High night temperature induces contrasting responses for spikelet fertility, spikelet tissue temperature, flowering characteristics and grain quality in rice
Onoriode Coast A B C , Richard H. Ellis A , Alistair J. Murdoch A , Cherryl Quiñones B and Krishna S. V. Jagadish B D
+ Author Affiliations
- Author Affiliations
A School of Agriculture, Policy and Development, University of Reading, Earley Gate, PO Box 237, Reading, RG6 6AR, UK.
B Crop and Environmental Sciences Division, International Rice Research Institute, DAPO Box 7777, Metro Manila, Philippines.
C Present address: CSIRO Agriculture Flagship, Locked Mail Bag 59, Narrabri, NSW 2390, Australia.
D Corresponding author. Email: k.jagadish@irri.org
Functional Plant Biology 42(2) 149-161 https://doi.org/10.1071/FP14104
Submitted: 2 April 2014 Accepted: 19 July 2014 Published: 4 September 2014
Abstract
Climate change is increasing night temperature (NT) more than day temperature (DT) in rice-growing areas. Effects of combinations of NT (24−35°C) from microsporogenesis to anthesis at one or more DT (30 or 35°C) at anthesis on rice spikelet fertility, temperature within spikelets, flowering pattern, grain weight per panicle, amylose content and gel consistency were investigated in contrasting rice cultivars under controlled environments. Cultivars differed in spikelet fertility response to high NT, with higher fertility associated with cooler spikelets (P < 0.01). Flowering dynamics were altered by high NT and a novel high temperature tolerance complementary mechanism, shorter flower open duration in cv. N22, was identified. High NT reduced spikelet fertility, grain weight per panicle, amylose content and gel consistency, whereas high DT reduced only gel consistency. Night temperature >27°C was estimated to reduce grain weight. Generally, high NT was more damaging to grain weight and selected grain quality traits than high DT, with little or no interaction between them. The critical tolerance and escape traits identified, i.e. spikelet cooling, relatively high spikelet fertility, earlier start and peak time of anthesis and shorter spikelet anthesis duration can aid plant breeding programs targeting resilience in warmer climates.
Additional keywords: flowering dynamics, grain quality, high night temperature, rice, spikelet fertility.
References
Cheng WG, Sakai H, Yagi K, Hasegawa T (2009) Interactions of elevated CO2 and night temperature on rice growth and yield. Agricultural and Forest Meteorology 149, 51–58.| Interactions of elevated CO2 and night temperature on rice growth and yield.Crossref | GoogleScholarGoogle Scholar |
Cooper NTW, Siebenmorgen TJ, Counce PA (2008) Effects of night time temperature during kernel development on rice physicochemical properties. Cereal Chemistry 85, 276–282.
| Effects of night time temperature during kernel development on rice physicochemical properties.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmvVajtLk%3D&md5=63fcf5348f90f8955161c72038223badCAS |
Counce PA, Keisling TC, Mitchell AJ (2000) A uniform, objective and adaptive system for expressing rice development. Crop Science 40, 436–443.
| A uniform, objective and adaptive system for expressing rice development.Crossref | GoogleScholarGoogle Scholar |
Fitzgerald MA, Resurreccion AP (2009) Maintaining the yield of edible rice in a warming world. Functional Plant Biology 36, 1037–1045.
| Maintaining the yield of edible rice in a warming world.Crossref | GoogleScholarGoogle Scholar |
Fukuoka M, Yoshimoto M, Hasegawa T (2012) MINCER: a novel instrument for monitoring the micrometeorology of rice canopies. Journal of Agricultural Meteorology 68, 135–147.
| MINCER: a novel instrument for monitoring the micrometeorology of rice canopies.Crossref | GoogleScholarGoogle Scholar |
IPCC (2013) Climate change 2013: the physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change.’ (Eds TF Stocker, D Qin, G-K Plattner, M Tignor, SK Allen, J Boschung, A Nauels, Y Xia, V Bex, PM Midgley) (Cambridge University Press, Cambridge, UK)
Ishimaru T, Hirabayashi H, Ida M, Takai T, San-Oh YA, Yoshinaga S, Ando I, Ogawa T, Motohiko K (2010) A genetic resource for early-morning flowering trait of wild rice Oryza officinalis to mitigate high temperature-induced spikelet sterility at anthesis. Annals of Botany 106, 515–520.
| A genetic resource for early-morning flowering trait of wild rice Oryza officinalis to mitigate high temperature-induced spikelet sterility at anthesis.Crossref | GoogleScholarGoogle Scholar | 20566680PubMed |
Jagadish SVK, Craufurd P, Wheeler T (2007) High temperature stress and spikelet fertility in rice (Oryza sativa L.). Journal of Experimental Botany 58, 1627–1635.
| High temperature stress and spikelet fertility in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsFeju7c%3D&md5=4e86891437742ab3e35a64ae9de41dd6CAS |
Jagadish SVK, Craufurd PQ, Wheeler TR (2008) Phenotyping parents of mapping populations of rice for heat tolerance during anthesis. Crop Science 48, 1140–1146.
| Phenotyping parents of mapping populations of rice for heat tolerance during anthesis.Crossref | GoogleScholarGoogle Scholar |
Jagadish SVK, Cairns J, Lafitte R, Wheeler TR, Price AH, Craufurd PQ (2010a) 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=c0457ca909522a7098e0268f5e3ed9bfCAS |
Jagadish SVK, Muthurajan R, Oane R, Wheeler TR, Heuer S, Bennett J, Craufurd PQ (2010b) 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=1a65f57861bbbd822cd26610b4dd14a0CAS |
Jagadish SVK, Craufurd P, Shi W, Oane R (2014) A phenotypic marker for quantifying heat stress impact during microsporogenesis in rice (Oryza sativa L.). Functional Plant Biology 41, 48–55.
| A phenotypic marker for quantifying heat stress impact during microsporogenesis in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvFCjtbfK&md5=7902622c7216452d8151b3370864c2aeCAS |
Julia C, Dingkuhn M (2012) Variation in time of day of anthesis in rice in different climatic environments. European Journal of Agronomy 43, 166–174.
| Variation in time of day of anthesis in rice in different climatic environments.Crossref | GoogleScholarGoogle Scholar |
Juliano BO (1971) A simplified assay for milled-rice amylose. Cereal Science Today 16, 334–360.
Kobayasi K, Matsui T, Yoshimoto M, Hasegawa T (2010) Effects of temperature, solar radiation, and vapor-pressure deficit on flower opening time in rice. Plant Production Science 13, 21–28.
| Effects of temperature, solar radiation, and vapor-pressure deficit on flower opening time in rice.Crossref | GoogleScholarGoogle Scholar |
Lanning SB, Siebenmorgen TJ, Counce PA, Ambardekar AA, Mauromoustakos A (2011) Extreme night time air temperatures in 2010 impact rice chalkiness and milling quality. Field Crops Research 124, 132–136.
| Extreme night time air temperatures in 2010 impact rice chalkiness and milling quality.Crossref | GoogleScholarGoogle Scholar |
Li HX, Chen Z, Hu MX, Wang ZM, Hua H, Yin CX, Zeng HL (2011) Different effects of night versus day high temperature on rice quality and accumulation profiling of rice grain proteins during grain filling. Plant Cell Reports 30, 1641–1659.
| Different effects of night versus day high temperature on rice quality and accumulation profiling of rice grain proteins during grain filling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVSitbjN&md5=db672acf88659be25f1a223c76fcf6b0CAS |
Little RR, Hilder GB, Dawson EH (1958) Differential effect of dilute alkali on 25 varieties of milled white rice. Cereal Chemistry 35, 111–126.
Liu J-X, 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 |
Lobell DB, Field CB (2007) Global scale climate–crop yield relationships and the impacts of recent warming. Environmental Research Letters 2, 014002
| Global scale climate–crop yield relationships and the impacts of recent warming.Crossref | GoogleScholarGoogle Scholar |
Lyman NB, Jagadish KSV, Nalley LL, Dixon BL, Siebenmorgen T (2013) Neglecting rice milling yield and quality underestimates economic losses from high-temperature stress. PLoS ONE 8, e72157
| Neglecting rice milling yield and quality underestimates economic losses from high-temperature stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlKls7rL&md5=b339f3dd5037be75cbc22131087c5e53CAS | 23991056PubMed |
Madan P, Jagadish SVK, Craufurd PQ, Fitzgerald M, Lafarge T, Wheeler TR (2012) Effect of elevated CO2 and high temperature on seed-set and grain quality of rice. Journal of Experimental Botany 63, 3843–3852.
| Effect of elevated CO2 and high temperature on seed-set and grain quality of rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVShtL7M&md5=4525b5953f485d8a855d0ea18a1dda93CAS | 22438302PubMed |
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, 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 |
Matsui T, Omasa K, Horie T (2001) The difference in sterility due to high temperatures during the flowering period among japonica-rice varieties. Plant Production Science 4, 90–93.
| The difference in sterility due to high temperatures during the flowering period among japonica-rice varieties.Crossref | GoogleScholarGoogle Scholar |
Mohammed AR, Tarpley L (2009a) High nighttime temperatures affect rice productivity through altered pollen germination and spikelet fertility. Agricultural and Forest Meteorology 149, 999–1008.
| High nighttime temperatures affect rice productivity through altered pollen germination and spikelet fertility.Crossref | GoogleScholarGoogle Scholar |
Mohammed AR, Tarpley L (2009b) Impact of high night time temperature on respiration, membrane stability, antioxidant capacity, and yield of rice plants. Crop Science 49, 313–322.
| Impact of high night time temperature on respiration, membrane stability, antioxidant capacity, and yield of rice plants.Crossref | GoogleScholarGoogle Scholar |
Mohammed AR, Tarpley L (2010) Effects of high night temperature and spikelet position on yield-related parameters of rice (Oryza sativa L.) plants. European Journal of Agronomy 33, 117–123.
| Effects of high night temperature and spikelet position on yield-related parameters of rice (Oryza sativa L.) plants.Crossref | GoogleScholarGoogle Scholar |
Morita S, Yonemaru J, Takanashi J (2005) Grain growth and endosperm cell size under high night temperatures in rice (Oryza sativa L.). Annals of Botany 95, 695–701.
| Grain growth and endosperm cell size under high night temperatures in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 15655104PubMed |
Nagarajan S, Jagadish SVK, Prasad ASH, Thomar AK, Anand A, Pal M, Agarwal PK (2010) Local climate affects growth, yield and grain quality of aromatic and non-aromatic rice in northwestern India. Agriculture, Ecosystems & Environment 138, 274–281.
| Local climate affects growth, yield and grain quality of aromatic and non-aromatic rice in northwestern India.Crossref | GoogleScholarGoogle Scholar |
Nashiyama I (1981) Temperature inside the flower of rice plants. Nihon Sakumotsu Gakkai Kiji 50, 54–58.
| Temperature inside the flower of rice plants.Crossref | GoogleScholarGoogle Scholar |
Parish RW, Phan HA, Iacuone S, Li SF (2012) Tapetal development and abiotic stress: a centre of vulnerability. Functional Plant Biology 39, 553–559.
| Tapetal development and abiotic stress: a centre of vulnerability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXltVyrsrY%3D&md5=94d309d075f5eeb00941a38e90043438CAS |
Peng S, Huang J, Sheehy JE, Laza RC, Visperas RM, Zhong X, Centeno GS, Khush GS, Cassman KG (2004) Rice yields decline with higher night temperature from global warming. Proceedings of the National Academy of Sciences of the United States of America 101, 9971–9975.
| Rice yields decline with higher night temperature from global warming.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvFOiu78%3D&md5=ddf63a289345b4b952bc26acf1ae9808CAS | 15226500PubMed |
Prasad PVV, Boote KJ, Allen JLH, 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 |
Rang ZW, Jagadish SVK, Zhou QM, Craufurd PQ, Heuer S (2011) Effect of high temperature and water stress on pollen germination and spikelet fertility in rice. Environmental and Experimental Botany 70, 58–65.
| Effect of high temperature and water stress on pollen germination and spikelet fertility in rice.Crossref | GoogleScholarGoogle Scholar |
Resurreccion AP, Hara T, Juliano BO, Yoshida S (1977) Effect of temperature during ripening on grain quality of rice. Soil Science and Plant Nutrition 23, 109–112.
| Effect of temperature during ripening on grain quality of rice.Crossref | GoogleScholarGoogle Scholar |
Satake T, Yoshida S (1978) High temperature-induced sterility in indica rices at flowering. Nihon Sakumotsu Gakkai Kiji 47, 6–17.
| High temperature-induced sterility in indica rices at flowering.Crossref | GoogleScholarGoogle Scholar |
Sheehy JE, Elmido A, Centeno G, Pablico PP (2005) Searching for new plants for climate change. Journal of Agricultural Meteorology 60, 463–468.
Sheehy JE, Mitchell PL, Ferrer AB (2006) Decline in rice grain yields with temperature: models and correlations can give different estimates. Field Crops Research 98, 151–156.
| Decline in rice grain yields with temperature: models and correlations can give different estimates.Crossref | GoogleScholarGoogle Scholar |
Shi W, Muthurajan R, Rahman H, Jagadeeshselvam N, 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=5a7314ed39b7c48b78d751702d930e05CAS | 23252708PubMed |
Sung DY, Kaplan F, Lee KJ, Guy CL (2003) Acquired tolerance to temperature extremes. Trends in Plant Science 8, 179–187.
| Acquired tolerance to temperature extremes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtFeqs7Y%3D&md5=f472940d14de0a842c7550106394d4b3CAS | 12711230PubMed |
Tashiro T, Wardlaw IF (1989) A comparison of the effect of high temperature on grain development in wheat and rice. Annals of Botany 64, 59–65.
Tran NA, Daygon VD, Resurreccion AP, Cuevas RP, Corpuz HM, Fitzgerald MA (2011) A single nucleotide polymorphism in the Waxy gene explains a significant component of gel consistency. Theoritical and Applied Genetics 123, 519–525.
| A single nucleotide polymorphism in the Waxy gene explains a significant component of gel consistency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpsFCqtL8%3D&md5=979b7766eaa75f90d74b2ab8702cc128CAS |
Tranel D, Knapp A, Perdomo A (2009) Chilling effects during maize tassel development and the lack of compensational plasticity. Crop Science 49, 1852–1858.
| Chilling effects during maize tassel development and the lack of compensational plasticity.Crossref | GoogleScholarGoogle Scholar |
Vose RS, Easterling DR, Gleason B (2005) Maximum and minimum temperature trends for the globe: an update through 2004. Geophysical Research Letters 32, L23822
| Maximum and minimum temperature trends for the globe: an update through 2004.Crossref | GoogleScholarGoogle Scholar |
WARDA (2008) ‘NERICA: the new rice for Africa – a compendium.’ (Eds EA Somado, RG Buei, SO Keya) (Africa Rice Center (WARDA) Headquarters: Cotonou, Benin)
Yoshida S, Satake T, Mackill DS (1981) High temperature stress in rice. International Rice Research Institute Research Paper Series 67, 1–15.
Ziska LH, Manalo PA (1996) Increasing night temperature can reduce seed set and potential yield of tropical rice. Australian Journal of Plant Physiology 23, 791–794.
| Increasing night temperature can reduce seed set and potential yield of tropical rice.Crossref | GoogleScholarGoogle Scholar |
