HSP90 interacts with VP37 to facilitate the cell-to-cell movement of broad bean wilt virus 2

ABSTRACT The systemic spread of viruses in plants requires successful viral cell-to-cell movement through plasmodesmata (PD). Viral movement proteins (MPs) interact with cellular proteins to modify and utilize host transport routes. Broad bean wilt virus 2 (BBWV2) moves from cell to cell as a virion...

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Main Authors: Myung-Hwi Kim, Seok-Yeong Jang, Ji-Soo Choi, Sora Kim, Yubin Lee, Suejin Park, Sun-Jung Kwon, Jang-Kyun Seo
Format: Article
Language:English
Published: American Society for Microbiology 2025-03-01
Series:mBio
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Online Access:https://journals.asm.org/doi/10.1128/mbio.02500-24
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author Myung-Hwi Kim
Seok-Yeong Jang
Ji-Soo Choi
Sora Kim
Yubin Lee
Suejin Park
Sun-Jung Kwon
Jang-Kyun Seo
author_facet Myung-Hwi Kim
Seok-Yeong Jang
Ji-Soo Choi
Sora Kim
Yubin Lee
Suejin Park
Sun-Jung Kwon
Jang-Kyun Seo
author_sort Myung-Hwi Kim
collection DOAJ
description ABSTRACT The systemic spread of viruses in plants requires successful viral cell-to-cell movement through plasmodesmata (PD). Viral movement proteins (MPs) interact with cellular proteins to modify and utilize host transport routes. Broad bean wilt virus 2 (BBWV2) moves from cell to cell as a virion through the PD gated by VP37, the MP of BBWV2. However, the host proteins that function in the cell-to-cell movement of BBWV2 remain unclear. In this study, we identified cellular heat shock protein 90 (HSP90) as an interacting partner of VP37. The interaction between HSP90 and VP37 was assessed using the yeast two-hybrid assay, co-immunoprecipitation, and bimolecular fluorescence complementation. Tobacco rattle virus-based virus-induced gene silencing analysis revealed that HSP90 silencing significantly inhibited the systemic spread of BBWV2 in Nicotiana benthamiana plants. Furthermore, in planta treatment with geldanamycin (GDA), an inhibitor of the chaperone function of HSP90, demonstrated the necessity of HSP90 in successful cell-to-cell movement and systemic infection of BBWV2. Interestingly, GDA treatment inhibited the HSP90-VP37 interaction at the PD, resulting in the inhibition of VP37-derived tubule formation through the PD. Our results suggest that the HSP90-VP37 interaction regulates VP37-derived tubule formation through the PD, thereby facilitating the cell-to-cell movement of BBWV2.IMPORTANCEThis study highlights the regulatory role of heat shock protein 90 (HSP90) in facilitating the cell-to-cell movement of broad bean wilt virus 2 (BBWV2). HSP90 interacted with VP37, the movement protein of BBWV2, specifically at plasmodesmata (PD). This study demonstrated that the HSP90-VP37 interaction is crucial for viral cell-to-cell movement and the formation of VP37-derived tubules, which are essential structures for virus transport through the PD. The ATP-dependent chaperone activity of HSP90 is integral to this interaction, as demonstrated by the inhibition of virus movement upon treatment with geldanamycin, which disrupts the function of HSP90. These findings elucidate the molecular mechanisms underlying the cell-to-cell movement of plant viruses and highlight the role of HSP90 in viral infection. This study suggests that the chaperone activity of HSP90 may function in changing the conformational structure of VP37, thereby facilitating the assembly and function of virus-induced structures required for viral cell-to-cell movement.
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spelling doaj-art-0ebd011fcd7f4eaabd2815e75aca495b2025-08-20T02:52:35ZengAmerican Society for MicrobiologymBio2150-75112025-03-0116310.1128/mbio.02500-24HSP90 interacts with VP37 to facilitate the cell-to-cell movement of broad bean wilt virus 2Myung-Hwi Kim0Seok-Yeong Jang1Ji-Soo Choi2Sora Kim3Yubin Lee4Suejin Park5Sun-Jung Kwon6Jang-Kyun Seo7Department of Agricultural Biotechnology, Seoul National University, Seoul, South KoreaDepartment of International Agricultural Technology, Seoul National University, Pyeongchang, South KoreaDepartment of International Agricultural Technology, Seoul National University, Pyeongchang, South KoreaDepartment of International Agricultural Technology, Seoul National University, Pyeongchang, South KoreaDepartment of International Agricultural Technology, Seoul National University, Pyeongchang, South KoreaDepartment of Horticulture, Jeonbuk National University, Jeonju, South KoreaInstitutes of Green Bio Science and Technology, Seoul National University, Pyeongchang, South KoreaDepartment of Agricultural Biotechnology, Seoul National University, Seoul, South KoreaABSTRACT The systemic spread of viruses in plants requires successful viral cell-to-cell movement through plasmodesmata (PD). Viral movement proteins (MPs) interact with cellular proteins to modify and utilize host transport routes. Broad bean wilt virus 2 (BBWV2) moves from cell to cell as a virion through the PD gated by VP37, the MP of BBWV2. However, the host proteins that function in the cell-to-cell movement of BBWV2 remain unclear. In this study, we identified cellular heat shock protein 90 (HSP90) as an interacting partner of VP37. The interaction between HSP90 and VP37 was assessed using the yeast two-hybrid assay, co-immunoprecipitation, and bimolecular fluorescence complementation. Tobacco rattle virus-based virus-induced gene silencing analysis revealed that HSP90 silencing significantly inhibited the systemic spread of BBWV2 in Nicotiana benthamiana plants. Furthermore, in planta treatment with geldanamycin (GDA), an inhibitor of the chaperone function of HSP90, demonstrated the necessity of HSP90 in successful cell-to-cell movement and systemic infection of BBWV2. Interestingly, GDA treatment inhibited the HSP90-VP37 interaction at the PD, resulting in the inhibition of VP37-derived tubule formation through the PD. Our results suggest that the HSP90-VP37 interaction regulates VP37-derived tubule formation through the PD, thereby facilitating the cell-to-cell movement of BBWV2.IMPORTANCEThis study highlights the regulatory role of heat shock protein 90 (HSP90) in facilitating the cell-to-cell movement of broad bean wilt virus 2 (BBWV2). HSP90 interacted with VP37, the movement protein of BBWV2, specifically at plasmodesmata (PD). This study demonstrated that the HSP90-VP37 interaction is crucial for viral cell-to-cell movement and the formation of VP37-derived tubules, which are essential structures for virus transport through the PD. The ATP-dependent chaperone activity of HSP90 is integral to this interaction, as demonstrated by the inhibition of virus movement upon treatment with geldanamycin, which disrupts the function of HSP90. These findings elucidate the molecular mechanisms underlying the cell-to-cell movement of plant viruses and highlight the role of HSP90 in viral infection. This study suggests that the chaperone activity of HSP90 may function in changing the conformational structure of VP37, thereby facilitating the assembly and function of virus-induced structures required for viral cell-to-cell movement.https://journals.asm.org/doi/10.1128/mbio.02500-24BBWV2VP37HSP90cell-to-cell movementtubule formation
spellingShingle Myung-Hwi Kim
Seok-Yeong Jang
Ji-Soo Choi
Sora Kim
Yubin Lee
Suejin Park
Sun-Jung Kwon
Jang-Kyun Seo
HSP90 interacts with VP37 to facilitate the cell-to-cell movement of broad bean wilt virus 2
mBio
BBWV2
VP37
HSP90
cell-to-cell movement
tubule formation
title HSP90 interacts with VP37 to facilitate the cell-to-cell movement of broad bean wilt virus 2
title_full HSP90 interacts with VP37 to facilitate the cell-to-cell movement of broad bean wilt virus 2
title_fullStr HSP90 interacts with VP37 to facilitate the cell-to-cell movement of broad bean wilt virus 2
title_full_unstemmed HSP90 interacts with VP37 to facilitate the cell-to-cell movement of broad bean wilt virus 2
title_short HSP90 interacts with VP37 to facilitate the cell-to-cell movement of broad bean wilt virus 2
title_sort hsp90 interacts with vp37 to facilitate the cell to cell movement of broad bean wilt virus 2
topic BBWV2
VP37
HSP90
cell-to-cell movement
tubule formation
url https://journals.asm.org/doi/10.1128/mbio.02500-24
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