Key Laboratory of Specialty Agri-Product Quality and Hazard Controlling Technology of Zhejiang, College of Life Sciences, China Jiliang University, Hangzhou 310018, China.
Plant Cell. 2024 Sep 3;36(9):3219-3236. doi: 10.1093/plcell/koae158.
Virus-induced drought tolerance presents a fascinating facet of biotic-abiotic interaction in plants, yet its molecular intricacies remain unclear. Our study shows that cowpea mild mottle virus (CPMMV) infection enhances drought tolerance in common bean (Phaseolus vulgaris) plants through a virus-derived small interfering RNA (vsiRNA)-activated autophagy pathway. Specifically, a 21 nt vsiRNA originating from the CPMMV Triple Gene Block1 (TGB1) gene targeted the 5' untranslated region (UTR) of the host Teosinte branched 1, Cycloidea, Proliferating Cell Factor (TCP) transcription factor gene PvTCP2, independent of the known role of TGB1 as an RNA silencing suppressor. This targeting attenuated the expression of PvTCP2, which encodes a transcriptional repressor, and in turn upregulated the core autophagy-related gene (ATG) PvATG8c, leading to activated autophagy activity surpassing the level induced by drought or CPMMV infection alone. The downstream EARLY RESPONSIVE TO DEHYDRATION (ERD) effector PvERD15 is a homologue of Arabidopsis thaliana AtERD15, which positively regulates stomatal aperture. PvERD15 was degraded in PvATG8c-mediated autophagy. Therefore, we establish a TGB1-PvTCP2-PvATG8c-PvERD15 module as a trans-kingdom fine-tuning mechanism that contributes to virus-induced drought tolerance in plant-drought-virus interactions.
病毒诱导的耐旱性是植物生物与非生物相互作用的一个迷人方面，但它的分子复杂性仍不清楚。我们的研究表明，豇豆花叶病毒（CPMMV）感染通过病毒衍生的小干扰 RNA（vsiRNA）激活自噬途径增强普通菜豆（Phaseolus vulgaris）植物的耐旱性。具体来说，源自 CPMMV Triple Gene Block1（TGB1）基因的 21nt vsiRNA 靶向宿主 Teosinte branched 1、Cycloidea、Proliferating Cell Factor（TCP）转录因子基因 PvTCP2 的 5'非翻译区（UTR），独立于 TGB1 作为 RNA 沉默抑制子的已知作用。这种靶向作用减弱了 PvTCP2 的表达，PvTCP2 编码一种转录抑制剂，进而上调核心自噬相关基因（ATG）PvATG8c，导致自噬活性激活超过单独干旱或 CPMMV 感染诱导的水平。下游 EARLY RESPONSIVE TO DEHYDRATION（ERD）效应因子 PvERD15 是拟南芥 AtERD15 的同源物，它正向调节气孔开度。PvERD15 在 PvATG8c 介导的自噬中降解。因此，我们建立了一个 TGB1-PvTCP2-PvATG8c-PvERD15 模块，作为一个跨领域的精细调节机制，有助于植物-干旱-病毒相互作用中的病毒诱导耐旱性。
