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Journal of Integrative Agriculture  2024, Vol. 23 Issue (9): 2989-3011    DOI: 10.1016/j.jia.2024.01.012
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Overexpression of PbrGA2ox1 enhances pear drought tolerance through the regulation of GA3-inhibited reactive oxygen species detoxification and abscisic acid signaling

Guoling Guo1*, Haiyan Zhang1*, Weiyu Dong1, Bo Xu1, 2, Youyu Wang1, 3, Qingchen Zhao1, 4, Lun Liu1, Xiaomei Tang1, Li Liu1, Zhenfeng Ye1, Wei Heng1, Liwu Zhu1#, Bing Jia1#

1 School of Horticulture, Anhui Agricultural University, Hefei 230036, China
2 Anhui Wanbang Pharmaceutical Technology Co., Ltd., Hefei 230036, China
3 Science and Technology Department, Anhui Agricultural University, Hefei 230036, China
4 Hunan Suncas Agriculture Science Co., Ltd., Changsha 410016, China
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摘要  
干旱胁迫是全球变暖持续加剧所导致一种毁灭性的自然灾害,严重威胁着梨树在内的多种园艺作物的产量和质量。赤霉素(Gibberellin,GA)在植物生长、发育和对干旱胁迫的反应中发挥重要的调控作用。已有研究表明,干旱胁迫条件下的植物体内赤霉素水平显著降低;然而,GA对梨树干旱胁迫的调控作用和其内在机制仍未可知。本研究结果表明,干旱胁迫显著抑制了梨叶内生物活性赤霉素(Bioactive GA,BGAs)的积累,并强烈诱导了叶绿体定位的赤霉素2–氧化酶(Gibberellin 2-oxidase1PbrGA2ox1)基因的表达。研究发现,PbrGA2ox1受外源脱落酸(Abiscisic acid,ABA)和赤霉酸(Gibberellic acid,GA3)处理的显著促进和抑制,并积极参与调控梨树的抗旱性。于烟草(Nicotiana benthamiana)内过表达该基因可显著增强其抗脱水和抗旱能力,而于梨叶(Pyrus betulaefolia)内以病毒诱导的基因沉默(Virus-induced gene silencing,VIGS)技术降低该基因的表达则增强了梨树的干旱敏感性。进一步研究结果显示,较野生型(Wild-type,WT)烟草株系而言,干旱胁迫条件下的PbrGA2ox1过表达株系内BGAs含量显著降低,活性氧(Reactive oxygen system,ROS)积累量显著下降,并伴随着ABA含量的显著升高和其信号转导的显著增强以及ROS清除能力的显著提升。然而,该基因的沉默则显著抑制了这一系列生物过程。此外,本研究还发现,外源GA3处理可抑制干旱胁迫条件下的ABA的生物合成和信号转导,并加重ROS毒害效应,从而降低梨树的干旱耐受性。总而言之,试验结果揭示了干旱胁迫抑制梨叶内BGAs积累的机制,并进一步阐述了GA影响植物耐旱性的作用机制。


Abstract  
Drought stress is a devastating natural disaster driven by the continuing intensification of global warming, which seriously threatens the productivity and quality of several horticultural crops, including pear.  Gibberellins (GAs) play crucial roles in plant growth, development, and responses to drought stress.  Previous studies have shown significant reductions of GA levels in plants under drought stress; however, our understanding of the intrinsic regulation mechanisms of GA-mediated drought stress in pear remains very limited.  Here, we show that drought stress can impair the accumulation of bioactive GAs (BGAs), and subsequently identified PbrGA2ox1 as a chloroplast-localized GA deactivation gene.  This gene was significantly induced by drought stress and abscisic acid (ABA) treatment, but was suppressed by GA3 treatment.  PbrGA2ox1-overexpressing transgenic tobacco plants (Nicotiana benthamiana) exhibited enhanced tolerance to dehydration and drought stresses, whereas knock-down of PbrGA2ox1 in pear (Pyrus betulaefolia) by virus-induced gene silencing led to elevated drought sensitivity.  Transgenic plants were hypersensitive to ABA, and had a lower BGAs content, enhanced reactive oxygen species (ROS) scavenging ability, and augmented ABA accumulation and signaling under drought stress compared to wild-type plants.  However, the opposite effects were observed with PbrGA2ox1 silencing in pear.  Moreover, exogenous GA3 treatment aggravated the ROS toxic effect and restrained ABA synthesis and signaling, resulting in the compromised drought tolerance of pear.  In summary, our results shed light on the mechanism by which BGAs are eliminated in pear leaves under drought stress, providing further insights into the mechanism regulating the effects of GA on the drought tolerance of plants.


Keywords:  pear       gibberellin       drought stress       PbrGA2ox1       reactive oxygen species       abscisic acid  
Received: 08 July 2023   Accepted: 21 December 2023
Fund: 
This work was financially supported by grants from the China Agriculture Research System (CARS-28-14), the Technical System of Fruit Industry in Anhui Province, China (AHCYTX-10), and the Scientific Research Projects for Postgraduates of Anhui Universities, China (YJS20210207).
About author:  Guoling Guo, E-mail: ggl1995@ahau.edu.cn; Haiyan Zhang, E-mail: 17855021950@139.com; #Correspondence Bing Jia, E-mail: jb1977@ahau.edu.cn; Liwu Zhu, E-mail: zhuliwu@ahau.edu.cn * These authors contributed equally to this study.

Cite this article: 

Guoling Guo, Haiyan Zhang, Weiyu Dong, Bo Xu, Youyu Wang, Qingchen Zhao, Lun Liu, Xiaomei Tang, Li Liu, Zhenfeng Ye, Wei Heng, Liwu Zhu, Bing Jia. 2024. Overexpression of PbrGA2ox1 enhances pear drought tolerance through the regulation of GA3-inhibited reactive oxygen species detoxification and abscisic acid signaling. Journal of Integrative Agriculture, 23(9): 2989-3011.

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