Please wait a minute...
Journal of Integrative Agriculture
Advanced Online Publication | Current Issue | Archive | Adv Search
Moderate soil drying mitigates high temperature-induced spikelet opening impairment by enhancing jasmonates accumulation in lodicules of photo-thermosensitive male-sterile rice

Weiyang Zhang1, 2#, Ying Liu1, 2, Wenqian Miao1, 2, Yujiao Zhou1, 2, Jun Miao1, 2, Kuanyu Zhu1, 2, Weilu Wang3, Yunji Xu3, Junfei Gu1, 2, Hao Zhang1, 2, Zhiqin Wang1, 2, Lijun Liu1, 2, Jianhua Zhang4, Jianchang Yang1, 2#

1 Jiangsu Key Laboratory of Crop Genetics and Physiology/ Jiangsu Key Laboratory of Crop Cultivation and Physiology/ Agricultural College, Yangzhou University, Yangzhou 225009, China

2 Jiangsu Co-Innovation Center for Modern Production Technology of Grain Crops, Yangzhou University, Yangzhou 225009, China

3 Joint International Research Laboratory of Agriculture and Agri-Product Safety, Yangzhou University, Yangzhou 225009, China

4 Department of Biology, Hong Kong Baptist University, Hong Kong 999077, China

 Highlights 

l Moderate soil drying (MD) mitigates high temperature (HT) stress on spikelet opening in PTGMS rice better than conventional well-watered (WW) method.

l MD regime maintains osmotic and redox homeostasis in lodicules of PTGMS rice under HT stress.

l Jasmonates mediate the effectiveness of MD regime in alleviating HT stress on spikelet opening of PTGMS rice.

Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  

本研究探讨了茉莉酸类物质(JAs)在适度土壤落干(MD)缓解高温胁迫诱导的光温敏核不育系(PTGMS)水稻开颖障碍中的作用。通过多年控温盆栽与露天田间试验,对两种PTGMS水稻品种在正常温度与高温条件下分别采用充分灌溉(WW)和MD策略进行系统对比。研究发现,与传统WW处理相比,MD处理显著提升了浆片中JAs的积累,有效缓解了高温诱导的开颖障碍及杂交制种产量损失。其保护机制主要通过以下途径实现:(1)促进淀粉水解为可溶性糖,(2)上调水通道蛋白基因表达,(3)增强抗氧化能力,从而维持浆片细胞的渗透压与氧化还原平衡。通过JAs缺陷突变体、不同JAs合成能力的转基因水稻以及外源JAs处理,进一步验证了JAs在这一机制中的核心作用。研究结果表明,MD通过调控JAs水平维持浆片的渗透压与氧化还原平衡,是一种比传统WW效的栽培策略,能够在高温胁迫下显著改善PTGMS水稻的开颖能力,提高杂交制种产量。



Abstract  

This study investigated the role of jasmonates (JAs) in mitigating high temperature (HT) stress-induced spikelet opening impairment in photo-thermosensitive genetic male-sterile (PTGMS) rice under controlled moderate soil drying (MD).  Two PTGMS rice varieties were grown under normal temperature (NT) and HT conditions, using paired well-watered (WW) and MD strategies during anthesis, in both controlled-climate pot and open-air field conditions over multiple years.  Compared to the conventional WW regime under HT stress, which significantly reduced JAs levels in lodicules and worsened spikelet opening impairment and hybrid seed yield loss, the MD treatment demonstrated significant protective effects.  The MD regime enhanced JAs accumulation in lodicules, effectively alleviating HT-induced spikelet opening impairment and hybrid seed yield reduction.  This protective mechanism operates through multiple pathways: (1) promoting starch hydrolysis into soluble sugars, (2) upregulating the expression of aquaporin genes, and (3) enhancing antioxidant capacity, thereby maintaining cellular osmotic and redox homeostasis in lodicules.  The crucial role of JAs in this mechanism was confirmed using JA-deficient mutants, transgenic rice lines with varying JA biosynthesis capacities, and exogenous JAs applications.  These findings indicate that MD is a more effective cultivation strategy than traditional WW in protecting PTGMS rice from HT stress, achieved by modulating JAs levels to maintain osmotic and redox homeostasis in lodicules, thus improving spikelet opening and hybrid seed yield under HT stress during anthesis.

Keywords:  high temperature       moderate soil drying              jasmonates              spikelet opening              photo-thermosensitive genetic male-sterile (PTGMS)              rice  
Online: 29 July 2025  
Fund: 

This work was supported by the National Natural Science Foundation of China (32372214, 32272198, 32071943, 31771710, and 32201888), the Jiangsu Agriculture Science and Technology Innovation Fund, China (CX(23)1035), the Priority Academic Program Development of Jiangsu Higher Education Institutions, China (PAPD-2020-01), and the Top Talent Supporting Program of Yangzhou University, China

About author:  #Correspondence Weiyang Zhang, E-mail: wyz@yzu.edu.cn; Jianchang Yang, E-mail: jcyang@yzu.edu.cn

Cite this article: 

Weiyang Zhang, Ying Liu, Wenqian Miao, Yujiao Zhou, Jun Miao, Kuanyu Zhu, Weilu Wang, Yunji Xu, Junfei Gu, Hao Zhang, Zhiqin Wang, Lijun Liu, Jianhua Zhang, Jianchang Yang. 2025. Moderate soil drying mitigates high temperature-induced spikelet opening impairment by enhancing jasmonates accumulation in lodicules of photo-thermosensitive male-sterile rice. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.07.026

Balcerowicz M. 2024. Timing is everything: OsMYC2 controls diurnal flower-opening time in rice. The Plant Journal, 119, 2583–2584.

Bo Y, Wang X, van Groenigen K J, Linquist B A, Müller C, Li T, Yang J, Jägermeyr J, Qin Y, Zhou F. 2024. Improved alternate wetting and drying irrigation increases global water productivity. Nature Food, 5, 1005–1013.

Brennan T, Frenkel C. 1977. Involvement of hydrogen peroxide in the regulation of senescence in pear. Plant Physiology, 59, 411–416.

Cai Q, Yuan Z, Chen M, Yin C, Luo Z, Zhao X, Liang W, Hu J, Zhang D. 2014. Jasmonic acid regulates spikelet development in rice. Nature Communications, 5, 3476.

Cao Y Y, Duan H, Yang L N, Wang Z Q, Liu L J, Yang J C. 2009. Effect of high temperature during heading and early grain filling on grain yield of indica rice cultivars differing in heat-tolerance and its physiological mechanism. Chinese Science Bulletin, 35, 512–521. (in Chinese)

Clarke S M, Cristescu S M, Miersch O, Harren F J M, Wasternack C, Mur L A J. 2009. Jasmonates act with salicylic acid to confer basal thermotolerance in Arabidopsis thaliana. New Phytologist, 182, 175–187.

Ding W, Gou Y, Li Y, Li J, Fang Y, Liu X, Zhu X, Ye R, Heng Y, Wang H, Shen R. 2024. A jasmonate-mediated regulatory network modulates diurnal floret opening time in rice. New Phytologist, 244, 176–191.

Du H, Liu H, Xiong L. 2013. Endogenous auxin and jasmonic acid levels are differentially modulated by abiotic stresses in rice. Frontiers in Plant Science, 4, 397.

Foyer C H, Hanke G. 2022. ROS production and signalling in chloroplasts: Cornerstones and evolving concepts. The Plant Journal, 111, 642–661.

Fu J, Huang Z H, Wang Z Q, Yang J C, Zhang J H. 2011. Pre-anthesis non-structural carbohydrate reserve in the stem enhances the sink strength of inferior spikelets during grain filling of rice. Field Crops Research, 123, 170–182.

Goossens J, Fernández-Calvo P, Schweizer F, Goossens A. 2016. Jasmonates: Signal transduction components and their roles in environmental stress responses. Plant Molecular Biology, 91, 673–689.

Gou Y, Heng Y, Ding W, Xu C, Tan Q, Li Y, Fang Y, Li X, Zhou D, Zhu X, Zhang M, Ye R, Wang H, Shen R. 2024. Natural variation in OsMYB8 confers diurnal floret opening time divergence between indica and japonica subspecies. Nature Communication, 15, 2262.

Guo L J, Xiao X P, Cheng K K, Li C, Yang Q, Tang H M, Tang W G, Peng Z H, Wang K. 2021. Study on irrigation depth to alleviate high temperature and heat damage of super early rice during grain-filling period. Journal of Irrigation and Drainage, 40, 62–70. (in Chinese)

Guo Q, Major I T, Kapali G, Howe G A. 2022. MYC transcription factors coordinate tryptophan-dependent defence responses and compromise seed yield in Arabidopsis. New Phytologist, 236, 132–145.

Guo Z, Zuo Y, Wang S, Zhang X, Wang Z, Liu Y, Shen Y. 2024. Early signaling enhance heat tolerance in Arabidopsis through modulating jasmonic acid synthesis mediated by HSFA2. International Journal of Biological Macromolecules, 267, 131256.

Hu T S, Zheng M Q, Zheng J Q, Luo X Y, Zhang Z Y, Pan W H, Guo T R, Mo Y W. 2020. Effect of high temperature and HgCl2 stress on physiological parameters and aquaporins genes expression in rice flowering stage. Journal of Hunan Agricultural University (Natural Sciences), 46, 262–270. (in Chinese)

Jiang N, Yu P, Fu W, Li G, Feng B, Chen T, Li H, Tao L, Fu G. 2020. Acid invertase confers heat tolerance in rice plants by maintaining energy homoeostasis of spikelets. Plant, Cell & Environment, 43, 1273–1287.

Kazan K. 2015. Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends in Plant Science20, 219–229.

Lesk C, Anderson W, Rigden A, Coast O, Jägermeyr J, McDermid S, Davis K F, Konar M. 2022. Compound heat and moisture extreme impacts on global crop yields under climate change. Nature Reviews Earth & Environment3, 872–889.

Li H, Testerink C, Zhang Y. 2021. How roots and shoots communicate through stressful times. Trends in Plant Science, 26, 940–952.

Li Y, Chen M, Khan A H, Ma Y, He X, Yang J, Zhang R, Ma H, Zuo C, Li Y, Kong J, Wang M, Zhu L, Zhang X, Min L. 2023. Histone H3 lysine 27 trimethylation suppresses jasmonate biosynthesis and signaling to affect male fertility under high temperature in cotton. Plant Communications, 4, 100660.

Liu L, Xu H, Liu S, Liu X J. 2023. China’s response to extreme weather events must be long term. Nature Food, 4, 1022–1023.

Liu L, Zou Z, Qian K, Xia C, He Y, Zeng H, Zhou X, Riemann M, Yin C. 2017. Jasmonic acid deficiency leads to scattered floret opening time in cytoplasmic male sterile rice Zhenshan 97A. Journal of Experimental Botany, 68, 4613–4625.

Liu X, Yang Y L, Lin W H, Tong J H, Huang Z G, Xiao L T. 2010. Determination of both jasmonic acid and methyl jasmonate in plant samples by liquid chromatography tandem mass spectrometry. Science Bulletin55, 2231–2235.

Long Y, Yoshida Y, Kajikawa Y. 2024. Extreme heat disproportionately exacerbates health issues by threatening fresh food supply. Nature Climate Change, 14, 1109–1111.

Maqbool S, Hassan M A, Xia X, York L M, Rasheed A, He Z. 2022. Root system architecture in cereals: Progress, challenges and perspective. The Plant Journal, 11, 23–42.

McCleary B V, Sheehan H. 1987. Measurement of cereal alpha-amylase: A new assay procedure. Journal of Cereal Science, 6, 237–251.

Miao J, Li X, Li X, Tan W, You A, Wu S, Tao Y, Chen C, Wang J, Zhang D, Gong Z, Yi C, Yang Z, Gu M, Liang G, Zhou Y. 2020. OsPP2C09, a negative regulatory factor in abscisic acid signalling, plays an essential role in balancing plant growth and drought tolerance in rice. New Phytologist, 227, 1417–1433.

Mittler R, Zandalinas S I, Fichman Y, Van Breusegem F. 2022. Reactive oxygen species signalling in plant stress responses. Nature reviews. Molecular Cell Biology, 23, 663–679.

Mou T M. 2016. The research progress and prospects of two-line hybrid rice in China. Science Bulletin, 61, 3761–3769. (in Chinese)

Muzaffar A, Chen Y S, Lee H T, Wu C C, Le T T, Liang J Z, Lu C H, Balasubramaniam H, Lo S F, Yu L C, Chan C H, Chen K T, Lee M H, Hsing Y I, Ho T D, Yu S M. 2024. A newly evolved rice-specific gene JAUP1 regulates jasmonate biosynthesis and signalling to promote root development and multi-stress tolerance. Plant Biotechnology Journal, 22, 1417–1432.

Oldroyd G E D, Leyser O. 2020. A plant's diet, surviving in a variable nutrient environment. Science, 368, eaba0196.

Pedersen O, Sauter M, Colmer T D, Nakazono M. 2021. Regulation of root adaptive anatomical and morphological traits during low soil oxygen. New Phytologist229, 42–49.

Qian Q, Guo L, Smith S, Li J. 2016. Breeding high-yield superior quality hybrid super rice by rational design. National Science Review, 3, 283–294.

Qiu D, Hu W, Zhou Y, Xiao J, Hu R, Wei Q H, Zhang Y, Feng J L, Sun F S, Sun J T, Yang G X, He G Y. 2021. TaASR1-D confers abiotic stress resistance by affecting ROS accumulation and ABA signalling in transgenic wheat. Plant Biotechnology Journal, 191, 588–1601.

Ramasamy S, Berge H F M T, Purushothaman S. 1997. Yield formation in rice in response to drainage and nitrogen application. Field Crops Research, 51, 65–82.

Sato H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K. 2024. Complex plant responses to drought and heat stress under climate change. Plant Journal, 117, 1873–1892.

Shekhawat K, Almeida-Trapp M, García-Ramírez G X, Hirt H. 2022. Beat the heat: Plant- and microbe-mediated strategies for crop thermotolerance. Trends in Plant Science, 27, 802–813.

Shi W J, Zhang X Z, Yang J, Impa S M, Wang D, Lai Y S,Yang Z J, Hang X, Wu J S, Zhang J H, Jagadish S V K. 2023. Irrigating with cooler water does not reverse high temperature impact on grain yield and quality in hybrid rice. The Crop Journal, 11, 904–913.

Song C, Cao Y, Dai J, Li G, Manzoor M A, Chen C, Deng H. 2022. The multifaceted roles of MYC2 in plants: Toward transcriptional reprogramming and stress tolerance by jasmonate signaling. Frontiers in Plant Science, 13, 868874.

Sun Q, Liu X, Kitagawa Y, Calamita G, Ding X. 2024. Plant aquaporins: Their roles beyond water transport. The Crop Journal, 12, 641–655.

Tian X, Wang F, Zhao Y, Lan T, Yu K, Zhang L, Qin Z, Hu Z, Yao Y, Ni Z, Sun Q, Rossi V, Peng H, Xin M. 2020. Heat shock transcription factor A1b regulates heat tolerance in wheat and Arabidopsis through OPR3 and jasmonate signalling pathway. Plant Biotechnology Journal, 18, 1109–1111.

Waadt R, Seller C A, Hsu P K, Takahashi Y, Munemasa S, Schroeder J I. 2022. Plant hormone regulation of abiotic stress responses. Nature Reviews Molecular Cell Biology, 23, 680–694.

Wang M, Zhu X, Huang Z, Chen M, Xu P, Liao S, Zhao Y, Gao Y, He J, Luo Y, Chen H, Wei X, Nie S, Dong J, Zhu L, Zhuang C, Zhao J, Liu Z, Zhou H. 2024. Controlling diurnal flower-opening time by manipulating the jasmonate pathway accelerates development of indica-japonica hybrid rice breeding. Plant Biotechnology Journal, 22, 2267–2281.

Wang W C, Cui K H, Hu Q Q, Wu H, Li G H, Huang J L, Peng S B. 2021. Response of spikelet water status to high temperature and its relationship with heat tolerance in rice. The Crop Journal, 9, 1344–1356.

Wang Y, Wang L, Zhou J Y, Hu S, Chen H, Xiang J, Zhang Y K, Zeng Y, Shi Q, Zhu D, Zhang Y. 2019. Research progress on heat stress of rice at flowering stage. Rice Science, 26, 1–10.

Wang Z. 2015. Flowering and seed-setting of rice. Science Press, Beijing, China. pp. 66–75. (in Chinese)

Wasternack C, Hause B. 2013. Jasmonates: Biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Annals of Botany, 111, 1021–1058.

Yang J C, Fei K Q, Chen J, Wang Z Q, Zhang W Y, Zhang J. H. 2020. Jasmonates alleviate spikelet-opening impairment caused by high temperature stress during anthesis of photo-thermo-sensitive genic male sterile rice lines. Food and Energy Security, 9, e233.

Yang J C, Miao W Q, Chen J. 2021. Roles of jasmonates and brassinosteroids in rice responses to high temperature stress-A review. The Crop Journal, 9, 977–985.

Yao Q, Li P, Wang X, Liao S, Wang P, Huang S. 2024. Molecular mechanisms underlying negative effects of transient heatwaves on crop fertility. Plant Communications, 5, 101009.

Yu J, Han J, Kim Y J, Song M, Yang Z, He Y, Fu R, Luo Z, Hu J, Liang W, Zhang D. 2017. Two rice receptor-like kinases maintain male fertility under changing temperatures. Proceedings of the National Academy of Sciences of the United States of America, 114, 12327–12332.

Yuan Z, Zhang D. 2015. Roles of jasmonate signalling in plant inflorescence and flower development. Current Opinion in Plant Biology, 27, 44–51.

Zhang W Y, Wu M Y, Zhong X H, Liu Y, Yang X X, Cai W, Zhu K Y, Zhang H, Gu J F, Wang Z Q, Liu L J, Zhang J H, Yang J C. 2024. Involvement of brassinosteroids and abscisic acid in spikelet degeneration in rice under soil drying during meiosis. Journal of Experimental Botany, 75, 1580–1600.

Zhang W Y, Yu J X, Xu Y J, Wang Z Q, Liu L J, Zhang H, Gu J F, Zhang J H, Yang J C. 2021. Alternate wetting and drying irrigation combined with the proportion of polymer-coated urea and conventional urea rates increases grain yield, water and nitrogen use efficiencies in rice. Field Crops Research268, 108165.

Zhang W Y, Zhou Y J, Li C Q, Zhu K Y, Xu Y J, Wang W L, Liu L J, Zhang H, Gu J F, Wang Z Q, Zhang J H, Yang J C. 2022. Post-anthesis moderate soil-drying facilitates source-to-sink remobilization of nitrogen via redistributing cytokinins in rice. Field Crops Research288, 108692.

Zhang Z L. 1998. Experimental guide in plant physiology. In: Introduction to China Higher Education. Beijing Press, China. pp. 62–64, 160–162. (in Chinese)

Zhao C, Liu B, Piao S, Wang X, Lobell D B, Huang Y, Huang M, Yao Y, Bassu S, Ciais P, Durand J L, Elliott J, Ewert F, Janssens I A, Li T, Lin E, Liu Q, Martre P, Müller C, Peng S, et al. 2017. Temperature increase reduces global yields of major crops in four independent estimates. Proceedings of the National Academy of Sciences of the United States of America, 114, 9326–9331.

Zhao Q, Guan X Y, Zhou L J, Asad M A U, Xu Y Q, Pan G, Cheng F M. 2023. ABA-triggered ROS burst in rice developing anthers is critical for tapetal programmed cell death induction and heat stress-induced pollen abortion. Plant, Cell & Environment, 46, 1453–1471.

Zhu T, Herrfurth C, Xin M, Savchenko T, Feussner I, Goossens A, De Smet I. 2021. Warm temperature triggers JOX and ST2A-mediated jasmonate catabolism to promote plant growth. Nature Communications, 12, 4804.

No related articles found!
No Suggested Reading articles found!