A rhabdovirus accessory protein inhibits jasmonic acid signaling in plants to attract insect vectors

Abstract 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...

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Published in:Plant physiology (Bethesda) 2022-09, Vol.190 (2), p.1349-1364
Main Authors: Gao, Dong-Min, Zhang, Zhen-Jia, Qiao, Ji-Hui, Gao, Qiang, Zang, Ying, Xu, Wen-Ya, Xie, Liang, Fang, Xiao-Dong, Ding, Zhi-Hang, Yang, Yi-Zhou, Wang, Ying, Wang, Xian-Bing
Format: Article
Language:English
Subjects:
Animals
Arabidopsis - metabolism
COP9 Signalosome Complex - metabolism
Cyclopentanes - metabolism
Hordeum - genetics
Hordeum - metabolism
Insect Vectors
Oxylipins - metabolism
Proteins - metabolism
Regular Issue Content
Rhabdoviridae - metabolism
Signal Transduction
Triticum - genetics
Triticum - metabolism
Ubiquitins - metabolism
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Summary:Abstract 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. A plant rhabdovirus accessory protein subverts JA signaling of host plants for insect vector attractiveness and efficient virus transmission.
ISSN:0032-0889
1532-2548
DOI:10.1093/plphys/kiac319