwin I, Koh H, Reinke R, Zhou Y, Lambrides C, Jiang W, Snell P, Redona E (2010) A QTL controlling low temperature induced spikelet sterility at booting stage in rice. Euphytica 176:291–301CrossRefGoogle Scholar
  34. Zeng YW, Li SC, Pu XY, Yang SM, Liu K, Gui M, Zhang H (2005) Ecological difference and correlation among cold tolerance traits at the booting stage for core collection of rice landrace in Yunnan, China. Zhongguo Shuidao Kexue 20:265–271Google Scholar
  35. 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 31:143–154CrossRefGoogle Scholar
  36. Zhang DS, Liang WQ, Yin CS, Zong J, Gu FW, Zhang DB (2010) OsC6, encoding a lipid transfer protein, is required for postmeiotic anther development in rice. Plant Physiol 154:149–162CrossRefPubMedPubMedCentralGoogle Scholar
  37. Zhang ZY, Li JJ, Pan YH, Li JL, Shi HL, Zeng YW, Guo HF, Yang SM, Zheng WW, Yu JP, Sun XM, Li GL, Ding YL, Ma L, Shen SQ, Dai LY, Zhang HL, Yang SH, Guo Y, Li ZC (2017) Natural variation in CTB4a enhances rice adaptation to cold habitats. Nat Commun 8:14788CrossRefPubMedPubMedCentralGoogle Scholar
  38. Zhou L, Zeng YW, 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 121:895–905CrossRefPubMedGoogle Scholar
  39. Zhou L, Zeng YW, Hu GL, Pan YH, Yang SM, You AQ, Zhang HL, Li JJ, Li ZC (2012) Characterization and identification of cold tolerant near-isogenic lines in rice. Breed Sci 62:196–201CrossRefPubMedPubMedCentralGoogle Scholar
  40. 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:e0145704CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Key Laboratory of Crop Heterosis and Utilization, Ministry of Education/Beijing Key Laboratory of Crop Genetic ImprovementChina Agricultural UniversityBeijingChina
  2. 2.Biotechnology and Genetic Resources InstituteYunnan Academy of Agricultural SciencesKunmingChina
  3. 3.Rice Research InstituteGuangxi Academy of Agricultural SciencesNanningChina
  4. 4.Hubei Key Laboratory of Food Crop Germplasm and Genetic Improvement, Food Crops InstituteHubei Academy of Agricultural SciencesWuhanChina

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