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Journal of Integrative Agriculture
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Brassinosteroids facilitate controlled soil drying to mitigate heat stress on pistil fertilization in photo-thermosensitive genetic male-sterile rice

Weiyang Zhang1, 2#, Wei Cai1, 2, Yujiao Zhou1, 2, Ying Liu1, 2, Wenqian Miao1, 2, Kuanyu Zhu1, 2, Weilu Wang3, Yunji Xu3, Yidi Sun4, Junfei Gu1, 2, Hao Zhang1, 2, Zhiqin Wang1, 2, Lijun Liu1,2, Jianhua Zhang5, 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 College of Hydraulic Science and Engineering, Yangzhou University, Yangzhou 225009, China

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

 Highlights 

l Moderate soil drying mitigates heat stress on pistil fertilization in PTGMS rice better than conventional well-watered method.

l Moderate soil drying maintains water and redox homeostasis in PTGMS rice plants under heat stress.

l Brassinosteroids mediate the effectiveness of moderate soil drying in alleviating heat stress on PTGMS rice.

 

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摘要  

全球范围内频繁发生的极端高温(HT)事件严重制约了水稻生产。本研究旨在探究轻度土壤落干(MD)这一可控措施能否替代传统的充分灌溉(WW)模式,从而更有效地缓解高温胁迫对光温敏核不育(PTGMS)水稻雌蕊受精的影响,并研究油菜素甾醇(BRs)在此过程中所起的作用。本研究选取两个PTGMS水稻品种,在开花期分别置于正常温度(NT)和HT处理,同时设置WWMD两种灌溉模式。在传统的WW模式下,淹水会使根系和雌蕊中的BRs因过度分解而含量降低,削弱了由根系活力驱动的主动吸水过程,也无法缓解因叶片气孔开放受限而受阻的蒸腾拉力所驱动的被动吸水过程。这导致植株体内水分失衡,抗坏血酸-谷胱甘肽(AsA - GSH)循环受到抑制,烟酰胺腺嘌呤二核苷酸磷酸氧化酶(NOX)活性过强,进而削弱了雌蕊功能。在HT胁迫下,这进一步加剧了雌蕊受精障碍,导致杂交种子产量下降。相反,采用MD模式可促进根系和雌蕊中BRs的合成并抑制其分解,从而增强根系活力和蒸腾驱动的吸水能力维持了植株的水分平衡。同时,MD模式通过抑制雌蕊中NOX的活性,增强AsA - GSH驱动的氧化还原稳态,保障了雌蕊功能,进而有效缓解了HT胁迫引起的雌蕊受精障碍和杂交种子产量损失。本研究还通过遗传学和化学方法进一步证实了BRs在介导MD缓解HT胁迫下PTGMS水稻雌蕊受精障碍中的确切功能。综上所述,与传统的WW模式相比,MD模式通过促进BRs含量增加能更有效地缓解HT胁迫对PTGMS水稻雌蕊受精的负面影响



Abstract  

Globally recurrent extreme high temperature (HT) events severely limit rice production.  This study investigated whether a controlled moderate soil drying (MD) could replace the conventional well-watered (WW) regime to more effectively mitigate HT stress on pistil fertilization in photo-thermosensitive genetic male-sterile (PTGMS) rice, and examined the role of brassinosteroids (BRs).  Two PTGMS rice varieties were cultivated under normal temperature (NT) and HT conditions, paired WW and MD strategies during anthesis.  In conventional WW regime, waterlogging reduces BRs levels in roots and pistils due to excessive decomposition, weakening active water uptake driven by root activity and failing to alleviate transpiration-pulled passive water extraction hampered by restricted stomatal openings.  Thereby, it causes water imbalance in plants and weakened pistil function due to a suppressed ascorbate-glutathione (AsA-GSH) cycle and hyperactive nicotinamide adenine dinucleotide phosphate oxidase (NOX) activity.  This exacerbates pistil fertilization impairment and hybrid seed yield loss under HT stress.  Conversely, by promoting BR synthesis and inhibiting its decomposition in roots and pistils, the MD strategy enhanced root activity and transpiration-driven water uptake.  It maintained plant water balance and supported pistil function through suppressed NOX activity and an enhanced AsA-GSH cycle-driven redox homeostasis.  Thus, it mitigated HT-induced pistil fertilization impairment and hybrid seed yield loss.  The precise function of BRs in moderating the protective effects of MD against the detrimental impacts of HT stress on pistil fertilization in PTGMS rice was confirmed through genetic and chemical approaches.  Consequently, a controlled MD method proved to be more effective than the conventional WW regime in alleviating HT stress on pistil fertilization in PTGMS rice by promoting BR enhancement.

Keywords:  high temperature              moderate soil drying              brassinosteroids              photo-thermosensitive genetic male-sterile (PTGMS) rice              pistil fertilization  
Online: 25 April 2025  
Fund: 

This work was supported by the National Natural Science Foundation of China (32372214, 31901445, 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, Wei Cai, Yujiao Zhou, Ying Liu, Wenqian Miao, Kuanyu Zhu, Weilu Wang, Yunji Xu, Yidi Sun, Junfei Gu, Hao Zhang, Zhiqin Wang, Lijun Liu, Jianhua Zhang, Jianchang Yang. 2025. Brassinosteroids facilitate controlled soil drying to mitigate heat stress on pistil fertilization in photo-thermosensitive genetic male-sterile rice. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.04.036

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