Dual Guardians of Immunity: FoRab10 and FoRab29 in Frankliniella occidentalis Confer Resistance to Tomato Spotted Wilt Orthotospovirus
Rab GTPase is critical for autophagy processes and is implicated in insect immunity against viruses. In this study, we aimed to investigate the role of FoRabs in the autophagic regulation of antiviral defense against tomato spotted wilt orthotospovirus (TSWV) in Frankliniella occidentalis. Transcrip...
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| Veröffentlicht in: | Journal of agricultural and food chemistry 2024-07, Vol.72 (30), p.16661-16673 |
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| container_title | Journal of agricultural and food chemistry |
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| creator | Zheng, Xiaobin Yuan, Jiangjiang Wan, Yanran Tang, Yingxi Cao, Hongyi Wang, Jing Qian, Kanghua Zhang, Ying Chen, Sirui Xu, Baoyun Zhang, Youjun Liang, Pei Wu, Qingjun |
| description | Rab GTPase is critical for autophagy processes and is implicated in insect immunity against viruses. In this study, we aimed to investigate the role of FoRabs in the autophagic regulation of antiviral defense against tomato spotted wilt orthotospovirus (TSWV) in Frankliniella occidentalis. Transcriptome analysis revealed the downregulation of FoRabs in viruliferous nymph and adults of F. occidentalis in response to TSWV infection. Manipulation of autophagy levels with 3-MA and Rapa treatments resulted in a 5- to 15-fold increase and a 38–64% decrease in viral titers, respectively. Additionally, interference with FoRab10 in nymphs and FoRab29 in adults led to a 20–90% downregulation of autophagy-related genes, a decrease in ATG8-II (an autophagy marker protein), and an increase in the TSWV titers by 1.5- to 2.5-fold and 1.3- to 2.0-fold, respectively. In addition, the leaf disk and the living plant methods revealed increased transmission rates of 20.8–41.6 and 68.3–88.3%, respectively. In conclusion, FoRab10 and FoRab29 play a role in the autophagic regulation of the antiviral defense in F. occidentalis nymphs and adults against TSWV, respectively. These findings offer insights into the intricate immune mechanisms functional in F. occidentalis against TSWV, suggesting potential targeted strategies for F. occidentalis and TSWV management. |
| doi_str_mv | 10.1021/acs.jafc.4c03412 |
| format | Article |
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In this study, we aimed to investigate the role of FoRabs in the autophagic regulation of antiviral defense against tomato spotted wilt orthotospovirus (TSWV) in Frankliniella occidentalis. Transcriptome analysis revealed the downregulation of FoRabs in viruliferous nymph and adults of F. occidentalis in response to TSWV infection. Manipulation of autophagy levels with 3-MA and Rapa treatments resulted in a 5- to 15-fold increase and a 38–64% decrease in viral titers, respectively. Additionally, interference with FoRab10 in nymphs and FoRab29 in adults led to a 20–90% downregulation of autophagy-related genes, a decrease in ATG8-II (an autophagy marker protein), and an increase in the TSWV titers by 1.5- to 2.5-fold and 1.3- to 2.0-fold, respectively. In addition, the leaf disk and the living plant methods revealed increased transmission rates of 20.8–41.6 and 68.3–88.3%, respectively. In conclusion, FoRab10 and FoRab29 play a role in the autophagic regulation of the antiviral defense in F. occidentalis nymphs and adults against TSWV, respectively. These findings offer insights into the intricate immune mechanisms functional in F. occidentalis against TSWV, suggesting potential targeted strategies for F. occidentalis and TSWV management.</description><identifier>ISSN: 0021-8561</identifier><identifier>ISSN: 1520-5118</identifier><identifier>EISSN: 1520-5118</identifier><identifier>DOI: 10.1021/acs.jafc.4c03412</identifier><identifier>PMID: 39021284</identifier><language>eng</language><publisher>United States: American Chemical Society</publisher><subject>Agricultural and Environmental Chemistry ; Animals ; Autophagy ; Disease Resistance - genetics ; Disease Resistance - immunology ; Insect Proteins - genetics ; Insect Proteins - immunology ; Insect Proteins - metabolism ; Nymph - genetics ; Nymph - growth & development ; Nymph - immunology ; Nymph - virology ; Plant Diseases - genetics ; Plant Diseases - immunology ; Plant Diseases - virology ; rab GTP-Binding Proteins - genetics ; rab GTP-Binding Proteins - immunology ; rab GTP-Binding Proteins - metabolism ; Solanum lycopersicum - genetics ; Solanum lycopersicum - immunology ; Solanum lycopersicum - virology ; Thysanoptera - genetics ; Thysanoptera - immunology ; Thysanoptera - virology ; Tospovirus - immunology ; Tospovirus - physiology</subject><ispartof>Journal of agricultural and food chemistry, 2024-07, Vol.72 (30), p.16661-16673</ispartof><rights>2024 American Chemical Society</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-a219t-fb80971b5361d162635956d200a7ce8253140e883df52aecf44e33ad426973e43</cites><orcidid>0000-0002-0344-5561 ; 0000-0002-3083-8918 ; 0000-0003-3508-6695</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://pubs.acs.org/doi/pdf/10.1021/acs.jafc.4c03412$$EPDF$$P50$$Gacs$$H</linktopdf><linktohtml>$$Uhttps://pubs.acs.org/doi/10.1021/acs.jafc.4c03412$$EHTML$$P50$$Gacs$$H</linktohtml><link.rule.ids>314,780,784,2765,27076,27924,27925,56738,56788</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39021284$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zheng, Xiaobin</creatorcontrib><creatorcontrib>Yuan, Jiangjiang</creatorcontrib><creatorcontrib>Wan, Yanran</creatorcontrib><creatorcontrib>Tang, Yingxi</creatorcontrib><creatorcontrib>Cao, Hongyi</creatorcontrib><creatorcontrib>Wang, Jing</creatorcontrib><creatorcontrib>Qian, Kanghua</creatorcontrib><creatorcontrib>Zhang, Ying</creatorcontrib><creatorcontrib>Chen, Sirui</creatorcontrib><creatorcontrib>Xu, Baoyun</creatorcontrib><creatorcontrib>Zhang, Youjun</creatorcontrib><creatorcontrib>Liang, Pei</creatorcontrib><creatorcontrib>Wu, Qingjun</creatorcontrib><title>Dual Guardians of Immunity: FoRab10 and FoRab29 in Frankliniella occidentalis Confer Resistance to Tomato Spotted Wilt Orthotospovirus</title><title>Journal of agricultural and food chemistry</title><addtitle>J. Agric. Food Chem</addtitle><description>Rab GTPase is critical for autophagy processes and is implicated in insect immunity against viruses. In this study, we aimed to investigate the role of FoRabs in the autophagic regulation of antiviral defense against tomato spotted wilt orthotospovirus (TSWV) in Frankliniella occidentalis. Transcriptome analysis revealed the downregulation of FoRabs in viruliferous nymph and adults of F. occidentalis in response to TSWV infection. Manipulation of autophagy levels with 3-MA and Rapa treatments resulted in a 5- to 15-fold increase and a 38–64% decrease in viral titers, respectively. Additionally, interference with FoRab10 in nymphs and FoRab29 in adults led to a 20–90% downregulation of autophagy-related genes, a decrease in ATG8-II (an autophagy marker protein), and an increase in the TSWV titers by 1.5- to 2.5-fold and 1.3- to 2.0-fold, respectively. In addition, the leaf disk and the living plant methods revealed increased transmission rates of 20.8–41.6 and 68.3–88.3%, respectively. In conclusion, FoRab10 and FoRab29 play a role in the autophagic regulation of the antiviral defense in F. occidentalis nymphs and adults against TSWV, respectively. These findings offer insights into the intricate immune mechanisms functional in F. occidentalis against TSWV, suggesting potential targeted strategies for F. occidentalis and TSWV management.</description><subject>Agricultural and Environmental Chemistry</subject><subject>Animals</subject><subject>Autophagy</subject><subject>Disease Resistance - genetics</subject><subject>Disease Resistance - immunology</subject><subject>Insect Proteins - genetics</subject><subject>Insect Proteins - immunology</subject><subject>Insect Proteins - metabolism</subject><subject>Nymph - genetics</subject><subject>Nymph - growth & development</subject><subject>Nymph - immunology</subject><subject>Nymph - virology</subject><subject>Plant Diseases - genetics</subject><subject>Plant Diseases - immunology</subject><subject>Plant Diseases - virology</subject><subject>rab GTP-Binding Proteins - genetics</subject><subject>rab GTP-Binding Proteins - immunology</subject><subject>rab GTP-Binding Proteins - metabolism</subject><subject>Solanum lycopersicum - genetics</subject><subject>Solanum lycopersicum - immunology</subject><subject>Solanum lycopersicum - virology</subject><subject>Thysanoptera - genetics</subject><subject>Thysanoptera - immunology</subject><subject>Thysanoptera - virology</subject><subject>Tospovirus - immunology</subject><subject>Tospovirus - physiology</subject><issn>0021-8561</issn><issn>1520-5118</issn><issn>1520-5118</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kMFO3DAQhq0KVBbovafKRw7NMrbjxOFWbVmKhLTSAuoxmrUd1TSxt7ZTiRfgucmyS289zUjz_b80HyGfGcwZcHaJOs2fsNPzUoMoGf9AZkxyKCRj6ojMYGIKJSt2Qk5TegIAJWv4SE5EM124Kmfk5fuIPb0ZMRqHPtHQ0dthGL3Lz1d0Gda4YUDRm_3OG-o8XUb0v3vnne17pEFrZ6zP2LtEF8F3NtK1TS5l9NrSHOhDGHAa99uQszX0p-szXcX8K-SQtuGvi2M6J8cd9sl-Oswz8ri8flj8KO5WN7eLb3cFctbkotsoaGq2kaJihlW8ErKRleEAWGuruBSsBKuUMJ3kaHVXllYINCWvmlrYUpyRi33vNoY_o025HVzSuz-8DWNqBSguoBFQTyjsUR1DStF27Ta6AeNzy6Dd2W8n--3OfnuwP0W-HNrHzWDNv8C77gn4ugfeomGMfnr2_32vXzWQrA</recordid><startdate>20240731</startdate><enddate>20240731</enddate><creator>Zheng, Xiaobin</creator><creator>Yuan, Jiangjiang</creator><creator>Wan, Yanran</creator><creator>Tang, Yingxi</creator><creator>Cao, Hongyi</creator><creator>Wang, Jing</creator><creator>Qian, Kanghua</creator><creator>Zhang, Ying</creator><creator>Chen, Sirui</creator><creator>Xu, Baoyun</creator><creator>Zhang, Youjun</creator><creator>Liang, Pei</creator><creator>Wu, Qingjun</creator><general>American Chemical Society</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-0344-5561</orcidid><orcidid>https://orcid.org/0000-0002-3083-8918</orcidid><orcidid>https://orcid.org/0000-0003-3508-6695</orcidid></search><sort><creationdate>20240731</creationdate><title>Dual Guardians of Immunity: FoRab10 and FoRab29 in Frankliniella occidentalis Confer Resistance to Tomato Spotted Wilt Orthotospovirus</title><author>Zheng, Xiaobin ; Yuan, Jiangjiang ; Wan, Yanran ; Tang, Yingxi ; Cao, Hongyi ; Wang, Jing ; Qian, Kanghua ; Zhang, Ying ; Chen, Sirui ; Xu, Baoyun ; Zhang, Youjun ; Liang, Pei ; Wu, Qingjun</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a219t-fb80971b5361d162635956d200a7ce8253140e883df52aecf44e33ad426973e43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Agricultural and Environmental Chemistry</topic><topic>Animals</topic><topic>Autophagy</topic><topic>Disease Resistance - genetics</topic><topic>Disease Resistance - immunology</topic><topic>Insect Proteins - genetics</topic><topic>Insect Proteins - immunology</topic><topic>Insect Proteins - metabolism</topic><topic>Nymph - genetics</topic><topic>Nymph - growth & development</topic><topic>Nymph - immunology</topic><topic>Nymph - virology</topic><topic>Plant Diseases - genetics</topic><topic>Plant Diseases - immunology</topic><topic>Plant Diseases - virology</topic><topic>rab GTP-Binding Proteins - genetics</topic><topic>rab GTP-Binding Proteins - immunology</topic><topic>rab GTP-Binding Proteins - metabolism</topic><topic>Solanum lycopersicum - genetics</topic><topic>Solanum lycopersicum - immunology</topic><topic>Solanum lycopersicum - virology</topic><topic>Thysanoptera - genetics</topic><topic>Thysanoptera - immunology</topic><topic>Thysanoptera - virology</topic><topic>Tospovirus - immunology</topic><topic>Tospovirus - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zheng, Xiaobin</creatorcontrib><creatorcontrib>Yuan, Jiangjiang</creatorcontrib><creatorcontrib>Wan, Yanran</creatorcontrib><creatorcontrib>Tang, Yingxi</creatorcontrib><creatorcontrib>Cao, Hongyi</creatorcontrib><creatorcontrib>Wang, Jing</creatorcontrib><creatorcontrib>Qian, Kanghua</creatorcontrib><creatorcontrib>Zhang, Ying</creatorcontrib><creatorcontrib>Chen, Sirui</creatorcontrib><creatorcontrib>Xu, Baoyun</creatorcontrib><creatorcontrib>Zhang, Youjun</creatorcontrib><creatorcontrib>Liang, Pei</creatorcontrib><creatorcontrib>Wu, Qingjun</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Journal of agricultural and food chemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zheng, Xiaobin</au><au>Yuan, Jiangjiang</au><au>Wan, Yanran</au><au>Tang, Yingxi</au><au>Cao, Hongyi</au><au>Wang, Jing</au><au>Qian, Kanghua</au><au>Zhang, Ying</au><au>Chen, Sirui</au><au>Xu, Baoyun</au><au>Zhang, Youjun</au><au>Liang, Pei</au><au>Wu, Qingjun</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Dual Guardians of Immunity: FoRab10 and FoRab29 in Frankliniella occidentalis Confer Resistance to Tomato Spotted Wilt Orthotospovirus</atitle><jtitle>Journal of agricultural and food chemistry</jtitle><addtitle>J. Agric. Food Chem</addtitle><date>2024-07-31</date><risdate>2024</risdate><volume>72</volume><issue>30</issue><spage>16661</spage><epage>16673</epage><pages>16661-16673</pages><issn>0021-8561</issn><issn>1520-5118</issn><eissn>1520-5118</eissn><abstract>Rab GTPase is critical for autophagy processes and is implicated in insect immunity against viruses. In this study, we aimed to investigate the role of FoRabs in the autophagic regulation of antiviral defense against tomato spotted wilt orthotospovirus (TSWV) in Frankliniella occidentalis. Transcriptome analysis revealed the downregulation of FoRabs in viruliferous nymph and adults of F. occidentalis in response to TSWV infection. Manipulation of autophagy levels with 3-MA and Rapa treatments resulted in a 5- to 15-fold increase and a 38–64% decrease in viral titers, respectively. Additionally, interference with FoRab10 in nymphs and FoRab29 in adults led to a 20–90% downregulation of autophagy-related genes, a decrease in ATG8-II (an autophagy marker protein), and an increase in the TSWV titers by 1.5- to 2.5-fold and 1.3- to 2.0-fold, respectively. In addition, the leaf disk and the living plant methods revealed increased transmission rates of 20.8–41.6 and 68.3–88.3%, respectively. In conclusion, FoRab10 and FoRab29 play a role in the autophagic regulation of the antiviral defense in F. occidentalis nymphs and adults against TSWV, respectively. These findings offer insights into the intricate immune mechanisms functional in F. occidentalis against TSWV, suggesting potential targeted strategies for F. occidentalis and TSWV management.</abstract><cop>United States</cop><pub>American Chemical Society</pub><pmid>39021284</pmid><doi>10.1021/acs.jafc.4c03412</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0002-0344-5561</orcidid><orcidid>https://orcid.org/0000-0002-3083-8918</orcidid><orcidid>https://orcid.org/0000-0003-3508-6695</orcidid></addata></record> |
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| subjects | Agricultural and Environmental Chemistry Animals Autophagy Disease Resistance - genetics Disease Resistance - immunology Insect Proteins - genetics Insect Proteins - immunology Insect Proteins - metabolism Nymph - genetics Nymph - growth & development Nymph - immunology Nymph - virology Plant Diseases - genetics Plant Diseases - immunology Plant Diseases - virology rab GTP-Binding Proteins - genetics rab GTP-Binding Proteins - immunology rab GTP-Binding Proteins - metabolism Solanum lycopersicum - genetics Solanum lycopersicum - immunology Solanum lycopersicum - virology Thysanoptera - genetics Thysanoptera - immunology Thysanoptera - virology Tospovirus - immunology Tospovirus - physiology |
| title | Dual Guardians of Immunity: FoRab10 and FoRab29 in Frankliniella occidentalis Confer Resistance to Tomato Spotted Wilt Orthotospovirus |
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