A plant cytorhabdovirus modulates locomotor activity of insect vectors to enhance virus transmission
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...
| Main Authors: | , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2023-09-01
|
| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-41503-3 |
| _version_ | 1797558562909585408 |
|---|---|
| author | 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 |
| author_facet | 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 |
| author_sort | Dong-Min Gao |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-03-10T17:32:13Z |
| format | Article |
| id | doaj.art-057bc43850ed410da44904188e12a212 |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-10T17:32:13Z |
| publishDate | 2023-09-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-057bc43850ed410da44904188e12a2122023-11-20T09:57:13ZengNature PortfolioNature Communications2041-17232023-09-0114111310.1038/s41467-023-41503-3A plant cytorhabdovirus modulates locomotor activity of insect vectors to enhance virus transmissionDong-Min Gao0Ji-Hui Qiao1Qiang Gao2Jiawen Zhang3Ying Zang4Liang Xie5Yan Zhang6Ying Wang7Jingyan Fu8Hua Zhang9Chenggui Han10Xian-Bing Wang11State Key Laboratory of Plant Environmental Resilience, College of Biological Sciences, China Agricultural UniversityState Key Laboratory of Plant Environmental Resilience, College of Biological Sciences, China Agricultural UniversityState Key Laboratory of Plant Environmental Resilience, College of Biological Sciences, China Agricultural UniversityState Key Laboratory of Animal Biotech Breeding, College of Biological Sciences, China Agricultural UniversityState Key Laboratory of Plant Environmental Resilience, College of Biological Sciences, China Agricultural UniversityState Key Laboratory of Plant Environmental Resilience, College of Biological Sciences, China Agricultural UniversityState Key Laboratory of Animal Biotech Breeding, College of Biological Sciences, China Agricultural UniversityMinistry of Agriculture and Rural Affairs Key Laboratory of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural UniversityState Key Laboratory of Animal Biotech Breeding, College of Biological Sciences, China Agricultural UniversityState Key Laboratory of Animal Biotech Breeding, College of Biological Sciences, China Agricultural UniversityMinistry of Agriculture and Rural Affairs Key Laboratory of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural UniversityState Key Laboratory of Plant Environmental Resilience, College of Biological Sciences, China Agricultural UniversityAbstract 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.https://doi.org/10.1038/s41467-023-41503-3 |
| spellingShingle | 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 A plant cytorhabdovirus modulates locomotor activity of insect vectors to enhance virus transmission Nature Communications |
| title | A plant cytorhabdovirus modulates locomotor activity of insect vectors to enhance virus transmission |
| title_full | A plant cytorhabdovirus modulates locomotor activity of insect vectors to enhance virus transmission |
| title_fullStr | A plant cytorhabdovirus modulates locomotor activity of insect vectors to enhance virus transmission |
| title_full_unstemmed | A plant cytorhabdovirus modulates locomotor activity of insect vectors to enhance virus transmission |
| title_short | A plant cytorhabdovirus modulates locomotor activity of insect vectors to enhance virus transmission |
| title_sort | plant cytorhabdovirus modulates locomotor activity of insect vectors to enhance virus transmission |
| url | https://doi.org/10.1038/s41467-023-41503-3 |
| work_keys_str_mv | AT dongmingao aplantcytorhabdovirusmodulateslocomotoractivityofinsectvectorstoenhancevirustransmission AT jihuiqiao aplantcytorhabdovirusmodulateslocomotoractivityofinsectvectorstoenhancevirustransmission AT qianggao aplantcytorhabdovirusmodulateslocomotoractivityofinsectvectorstoenhancevirustransmission AT jiawenzhang aplantcytorhabdovirusmodulateslocomotoractivityofinsectvectorstoenhancevirustransmission AT yingzang aplantcytorhabdovirusmodulateslocomotoractivityofinsectvectorstoenhancevirustransmission AT liangxie aplantcytorhabdovirusmodulateslocomotoractivityofinsectvectorstoenhancevirustransmission AT yanzhang aplantcytorhabdovirusmodulateslocomotoractivityofinsectvectorstoenhancevirustransmission AT yingwang aplantcytorhabdovirusmodulateslocomotoractivityofinsectvectorstoenhancevirustransmission AT jingyanfu aplantcytorhabdovirusmodulateslocomotoractivityofinsectvectorstoenhancevirustransmission AT huazhang aplantcytorhabdovirusmodulateslocomotoractivityofinsectvectorstoenhancevirustransmission AT chengguihan aplantcytorhabdovirusmodulateslocomotoractivityofinsectvectorstoenhancevirustransmission AT xianbingwang aplantcytorhabdovirusmodulateslocomotoractivityofinsectvectorstoenhancevirustransmission AT dongmingao plantcytorhabdovirusmodulateslocomotoractivityofinsectvectorstoenhancevirustransmission AT jihuiqiao plantcytorhabdovirusmodulateslocomotoractivityofinsectvectorstoenhancevirustransmission AT qianggao plantcytorhabdovirusmodulateslocomotoractivityofinsectvectorstoenhancevirustransmission AT jiawenzhang plantcytorhabdovirusmodulateslocomotoractivityofinsectvectorstoenhancevirustransmission AT yingzang plantcytorhabdovirusmodulateslocomotoractivityofinsectvectorstoenhancevirustransmission AT liangxie plantcytorhabdovirusmodulateslocomotoractivityofinsectvectorstoenhancevirustransmission AT yanzhang plantcytorhabdovirusmodulateslocomotoractivityofinsectvectorstoenhancevirustransmission AT yingwang plantcytorhabdovirusmodulateslocomotoractivityofinsectvectorstoenhancevirustransmission AT jingyanfu plantcytorhabdovirusmodulateslocomotoractivityofinsectvectorstoenhancevirustransmission AT huazhang plantcytorhabdovirusmodulateslocomotoractivityofinsectvectorstoenhancevirustransmission AT chengguihan plantcytorhabdovirusmodulateslocomotoractivityofinsectvectorstoenhancevirustransmission AT xianbingwang plantcytorhabdovirusmodulateslocomotoractivityofinsectvectorstoenhancevirustransmission |