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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

A phenotypic marker for quantifying heat stress impact during microsporogenesis in rice (Oryza sativa L.)

Krishna S. V. Jagadish A B E , Peter Craufurd B C , Wanju Shi A D and Rowena Oane A
+ Author Affiliations
- Author Affiliations

A International Rice Research Institute, DAPO Box 7777, Metro Manila, Philippines.

B Plant Environment Laboratory, University of Reading, Cutbush Lane, Shinfield, Reading, RG2 9AF, UK.

C International Crops Research Institute for the Semiarid Tropics, Patancheru, Andhra Pradesh 502324, India.

D College of Agronomy, Hunan Agricultural University, Changsha, Hunan 410128, China.

E Corresponding author. Email: k.jagadish@irri.org

Functional Plant Biology 41(1) 48-55 https://doi.org/10.1071/FP13086
Submitted: 6 April 2013  Accepted: 3 July 2013   Published: 30 July 2013

Abstract

Gametogenesis in rice (Oryza sativa L.), and particularly male gametogenesis, is a critical developmental stage affected by different abiotic stresses. Research on this stage is limited, as flowering stage has been the major focus for research to date. Our main objective was to identify a phenotypic marker for male gametogenesis and the duration of exposure needed to quantify the impact of heat stress at this stage. Spikelet size coinciding with microsporogenesis was identified using parafilm sectioning, and the panicle (spikelet) growth rate was established. The environmental stability of the marker was ascertained with different nitrogen (75 and 125 kg ha–1) and night temperature (22°C and 28°C) combinations under field conditions. A distance of –8 to –9 cm between the collar of the last fully opened leaf and the flag leaf collar, which was yet to emerge was identified as the environmentally stable phenotypic marker. Heat stress (38°C) imposed using the identified marker induced 8–63% spikelet sterility across seven genetically diverse rice genotypes. Identifying the right stage based on the marker information and imposing 6 consecutive days of heat stress ensures that >95% of the spikelets in a panicle are stressed spanning across the entire microsporogenesis stage.

Additional keywords: flag leaf, heat stress, microsporogenesis, rice, spikelet, tetrad formation.


References

Andaya VC, Mackill DJ (2003) QTLs conferring cold tolerance at the booting stage of rice using recombinant inbred lines from a japonica × indica cross. Theoretical and Applied Genetics 106, 1084–1090.

Bernier J, Kumar A, Ramaiah V, Spaner D, Atlin GN (2007) A large-effect QTL for grain yield under reproductive-stage drought stress in upland rice. Crop Science 47, 507–516.
A large-effect QTL for grain yield under reproductive-stage drought stress in upland rice.Crossref | GoogleScholarGoogle Scholar |

Endo M, Tsuchiya T, Hamada K, Kawamura S, Yano K, Ohshima M, Higashitani A, Watanabe M, Kawagishi-Kobayashi M (2009) High temperatures cause male sterility in rice plants with transcriptional alterations during pollen development. Plant & Cell Physiology 50, 1911–1922.
High temperatures cause male sterility in rice plants with transcriptional alterations during pollen development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVajur7E&md5=e53c5089a89a6a798e4c81565ae7961aCAS |

Hedhly A (2011) Sensitivity of flowering plant gametophytes to temperature fluctuations. Environmental and Experimental Botany 74, 9–16.
Sensitivity of flowering plant gametophytes to temperature fluctuations.Crossref | GoogleScholarGoogle Scholar |

Hobo T, Suwabe K, Aya K, Suzuki G, Yano K, Ishimizu T, Fujita M, Kikuchi S, Hamada K, Miyano M, Fujioka T, Kaneko F, Kazama T, Mizuta Y, Takahashi H, Shiono K, Nakazono M, Tsutsumi N, Nagamura Y, Kurata N, Watanabe M, Matsuoka M (2008) Various spatiotemporal expression profiles of anther-expressed genes in rice. Plant & Cell Physiology 49, 1417–1428.
Various spatiotemporal expression profiles of anther-expressed genes in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVaiurrO&md5=9a7bb43057d79e9121d57873d2c6501dCAS |

IPCC (2007) Summary for policy makers. In ‘Climate change 2007: the physical science basis. Contribution of Working Group I to the fourth assessment report of the Intergovernmental Panel on Climate Change’. (Eds SD Solomon, M Qin, Z Manning, M Chen, M Marquis, KB Avery, M Tignor, HL Miller) pp. 12–25. (Cambridge University Press: Cambridge)

Jagadish SVK, Craufurd PQ, Wheeler TR (2008) Phenotyping parents of mapping populations of rice (Oryza sativa L.) for heat tolerance during anthesis. Crop Science 48, 1140–1146.
Phenotyping parents of mapping populations of rice (Oryza sativa L.) for heat tolerance during anthesis.Crossref | GoogleScholarGoogle Scholar |

Jagadish SVK, Muthurajan R, Oane R, Wheeler TR, Heuer S, Bennett J, Craufurd PQ (2010a) Physiological and proteomic approaches to address heat tolerance during anthesis in rice (Oryza sativa L.). Journal of Experimental Botany 61, 143–156.
Physiological and proteomic approaches to address heat tolerance during anthesis in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFGgu7fJ&md5=824447bac181c9375fb1d2d3527a603aCAS |

Jagadish SVK, Cairns J, Lafitte R, Wheeler TR, Price AH, Craufurd PQ (2010b) Genetic analysis of heat tolerance at anthesis in rice. Crop Science 50, 1633–1641.
Genetic analysis of heat tolerance at anthesis in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1Omur7P&md5=adb9e9c55594b2836d6316860177fe83CAS |

Jagadish SVK, Muthurajan R, Rang ZW, Malo R, Heuer S, Bennett J, Craufurd PQ (2011) Spikelet proteomic response to combined water deficit and heat stress in rice (Oryza sativa cv. N22). Rice 4, 1–11.
Spikelet proteomic response to combined water deficit and heat stress in rice (Oryza sativa cv. N22).Crossref | GoogleScholarGoogle Scholar |

Ji X, Shiran B, Wan J, Lewis DC, Jenkins CLD, Condon AG, Richards RA, Dolferus R (2010) Importance of pre-anthesis anther sink strength for maintenance of grain number during reproductive stage water stress in wheat. Plant, Cell & Environment 33, 926–942.
Importance of pre-anthesis anther sink strength for maintenance of grain number during reproductive stage water stress in wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnvVagsb4%3D&md5=ab34326906c510141684c61d9ebd9f21CAS |

Ji X, Dong B, Shiran B, Talbot MJ, Edlington JE, Hughes T, White RG, Gubler F, Dolferus R (2011) Control of abscisic acid catabolism and abscisic acid homeostasis is important for reproductive stage stress tolerance in cereals. Plant Physiology 156, 647–662.
Control of abscisic acid catabolism and abscisic acid homeostasis is important for reproductive stage stress tolerance in cereals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvFWrsb0%3D&md5=e3716879b786ec48e4b494595ef41142CAS | 21502188PubMed |

Kerim T, Imin N, Weinman JJ, Rolfe BG (2003) Proteome analysis of male gametophyte development in rice anthers. Proteomics 3, 738–751.
Proteome analysis of male gametophyte development in rice anthers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjvFGisbw%3D&md5=ac1eaa7536f1650e4f917f474777ad3cCAS | 12748952PubMed |

Kumar A, Bernier J, Verulkar S, Lafitte HR, Atlin GN (2008) Breeding for drought tolerance: direct selection for yield, response to selection and use of drought-tolerant donors in upland and lowland-adapted populations. Field Crops Research 107, 221–231.
Breeding for drought tolerance: direct selection for yield, response to selection and use of drought-tolerant donors in upland and lowland-adapted populations.Crossref | GoogleScholarGoogle Scholar |

Liu JX, Bennett J (2011) Reversible and irreversible drought-induced changes in the anther proteome of rice (Oryza sativa L.) genotypes IR64 and Moroberekan. Molecular Plant 4, 59–69.
Reversible and irreversible drought-induced changes in the anther proteome of rice (Oryza sativa L.) genotypes IR64 and Moroberekan.Crossref | GoogleScholarGoogle Scholar | 20643753PubMed |

Matsui T, Omasa K, Horie T (2000) High temperature at flowering inhibits swelling of pollen grains, a driving force for thecae dehiscence in rice (Oryza sativa L.). Plant Production Science 3, 430–434.
High temperature at flowering inhibits swelling of pollen grains, a driving force for thecae dehiscence in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar |

Nishiyama I (1970) Male sterility caused by cooling treatment at the meiotic stage in rice plants. IV: Respiratory activity of anthers following cooling treatment at the meiotic stage. Proceedings of the Crop Science Society of Japan 39, 65–70.
Male sterility caused by cooling treatment at the meiotic stage in rice plants. IV: Respiratory activity of anthers following cooling treatment at the meiotic stage.Crossref | GoogleScholarGoogle Scholar |

Nishiyama I (1976) Male sterility caused by cooling treatment at the young microspore stage in rice plants. Proceedings of the Crop Science Society of Japan 45, 254–262.
Male sterility caused by cooling treatment at the young microspore stage in rice plants.Crossref | GoogleScholarGoogle Scholar |

Oliver SN, Dongen JTV, Alfred SC, Mamun EA, Zhao X, 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 & 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=61187d8cd2d8b60481e114a0ae1ed2a6CAS |

Oliver SN, Dennis ES, Dolferus R (2007) ABA regulates apoplastic sugar transport and is a potential signal for cold-induced pollen sterility in rice. Plant & Cell Physiology 48, 1319–1330.
ABA regulates apoplastic sugar transport and is a potential signal for cold-induced pollen sterility in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFyksrfO&md5=e0e918be0287c30e2cef7a2da64512b3CAS |

Peet MM, Willits DH, Gardner R (1997) Response of ovule development and post-pollen production processes in male-sterile tomatoes to chronic, sub-acute high temperature stress. Journal of Experimental Botany 48, 101–111.
Response of ovule development and post-pollen production processes in male-sterile tomatoes to chronic, sub-acute high temperature stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhtlensrY%3D&md5=ee068b7a0146569fc840927767d00771CAS |

Prasad PVV, Boote KJ, Allen LH, Sheehy JE, Thomas JMG (2006) Species, ecotype and cultivar differences in spikelet fertility and harvest index of rice in response to high temperature stress. Field Crops Research 95, 398–411.
Species, ecotype and cultivar differences in spikelet fertility and harvest index of rice in response to high temperature stress.Crossref | GoogleScholarGoogle Scholar |

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

Shi W, Muthurajan R, Rahman H, Selvam J, Peng S, Zou Y, Jagadish KSV (2013) Source–sink dynamics and proteomic reprogramming under elevated night temperature and their impact on rice yield and grain quality. New Phytologist 197, 825–837.
Source–sink dynamics and proteomic reprogramming under elevated night temperature and their impact on rice yield and grain quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmslKlsA%3D%3D&md5=f17c73b41494cf5774ef1577adfdf5c3CAS | 23252708PubMed |

Thakur P, Kumar S, Malik JA, Berger JD, Nayyar H (2010) Cold stress effects on reproductive development in grain crops: an overview. Environmental and Experimental Botany 67, 429–443.
Cold stress effects on reproductive development in grain crops: an overview.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVGmur3L&md5=3f83e933c5994a5205437fb9cca9053cCAS |

Venuprasad R, Sta Cruz MT, Amante M, Magbanua R, Kumar A, Atlin GN (2008) Response to two cycles of divergent selection for grain yield under drought stress in four rice breeding populations. Field Crops Research 107, 232–244.
Response to two cycles of divergent selection for grain yield under drought stress in four rice breeding populations.Crossref | GoogleScholarGoogle Scholar |

Wassmann R, Jagadish SVK, Sumfleth K, Pathak H, Howell G, Ismail A, Serraj R, Redoña E, Singh RK, Heuer S (2009) Regional vulnerability of climate change impacts on Asian rice production and scope for adaptation. Advances in Agronomy 102, 91–133.
Regional vulnerability of climate change impacts on Asian rice production and scope for adaptation.Crossref | GoogleScholarGoogle Scholar |

Yoshida S, Satake T, Mackill DS (1981) High temperature stress in rice. IRRI Research Paper Series 67.

Zinn KE, Tunc-Ozdemir M, Harper JF (2010) Temperature stress and plant sexual reproduction: uncovering the weakest links. Journal of Experimental Botany 61, 1959–1968.
Temperature stress and plant sexual reproduction: uncovering the weakest links.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlsFGjsb8%3D&md5=ce84baf2fe4fd96620635590a97ad30cCAS | 20351019PubMed |