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Research paper | Open Access

Response of spikelet water status to high temperature and its relationship with heat tolerance in rice

Wencheng Wanga, Kehui Cuia,b( ), Qiuqian Hua, Chao Wua,1, Guohui Lia,2, Jianliang Huanga, Shaobing Penga
National Key Laboratory of Crop Genetic Improvement, MOA Key Laboratory of Crop Ecophysiology and Farming System in the Middle Reaches of the Yangtze River, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, Hubei, China
Hubei Collaborative Innovation for Grain Industry, Yangtze University, Jingzhou 434023, Hubei, China

1 Present address: Guangxi Key Laboratory of Functional Phytochemicals Research and Utilization, Guangxi Institute of Botany, the Chinese Academy of Sciences, Guilin 541006, Guangxi, China.

2 Present address: College of Agronomy, Yangzhou University, Yangzhou 221116, Jiangsu, China.

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Abstract

In rice, high-temperature stress (HT) during flowering results in decreased grain yield via a reduction in spikelet fertility; however, the effect of plant water status on spikelet fertility under HT remains unknown. To investigate the relationship between spikelet water status and spikelet fertility under HT, two experiments were performed under temperature-controlled conditions using four genotypes with varying tolerance to HT. Rice plants were exposed to HT for seven consecutive days during the flowering stage under three soil water treatments (soil water potential 0, −20, and −40 kPa), as well as under hydroponic conditions in a separate experiment. HT significantly decreased spikelet fertility, pollen fertility, and anther dehiscence under each of the three water treatments. HT significantly increased the spikelet transpiration rate, and this change was accompanied by a significant decrease in the internal temperature of the spikelets. HT decreased pollen grain diameter in heat-sensitive genotypes. HT had varying effects on the water potential of panicles and anthers but increased anther soluble-sugar concentration. Different aquaporin genes showed different expression profiles under HT, and the expression levels of PIPs for plasma membrane intrinsic proteins and TIPs for tonoplast intrinsic proteins increased in anthers but decreased in glumes. Correlation analyses showed that anther dehiscence and pollen (spikelet) fertility were tightly associated with anther water status, and the expression levels of almost all anther aquaporin genes were significantly correlated with anther dehiscence under HT. In summary, an increased spikelet transpiration rate and decreased internal spikelet temperature were associated with alleviation of the effects of HT in rice genotypes with varying degrees of heat tolerance, and the response of spikelet water status to HT, involving increased total expression of aquaporins and soluble sugar content, thereby improved pollen fertility, anther dehiscence, and spikelet fertility, especially in heat-resistant genotypes. The heat-resistant genotypes N22 and SY63 may adopt different approaches to reduce heat damage.

Keywords

Heat stressRice (Oryza sativa L.)AquaporinsSpikelet fertilitySpikelet water status

References

[1]

J. Zhang, X.M. Li, H.X. Lin, K. Chong, Crop improvement through temperature resilience, Annu. Rev. Plant Biol. 70 (2019) 753-780.
Crossref Google Scholar
[2]
Gaupp F. Hall J. Mitchell D. Dadson S. Increasing risks of multiple breadbasket failure under 1.5 and 2 ℃ global warmingAgric. Syst.2019175344510.1016/j.agsy.2019.05.010

F. Gaupp, J. Hall, D. Mitchell, S. Dadson, Increasing risks of multiple breadbasket failure under 1.5 and 2 ℃ global warming, Agric. Syst. 175 (2019) 34-45.
Crossref Google Scholar
[3]
N. Alexandratos, J. Bruinsma, World agriculture towards 2030/2050: the 2012 revision, ESA Working Papers 12-03, 2012, https://doi.org/10.22004/ag.econ.288998.
[4]

D.K. Ray, N.D. Mueller, P.C. West, J.A. Foley, J.P. Hart, Yield trends are insufficient to double global crop production by 2050, PLoS ONE 8 (2013) e66428.
Crossref Google Scholar
[5]

P.A.J. van Oort, S.J. Zwart, Impacts of climate change on rice production in Africa and causes of simulated yield changes, Glob. Chang. Biol. 24 (2018) 1029-1045.
Crossref Google Scholar
[6]

S. Peng, J. Huang, J.E. Sheehy, R.C. Laza, R.M. Visperas, X. Zhong, G.S. Centeno, G.S. Khush, K.G. Cassman, Rice yields decline with higher night temperature from global warming, Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 9971-9975.
Crossref Google Scholar
[7]

J.R. Welch, J.R. Vincent, M. Auffhammer, P.F. Moya, A. Dobermann, D. Dawe, Rice yields in tropical/subtropical Asia exhibit large but opposing sensitivities to minimum and maximum temperatures, Proc. Natl. Acad. Sci. U. S. A. 107 (2010) 14562-14567.
Crossref Google Scholar
[8]

N.B. Lyman, K.S.V. Jagadish, L.L. Nalley, B.L. Dixon, T. Siebenmorgen, Neglecting rice milling yield and quality underestimates economic losses from high-temperature stress, PLoS ONE 8 (2013) e72157.
Crossref Google Scholar
[9]

W.S. Jung, K.J. Lee, B.W. Lee, Responses of spikelet fertility to air, spikelet, and panicle temperatures and vapor pressure deficit in rice, J. Crop Sci. Biotechnol. 18 (2015) 209-218.
Crossref Google Scholar
[10]

W.M.W. Weerakoon, A. Maruyama, K. Ohba, Impact of humidity on temperature-induced grain sterility in rice (Oryza sativa L.), J. Agron. Crop Sci. 194 (2008) 135-140.
Crossref Google Scholar
[11]

C. Yan, Y. Ding, Q. Wang, Z. Liu, G. Li, I. Muhammad, S. Wang, The impact of relative humidity, genotypes and fertilizer application rates on panicle, leaf temperature, fertility and seed setting of rice, J. Agric. Sci. 148 (2010) 329-339.
Crossref Google Scholar
[12]

C. Julia, M. Dingkuhn, Predicting temperature induced sterility of rice spikelets requires simulation of crop-generated microclimate, Eur. J. Agron. 49 (2013) 50-60.
Crossref Google Scholar
[13]

C. Zhang, G. Fu, X. Yang, Y. Yang, X. Zhao, T. Chen, X. Zhang, Q. Jin, L. Tao, Heat stress effects are stronger on spikelets than on flag leaves in rice due to differences in dissipation capacity, J. Agron. Crop Sci. 202 (2016) 394-408.
Crossref Google Scholar
[14]

T. Matsui, K. Kobayasi, M. Yoshimoto, T. Hasegawa, 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 (2007) 57-63.
Crossref Google Scholar
[15]

M. Fukuoka, M. Yoshimoto, T. Hasegawa, Varietal range in transpiration conductance of flowering rice panicle and its impact on panicle temperature, Plant Prod. Sci. 15 (2012) 258-264.
Crossref Google Scholar
[16]

T. Matsui, K. Kobayasi, H. Kagata, T. Horie, Correlation between viability of pollination and length of basal dehiscence of the theca in rice under a hot-and-humid condition, Plant Prod. Sci. 8 (2005) 109-114.
Crossref Google Scholar
[17]

S.V.K. Jagadish, R. Muthurajan, R. Oane, T.R. Wheeler, S. Heuer, J. Bennett, P.Q. Craufurd, Physiological and proteomic approaches to address heat tolerance during anthesis in rice (Oryza sativa L.), J. Exp. Bot. 61 (2010) 143-156.
Crossref Google Scholar
[18]

C. Wu, K. Cui, W. Wang, Q. Li, S. Fahad, Q. Hu, J. Huang, L. Nie, S. Peng, Heat-induced phytohormone changes are associated with disrupted early reproductive development and reduced yield in rice, Sci. Rep. 6 (2016) 34978.
Crossref Google Scholar
[19]

O. Coast, A.J. Murdoch, R.H. Ellis, F.R. Hay, K.S.V. Jagadish, Resilience of rice (Oryza spp.) pollen germination and tube growth to temperature stress, Plant Cell Environ. 39 (2016) 26-37.
Crossref Google Scholar
[20]

T. Matsui, K. Omasa, T. Horie, The difference in sterility due to high temperatures during the flowering period among japonica-rice varieties, Plant Prod. Sci. 4 (2001) 90-93.
Crossref Google Scholar
[21]

W. Shi, X. Li, R.C. Schmidt, P.C. Struik, X. Yin, S.V.K. Jagadish, Pollen germination and in vivo fertilization in response to high-temperature during flowering in hybrid and inbred rice, Plant Cell Environ. 41 (2018) 1287-1297.
Crossref Google Scholar
[22]

L. Beauzamy, N. Nakayama, A. Boudaoud, Flowers under pressure: ins and outs of turgor regulation in development, Ann. Bot. 114 (2014) 1517-1533.
Crossref Google Scholar
[23]

C.J. Keijzer, The processes of anther dehiscence and pollen dispersal I. the opening mechanism of longitudinally dehiscing anthers, New Phytol. 105 (1987) 478-498.
Crossref Google Scholar
[24]

T. Matsui, K. Omasa, T. Horie, Rapid swelling of pollen grains in response to floret opening unfolds anther locules in rice (Oryza sativa L.), Plant Prod. Sci. 2 (1999) 196-199.
Crossref Google Scholar
[25]

T. Matsui, K. Omasa, T. Horie, High temperature at flowering inhibits swelling of pollen grains, a driving force for thecae dehiscence in rice (Oryza sativa L.), Plant Prod. Sci. 3 (2000) 430-434.
Crossref Google Scholar
[26]

Y. Pécrix, G. Rallo, H. Folzer, M. Cigna, S. Gudin, M. Le Bris, Polyploidization mechanisms: temperature environment can induce diploid gamete formation in Rosa sp., J. Exp. Bot. 62 (2011) 3587-3597.
Crossref Google Scholar
[27]

S. Ku, H. Yoon, H.S. Suh, Y.Y. Chung, Male-sterility of thermosensitive genic male-sterile rice is associated with premature programmed cell death of the tapetum, Planta 217 (2003) 559-565.
Crossref Google Scholar
[28]

M. Djanaguiraman, R. Perumal, S.V.K. Jagadish, I.A. Ciampitti, R. Welti, P.V.V. Prasad, Sensitivity of sorghum pollen and pistil to high-temperature stress, Plant Cell Environ. 41 (2018) 1065-1082.
Crossref Google Scholar
[29]

R.W. Parish, H.A. Phan, S. Iacuone, S.F. Li, Tapetal development and abiotic stress: a centre of vulnerability, Funct. Plant Biol. 39 (2012) 553.
Crossref Google Scholar
[30]

X. Li, L.M. Lawas, R. Malo, U. Glaubitz, A. Erban, R. Mauleon, S. Heuer, E. Zuther, J. Kopka, D.K. Hincha, K.S. Jagadish, Metabolic and transcriptomic signatures of rice floral organs reveal sugar starvation as a factor in reproductive failure under heat and drought stress, Plant Cell Environ. 38 (2015) 2171-2192.
Crossref Google Scholar
[31]

L. Min, Y. Li, Q. Hu, L. Zhu, W. Gao, Y. Wu, Y. Ding, S. Liu, X. Yang, X. Zhang, Sugar and auxin signaling pathways respond to high-temperature stress during anther development as revealed by transcript profiling analysis in cotton, Plant Physiol. 164 (2014) 1293-1308.
Crossref Google Scholar
[32]

D.E. Aylor, Rate of dehydration of corn (Zea mays L.) pollen in the air, J. Exp. Bot. 54 (2003) 2307-2312.
Crossref Google Scholar
[33]

Z.P. Song, B.R. Lu, J.K. Chen, A study of pollen viability and longevity in Oryza rufipogon, O. sativa, and their hybrids, Int. Rice Res. Notes. 26 (2001) 31-32.
Google Scholar
[34]

A. Marceau, S. Saint-Jean, B. Loubet, X. Foueillassar, L. Huber, Biophysical characteristics of maize pollen: Variability during emission and consequences on cross-pollination risks, Field Crops Res. 127 (2012) 51-63.
Crossref Google Scholar
[35]

A. Wahid, T.J. Close, Expression of dehydrins under heat stress and their relationship with water relations of sugarcane leaves, Biol. Plant. 51 (2007) 104-109.
Crossref Google Scholar
[36]

S. Rehman, S.J. Yun, Developmental regulation of K accumulation in pollen, anthers, and papillae: are anther dehiscence, papillae hydration, and pollen swelling leading to pollination and fertilization in barley (Hordeum vulgare L.) regulated by changes in K concentration? J. Exp. Bot. 57 (2006) 1315-1321.
Crossref Google Scholar
[37]

F. Chaumont, S.D. Tyerman, Aquaporins: highly regulated channels controlling plant water relations, Plant Physiol. 164 (2014) 1600-1618.
Crossref Google Scholar
[38]

M. Bots, F. Vergeldt, M. Wolters-Arts, K. Weterings, H. van As, C. Mariani, Aquaporins of the PIP2 class are required for efficient anther dehiscence in tobacco, Plant Physiol. 137 (2005) 1049-1056.
Crossref Google Scholar
[39]

Z. Tong, Q. Li, Y. Yang, F. Dai, J. Gao, B.o. Hong, Isolation and expression analysis of LoPIP2, a lily (Lilium Oriental Hybrids) aquaporin gene involved in desiccation-induced anther dehiscence, Sci. Hortic. 164 (2013) 316-322.
Crossref Google Scholar
[40]

G. Soto, K. Alleva, M.A. Mazzella, G. Amodeo, J.P. Muschietti, AtTIP1;3 and AtTIP5;1, the only highly expressed Arabidopsis pollen-specific aquaporins, transport water and urea, FEBS Lett. 582 (2008) 4077-4082.
Crossref Google Scholar
[41]

J.A.P. Di Giorgio, G.P. Bienert, N.D. Ayub, A. Yaneff, M.L. Barberini, M.A. Mecchia, G. Amodeo, G.C. Soto, J.P. Muschietti, Pollen-specific aquaporins NIP4;1 and NIP4;2 are required for pollen development and pollination in Arabidopsis thaliana, Plant Cell 28 (2016) 1053-1077.
Crossref Google Scholar
[42]

G. Soto, R. Fox, N. Ayub, K. Alleva, F. Guaimas, E.J. Erijman, A. Mazzella, G. Amodeo, J. Muschietti, TIP5;1 is an aquaporin specifically targeted to pollen mitochondria and is probably involved in nitrogen remobilization in Arabidopsis thaliana, Plant J. 64 (2010) 1038-1047.
Crossref Google Scholar
[43]

J.A. Pérez Di Giorgio, M.L. Barberini, G. Amodeo, J.P. Muschietti, Pollen aquaporins: what are they there for? Plant Signal. Behav. 11 (2016) e1217375.
Crossref Google Scholar
[44]

Z. Wang, H. Li, X. Liu, Y. He, H. Zeng, Reduction of pyruvate orthophosphate dikinase activity is associated with high temperature-induced chalkiness in rice grains, Plant Physiol. Biochem. 89 (2015) 76-84.
Crossref Google Scholar
[45]

C. Wu, K. Cui, W. Wang, Q. Li, S. Fahad, Q. Hu, J. Huang, L. Nie, P.K. Mohapatra, S. Peng, Heat-induced cytokinin transportation and degradation are associated with aeduced panicle cytokinin expression and fewer spikelets per panicle in rice, Front. Plant Sci. 8 (2017) 371.
Crossref Google Scholar
[46]
S. Yoshida, D.A. Forno, J.H. Cock, K.A. Gomez, Laboratory manual for physiological studies of rice, International Rice Research Institute Press, Manila, the Philippines, 1976.
[47]

T.A. Gunawardena, S. Fukai, F.P.C. Blamey, Low temperature induced spikelet sterility in rice. II. Effects of panicle and root temperatures, Aust. J. Agric. Res. 54 (2003) 947-995.
Crossref Google Scholar
[48]

K.J. Livak, T.D. Schmittgen, Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method, Methods 25 (2001) 402-408.
Crossref Google Scholar
[49]

Z.W. Rang, S.V.K. Jagadish, Q.M. Zhou, P.Q. Craufurd, S. Heuer, Effect of high temperature and water stress on pollen germination and spikelet fertility in rice, Environ. Exp. Bot. 70 (2011) 58-65.
Crossref Google Scholar
[50]

S.V.K. Jagadish, M. Raveendran, Z.W. Rang, R. Malo, S. Heuer, J. Bennett, P.Q. Craufurd, Spikelet proteomic response to combined water deficit and heat stress in rice (Oryza sativa cv. N22), Rice 4 (2011) 1-11.
Crossref Google Scholar
[51]

J.X. Liu, D.Q. Liao, R. Oane, L. Estenor, X.E. Yang, Z.C. Li, J. Bennett, Genetic variation in the sensitivity of anther dehiscence to drought stress in rice, Field Crops Res. 97 (2006) 87-100.
Crossref Google Scholar
[52]

N. Firon, M. Nepi, E. Pacini, Water status and associated processes mark critical stages in pollen development and functioning, Ann. Bot. 109 (2012) 1201-1213.
Crossref Google Scholar
[53]

S.V.K. Jagadish, M.V.R. Murty, W.P. Quick, Rice responses to rising temperatures-challenges, perspectives and future directions, Plant Cell Environ. 38 (2015) 1686-1698.
Crossref Google Scholar
[54]

L.M.F. Lawas, W. Shi, M. Yoshimoto, T. Hasegawa, D.K. Hincha, E. Zuther, S.V.K. Jagadish, Combined drought and heat stress impact during flowering and grain filling in contrasting rice cultivars grown under field conditions, Field Crops Res. 229 (2018) 66-77.
Crossref Google Scholar
[55]

M. Nepi, L. Cresti, M. Guarnieri, E. Pacini, Effect of relative humidity on water content, viability and carbohydrate profile of Petunia hybrida and Cucurbita pepo pollen, Plant Syst. Evol. 284 (2010) 57-64.
Crossref Google Scholar
[56]

S. Das, P. Krishnan, M. Nayak, B. Ramakrishnan, High temperature stress effects on pollens of rice (Oryza sativa L.) genotypes, Environ. Exp. Bot. 101 (2014) 36-46.
Crossref Google Scholar
[57]

J. Sakurai, F. Ishikawa, T. Yamaguchi, M. Uemura, M. Maeshima, Identification of 33 rice aquaporin genes and analysis of their expression and function, Plant Cell Physiol. 46 (2005) 1568-1577.
Crossref Google Scholar
[58]

H. Hayashi, J. Ishikawa-Sakurai, M. Murai-Hatano, A. Ahamed, M. Uemura, Aquaporins in developing rice grains, Biosci. Biotechnol. Biochem. 79 (2015) 1422-1429.
Crossref Google Scholar
[59]

C. Maurel, L. Verdoucq, O. Rodrigues, Aquaporins and plant transpiration, Plant Cell Environ. 39 (2016) 2580-2587.
Crossref Google Scholar
[60]

F. Xu, K. Wang, W. Yuan, W. Xu, S. Liu, H.J. Kronzucker, G. Chen, R. Miao, M. Zhang, M. Ding, L. Xiao, L. Kai, J. Zhang, Y. Zhu, Overexpression of rice aquaporin OsPIP1;2 improves yield by enhancing mesophyll CO2 conductance and phloem sucrose transport, J. Exp. Bot. 70 (2019) 671-681.
Crossref Google Scholar
[61]

R.K. Vandeleur, G. Mayo, M.C. Shelden, M. Gilliham, B.N. Kaiser, S.D. Tyerman, The role of plasma membrane intrinsic protein aquaporins in water transport through roots: diurnal and drought stress responses reveal different strategies between isohydric and anisohydric cultivars of grapevine, Plant Physiol. 149 (2009) 445-460.
Crossref Google Scholar
[62]

A. Pou, H. Medrano, J. Flexas, S.D. Tyerman, A putative role for TIP and PIP aquaporins in dynamics of leaf hydraulic and stomatal conductances in grapevine under water stress and re-watering, Plant Cell Environ. 36 (2013) 828-843.
Crossref Google Scholar
[63]

B. Parent, C. Hachez, E. Redondo, T. Simonneau, F. Chaumont, F. Tardieu, Drought and abscisic acid effects on aquaporin content translate into changes in hydraulic conductivity and leaf growth rate: a trans-scale approach, Plant Physiol. 149 (2009) 2000-2012.
Crossref Google Scholar
[64]

Z. Qian, J. Song, F. Chaumont, Q. Ye, Differential responses of plasma membrane aquaporins in mediating water transport of cucumber seedlings under osmotic and salt stresses, Plant Cell Environ. 38 (2015) 461-473.
Crossref Google Scholar
[65]

A. Maruyama, W.M.W. Weerakoon, Y. Wakiyama, K. Ohba, Effects of increasing temperatures on spikelet fertility in different rice cultivars based on temperature gradient chamber experiments, J. Agron. Crop Sci. 199 (2013) 416-423.
Crossref Google Scholar
[66]

T.P. Gotame, D.W. Cullen, J. Graham, P.E. Hedley, K. Smith, J. Morris, L. Andersen, K.K. Petersen, Effect of short-term exposure to high-temperature on total gene expression in the leaves of four raspberry (Rubus idaeus L.) cultivars, J. Hortic. Sci. Biotechnol. 89 (2014) 532-541.
Crossref Google Scholar
[67]

P.V.V. Prasad, K.J. Boote, L.H. Allen, J.E. Sheehy, J.M.G. Thomas, Species, ecotype and cultivar differences in spikelet fertility and harvest index of rice in response to high temperature stress, Field Crops Res. 95 (2006) 398-411.
Crossref Google Scholar
[68]

T. Satake, S. Yoshida, High temperature-induced sterility in India rice at flowering, Jpn. J. Crop Sci. 47 (1978) 6-17.
Crossref Google Scholar
[69]

D.S. Selote, R. Khanna-Chopra, Drought-induced spikelet sterility is associated with an inefficient antioxidant defence in rice panicles, Physiol. Plant. 121 (2004) 462-471.
Crossref Google Scholar
The Crop Journal
Volume 9 Issue 6,
December 2021
Pages 1344-1356
DOI: 10.1016/j.cj.2020.11.010
Cite this article:
Wang W, Cui K, Hu Q, et al. Response of spikelet water status to high temperature and its relationship with heat tolerance in rice. The Crop Journal, 2021, 9(6): 1344-1356. https://doi.org/10.1016/j.cj.2020.11.010

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Received: 25 July 2020
Revised: 11 November 2020
Accepted: 18 November 2020
Published: 26 January 2021
© 2021 Crop Science Society of China and Institute of Crop Science, CAAS.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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