Molecular Breeding

, 38:52 | Cite as

Temperature-dependent QTLs in indica alleles for improving grain quality in rice: increased prominence of QTLs responsible for reduced chalkiness under high-temperature conditions

  • Tomio Terao
  • Tatsuro Hirose


Quantitative trait loci (QTLs) for the apparent quality of brown rice under high temperatures during ripening were analyzed using chromosomal segment substitution lines. Segments from the indica cultivar Habataki were substituted into a japonica cultivar with a Sasanishiki background. We found the following two QTLs for increasing grain quality in the Habataki allele on chromosome 3: (1) qTW3-2, located near the marker RM14702, decreased the percentage of total white immature (TWI) grains, and (2) qRG3-2, located near RM3766, increased the percentage of regular grains. The effects of these two QTLs were more obvious under high-temperature ripening conditions; hence, these loci are considered QTLs not only for reducing TWI grains but also for increasing high-temperature tolerance. Additionally, we found two QTLs, i.e., qTW3-1 and qRG3-1, responsible for reduced grain quality near RM14314 on chromosome 3. Although the QTL for narrow grains in the Habataki allele qNG3 was genetically linked to qTW3-2, the effect was only slightly significant, and the length/width ratio of qNG3-carrying grains was within the range observed in widely grown japonica cultivars. Incorporating the Habataki region, including qRG3-2 and qTW3-2 but not qTW3-1 and qRG3-1, in addition to previously reported grain quality QTLs in breeding japonica cultivars will improve high-temperature tolerance and grain quality.


High-temperature tolerance QTL Grain quality Rice (Oryza sativa L.) 



We are grateful to Mr. Tokuya Genba, Mr. Hiroyuki Nakagawa, Mr. Tuyoshi Kotake, Mr. Masanori Ichihashi, Mr. Shinobu Yuminamochi, Mr. Koushi Yazaki, Mr. Susumu Saitou, Mr. Ken-ichi Koide, Ms. Keiko Nozaki, Ms. Setsuko Hayashi, and Ms. Kiiko Takatsuto for their excellent technical assistance.


This study was supported by Japan Society for the Promotion of Science KAKENHI grants 24580030 and 15K0280.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

11032_2018_807_MOESM1_ESM.doc (3.8 mb)
ESM 1 (DOC 3.76 mb)


  1. Ando T, Yamamoto T, Shimizu T, Ma XF, Shomura A, Takeuchi Y, Lin SY, Yano M (2008) Genetic dissection and pyramiding of quantitative traits for panicle architecture by using chromosomal segment substitution lines in rice. Theor Appl Genet 116:881–890. CrossRefPubMedGoogle Scholar
  2. Broman KW, Sen S (2009) A guide to QTL mapping with R/qtl. Springer, New York, pp 75–133Google Scholar
  3. Chiba M, Terao T (2014) Open-top chambers with solar-heated air introduction tunnels for the high-temperature treatment of paddy fields. Plant Prod Sci 17:152–165. CrossRefGoogle Scholar
  4. Chiba M, Matsumura O, Terao T, Takahashi Y, Watanabe H (2009) Improvement of grain quality and yield by deep-flood irrigation. Jpn J Crop Sci 78:455–464. CrossRefGoogle Scholar
  5. He P, Li SG, Qian Q, Ma YQ, Li JZ, Wang WM, Chen Y, Zhu LH (1999) Genetic analysis of rice grain quality. TAG Theor Appl Genet 98:502–508. CrossRefGoogle Scholar
  6. International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800. CrossRefGoogle Scholar
  7. Ishimaru K, Hirotsu N, Madoka Y, Murakami N, Hara N, Onodera H, Kashiwagi T, Ujiie K, Shimizu B, Onishi A, Miyagawa H, Katoh E (2013) Loss of function of the IAA-glucose hydrolase gene TGW6 enhances rice grain weight and increases yield. Nat Genet 45:707–711. CrossRefPubMedGoogle Scholar
  8. Kobayashi A, Sonoda J, Sugimoto K, Kondo M, Iwasawa N, Hayashi T, Tomita K, Yano M, Shimizu T (2013) Detection and verification of QTLs associated with heat-induced quality decline of rice (Oryza sativa L.) using recombinant inbred lines and near-isogenic lines. Breed Sci 63:339–346. CrossRefPubMedPubMedCentralGoogle Scholar
  9. Kondo M, Iwasawa N, Yoshida H, Hakagawa H, Ohno H, Nakazono K, Usui Y, Tokida T, Hasegawa T, Kuwagata T, Morita S, Nagata K (2012) Factors influencing the appearance quality in rice under high temperature in 2010. Jpn J Crop Sci 81 (Extra issue 1):120–121. Accessed 16 Oct 2017
  10. Li J, Xiao J, Grandillo S, Jiang L, Wan Y, Deng Q, Yuan L, McCouch SR (2004) QTL detection for rice grain quality traits using an interspecific backcross population derived from cultivated Asian (O. sativa L.) and African (O. Glaberrima S.) rice. Genome 47:697–704. CrossRefPubMedGoogle Scholar
  11. Li Y, Fan C, Xing Y, Jiang Y, Luo L, Sun L, Shao D, Xu C, Li X, Xiao J, He Y, Zhang Q (2011) Natural variation in GS5 plays an important role in regulating grain size and yield in rice. Nat Genet 43:1266–1269. CrossRefPubMedGoogle Scholar
  12. Li Y, Fan C, Xing Y, Yun P, Luo L, Yan B, Peng B, Xie W, Wang G, Li X, Xiao J, Xu C, He Y (2014) Chalk5 encodes a vacuolar H+-translocating pyrophosphatase influencing grain chalkiness in rice. Nat Genet 46:398–404. CrossRefPubMedGoogle Scholar
  13. Liu X, Wan X, Ma X, Wan J (2011) Dissecting the genetic basis for the effect of rice chalkiness, amylose content, protein content, and rapid viscosity analyzer profile characteristics on the eating quality of cooked rice using the chromosome segment substitution line population across eight environments. Genome 54:64–80. CrossRefPubMedGoogle Scholar
  14. Morita S (2008) Prospect for developing measures to prevent high-temperature damage to rice grain ripening. Jpn J Crop Sci 77:1–12. CrossRefGoogle Scholar
  15. Murata K, Iyama Y, Yamaguchi T, Ozaki H, Kidani Y, Ebitani T (2014) Identification of a novel gene (Apq1) from the indica rice cultivar ‘Habataki’ that improves the quality of grains produced under high temperature stress. Breed Sci 64:273–281. CrossRefPubMedPubMedCentralGoogle Scholar
  16. Peng B, Wang L, Fan C, Jiang G, Luo L, Li Y, He Y (2014) Comparative mapping of chalkiness components in rice using five populations across two environments. BMC Genet 15:49. CrossRefPubMedPubMedCentralGoogle Scholar
  17. Qiu X, Chen K, Lv W, Ou X, Zhu Y, Xing D, Yang L, Fan F, Yang J, Xu J, Zheng T, Li Z (2017) Examining two sets of introgression lines reveals background-independent and stably expressed QTL that improve grain appearance quality in rice (Oryza sativa L.) Theor Appl Genet 130:951–967. CrossRefPubMedPubMedCentralGoogle Scholar
  18. Shirasawa K, Sekii T, Ogihara Y, Yamada T, Shirasawa S, Kishitani S, Sasaki K, Nishimura M, Nagano K, Nishio T (2013) Identification of the chromosomal region responsible for high-temperature stress tolerance during the grain-filling period in rice. Mol Breed 32:223–232. CrossRefGoogle Scholar
  19. Shomura A, Izawa T, Ebana K, Ebitani T, Kanegae H, Konishi S, Yano M (2008) Deletion in a gene associated with grain size increased yields during rice domestication. Nat Genet 40:1023–1028. CrossRefPubMedGoogle Scholar
  20. Song XJ, Huang W, Shi M, Zhu MZ, Lin HX (2007) A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat Genet 39:623–630. CrossRefPubMedGoogle Scholar
  21. Tashiro T, Wardlaw I (1991) The effect of high temperature on kernel dimensions and the type and occurrence of kernel damage in rice. Aust J Agric Res 42:485–496. CrossRefGoogle Scholar
  22. Terao T, Hirose T (2015) Control of grain protein contents through SEMIDWARF1 mutant alleles: sd1 increases the grain protein content in Dee-geo-woo-Gen but not in Reimei. Mol Genet Genomics 290:939–954. CrossRefPubMedGoogle Scholar
  23. Terao T, Chiba M, Hirose T (2010a) A simple equipment to screen the rice strains tolerant to high temperature in the ripening processes. Jpn J Crop Sci 79:166–173. CrossRefGoogle Scholar
  24. Terao T, Nagata K, Morino K, Hirose T (2010b) A gene controlling the number of primary rachis branches also controls the vascular bundle formation and hence is responsible to increase the harvest index and grain yield in rice. Theor Appl Genet 120:875–893. CrossRefPubMedGoogle Scholar
  25. Terashima K, Saito Y, Sakai N, Watanabe T, Ogata T, Akita S (2001) Effects of high air temperature in summer of 1999 on ripening and grain quality of rice. Jpn J Crop Sci 70:449–458. CrossRefGoogle Scholar
  26. Wakamatsu K, Sasaki O, Uezono I, Tanaka A (2007) Effects of high air temperature during the ripening period on the grain quality of rice in warm regions of Japan. Jpn J Crop Sci 76:71–78. CrossRefGoogle Scholar
  27. Wan XY, Wan JM, Weng JF, Jiang L, Bi JC, Wang CM, Zhai HQ (2005) Stability of QTLs for rice grain dimension and endosperm chalkiness characteristics across eight environments. Theor Appl Genet 110:1334–1346. CrossRefPubMedGoogle Scholar
  28. Wang H, Qi M, Cutler AJ (1993) A simple method of preparing plant samples for PCR. Nucleic Acids Res 21:4153–4154. CrossRefPubMedPubMedCentralGoogle Scholar
  29. Wang S, Basten CJ, Zeng Z-B (2012a) Windows QTL Cartographer 2.5. Department of Statistics. North Carolina State University, Raleigh, NC. Accessed 7 Aug 2017
  30. Wang S, Wu K, Yuan Q, Liu X, Liu Z, Lin X, Zeng R, Zhu H, Dong G, Qian Q, Zhang G, Fu X (2012b) Control of grain size, shape and quality by OsSPL16 in rice. Nat Genet 44:950–954. CrossRefPubMedGoogle Scholar
  31. Weng J, Gu S, Wan X, Gao H, Guo T, Su N, Lei C, Zhang X, Cheng Z, Guo X, Wang J, Jiang L, Zhai H, Wan J (2008) Isolation and initial characterization of GW5, a major QTL associated with rice grain width and weight. Cell Res 18:1199–1209. CrossRefPubMedGoogle Scholar
  32. Yamakawa H, Hirose T, Kuroda M, Yamaguchi T (2007) Comprehensive expression profiling of rice grain filling-related genes under high temperature using DNA microarray. Plant Physiol 144:258–277. CrossRefPubMedPubMedCentralGoogle Scholar
  33. Yamakawa H, Ebitani T, Terao T (2008) Comparison between locations of QTLs for grain chalkiness and genes responsive to high temperature during grain filling on the rice chromosome map. Breed Sci 58:337–343. CrossRefGoogle Scholar
  34. Yoshida S, Hara T (1977) Effects of air temperature and light on grain filling of an indica and a japonica rice (Oryza sativa L.) under controlled environmental conditions. Soil Sci Plant Nutr 23:93–107. CrossRefGoogle Scholar
  35. Yun YT, Chung CT, Lee YJ, Na HJ, Lee JC, Lee SG, Lee KW, Yoon YH, Kang JW, Lee HS, Lee JY, Ahn SN (2016) QTL mapping of grain quality traits using introgression lines carrying Oryza rufipogon chromosome segments in Japonica rice. Rice 9:62. CrossRefPubMedPubMedCentralGoogle Scholar
  36. Zhao X, Fitzgerald M (2013) Climate change: implications for the yield of edible rice. PLoS One 8:e66218. CrossRefPubMedPubMedCentralGoogle Scholar
  37. Zhao X, Daygon VD, McNally KL, Hamilton RS, Xie F, Reinke RF, Fitzgerald MA (2016) Identification of stable QTLs causing chalk in rice grains in nine environments. Theor Appl Genet 129:141–153. CrossRefPubMedGoogle Scholar
  38. Zhou L, Chen L, Jiang L, Zhang W, Liu L, Liu X, Zhao Z, Liu S, Zhang L, Wang J, Wan J (2009) Fine mapping of the grain chalkiness QTL qPGWC-7 in rice (Oryza sativa L.) Theor Appl Genet 118:581–590. CrossRefPubMedGoogle Scholar
  39. Zhu L, Shah F, Nie L, Cui K, Shah T, Wu W, Chen Y, Chen C, Wang K, Wang Q, Lian Y, Huang J (2013) Efficacy of sowing date adjustment as a management strategy to cope with rice (Oryza sativa L.) seed quality deterioration due to elevated temperature. Aust J Crop Sci 7:543–549Google Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Hokuriku Research Station, Central Region Agricultural Research CenterNational Agriculture and Food Research OrganizationNiigataJapan

Personalised recommendations