Plasmodesmata‐associated Flotillin positively regulates broad‐spectrum virus cell‐to‐cell trafficking

Summary Viral diseases seriously threaten rice production. Plasmodesmata (PD)‐associated proteins are deemed to play a key role in viral infection in host plants. However, few PD‐associated proteins have been discovered in rice to afford viral infection. Here, inspired by the infection mechanism in...

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Veröffentlicht in:Plant biotechnology journal 2024-05, Vol.22 (5), p.1387-1401
Hauptverfasser: Ge, Panpan, Lu, Hong, Wang, Wei, Ma, Yonghuan, Li, Yi, Zhou, Tong, Wei, Taiyun, Wu, Jianguo, Cui, Feng
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container_issue 5
container_start_page 1387
container_title Plant biotechnology journal
container_volume 22
creator Ge, Panpan
Lu, Hong
Wang, Wei
Ma, Yonghuan
Li, Yi
Zhou, Tong
Wei, Taiyun
Wu, Jianguo
Cui, Feng
description Summary Viral diseases seriously threaten rice production. Plasmodesmata (PD)‐associated proteins are deemed to play a key role in viral infection in host plants. However, few PD‐associated proteins have been discovered in rice to afford viral infection. Here, inspired by the infection mechanism in insect vectors, we identified a member of the Flotillin family taking part in the cell‐to‐cell transport of rice stripe virus (RSV) in rice. Flotillin1 interacted with RSV nucleocapsid protein (NP) and was localized on PD. In flotillin1 knockout mutant rice, which displayed normal growth, RSV intercellular movement was retarded, leading to significantly decreased disease incidence. The PD pore sizes of the mutant rice were smaller than those of the wild type due to more callose deposits, which was closely related to the upregulation of two callose synthase genes. RSV infection stimulated flotillin1 expression and enlarged the PD aperture via RSV NP. In addition, flotillin1 knockout decreased disease incidences of southern rice black‐streaked dwarf virus (SRBSDV) and rice dwarf virus (RDV) in rice. Overall, our study reveals a new PD‐associated protein facilitating virus cell‐to‐cell trafficking and presents the potential of flotillin1 as a target to produce broad‐spectrum antiviral rice resources in the future.
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Plasmodesmata (PD)‐associated proteins are deemed to play a key role in viral infection in host plants. However, few PD‐associated proteins have been discovered in rice to afford viral infection. Here, inspired by the infection mechanism in insect vectors, we identified a member of the Flotillin family taking part in the cell‐to‐cell transport of rice stripe virus (RSV) in rice. Flotillin1 interacted with RSV nucleocapsid protein (NP) and was localized on PD. In flotillin1 knockout mutant rice, which displayed normal growth, RSV intercellular movement was retarded, leading to significantly decreased disease incidence. The PD pore sizes of the mutant rice were smaller than those of the wild type due to more callose deposits, which was closely related to the upregulation of two callose synthase genes. RSV infection stimulated flotillin1 expression and enlarged the PD aperture via RSV NP. In addition, flotillin1 knockout decreased disease incidences of southern rice black‐streaked dwarf virus (SRBSDV) and rice dwarf virus (RDV) in rice. Overall, our study reveals a new PD‐associated protein facilitating virus cell‐to‐cell trafficking and presents the potential of flotillin1 as a target to produce broad‐spectrum antiviral rice resources in the future.</description><identifier>ISSN: 1467-7644</identifier><identifier>EISSN: 1467-7652</identifier><identifier>DOI: 10.1111/pbi.14274</identifier><identifier>PMID: 38130080</identifier><language>eng</language><publisher>England: John Wiley and Sons Inc</publisher><subject>1,3-beta-glucan synthase ; biotechnology ; callose ; disease incidence ; Flotillin ; insects ; mutants ; nucleocapsid proteins ; plasmodesmata ; plasmodesmata‐associated protein ; rice ; Rice dwarf virus ; Rice stripe tenuivirus ; rice stripe virus ; Southern rice black-streaked dwarf virus ; viruses</subject><ispartof>Plant biotechnology journal, 2024-05, Vol.22 (5), p.1387-1401</ispartof><rights>2023 The Authors. published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley &amp; Sons Ltd.</rights><rights>2023 The Authors. 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Plasmodesmata (PD)‐associated proteins are deemed to play a key role in viral infection in host plants. However, few PD‐associated proteins have been discovered in rice to afford viral infection. Here, inspired by the infection mechanism in insect vectors, we identified a member of the Flotillin family taking part in the cell‐to‐cell transport of rice stripe virus (RSV) in rice. Flotillin1 interacted with RSV nucleocapsid protein (NP) and was localized on PD. In flotillin1 knockout mutant rice, which displayed normal growth, RSV intercellular movement was retarded, leading to significantly decreased disease incidence. The PD pore sizes of the mutant rice were smaller than those of the wild type due to more callose deposits, which was closely related to the upregulation of two callose synthase genes. RSV infection stimulated flotillin1 expression and enlarged the PD aperture via RSV NP. In addition, flotillin1 knockout decreased disease incidences of southern rice black‐streaked dwarf virus (SRBSDV) and rice dwarf virus (RDV) in rice. Overall, our study reveals a new PD‐associated protein facilitating virus cell‐to‐cell trafficking and presents the potential of flotillin1 as a target to produce broad‐spectrum antiviral rice resources in the future.</description><subject>1,3-beta-glucan synthase</subject><subject>biotechnology</subject><subject>callose</subject><subject>disease incidence</subject><subject>Flotillin</subject><subject>insects</subject><subject>mutants</subject><subject>nucleocapsid proteins</subject><subject>plasmodesmata</subject><subject>plasmodesmata‐associated protein</subject><subject>rice</subject><subject>Rice dwarf virus</subject><subject>Rice stripe tenuivirus</subject><subject>rice stripe virus</subject><subject>Southern rice black-streaked dwarf virus</subject><subject>viruses</subject><issn>1467-7644</issn><issn>1467-7652</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><recordid>eNqFkc1u1DAUhS1ExZRpF7wAyhIWaf2bOCtEK0orVeosYG059s1gcOJgJ4NmxyPwjDwJHqYdwaKqZdlXvp-P7tFB6BXBZySv87F1Z4TTmj9Dx4RXdVlXgj4_1Jwv0MuUvmJMSSWqF2jBJGEYS3yM-pXXqQ8WUq8n_fvnL51SME5PYIsrHybnvRuKMSQ3uQ34bRFhPfvcTkUbg7b5RxrBTHHui42LcyoMeJ9fp5CPXV1MUXedM9_csD5BR532CU7v7yX6fPXh0-V1eXv38eby_W1pOG54yQkVrLG1Fi20tZRtJ2W2pyU12rStqAhmLPuiYIztrAUqaguMECZ4bVnFlujdXnec2x6sgSEP4dUYXa_jVgXt1P-dwX1R67BRhGBKa9lkhTf3CjF8nyFNqndpZ0cPEOakGBF5N7TBT6KZEYIKmT0t0ds9amJIKUJ3GIlgtYtS5SjV3ygz-_pfDwfyIbsMnO-BH87D9nEltbq42Uv-ATOQr2U</recordid><startdate>202405</startdate><enddate>202405</enddate><creator>Ge, Panpan</creator><creator>Lu, Hong</creator><creator>Wang, Wei</creator><creator>Ma, Yonghuan</creator><creator>Li, Yi</creator><creator>Zhou, Tong</creator><creator>Wei, Taiyun</creator><creator>Wu, Jianguo</creator><creator>Cui, Feng</creator><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-6215-7159</orcidid></search><sort><creationdate>202405</creationdate><title>Plasmodesmata‐associated Flotillin positively regulates broad‐spectrum virus cell‐to‐cell trafficking</title><author>Ge, Panpan ; Lu, Hong ; Wang, Wei ; Ma, Yonghuan ; Li, Yi ; Zhou, Tong ; Wei, Taiyun ; Wu, Jianguo ; Cui, Feng</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4094-412539d7a5beb788bf88427a82cacbb5610337642eccdfdde257de3113547d363</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>1,3-beta-glucan synthase</topic><topic>biotechnology</topic><topic>callose</topic><topic>disease incidence</topic><topic>Flotillin</topic><topic>insects</topic><topic>mutants</topic><topic>nucleocapsid proteins</topic><topic>plasmodesmata</topic><topic>plasmodesmata‐associated protein</topic><topic>rice</topic><topic>Rice dwarf virus</topic><topic>Rice stripe tenuivirus</topic><topic>rice stripe virus</topic><topic>Southern rice black-streaked dwarf virus</topic><topic>viruses</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ge, Panpan</creatorcontrib><creatorcontrib>Lu, Hong</creatorcontrib><creatorcontrib>Wang, Wei</creatorcontrib><creatorcontrib>Ma, Yonghuan</creatorcontrib><creatorcontrib>Li, Yi</creatorcontrib><creatorcontrib>Zhou, Tong</creatorcontrib><creatorcontrib>Wei, Taiyun</creatorcontrib><creatorcontrib>Wu, Jianguo</creatorcontrib><creatorcontrib>Cui, Feng</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Plant biotechnology journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ge, Panpan</au><au>Lu, Hong</au><au>Wang, Wei</au><au>Ma, Yonghuan</au><au>Li, Yi</au><au>Zhou, Tong</au><au>Wei, Taiyun</au><au>Wu, Jianguo</au><au>Cui, Feng</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Plasmodesmata‐associated Flotillin positively regulates broad‐spectrum virus cell‐to‐cell trafficking</atitle><jtitle>Plant biotechnology journal</jtitle><addtitle>Plant Biotechnol J</addtitle><date>2024-05</date><risdate>2024</risdate><volume>22</volume><issue>5</issue><spage>1387</spage><epage>1401</epage><pages>1387-1401</pages><issn>1467-7644</issn><eissn>1467-7652</eissn><abstract>Summary Viral diseases seriously threaten rice production. Plasmodesmata (PD)‐associated proteins are deemed to play a key role in viral infection in host plants. However, few PD‐associated proteins have been discovered in rice to afford viral infection. Here, inspired by the infection mechanism in insect vectors, we identified a member of the Flotillin family taking part in the cell‐to‐cell transport of rice stripe virus (RSV) in rice. Flotillin1 interacted with RSV nucleocapsid protein (NP) and was localized on PD. In flotillin1 knockout mutant rice, which displayed normal growth, RSV intercellular movement was retarded, leading to significantly decreased disease incidence. The PD pore sizes of the mutant rice were smaller than those of the wild type due to more callose deposits, which was closely related to the upregulation of two callose synthase genes. RSV infection stimulated flotillin1 expression and enlarged the PD aperture via RSV NP. In addition, flotillin1 knockout decreased disease incidences of southern rice black‐streaked dwarf virus (SRBSDV) and rice dwarf virus (RDV) in rice. Overall, our study reveals a new PD‐associated protein facilitating virus cell‐to‐cell trafficking and presents the potential of flotillin1 as a target to produce broad‐spectrum antiviral rice resources in the future.</abstract><cop>England</cop><pub>John Wiley and Sons Inc</pub><pmid>38130080</pmid><doi>10.1111/pbi.14274</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0001-6215-7159</orcidid><oa>free_for_read</oa></addata></record>
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subjects 1,3-beta-glucan synthase
biotechnology
callose
disease incidence
Flotillin
insects
mutants
nucleocapsid proteins
plasmodesmata
plasmodesmata‐associated protein
rice
Rice dwarf virus
Rice stripe tenuivirus
rice stripe virus
Southern rice black-streaked dwarf virus
viruses
title Plasmodesmata‐associated Flotillin positively regulates broad‐spectrum virus cell‐to‐cell trafficking
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