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

Author

Listed:
  • Dong-Min Gao

    (China Agricultural University)

  • Ji-Hui Qiao

    (China Agricultural University)

  • Qiang Gao

    (China Agricultural University
    China Agricultural University)

  • Jiawen Zhang

    (China Agricultural University)

  • Ying Zang

    (China Agricultural University)

  • Liang Xie

    (China Agricultural University)

  • Yan Zhang

    (China Agricultural University)

  • Ying Wang

    (China Agricultural University)

  • Jingyan Fu

    (China Agricultural University)

  • Hua Zhang

    (China Agricultural University)

  • Chenggui Han

    (China Agricultural University)

  • Xian-Bing Wang

    (China Agricultural University)

Abstract

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.

Suggested Citation

  • Dong-Min Gao & Ji-Hui Qiao & Qiang Gao & Jiawen Zhang & Ying Zang & Liang Xie & Yan Zhang & Ying Wang & Jingyan Fu & Hua Zhang & Chenggui Han & Xian-Bing Wang, 2023. "A plant cytorhabdovirus modulates locomotor activity of insect vectors to enhance virus transmission," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41503-3
    DOI: 10.1038/s41467-023-41503-3
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    References listed on IDEAS

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    1. Kevin P Keegan & Suraj Pradhan & Ji-Ping Wang & Ravi Allada, 2007. "Meta-Analysis of Drosophila Circadian Microarray Studies Identifies a Novel Set of Rhythmically Expressed Genes," PLOS Computational Biology, Public Library of Science, vol. 3(11), pages 1-1, November.
    2. Yan Zhang & Ye Wang & Xie’an Feng & Shuo Zhang & Xueqiang Xu & Lingyu Li & Shudong Niu & Yingnan Bo & Chao Wang & Zhen Li & Guoliang Xia & Hua Zhang, 2021. "Oocyte-derived microvilli control female fertility by optimizing ovarian follicle selection in mice," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
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    Cited by:

    1. Suining Deng & Siqi Jiang & Baoshen Liu & Tao Zhong & Qingcai Liu & Jianju Liu & Yuanliang Liu & Can Yin & Chen Sun & Mingliang Xu, 2024. "ZmGDIα-hel counters the RBSDV-induced reduction of active gibberellins to alleviate maize rough dwarf virus disease," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

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