Zu Hongyue, Zhang Jing, Bai Weiwei, Kuai Peng, Cheng Jingli, Lu Jing, Lou Yonggen, Li Ran
State Key Laboratory of Rice Biology and Breeding, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, Hangzhou, 310058, China.
Zhejiang Provincial Center for Disease Control and Prevention, Hangzhou, 310057, China.
Plant J. 2024 Dec;120(5):2000-2013. doi: 10.1111/tpj.17094. Epub 2024 Oct 21.
Polyamines (PAs) along with their conjugated forms, are important mediators of plant defense mechanisms against both biotic and abiotic stresses. Flavin-containing polyamine oxidases (PAOs) regulate PA levels through terminal oxidation. To date, the role of PAOs in plant-herbivore interaction remains poorly understood. We discovered that infestation by the brown planthopper (BPH) disrupts PA homeostasis within the leaf sheaths of rice plants, which co-occurs with the upregulation of OsPAO6, a tissue-specific inducible, apoplast-localized enzyme that regulates the terminal catabolism of spermidine (Spd) and spermine. Functional analysis using CRISPR-Cas9 genome-edited plants revealed that pao6 mutants accumulated significantly higher levels of Spd and phenylpropanoid-conjugated Spd in response to BPH infestation compared to wild-type controls. In addition, BPH feeding on pao6 mutants led to increased honeydew excretion and plant damage by female adults, consistent with in vitro experiments in which Spd enhanced BPH feeding. Furthermore, OsPAO6 transcription is regulated by jasmonate (JA) signaling, and it is dependent on MYC2, which directly binds to the G-box-like motif in the OsPAO6 promoter. Our findings reveal an important role of OsPAO6 in regulating polyamine catabolism in JA-induced responses triggered by herbivore attacks in rice.
多胺（PAs）及其共轭形式是植物抵御生物和非生物胁迫的防御机制的重要介质。含黄素的多胺氧化酶（PAOs）通过末端氧化调节多胺水平。迄今为止，PAOs在植物与食草动物相互作用中的作用仍知之甚少。我们发现，褐飞虱（BPH）的侵害会破坏水稻叶鞘内的多胺稳态，这与OsPAO6的上调同时发生，OsPAO6是一种组织特异性诱导、质外体定位的酶，可调节亚精胺（Spd）和精胺的末端分解代谢。使用CRISPR-Cas9基因编辑植物进行的功能分析表明，与野生型对照相比，pao6突变体在受到BPH侵害时积累的Spd和苯丙烷共轭Spd水平显著更高。此外，以pao6突变体为食的BPH导致雌性成虫的蜜露排泄增加和植物损伤，这与Spd增强BPH取食的体外实验结果一致。此外，OsPAO6转录受茉莉酸（JA）信号调控，并且依赖于MYC2，MYC2直接与OsPAO6启动子中的G-box样基序结合。我们的研究结果揭示了OsPAO6在调节水稻中食草动物攻击引发的JA诱导反应中的多胺分解代谢方面的重要作用。
