Hostname: page-component-76fb5796d-zzh7m Total loading time: 0 Render date: 2024-04-26T04:29:30.887Z Has data issue: false hasContentIssue false
  • English
  • Français

Spikelet fertility and heat shock transcription factor (Hsf) gene responses to heat stress in tolerant and susceptible rice (Oryza sativa L.) genotypes

Published online by Cambridge University Press:  29 August 2019

C. Malumpong Open the ORCID record for C. Malumpong [Opens in a new window] ,
S. Cheabu ,
C. Mongkolsiriwatana ,
W. Detpittayanan  and
A. Vanavichit
C. Malumpong*
Affiliation:
Department of Agronomy, Faculty of Agriculture at Kamphaeng Saen, Kasetsart University, Nakhon Pathom 73140, Thailand Rice Science Center & Rice Gene Discovery Unit, Kasetsart University, Kamphaeng Sean Campus, Nakhon Pathom 73140, Thailand
S. Cheabu
Affiliation:
Rice Science Center & Rice Gene Discovery Unit, Kasetsart University, Kamphaeng Sean Campus, Nakhon Pathom 73140, Thailand Faculty of Agriculture, Princess of Naradhiwas University, Naradhiwas 96000, Thailand
C. Mongkolsiriwatana
Affiliation:
Division of Genetics, Department of Science, Faculty of Liberal Arts and Science, Kasetsart University, Kamphaeng Sean Campus, Nakron Pathom 73140, Thailand
W. Detpittayanan
Affiliation:
Department of Agronomy, Faculty of Agriculture at Kamphaeng Saen, Kasetsart University, Nakhon Pathom 73140, Thailand
A. Vanavichit
Affiliation:
Department of Agronomy, Faculty of Agriculture at Kamphaeng Saen, Kasetsart University, Nakhon Pathom 73140, Thailand Rice Science Center & Rice Gene Discovery Unit, Kasetsart University, Kamphaeng Sean Campus, Nakhon Pathom 73140, Thailand
*
Author for correspondence: C. Malumpong, E-mail: agrcnm@ku.ac.th
Get access Rights & Permissions [Opens in a new window]

Abstract

The reproductive stage of rice is the most sensitive to heat stress, which can lead to spikelet sterility. Thus, heat-tolerant and heat-susceptible genotypes were used to investigate their differences in terms of phenotypic responses and expression changes of Hsf genes at the pre-flowering stage under heat stress. Results clearly showed that panicles had the highest temperature compared with other plant parts under both natural and heated conditions. However, the temperatures of tolerant and susceptible genotypes were not significantly different. In terms of spikelet fertility, the tolerant lines M9962 and M7988 had high seed set because their anther dehiscence, pollen viability and pollen germination were only slightly affected. In contrast, the susceptible line Sinlek showed severe effects at all steps of fertilization, and the pollen viability of M7766 was slightly affected under heat stress but was more affected in terms of anther dehiscence and pollen germination. Both susceptible lines showed dramatically decreased seed set. In addition, the expression of six HsfA genes in the flag leaves and spikelets at the R2 stage of plants under heat stress showed different responses. Notably, expression of the HsfA2a gene was predominantly upregulated in the flag leaf and spikelets under heat stress in M9962. Therefore, it can be concluded that heat stress has severe effects on the stamen, and that different genotypes have different susceptibilities to heat stress.

Keywords

Heat shock transcription factorheat stressricespikelet fertility
Type
Crops and Soils Research Paper
Information
The Journal of Agricultural Science , Volume 157 , Issue 4 , May 2019 , pp. 283 - 299
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Almoguera, C, Rojas, A, Diaz-Martin, J, Prieto-Dapena, P, Carranco, R and Jordano, J (2002) A seed-specific heat-shock transcription factor involved in developmental regulation during embryogenesis in sunflower. Journal of Biological Chemistry 277, 43866–43872.Google Scholar
Arshad, MS, Farook, M, Ash, F, Jagadish, KSV, Prasad, PVV and Siddique, KHM (2017) Thermal stress impacts reproductive development and grain yield in rice. Plant Physiology and Biochemistry 115, 57–72.Google Scholar
Ayeneh, A, van Ginkel, M, Reynolds, MP and Ammar, K (2002) Comparison of leaf, spike, peduncle and canopy temperature depression in wheat under heat stress. Field Crops Research 79, 173–184.Google Scholar
Baker, JT, Allen, LH Jr and Boote, KJ (1992) Temperature effects on rice at elevated CO2 concentration. Journal of Experimental Botany 43, 959–964.Google Scholar
Baniwal, SK, Bharti, K, Chan, KY, Fauth, M, Ganguli, A, Kotak, S, Mishra, S K, Nover, L, Port, M, Scharf, K D, Tripp, J, Weber, C, Zielinski, D and von Koskull-Döring, P (2004) Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. Journal of Biosciences 29, 471–487.Google Scholar
Barnabas, B, Jager, K and Feher, A (2008) The effect of drought and heat stress on reproductive processes in cereals. Plant, Cell and Environment 31, 11–38.Google Scholar
Cao, YY, Duan, H, Yang, LN, Wang, ZQ, Zhou, SC and Yang, JC (2008) Effect of heat stress during meiosis on grain yield of rice cultivars differing in heat tolerance and its physiological mechanism. Acta Agronomica Sinica 34, 2134–2142.Google Scholar
Cao, YY, Duan, H, Yang, LN, Wang, ZQ, Liu, LJ and Yang, JC (2009) Effect of high temperature during heading and early filling on grain yield and physiological characteristics in indica rice. Acta Agronomica Sinica 35, 512–521.Google Scholar
Chaturvedi, AK, Bahuguna, RN, Shah, D, Pal, M and Jagadish, SVK (2017) High temperature stress during flowering and grain filling offsets beneficial impact of elevated CO2 on assimilate partitioning and sink strength in rice. Scientific Reports 7, 8227.Google Scholar
Cheabu, S, Moung-Ngam, P, Arikit, S, Vanavichit, A and Malumpong, C (2018) Effects of heat stress at vegetative and reproductive stages on spikelet fertility. Rice Science 25, 218–226.Google Scholar
Cheabu, S, Panichawong, N, Rattanametta, P, Wasuri, B, Kasemsap, P, Arikit, S, Vanavichit, A and Malumpong, C (2019) Screening for spikelet fertility and validation of heat tolerance in a large rice (Oryza sativa L.) mutant population. Rice Science 26, 229–238.Google Scholar
Counce, PA, Keisling, TC and Mitchell, AJ (2000) A uniform, objective, and adaptive system for expressing rice development. Crop Science 40, 436–443.Google Scholar
Das, S, Krishnan, P, Nayak, M and Ramakrishnan, B (2014) High temperature stress effects on pollens of rice (Oryza sativa L.) genotypes. Environmental and Experimental Botany 101, 36–46.Google Scholar
Endo, M, Tsuchiya, T, Hamada, K, Kawamura, S, Yano, K, Ohshima, M, Higashitani, A, Watanabe, M and Kawagishi-Kobayashi, M (2009) High temperatures cause male sterility in rice plants with transcriptional alterations during pollen development. Plant and Cell Physiology 50, 1911–1922.Google Scholar
Folsom, JJ, Begcy, K, Hao, X, Wang, D and Walia, H (2014) Rice fertilization-independent endosperm1 regulates seed size under heat stress by controlling early endosperm development. Plant Physiology 165, 238–248.Google Scholar
Fu, G, Feng, B, Zhang, C, Yang, Y, Yang, X, Chen, T, Zhao, X, Zhang, X, Jin, Q and Tao, L (2016) Heat stress is more damaging to superior spikelets than inferiors of rice (Oryza sativa L.) due to their different organ temperatures. Frontiers in Plant Science 8, 1637.Google Scholar
Hartl, FU and Hayer-Hartl, M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295, 1852–1858.Google Scholar
IPCC (2014) Summary for policy makers. In Climate Change 2014; Mitigation of Climate Change. Cambridge, UK: Cambridge University Press, pp. 1–32.Google Scholar
IRRI (2013) Temperature. In Standard Evaluation System (SES) for Rice, 5th Edn. Manila, The Philippines: IRRI, pp. 35–36.Google Scholar
Jagadish, SVK, Craufurd, PQ and Wheeler, TR (2007) High temperature stress and spikelet fertility in rice (Oryza sativa L.). Journal of Experimental Botany 58, 1627–1635.Google Scholar
Jagadish, SVK, Craufurd, PQ and Wheeler, TR (2008) Phenotyping parents of mapping populations of rice for heat tolerance during anthesis. Crop Science 48, 1140–1146.Google Scholar
Jagadish, SVK, Muthurajan, R, Oane, R, Wheeler, TR, Heuer, S, Bennett, J and Craufurd, PQ (2010) Physiological and proteomic approaches to address heat tolerance during anthesis in rice (Oryza sativa L.). Journal of Experimental Botany 61, 143–156.Google Scholar
Jagadish, KSV, Craufurd, P, Shi, W and Oane, R (2013) A phenotypic marker for quantifying heat stress impact during microsporogenesis in rice (Oryza sativa L.). Functional Plant Biology 41, 48–55.Google Scholar
Keijzer, CJ (1987) The processes of anther dehiscence and pollen dispersal. I. The opening mechanism of longitudinally dehiscing anthers. New Phytologist 105, 487–498.Google Scholar
Kobayasi, K, Matsui, T, Murata, Y and 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.Google Scholar
Kotak, S, Port, M, Ganguli, A, Bicker, F and Von Koskull-Döring, P (2004) Characterization of C-terminal domains of Arabidopsis heat stress transcription factors (Hsfs) and identification of a new signature combination of plant class A Hsfs with AHA and NES motifs essential for activator function and intracellular localization. Plant Journal 39, 98–112.Google Scholar
Liao, JL, Zhang, HY, Shao, XL, Zhong, PA and Huang, YJ (2011) Identification for heat tolerance in backcross recombinant lines and screening of backcross introgression lines with heat tolerance at milky stage in rice. Rice Science 18, 279–286.Google Scholar
Liu, AL, Zou, J, Zhang, XW, Zhou, XY, Wang, WF, Xiong, XY, Chen, LY and Chen, XB (2010) Expression profiles of class a rice heat shock transcription factor genes under abiotic stresses. Journal of Plant Biology 53, 142–149.Google Scholar
Livak, KJ and Schmittgen, DT (2001) Analysis of relative gene expression data using real time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.Google Scholar
Mackill, DJ, Coffman, WR and Rutger, JN (1982) Pollen shedding and combining ability for high temperature tolerance in rice. Crop Science 22, 730–733.Google Scholar
Matsui, T and Omasa, K (2002) Rice (Oryza sativa L.) cultivars tolerant to high temperature at flowering: anther characteristics. Annals of Botany 89, 683–687.Google Scholar
Matsui, T, Omasa, K and 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.Google Scholar
Matsui, T, Omasa, K and Horie, T (2001 a) The difference in sterility due to high temperatures during the flowering period among japonica rice varieties. Plant Production Science 4, 90–93.Google Scholar
Matsui, T, Omasa, K and Horie, T (2001 b) Comparison between anthers of two rice (Oryza saliva L.) cultivars with tolerance to high temperatures at flowering or susceptibility. Plant Production Science 4, 36–40.Google Scholar
Matsui, T, Kobayasi, K, Kagata, H and 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.Google Scholar
Matthews, RB, Kropff, MJ, Bachelet, D and Van Laar, HH (1995) Executive summary. In Matthews, RB, Kropff, MJ, Bachelet, D, Van Laar, HH (eds). Modelling the Impact of Climate Change on Rice Production in Asia. Wallingford, UK: CABI, pp. xi–xiv.Google Scholar
Mesihovic, A, Iannacone, R, Firon, N and Fragkostefanakis, S (2016) Heat stress regimes for the investigation of pollen thermotolerance in crop plants. Plant Reproduction 29, 93–105.Google Scholar
Mizutani, M and Ohta, D (2010) Diversification of P450 genes during land plant evolution. Annual Review of Plant Biology 61, 291–315.Google Scholar
Morita, S, Wada, H and Matsue, Y (2016) Countermeasures for heat damage in rice grain quality under climate change. Plant Production Science 19, 1–11.Google Scholar
Nakagawa, H, Horie, T and Matsui, T (2002) Effects of climate change on rice production and adaptive technologies. In Mew, TW, Brar, DS, Peng, S, Dawe, D and Hardy, B (eds), Rice Science: Innovations and Impact for Livelihood. Manila, The Philippines: International Rice Research Institute, pp. 635–657.Google Scholar
Nover, L, Bharti, K, Döring, P, Mishra, SK, Ganguli, A and Scharf, KD (2001) Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? Cell Stress & Chaperones 6, 177–189.Google Scholar
Pacini, E and Dolferus, R (2016) The trials and tribulations of the plant male gametophyte; understanding reproductive stage stress tolerance. In Shanker, AK and Shanker, C (eds), Abiotic and Biotic Stress in Plants – Recent Advances and Future Perspectives. London, UK: IntechOpen. DOI: 10.5772/61671. Available from: https://www.intechopen.com/books/abiotic-and-biotic-stress-in-plants-recent-advances-and-future-perspectives/the-trials-and-tribulations-of-the-plant-male-gametophyte-understanding-reproductive-stage-stress-to (accessed 17 July 2019).Google Scholar
Pararajasingham, S and Hunt, LA (1991) Wheat spike temperature in relation to base temperature for grain filling duration. Canadian Journal of Plant Science 71, 63–69.Google Scholar
Peng, S, Huang, J, Sheehy, JE, Laza, RC, Visperas, RM, Zhong, X, Centeno, GS, Khush, GS and 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.Google Scholar
Phan, TTT, Ishibashi, Y, Miyazaki, M, Tran, HT, Okamura, K, Tanaka, S, Nakamura, J, Yuasa, T and Iwaya-Inoue, M (2013) High temperature-induced repression of the rice sucrose transporter (OsSUT1) and starch synthesis-related genes in sink and source organs at milky ripening stage causes chalky grains. Journal of Agronomy and Crop Science 199, 178–188.Google Scholar
Poli, Y, Basava, R K, Panigrahy, M, Vinukonda, VP, Dokula, NR, Voleti, SR, Desiraju, S and Neelamraju, S (2013) Characterization of a Nagina22 rice mutant for heat tolerance and mapping of yield traits. Rice 6, 36.Google Scholar
Port, M, Tripp, J, Zielinski, D, Weber, C, Heerklotz, D, Winkelhaus, S, Bublak, D and Scharf, KD (2004) Role of Hsp17.4-CII as coregulator and cytoplasmic retention factor of tomato heat stress transcription factor HsfA2. Plant Physiology 135, 1457–1470.Google Scholar
Prasad, PVV, Boote, KJ and Allen, LH (2006 a) Adverse high temperature effects on pollen viability, seed-set, seed yield and harvest index of grain-sorghum (Sorghum bicolor L. Moench) are more severe at elevated carbon dioxide due to higher tissue temperatures. Agricultural and Forest Meteorology 139, 237–251.Google Scholar
Prasad, PVV, Boote, KJ, Allen, LH, Sheehy, JE and Thomas, JMG (2006 b) 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.Google Scholar
Rang, ZW, Jagadish, SVK, Zhou, QM, Craufurd, PQ and 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.Google Scholar
R Core Team (2014) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Rieu, I, Twell, D and Firon, N (2017) Pollen development at high temperature: from acclimation to collapse. Plant Physiology 173, 1967–1976.Google Scholar
Sakata, T and Higashitani, A (2008) Male sterility accompanied with abnormal anther development in plants genes and environmental stresses with special reference to high temperature injury. International Journal of Developmental Biology 2, 42–51.Google Scholar
Satake, T and Yoshida, S (1978) High temperature induced sterility in indica rices at flowering. Japanese Journal of Crop Science 47, 6–17.Google Scholar
Scharf, KD, Heider, H, Höhfeld, I, Lyck, R, Schmidt, E and Nover, L (1998) The tomato Hsf system: HsfA2 needs interaction with HsfA1 for efficient nuclear import and may be localized in cytoplasmic heat stress granules. Molecular and Cellular Biology 18, 2240–2251.Google Scholar
Shah, F, Huang, J, Cui, K, Nie, L, Shah, T, Chen, C and Wang, K (2011) Impact of high-temperature stress on rice plant and its traits related to tolerance. Journal of Agricultural Science 149, 545–556.Google Scholar
Sheehy, JE, Mitchell, PL, Beerling, DJ, Tsukaguchi, T and Woodward, FI (1998) Temperature of rice spikelets: thermal damage and the concept of a thermal burden. Agronomie 18, 449–460.Google Scholar
Shi, W, Ishimaru, T, Gannaban, RB, Oane, W and Jagadish, SVK (2015) Popular rice (Oryza sativa L.) cultivars show contrasting responses to heat stress at gametogenesis and anthesis. Crop Science 55, 589–596.Google Scholar
Song, ZP, Lu, BR and Chen, JK (2001) A study of pollen viability and longevity in Oryza rufipogon, O. sativa, and their hybrids. International Rice Research Notes 26, 31–32.Google Scholar
Tang, RS, Zheng, JC, Jin, ZQ, Zhang, DD, Huang, YH and Chen, LG (2008) Possible correlation between high temperature-induced floret sterility and endogenous levels of IAA gas and ABA in rice (Oryza sativa L.). Plant Growth Regulation 54, 37–43.Google Scholar
Wada, T, Miyahara, K, Sonoda, JY, Tsukaguchi, T, Miyazaki, M, Tsubone, M, Ando, T, Ebana, K, Yamamoto, T, Iwasawa, N, Umemoto, T, Kondo, M and Yano, M (2015) Detection of QTLs for white-back and basal-white grains caused by high temperature during ripening period in japonica rice. Breeding Science 65, 216–225.Google Scholar
Wahid, A, Gelani, S, Ashraf, M and Foolad, MR (2007) Heat tolerance in plants: an overview. Environmental and Experimental Botany 61, 199–223.Google Scholar
Wassmann, R and Dobermann, A (2007) Climate change adaptation through rice production in regions with high poverty levels. Ejournal of SAT Agricultural Research 4, 1–24.Google Scholar
Wassmann, R, Jagadish, SVK, Sumfleth, K, Pathak, H, Howell, G, Ismail, A, Serraj, R, Redona, E, Singh, R K and Heuer, S (2009) Regional vulnerability of climate change impacts on Asian rice production and scope for adaptation. Advance Agronomy 102, 91–133.Google Scholar
Weerakoon, WMW, Maruyama, A and Ohba, K (2008) Impact of humidity on temperature-induced grain sterility in rice (Oryza sativa L.). Journal Agronomy and Crop Science 194, 135–140.Google Scholar
Welch, JR, Vincent, JR, Auffhammer, M, Moya, PF, Dobermann, A and Dawe, D (2010) Rice yields in tropical/subtropical Asia exhibit large but opposing sensitivities to minimum and maximum temperatures. Proceedings of the National Academy of Sciences of the United States of America 107, 14562–14567.Google Scholar
Wilson, ZA, Song, J, Taylor, B and Yang, C (2011) The final split: the regulation of anther dehiscence. Journal of Experimental Botany 62, 1633–1649.Google Scholar
Wu, C (1995) Heat shock transcription factors: structure and regulation. Annual Review of Cell and Developmental Biology 11, 441–469.Google Scholar
Yan, C, Ding, YF, Liu, ZH, Wang, QS, Li, GH, Ying, HE and Wang, SH (2008) Temperature difference between the air and organs of rice plant and its relation to spikelet fertility. Agricultural Sciences in China 7, 678–685.Google Scholar
Yan, C, Ding, Y, Wang, Q, Liu, Z, Li, G, Muhammad, I and Wang, S (2010) The impact of relative humidity, genotypes and fertilizer application rates on panicle, leaf temperature, fertility and seed setting of rice. Journal of Agricultural Science 148, 329–339.Google Scholar
Yoshida, S, Satake, T and Mackill, DS (1981) High Temperature Stress in Rice. IRRI Research Paper Series no. 67. Manila, The Philippines: IRRI.Google Scholar
Zhang, GL, Chen, LY, Zhang, ST, Zheng, H and Liu, GH (2009) Effects of high temperature stress on microscopic and ultrastructural characteristics of mesophyll cells in flag leaves of rice. Rice Science 16, 65–71.Google Scholar
Zhang, CX, Fu, GF, Yang, XQ, Yang, YJ, Zhao, X, Chen, TT, Zhang, XF, Jin, QY and Tao, LX (2016) Heat stress effects are stronger on spikelets than on flag leaves in rice due to differences in dissipation capacity. Journal of Agronomy and Crop Science 202, 394–408.Google Scholar