Skip to main content

Advertisement

SpringerLink
Log in

Marker-assisted pyramiding of QTLs for heat tolerance and escape upgrades heat resilience in rice (Oryza sativa L.)

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

This study demonstrated that pyramiding of early morning flowering and heat tolerance QTLs (qEMF3 and qHTSF4.1) in rice is an efficient approach to maintain high spikelet fertility under high-temperature stress at flowering stage.

Abstract

High temperature at flowering stage of rice causes low spikelet fertility and low yield. To cope with high-temperature stress brought by climate change, two strategies were proposed to develop heat-resilient rice varieties. One is to escape the high temperature by flowering early in the morning, another is to enhance tolerance to high-temperature stress per se. Two promising QTLs for early morning flowering (qEMF3) and heat tolerance (qHTSF4.1) were introgressed into IR64 background, and Near isogenic lines (NILs) IR64 + qEMF3 (IR64EMF3) and IR64 + qHTSF4.1 (IR64HT4) were developed in previous studies. In this study, a QTL pyramiding line IR64 + qHTSF4.1 + qEMF3 (IR64HT4EMF3) was developed by marker-assisted selection of the progenies of previous NILs. The NILs were subjected to different high-temperature regimes in the indoor growth chambers and different locations in the field. In the indoor growth chambers, when high temperature starts early (before 11:00 am), IR64HT4 and IR64HT4EMF3 had higher spikelet fertility than IR64EMF3; when high temperature comes later (after 11:00 am), IR64EMF3 and IR64HT4EMF3 had higher spikelet fertility than IR64HT4. The flowering pattern of the IR64HT4EMF3 was earlier than IR64HT4, but similar to IR64EMF3 in the glasshouse, field and indoor growth chambers. IR64HT4EMF3 showed higher spikelet fertility than IR64EMF3 and IR64HT4 in the field in the Philippines. Thus, combination of early morning flowering and heat tolerance QTLs is an elegant breeding strategy to cope with future extreme climate.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

The data supporting the findings of this study are available within the article and its supplementary materials. Raw data of this study are available from the corresponding author [C. Ye] on request.

References

  • Battisti D, Naylor R (2009) Historical warning of future food incesurity with unprecedented seasonal heat. Science 323:240–244

    Article  CAS  PubMed  Google Scholar 

  • Cao L, Zhao J, Zhan X, Li D, He L, Cheng S (2003) Mapping QTLs for heat tolerance and correlation between heat tolerance and photosynthetic rate in rice. Chin J Rice Sci 17:223–227

    CAS  Google Scholar 

  • Chen Q, Yu S, Li C, Mou T (2008) Identification of QTLs for heat tolerance at flowering stage in rice. Scientia Agricultura Sinica 41:315–321

    CAS  Google Scholar 

  • Cheng L, Wang J, Uzokwe V, Meng L, Wang Y, Sun Y, Zhu L, Xu J, Li Z (2012) Genetic analysis of cold tolerance at seedling stage and heat tolerance at anthesis in rice. J Integr Agric 11:359–367

    Article  Google Scholar 

  • Hasegawa T, Yoshimoto M, Kuwagata T, Ishigooka Y, Kondo M, Ishimaru T (2009) The impact of global warming on rice production: lessons from spikelet sterility observed under the record hot summer of 2007. NIAES Annual Report 2008:23–25

    Google Scholar 

  • Hirabayashi H, Sasaki K, Kambe T, Gannaban RB, Miras MA, Mendioro MS, Simon EV, Lumanglas PD, Fujita D, Takemoto-Kuno Y, Takeuchi Y, Kaji R, Kondo M, Kobayashi N, Ogawa T, Ando I, Jagadish KS, Ishimaru T (2015) qEMF3, a novel QTL for the early-morning flowering trait from wild rice, Oryza officinalis, to mitigate heat stress damage at flowering in rice. O Sativa J Exp Bot 66:1227–1236

    Article  CAS  PubMed  Google Scholar 

  • Ishimaru T, Hirabayashi H, Ida M, Takai T, San-Oh Y, Yoshinaga S, Ando I, Ogawa T, Kondo M (2010) A genetic resource for early-morning flowering trait of wild rice Oryza officinalis to mitigate high temperature-induced spikelet sterility at anthesis. Ann Bot 106:515–520

    Article  PubMed  PubMed Central  Google Scholar 

  • Ishimaru T, Hirabayashi H, Sasaki K, Ye C, Kobayashi A (2016a) Breeding efforts to mitigate damage by heat stress to spikelet sterility and grain quality. Plant Prod Sci 19:12–21

    Article  CAS  Google Scholar 

  • Ishimaru T, Seefong X, Nallathambi J, Rajendran S, Yoshimoto M, Phoudalay L, Benjamin S, Hasegawa T, Hayashi K, Gurusamy A, Muthurajan R, Jagadish S (2016b) Quantifying rice spikelet sterility in potential heat-vulnerable regions: field surveys in southern Laos and southern India. Field Crop Res 190:3–9

    Article  Google Scholar 

  • Jagadish S, Craufurd P, Wheeler T (2007) High temperature stress and spikelet fertility in rice. J Exp Bot 58:1627–1635

    Article  CAS  PubMed  Google Scholar 

  • Jagadish S, Cairns J, Lafitte R, Wheeler T, Price A, Craufurd P (2010a) Genetic analysis of heat tolerance at anthesis in rice. Crop Sci 50:1633–1641

    Article  CAS  Google Scholar 

  • Jagadish S, Muthurajan R, Oane R, Wheeler T, Heuer S, Bennett J, Craufurd Q (2010b) Physiological and proteomic approaches to address heat tolerance during anthesis in rice. J Exp Bot 61:143–156

    Article  CAS  PubMed  Google Scholar 

  • Lafarge T, Bueno C, Frouin J, Jacquin L, Courtois B, Ahmadi N (2017) Genome-wide association analysis for heat tolerance at flowering detected a large set of genes involved in adaptation to thermal and other stresses. PLoS ONE 12:e0171254

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li C, Peng C, Zhao Q, Xie P, Chen W (2004) Characteristic analysis of the abnormal high temperature in 2003 midsummer in Wuhan City. J Central China Normal Univ 38:379–381

    Google Scholar 

  • Mackill D, Coffman W, Rutger J (1982) Pollen shedding and combining ability for high temperature tolerance in rice. Crop Sci 22:730–733

    Article  Google Scholar 

  • Manigbas N, Lambio L, Madrid L, Cardenas C (2014) Germplasm Innovation of Heat Tolerance in Rice for Irrigated Lowland Conditions in the Philippines. Rice Sci 21:162–169

    Article  Google Scholar 

  • Matsui T (2009) Floret sterility induced by high temperatures at the flowering stage in rice. Japanese J Crop Sci 78:303–311

    Article  Google Scholar 

  • Matsui T, Omasa K (2002) Rice cultivars tolerant to high temperature at flowering: Anther characteristics. Ann Bot 89:683–687

    Article  PubMed  PubMed Central  Google Scholar 

  • Matsui T, Kobayasi K, Yoshimoto M, Hasegawa T (2007) Stability of rice pollination in the field under hot and dry conditions in the Riverina Region of New South Wales, Australia. Plant Prod Sci 10:57–63

    Article  Google Scholar 

  • Matsushima S, Ikewada H, Maeda A, Honma S, Niki H (1982) Studies on rice cultivation in the tropics. 1. Yielding and ripening responses of the rice plant to the extremely hot and dry climate in Sudan. Jpn J Tropic Agric 26:19–25

    Google Scholar 

  • Nishiyama I, Satake T (1981) High temperature damage in the rice plant. Jpn J Tropic Agric 25:14–19

    Google Scholar 

  • Osada A, Sasiprapa V, Rahong M, Dhammanuvong S, Chakrabandho H (1973) Abnormal occurrence of empty grains of indica rice plants in the dry hot season in Thailand. Proc Crop Sci Soc Japan 42:103–109

    Article  Google Scholar 

  • Poli Y, Basava R, Panigrahy M, Vinukonda V, Dokula N, Voleti S, Desiraju S, Neelamraju S (2013) Characterization of a Nagina22 rice mutant for heat tolerance and mapping of yield traits. Rice (new York, NY) 6:36

    Google Scholar 

  • Prasad P, Boote K, Allen L, Sheehy J, Thomas J (2006) Species, ecotype and cultivar differences in spikelet fertility and harvest index of rice in response to high temperature stress. Field Crop Res 95:398–411

    Article  Google Scholar 

  • Satake T, Yoshida S (1978) High temperature induced sterility in Indica rice at flowering. Japanese J Crop Sci 47:6–17

    Article  Google Scholar 

  • Shi W, Ishimaru T, Gannaban R, Oane W, Jagadish S (2015) Popular rice cultivars show contrasting responses to heat stress at gametogenesis and anthesis. Crop Sci 55:589–596

    Article  Google Scholar 

  • Shi W, Li X, Schmidt R, Struik P, Yin X, Jagadish S (2018) Pollen germination and in vivo fertilization in response to high-temperature during flowering in hybrid and inbred rice. Plant, Cell Environ 41:1287–1297

    Article  CAS  Google Scholar 

  • Takai T, Lumanglas P, Simon E (2020) Genetic mechanism of heat stress tolerance at anthesis among three different rice varieties with different fertilities under heat stress. Plant Prod Sci 23:529–538

    Article  Google Scholar 

  • Thomson M, Singh N, Dwiyanti M, Wang D, Wright M, Perez F, DeClerck G, Chin J, Malitic-Layaoen G, Juanillas V, Dilla-Ermita C, Mauleon R, Kretzschmar T, McCouch S (2017) Large-scale deployment of a rice 6 K SNP array for genetics and breeding applications. Rice (new York, NY) 10:40

    Google Scholar 

  • Tian X, Matsui T, Li S, Yoshimoto M, Kobayasi K, Hasegawa T (2010) Heat-induced floret sterility of hybrid rice (Oryza sativa L.) cultivars under humid and low wind conditions in the field of Jianghan basin. China Plant Prod Sci 13:243–251

    Article  Google Scholar 

  • Vivitha P, Raveendran M, Vijayalakshmi D (2017) Introgression of QTLs Controlling Spikelet Fertility Maintains Membrane Integrity and Grain Yield in Improved White Ponni Derived Progenies Exposed to Heat Stress. Rice Sci 24:32–40

    Article  Google Scholar 

  • Wassmann R, Jagadish S, Heuer S, Ismail A, Redona E, Serraj R, Singh R, Howell G, Pathak H, Sumfleth K (2009) Climate change affecting rice production: The physiological and agronomic basis for possible adaptation strategies. Adv Agron 101:59–122

    Article  Google Scholar 

  • Weerakoon W, Maruyama A, Ohba K (2008) Impact of humidity on temperature-induced grain sterility in rice. J Agron Crop Sci 194:135–140

    Article  Google Scholar 

  • Xiao Y, Pan Y, Luo L, Deng H, Zhang G, Tang W, Chen L (2011a) Quantitative trait loci associated with pollen fertility under high temperature stress at flowering stage in rice. Rice Sci 18:204–209

    Article  Google Scholar 

  • Xiao Y, Pan Y, Luo L, Zhang G, Deng H, Dai L, Liu X, Tang W, Chen L, Wang G (2011b) Quantitative trait loci associated with seed set under high temperature stress at the flowering stage in rice. Euphytica 178:331–338

    Article  Google Scholar 

  • Yang H, Huang Z, Jiang Z, Wang X (2004) High temperature damage and its protective technologies of early and middle season rice in Anhui province. J Anhui Agri Sci 32:3–4

    Google Scholar 

  • Ye C, Argayoso M, Redoña E, Sierra S, Laza M, Dilla C, Mo Y, Thomson M, Chin J, Delaviña C, Diaz G, Hernandez J (2012) Mapping QTL for heat tolerance at flowering stage in rice using SNP markers. Plant Breeding 131:33–41

    Article  CAS  Google Scholar 

  • Ye C, Tenorio F, Argayoso M, Laza M, Koh H, Redona E, Jagadish K, Gregorio G (2015a) Identifying and confirming quantitative trait loci associated with heat tolerance at flowering stage in different rice populations. BMC Genet 16:41

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ye C, Tenorio F, Redona E, Morales-Cortezano P, Cabrega G, Jagadish K, Gregorio G (2015b) Fine-mapping and validating qHTSF4.1 to increase spikelet fertility under heat stress at flowering in rice. Theor Appl Genet 128:1507–15017

    Article  CAS  PubMed  Google Scholar 

  • Zhang T, Yang L, Jiang K, Huang M, Sun Q, Chen W, Zheng J (2008) QTL mapping for heat tolerance of the tassel period of rice. Molecular Plant Breeding 6:867–873

    CAS  Google Scholar 

  • Zhang G, Chen L, Xiao G, Xiao Y, Chen X, Zhang S (2009) Bulked segregant analysis to detect QTL related to heat tolerance in rice using SSR markers. Agri Sci China 8:482–487

    Article  CAS  Google Scholar 

Download references

Funding

This study was supported by the Bill & Melinda Gates Foundation project, Cereal Systems Initiative for South Asia (CSISA); the German Federal Ministry for Economic Cooperation and Development (BMZ) project, Safeguarding Asian Rice Production from a Rapidly Warming Climate; the Japanese government (MOFA and MAFF) under the IRRI-Japan Collaborative Research Project; and the Chinese national mutation breeding project of main crops, Technological Innovation and Variety Development of Rice Using Space Mutation Breeding (2016YFD0102102).

Author information

Author notes

  1. Tsutomu Ishimaru

    Present address: Hokuriku Research Station, Central Region Agricultural Research Center, National Agriculture and Food Research Organization, Joetsu, Niigata, 941-0193, Japan

Authors and Affiliations

  1. Huazhi Biotechnology Co. Ltd, 618 Heping Road, Changsha, 410125, Hunan, China

    Changrong Ye, Le Li, Yu Long, Zhizhou He & Shunxue Tang

  2. Japan International Research Center for Agricultural Sciences (JIRCAS), 1-1 Ohwashi, Tsukuba, Ibaraki, 305-8686, Japan

    Tsutomu Ishimaru & Zhenxi Su

  3. International Rice Research Institute, PABO Box 7777, Metro Manila, Philippines

    Changrong Ye, Tsutomu Ishimaru & Leslie Lambio

  4. Division of New Genetics, Yezin Agricultural University (YAU), Nay Pyi Taw, 15013, Myanmar

    Than Myint Htun

  5. Institute of Food Crops, Yunnan Academy of Agricultural Sciences, 2238 Beijing Road, Kunming, 650205, Yunnan, China

    Zhenxi Su

Authors
  1. Changrong Ye
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tsutomu Ishimaru
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Leslie Lambio
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Le Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yu Long
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zhizhou He
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Than Myint Htun
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Shunxue Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Zhenxi Su
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

CY, TI and ZS designed the experiments. CY, TI, LL and TMH conducted the experiments. CY, LL, YL and ZH analyzed the data. CY and TI wrote the paper. ST supervised the writing and editing.

Corresponding authors

Correspondence to Changrong Ye or Zhenxi Su.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Takuji Sasaki.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 15 kb)

Supplementary file2 (PDF 227 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ye, C., Ishimaru, T., Lambio, L. et al. Marker-assisted pyramiding of QTLs for heat tolerance and escape upgrades heat resilience in rice (Oryza sativa L.). Theor Appl Genet 135, 1345–1354 (2022). https://doi.org/10.1007/s00122-022-04035-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-022-04035-w

Search

Navigation