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Journal of Integrative Agriculture  2024, Vol. 23 Issue (10): 3506-3521    DOI: 10.1016/j.jia.2024.05.032
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Enhancer of Shoot Regeneration 2 (ESR2) regulates pollen maturation and vitality in watermelon (Citrullus lanatus)
Hu Wang1, 2, Lihong Cao2, Yalu Guo2, Zheng Li2#, Huanhuan Niu1, 2#

1 College of Horticulture, Henan Agricultural University, Zhengzhou 450002, China

2 State Key Laboratory of Crop Stress Biology in Arid Areas, College of Horticulture, Northwest A&F University, Yangling 712100, China

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摘要  西瓜(Citrullus lanatus)作为一种具有高经济价值和营养价值的水果,在全球的水果生产和消费中具有重要意义。探索西瓜雄性生殖发育的调控网络,对开发雄性不育材料和促进西瓜杂交育种具有重要意义。虽然西瓜雄性生殖发育的调控机制对于研究西瓜雄性不育具有重要意义,但目前的相关研究仍较为缺乏。在本研究中,我们确定了APETALA2/乙烯响应因子(AP2/ERF)超家族中VIIIb亚类成员ClESR2是花粉后期发育的关键因子。RNA原位杂交证实,ClESR2在花药发育后期的绒毡层和未成熟的花粉中有显著的表达。进一步的研究发现ClESR2转基因植株的花粉在发育后期表现出形态和活力上的重大缺陷。RNA-seq和蛋白互作分析证实,ClESR2通过在转录和蛋白水平上对绒粘层降解和花粉成熟的相关通路和因子进行调控,影响花粉形态和育性。总之,本研究证实西瓜ClESR2在维持西瓜花粉成熟和活力中起到重要作用。本研究有助于进一步解析西瓜雄性生殖发育过程,为开发西瓜雄性不育材料提供理论依据。

Abstract  
Watermelon (Citrullus lanatus) holds global significance as a fruit with high economic and nutritional value.  Exploring the regulatory network of watermelon male reproductive development is crucial for developing male sterile materials and facilitating cross-breeding.  Despite its importance, there is a lack of research on the regulation mechanism of male reproductive development in watermelon.  In this study, we identified that ClESR2, a VIIIb subclass member in the APETALA2/Ethylene Responsive Factor (AP2/ERF) superfamily, was a key factor in pollen development.  RNA in situ hybridization confirmed significant ClESR2 expression in the tapetum and pollen during the later stage of anther development.  The pollens of transgenic plants showed major defects in morphology and vitality at the late development stage.  The RNA-seq and protein interaction assay confirmed that ClESR2 regulates pollen morphology and fertility by interacting with key genes involved in pollen development at both transcriptional and protein levels.  These suggest that Enhancer of Shoot Regeneration 2 (ESR2) plays an important role in pollen maturation and vitality.  This study helps understand the male reproductive development of watermelon, providing a theoretical foundation for developing male sterile materials.


Keywords:  ESR2        watermelon        overexpression        pollen maturation        pollen vitality  
Received: 23 August 2023   Accepted: 19 April 2024
Fund: 
Thanks for the funding support from the National Key Research and Development Program of China (2022YFD1602000), the National Natural Science Foundation of China (32202514, U22A20498 and 32072596), the Joint Fund of Henan Province Science and Technology Research and Development Plan, China (222103810009), the Science and Technology Innovation Team of Shaanxi, China (2021TD-32), and the China Postdoctoral Science Foundation (2022M711064 and 2023M741062).
About author:  #Correspondence Zheng Li, E-mail: lizheng82@nwsuaf.edu.cn; Huanhuan Niu, E-mail: niuhh@henau.edu.cn

Cite this article: 

Hu Wang, Lihong Cao, Yalu Guo, Zheng Li, Huanhuan Niu. 2024. Enhancer of Shoot Regeneration 2 (ESR2) regulates pollen maturation and vitality in watermelon (Citrullus lanatus). Journal of Integrative Agriculture, 23(10): 3506-3521.

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