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RESEARCH ARTICLE

Rice-cold tolerance across reproductive stages

J. H. Mitchell A D , S. L. Zulkafli A , J. Bosse A , B. Campbell A , P. Snell B , E. S. Mace C , I. D. Godwin A and S. Fukai A
+ Author Affiliations
- Author Affiliations

A The University of Queensland, School of Agriculture and Food Sciences, Brisbane, Qld 4072, Australia.

B Department of Primary Industries, Yanco Agricultural Institute, Yanco, NSW 2703, Australia.

C Department of Agriculture, Fisheries and Forestry, Hermitage Research Facility, Warwick, Qld 4370, Australia.

D Corresponding author. Email: jaquie.mitchell@uq.edu.au

Crop and Pasture Science 67(8) 823-833 https://doi.org/10.1071/CP15331
Submitted: 30 September 2015  Accepted: 4 March 2016   Published: 17 August 2016

Abstract

Cold temperature stress at the reproductive stage, particularly at booting and flowering stages can cause significant reductions in rice (Oryza sativa L.) yield particularly at high latitudes and elevation. Although genotypic variation for cold tolerance is known to exist, the tolerance mechanisms and genotypic consistency across the stages are yet to be understood for segregating populations. Three experiments were conducted under controlled temperature glasshouse conditions to determine floral characteristics that were associated with cold tolerance at the flowering stage and to determine genotypic consistency at the booting and flowering stages. Twenty F5 Reiziq × Lijiangheigu lines from two extreme phenotypic bulks selected for cold tolerance at booting stage in the F2 generation were utilised.

Spikelet sterility under cold stress at booting was significantly correlated with spikelet sterility under cold stress at flowering (r = 0.62**) with five lines identified as cold tolerant across reproductive stages. There was also a positive correlation (r = 0.47*) between spikelet sterility under cold stress at booting at the F5 and at the F2 generation. The quantitative trait loci (QTL; qLTSPKST10.1) previously identified on chromosome 10 contributing to spikelet sterility within the F2 generation, was also identified in the F5 generation. Additionally, genomic regions displaying significant segregation between the progenies contrasting for their cold tolerance response phenotype were identified on chromosomes 5 and 7 with Lijiangheigu as allelic donor and an estimated reduction in spikelet sterility of 25% and 27%, respectively. Although genotypic variation in spikelet sterility at the booting stage was not related to the development rate for heading or flowering, those cold-tolerant genotypes at the flowering stage were the quickest to complete flowering. Cold-tolerant genotypes at the flowering stage had larger numbers of dehisced anthers and subsequently pollen number on stigma, which contributed to reduced spikelet sterility. It is concluded that enhanced anther dehiscence plays a significant role in improved cold tolerance at the flowering stage.

Additional keywords: anther dehiscence, cold temperature stress, early generation selection, pollen number, spikelet sterility.


References

Andaya VC, Tai TH (2006) Fine mapping of the qCTS12 locus, a major QTL for seedling cold tolerance in rice. Theoretical and Applied Genetics 113, 467–475.
Fine mapping of the qCTS12 locus, a major QTL for seedling cold tolerance in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xms1Oitrk%3D&md5=bb61588f358de8cac48962680f5c4446CAS | 16741739PubMed |

da Cruz RP, Sperotto RA, Cargnelutti D, Adamski JM, de FreitasTerra T, Fett JP (2013) Avoiding damage and achieving cold tolerance in rice plants. Food and Energy Security 2, 96–119.
Avoiding damage and achieving cold tolerance in rice plants.Crossref | GoogleScholarGoogle Scholar |

Farrell T, Fox K, Williams R, Fukai S, Reinke R, Lewin L (2001) Temperature constraints to rice production in Australia and Lao PDR: a shared problem. In ‘Increased lowland rice production in the Mekong region’. ACIAR Proceedings 101. (Eds S Fukai, J Basnayake) pp. 129–137. (Australian Centre for International Agricultural Research: Canberra, ACT)

Farrell TC, Fox KM, Williams RL, Fukai S (2004) Australia: new screening method for cold tolerance during the reproductive stage in rice. In ‘New directions for a diverse planet. Proceedings of the 4th International Crop Science Congress’. Brisbane, Australia, 26 Sept.–1 Oct. 2004. (Ed. T Fischer) (The Regional Institute: Gosford, NSW) Available at: www.cropscience.org.au (accessed 26 February 2016)

Farrell TC, Fox KM, Williams RL, Fukai S, Lewin LG (2006a) Minimising cold damage during reproductive development among temperate rice genotypes. II. Genotypic variation and flowering traits related to cold tolerance screening. Australian Journal of Agricultural Research 57, 89–100.
Minimising cold damage during reproductive development among temperate rice genotypes. II. Genotypic variation and flowering traits related to cold tolerance screening.Crossref | GoogleScholarGoogle Scholar |

Farrell TC, Fukai S, Williams RL (2006b) Minimising cold damage during reproductive development among temperate rice genotypes. I. Avoiding low temperature with the use of appropriate sowing time and photoperiod-sensitive varieties. Australian Journal of Agricultural Research 57, 75–88.
Minimising cold damage during reproductive development among temperate rice genotypes. I. Avoiding low temperature with the use of appropriate sowing time and photoperiod-sensitive varieties.Crossref | GoogleScholarGoogle Scholar |

Gunawardena TA, Fukai S (2005) The interaction of nitrogen application and temperature during reproductive stage on spikelet sterility in field-grown rice. Australian Journal of Agricultural Research 56, 625–636.
The interaction of nitrogen application and temperature during reproductive stage on spikelet sterility in field-grown rice.Crossref | GoogleScholarGoogle Scholar |

Gunawardena TA, Fukai S, Blamey FPC (2003) Low temperature induced spikelet sterility in rice. I. Nitrogen fertilisation and sensitive reproductive period. Australian Journal of Agricultural Research 54, 937–946.
Low temperature induced spikelet sterility in rice. I. Nitrogen fertilisation and sensitive reproductive period.Crossref | GoogleScholarGoogle Scholar |

Husson F, Josse J, Le S, Mazet J (2015) FactoMineR: Multivariate Exploratory Data Analysis and Data Mining. France. http://factominer.free.fr

Isbell R (2002) ‘The Australian soil classification.’ (CSIRO Publishing: Melbourne)

Ito N (1978) Male-sterility caused by cooling treatment at young microspore stage in rice plants. 16. Changes in carbohydrates, nitrogenous and phosphorus-compounds in rice anthers after cooling treatment. Japanese Journal of Crop Science 47, 318–323.
Male-sterility caused by cooling treatment at young microspore stage in rice plants. 16. Changes in carbohydrates, nitrogenous and phosphorus-compounds in rice anthers after cooling treatment.Crossref | GoogleScholarGoogle Scholar |

Kassambara A (2015) factoextra: Visualization of the outputs of a multivariate analysis. R Package version 1.0.1. www.sthda.com/english/rpkgs/factoextra/ (accessed October 2015)

Khan DR, Mackill DJ, Vergara BS (1986) Selection for tolerance to low temperature-induced spikelet sterility at anthesis in rice1. Crop Science 26, 694–698.
Selection for tolerance to low temperature-induced spikelet sterility at anthesis in rice1.Crossref | GoogleScholarGoogle Scholar |

Kobayashi K, Matsui T, Murata Y, Yamamoto M (2011) Percentage of dehisced thecae and length of dehiscence control pollination stability of rice cultivars at high temperatures. Plant Production Science 14, 89–95.
Percentage of dehisced thecae and length of dehiscence control pollination stability of rice cultivars at high temperatures.Crossref | GoogleScholarGoogle Scholar |

Matsui T, Kagata H (2003) Characteristics of floral organs related to reliable self-pollination in rice (Oryza sativa L.). Annals of Botany 91, 473–477.
Characteristics of floral organs related to reliable self-pollination in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 12588727PubMed |

Matsui T, Omasa K (2002) Rice (Oryza sativa L.) cultivars tolerant to high temperature at flowering: anther characteristics. Annals of Botany 89, 683–687.
Rice (Oryza sativa L.) cultivars tolerant to high temperature at flowering: anther characteristics.Crossref | GoogleScholarGoogle Scholar | 12102523PubMed |

Matsui T, Kobayasi K, Kagata H, Horie T (2005) Correlation between viability of pollination and length of basal dehiscence of the theca in rice under a hot-and-humid condition. Plant Production Science 8, 109–114.
Correlation between viability of pollination and length of basal dehiscence of the theca in rice under a hot-and-humid condition.Crossref | GoogleScholarGoogle Scholar |

Nishiyama I (1982) Male-sterility caused by cooling treatment at the young microspore stage in rice plants. 23. Anther length, pollen number and the difference in susceptibility to coolness among spikelets on the panicle. Japanese Journal of Crop Science 51, 462–469.
Male-sterility caused by cooling treatment at the young microspore stage in rice plants. 23. Anther length, pollen number and the difference in susceptibility to coolness among spikelets on the panicle.Crossref | GoogleScholarGoogle Scholar |

Nishiyama I (1984) Climatic influence on pollen formation and fertilization. In ‘Developments in crop science’. Vol. 7. (Eds T Shigesaburo, T Norindo) pp. 153–171. (Elsevier: Oliver, SN)

Oliver SN, Van Dongen JT, Alfred SC, Mamun EA, Zhao XC, Saini HS, Fernandes SF, Blanchard CL, Sutton BG, Geigenberger P, Dennis ES, Dolferus R (2005) Cold-induced repression of the rice anther-specific cell wall invertase gene OSINV4 is correlated with sucrose accumulation and pollen sterility. Plant, Cell and Environment 28, 1534–1551.
Cold-induced repression of the rice anther-specific cell wall invertase gene OSINV4 is correlated with sucrose accumulation and pollen sterility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnvVynuw%3D%3D&md5=2b761d75aa01b1cf379ddcb9fbdd4659CAS |

Powell B (1982) Soils of the Gatton Research Station. Queensland Department of Primary Industries Bulletin, QB82005, 21. Brisbane.

Reinke R, Beecher G, Dunn B, Snell P (2012) Temperate rice in Australia. In ‘Advances in temperate rice research’. (Eds KK Jena, B Hardy) pp. 1–14. (International Rice Research Institute: Los Baños, Philippines)

Rogers SO, Bendich AJ (1985) Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant-tissues. Plant Molecular Biology 5, 69–76.
Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant-tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXlvFalsrk%3D&md5=f437dd3f64ca456d67ade14d73eaa63aCAS | 24306565PubMed |

Saito K, Miura K, Nagano K, Hayanosaito Y, Saito A, Araki H, Kato A (1995) Chromosomal location of quantitative trait loci for cool tolerance at the booting stage in rice variety Norin-PL8. Breeding Science 45, 337–340.

Satake T (1991) Male-sterility caused by cooling treatment at the young microspore stage in rice plants. Japanese Journal of Crop Science 60, 523–528.
Male-sterility caused by cooling treatment at the young microspore stage in rice plants.Crossref | GoogleScholarGoogle Scholar |

Satake T, Hayase H (1970) Male sterility caused by cooling treatment at the young microspore stage in rice plants. V. Estimation of pollen developmental stage and the most sensitive stage to coolness. Proceedings Crop Science Society of Japan 39, 468–473.
Male sterility caused by cooling treatment at the young microspore stage in rice plants. V. Estimation of pollen developmental stage and the most sensitive stage to coolness.Crossref | GoogleScholarGoogle Scholar |

Satake T, Yoshida S (1978) High temperature-induced sterility in indica rices at flowering. Japanese Journal of Crop Science 47, 6–17.
High temperature-induced sterility in indica rices at flowering.Crossref | GoogleScholarGoogle Scholar |

Shinada H, Iwata N, Sato T, Fujino K (2013) Genetical and morphological characterization of cold tolerance at fertilization stage in rice. Breeding Science 63, 197–204.
Genetical and morphological characterization of cold tolerance at fertilization stage in rice.Crossref | GoogleScholarGoogle Scholar | 23853514PubMed |

Shinada H, Iwata N, Sato T, Fujino K (2014) QTL pyramiding for improving of cold tolerance at fertilization stage in rice. Breeding Science 63, 483–488.
QTL pyramiding for improving of cold tolerance at fertilization stage in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtVyiu7%2FL&md5=fce88bcb77ec5892c12c647be48a15b4CAS | 24757388PubMed |

Tian XH, Matsui T, Li SH, 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 Production Science 13, 243–251.
Heat-induced floret sterility of hybrid rice (Oryza sativa L.) cultivars under humid and low wind conditions in the field of Jianghan Basin, China.Crossref | GoogleScholarGoogle Scholar |

Troldahl D, Snell P, Pallas L, Ovenden B (2014) Rice variety guide – 2014–15. NSW Government, Department of Primary Industries primefact. www.dpi.nsw.gov.au/content/agriculture/broadacre/summer-crops/rice

Ye C, Fukai S, Godwin I, Reinke R, Snell P, Schiller J, Basnayake J (2009) Cold tolerance in rice varieties at different growth stages. Crop & Pasture Science 60, 328–338.
Cold tolerance in rice varieties at different growth stages.Crossref | GoogleScholarGoogle Scholar |

Ye C, Fukai S, Godwin ID, 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, 291–301.
A QTL controlling low temperature induced spikelet sterility at booting stage in rice.Crossref | GoogleScholarGoogle Scholar |

Yoshida S (1981) ‘Fundamentals of rice crop science.’ (IRRI: Los Baños, Philippines)