State Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, China.
College of Plant Protection, China Agricultural University, Beijing 100193, China.
Plant Physiol. 2022 Sep 28;190(2):1349-1364. doi: 10.1093/plphys/kiac319.
Plant rhabdoviruses heavily rely on insect vectors for transmission between sessile plants. However, little is known about the underlying mechanisms of insect attraction and transmission of plant rhabdoviruses. In this study, we used an arthropod-borne cytorhabdovirus, Barley yellow striate mosaic virus (BYSMV), to demonstrate the molecular mechanisms of a rhabdovirus accessory protein in improving plant attractiveness to insect vectors. Here, we found that BYSMV-infected barley (Hordeum vulgare L.) plants attracted more insect vectors than mock-treated plants. Interestingly, overexpression of BYSMV P6, an accessory protein, in transgenic wheat (Triticum aestivum L.) plants substantially increased host attractiveness to insect vectors through inhibiting the jasmonic acid (JA) signaling pathway. The BYSMV P6 protein interacted with the constitutive photomorphogenesis 9 signalosome subunit 5 (CSN5) of barley plants in vivo and in vitro, and negatively affected CSN5-mediated deRUBylation of cullin1 (CUL1). Consequently, the defective CUL1-based Skp1/Cullin1/F-box ubiquitin E3 ligases could not mediate degradation of jasmonate ZIM-domain proteins, resulting in compromised JA signaling and increased insect attraction. Overexpression of BYSMV P6 also inhibited JA signaling in transgenic Arabidopsis (Arabidopsis thaliana) plants to attract insects. Our results provide insight into how a plant cytorhabdovirus subverts plant JA signaling to attract insect vectors.
植物弹状病毒严重依赖昆虫媒介在固着植物之间传播。然而，对于昆虫吸引和植物弹状病毒传播的潜在机制知之甚少。在这项研究中，我们使用了一种节肢动物传播的细胞弹状病毒——大麦黄花条纹花叶病毒（Barley yellow striate mosaic virus，BYSMV），来证明弹状病毒辅助蛋白在提高植物对昆虫媒介吸引力方面的分子机制。在这里，我们发现感染 BYSMV 的大麦（Hordeum vulgare L.）植物比模拟处理的植物更能吸引昆虫媒介。有趣的是，在转基因小麦（Triticum aestivum L.）植物中过量表达辅助蛋白 BYSMV P6，通过抑制茉莉酸（jasmonic acid，JA）信号通路，显著增加了宿主对昆虫媒介的吸引力。BYSMV P6 蛋白在体内和体外与大麦植物的组成型光形态建成 9 信号体亚基 5（constitutive photomorphogenesis 9 signalosome subunit 5，CSN5）相互作用，并负调控 CSN5 介导的 CUL1 去泛素化。因此，基于缺陷的 CUL1 的 Skp1/Cullin1/F-box 泛素 E3 连接酶不能介导茉莉酸 ZIM 结构域蛋白的降解，导致 JA 信号受损和昆虫吸引力增加。过量表达 BYSMV P6 也抑制了转基因拟南芥（Arabidopsis thaliana）植物中的 JA 信号，以吸引昆虫。我们的研究结果为植物细胞弹状病毒如何劫持植物 JA 信号以吸引昆虫媒介提供了新的认识。
