A plant cytorhabdovirus modulates locomotor activity of insect vectors to enhance virus transmission

• Published in: Nature communications Vol. 14; no. 1; p. 5754
• Main Authors: Gao, Dong-Min, Qiao, Ji-Hui, Gao, Qiang, Zhang, Jiawen, Zang, Ying, Xie, Liang, Zhang, Yan, Wang, Ying, Fu, Jingyan, Zhang, Hua, Han, Chenggui, Wang, Xian-Bing
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 16.09.2023; Nature Publishing Group; Nature Portfolio
• Subjects: 13/1; 13/51; 13/89; 14/19; 38/111; 38/35; 59; 631/326/596/2557; 631/326/596/2563; 64/24; 82/83; Central nervous system; Circadian rhythm; Circadian rhythms; CLOCK protein; Cullin; Disease transmission; Humanities and Social Sciences; Hyperactivity; Insects; Locomotor activity; Molecular modelling; multidisciplinary; Phloem; Plant virus diseases; Plant viruses; Protein P6; Proteins; Regulatory mechanisms (biology); Science; Science (multidisciplinary); Vectors; Viruses
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-023-41503-3

Transmission of many plant viruses relies on phloem-feeding insect vectors. However, how plant viruses directly modulate insect behavior is largely unknown. Barley yellow striate mosaic virus (BYSMV) is transmitted by the small brown planthopper (SBPH, Laodelphax striatellus ). Here, we show that BYSMV infects the central nervous system (CNS) of SBPHs, induces insect hyperactivity, and prolongs phloem feeding duration. The BYSMV accessory protein P6 interacts with the COP9 signalosome subunit 5 (LsCSN5) of SBPHs and suppresses LsCSN5-regulated de-neddylation from the Cullin 1 (CUL1), hereby inhibiting CUL1-based E3 ligases-mediated degradation of the circadian clock protein Timeless (TIM). Thus, virus infection or knockdown of LsCSN5 compromises TIM oscillation and induces high insect locomotor activity for transmission. Additionally, expression of BYSMV P6 in the CNS of transgenic Drosophila melanogaster disturbs circadian rhythm and induces high locomotor activity. Together, our results suggest the molecular mechanisms whereby BYSMV modulates locomotor activity of insect vectors for transmission. Most plant viruses are transmitted by insect vectors in finely regulatory mechanisms. Here, the authors show that a plant rhabdovirus can modify circadian rhythm of its insect vectors and enhances locomotor activity for efficient transmission.