Chemosensory protein regulates the behavioural response of Frankliniella intonsa and Frankliniella occidentalis to tomato zonate spot virus-Infected pepper (Capsicum annuum)
Many herbivorous insects rely on plant volatiles to locate their host plants. Vector-borne viral infections induce changes in plant volatiles, which render infected plants more attractive to insect vectors. However, the detailed mechanisms underlying the olfactory responses of insect vectors induced...
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| creator | Li, Heng Chen, Yixin Lu, Chengcong Tian, Houjun Lin, Shuo Wang, Liang Linghu, Tingting Zheng, Xue Wei, Hui Fan, Xiaojing Chen, Yong |
| description | Many herbivorous insects rely on plant volatiles to locate their host plants. Vector-borne viral infections induce changes in plant volatiles, which render infected plants more attractive to insect vectors. However, the detailed mechanisms underlying the olfactory responses of insect vectors induced by the volatiles produced by virus-infected plants are poorly understood. Here, we show that volatiles emitted by pepper (Capsicum annuum) plants infected with tomato zonate spot virus (TZSV), particularly the volatile cis-3-hexenal, which is recognized by chemosensory protein 1 of the thrips Frankliniella intonsa (FintCSP1), are more attractive to F. intonsa than the volatiles emitted by non-infected pepper plants. FintCSP1 is highly abundant in the antenna of F. intonsa. Silencing of FintCSP1 significantly decreased electroantennogram responses of F. intonsa antennae to cis-3-hexenal and impaired thrips' responses to TZSV-infected pepper plants and cis-3-hexenal, as assessed using a Y-tube olfactometer. Three-dimensional model predictions indicated that FintCSP1 consists of seven α-helixes and two disulfide bridges. Molecular docking analysis suggested that cis-3-hexenal is positioned deep inside the binding pocket of FintCSP1 and binds to residues of the protein. We combined site-directed mutagenesis and fluorescence binding assays and identified three hydrophilic residues, Lys26, Thr28, and Glu67, of FintCSP1 as being critical for cis-3-hexenal binding. Furthermore, CSP of F. occidentalis (FoccCSP) is also a key olfactory protein involved in modulating the behaviour of F. occidentalis to TZSV-infected pepper. This study revealed the specific binding characteristics of CSPs to cis-3-hexenal and confirmed the general hypothesis that virus infections induce changes in host volatiles, which can be recognized by the olfactory proteins of the insect vector to enhance vector attraction and this may facilitate viral spread and transmission. |
| doi_str_mv | 10.1371/journal.ppat.1011380 |
| format | Article |
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Vector-borne viral infections induce changes in plant volatiles, which render infected plants more attractive to insect vectors. However, the detailed mechanisms underlying the olfactory responses of insect vectors induced by the volatiles produced by virus-infected plants are poorly understood. Here, we show that volatiles emitted by pepper (Capsicum annuum) plants infected with tomato zonate spot virus (TZSV), particularly the volatile cis-3-hexenal, which is recognized by chemosensory protein 1 of the thrips Frankliniella intonsa (FintCSP1), are more attractive to F. intonsa than the volatiles emitted by non-infected pepper plants. FintCSP1 is highly abundant in the antenna of F. intonsa. Silencing of FintCSP1 significantly decreased electroantennogram responses of F. intonsa antennae to cis-3-hexenal and impaired thrips' responses to TZSV-infected pepper plants and cis-3-hexenal, as assessed using a Y-tube olfactometer. Three-dimensional model predictions indicated that FintCSP1 consists of seven α-helixes and two disulfide bridges. Molecular docking analysis suggested that cis-3-hexenal is positioned deep inside the binding pocket of FintCSP1 and binds to residues of the protein. We combined site-directed mutagenesis and fluorescence binding assays and identified three hydrophilic residues, Lys26, Thr28, and Glu67, of FintCSP1 as being critical for cis-3-hexenal binding. Furthermore, CSP of F. occidentalis (FoccCSP) is also a key olfactory protein involved in modulating the behaviour of F. occidentalis to TZSV-infected pepper. This study revealed the specific binding characteristics of CSPs to cis-3-hexenal and confirmed the general hypothesis that virus infections induce changes in host volatiles, which can be recognized by the olfactory proteins of the insect vector to enhance vector attraction and this may facilitate viral spread and transmission.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1011380</identifier><identifier>PMID: 37155712</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Allelochemicals ; Analysis ; Animals ; Antennae ; Binding ; Biology and Life Sciences ; Capsicum ; Capsicum annuum ; Chemoreception ; Diseases ; Flowers & plants ; Fluorescence ; Frankliniella intonsa ; Genes ; Health aspects ; Hex-3-enal ; Host plants ; Infection ; Infections ; Influence ; Insects ; Ligands ; Medicine and Health Sciences ; Molecular docking ; Molecular Docking Simulation ; Odors ; Peppers ; Physical Sciences ; Plant Viruses ; Plant-pathogen relationships ; Protein binding ; Proteins ; Research and Analysis Methods ; Residues ; Signal transduction ; Site-directed mutagenesis ; Solanum lycopersicum ; Statistical significance ; Sweet peppers ; Three dimensional models ; Thrips ; Thysanoptera - physiology ; Tomatoes ; Vectors ; Vegetables ; Viral proteins ; Virus diseases ; Viruses ; VOCs ; Volatile organic compounds ; Volatiles ; Winter</subject><ispartof>PLoS pathogens, 2023-05, Vol.19 (5), p.e1011380-e1011380</ispartof><rights>Copyright: © 2023 Li et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2023 Public Library of Science</rights><rights>2023 Li et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2023 Li et al 2023 Li et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c662t-ac25f6dfb11a070f9353209598477df0f4cc79e33385c55ca6b82a6f5191bd5b3</citedby><cites>FETCH-LOGICAL-c662t-ac25f6dfb11a070f9353209598477df0f4cc79e33385c55ca6b82a6f5191bd5b3</cites><orcidid>0000-0002-3441-9155 ; 0000-0003-4110-2698</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10194981/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10194981/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37155712$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Carr, John P.</contributor><creatorcontrib>Li, Heng</creatorcontrib><creatorcontrib>Chen, Yixin</creatorcontrib><creatorcontrib>Lu, Chengcong</creatorcontrib><creatorcontrib>Tian, Houjun</creatorcontrib><creatorcontrib>Lin, Shuo</creatorcontrib><creatorcontrib>Wang, Liang</creatorcontrib><creatorcontrib>Linghu, Tingting</creatorcontrib><creatorcontrib>Zheng, Xue</creatorcontrib><creatorcontrib>Wei, Hui</creatorcontrib><creatorcontrib>Fan, Xiaojing</creatorcontrib><creatorcontrib>Chen, Yong</creatorcontrib><title>Chemosensory protein regulates the behavioural response of Frankliniella intonsa and Frankliniella occidentalis to tomato zonate spot virus-Infected pepper (Capsicum annuum)</title><title>PLoS pathogens</title><addtitle>PLoS Pathog</addtitle><description>Many herbivorous insects rely on plant volatiles to locate their host plants. Vector-borne viral infections induce changes in plant volatiles, which render infected plants more attractive to insect vectors. However, the detailed mechanisms underlying the olfactory responses of insect vectors induced by the volatiles produced by virus-infected plants are poorly understood. Here, we show that volatiles emitted by pepper (Capsicum annuum) plants infected with tomato zonate spot virus (TZSV), particularly the volatile cis-3-hexenal, which is recognized by chemosensory protein 1 of the thrips Frankliniella intonsa (FintCSP1), are more attractive to F. intonsa than the volatiles emitted by non-infected pepper plants. FintCSP1 is highly abundant in the antenna of F. intonsa. Silencing of FintCSP1 significantly decreased electroantennogram responses of F. intonsa antennae to cis-3-hexenal and impaired thrips' responses to TZSV-infected pepper plants and cis-3-hexenal, as assessed using a Y-tube olfactometer. Three-dimensional model predictions indicated that FintCSP1 consists of seven α-helixes and two disulfide bridges. Molecular docking analysis suggested that cis-3-hexenal is positioned deep inside the binding pocket of FintCSP1 and binds to residues of the protein. We combined site-directed mutagenesis and fluorescence binding assays and identified three hydrophilic residues, Lys26, Thr28, and Glu67, of FintCSP1 as being critical for cis-3-hexenal binding. Furthermore, CSP of F. occidentalis (FoccCSP) is also a key olfactory protein involved in modulating the behaviour of F. occidentalis to TZSV-infected pepper. This study revealed the specific binding characteristics of CSPs to cis-3-hexenal and confirmed the general hypothesis that virus infections induce changes in host volatiles, which can be recognized by the olfactory proteins of the insect vector to enhance vector attraction and this may facilitate viral spread and transmission.</description><subject>Allelochemicals</subject><subject>Analysis</subject><subject>Animals</subject><subject>Antennae</subject><subject>Binding</subject><subject>Biology and Life Sciences</subject><subject>Capsicum</subject><subject>Capsicum annuum</subject><subject>Chemoreception</subject><subject>Diseases</subject><subject>Flowers & plants</subject><subject>Fluorescence</subject><subject>Frankliniella intonsa</subject><subject>Genes</subject><subject>Health aspects</subject><subject>Hex-3-enal</subject><subject>Host plants</subject><subject>Infection</subject><subject>Infections</subject><subject>Influence</subject><subject>Insects</subject><subject>Ligands</subject><subject>Medicine and Health Sciences</subject><subject>Molecular docking</subject><subject>Molecular Docking Simulation</subject><subject>Odors</subject><subject>Peppers</subject><subject>Physical Sciences</subject><subject>Plant Viruses</subject><subject>Plant-pathogen relationships</subject><subject>Protein binding</subject><subject>Proteins</subject><subject>Research and Analysis Methods</subject><subject>Residues</subject><subject>Signal transduction</subject><subject>Site-directed mutagenesis</subject><subject>Solanum lycopersicum</subject><subject>Statistical significance</subject><subject>Sweet peppers</subject><subject>Three dimensional models</subject><subject>Thrips</subject><subject>Thysanoptera - physiology</subject><subject>Tomatoes</subject><subject>Vectors</subject><subject>Vegetables</subject><subject>Viral proteins</subject><subject>Virus diseases</subject><subject>Viruses</subject><subject>VOCs</subject><subject>Volatile organic compounds</subject><subject>Volatiles</subject><subject>Winter</subject><issn>1553-7374</issn><issn>1553-7366</issn><issn>1553-7374</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqVk89u1DAQxiMEoqXwBggicWkPu9hxbCcnVK0orFSBxJ-z5TiTXZfEDrazorwT78gsu626VS8olhx5fvNN5nMmy15SMqdM0rdXfgpO9_Nx1GlOCaWsIo-yY8o5m0kmy8d33o-yZzFeEVJSRsXT7AjzOZe0OM7-LNYw-Agu-nCdj8EnsC4PsJp6nSDmaQ15A2u9sVhO9xiJo3cRct_lF0G7H711Fvpe59YlDOhcu_ZexBtjW3BJ9xYFPa5B4_bbOyyRo17KNzZMcbZ0HZgEbT7COELITxd6jNZMA4q6aRrOnmdPOt1HeLHfT7LvF--_LT7OLj9_WC7OL2dGiCLNtCl4J9quoVQTSbqacVaQmtdVKWXbka40RtbAGKu44dxo0VSFFh2nNW1a3rCT7PVOd-x9VHunoyqqQlREECmRWO6I1usrNQY76HCtvLbq34EPK6VDsqYHZWopKWlEYaqmpIbXBZO803XDAKgoBWq921ebmgFag1ah1QeihxFn12rlNwpvvS7riqLC6V4h-J8TxKQGG83WfAd-2n44pVygASWib-6hD7e3p1YaO7Cu81jYbEXVueRUEI5_G1LzByh8Whis8Q46i-cHCWcHCcgk-JVWeopRLb9--Q_20yFb7lgTfIwBulvzKFHbablpUm2nRe2nBdNe3TX-NulmPNhfKZQT_g</recordid><startdate>20230501</startdate><enddate>20230501</enddate><creator>Li, Heng</creator><creator>Chen, Yixin</creator><creator>Lu, Chengcong</creator><creator>Tian, Houjun</creator><creator>Lin, Shuo</creator><creator>Wang, Liang</creator><creator>Linghu, Tingting</creator><creator>Zheng, Xue</creator><creator>Wei, Hui</creator><creator>Fan, Xiaojing</creator><creator>Chen, Yong</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QL</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-3441-9155</orcidid><orcidid>https://orcid.org/0000-0003-4110-2698</orcidid></search><sort><creationdate>20230501</creationdate><title>Chemosensory protein regulates the behavioural response of Frankliniella intonsa and Frankliniella occidentalis to tomato zonate spot virus-Infected pepper (Capsicum annuum)</title><author>Li, Heng ; Chen, Yixin ; Lu, Chengcong ; Tian, Houjun ; Lin, Shuo ; Wang, Liang ; Linghu, Tingting ; Zheng, Xue ; Wei, Hui ; Fan, Xiaojing ; Chen, Yong</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c662t-ac25f6dfb11a070f9353209598477df0f4cc79e33385c55ca6b82a6f5191bd5b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Allelochemicals</topic><topic>Analysis</topic><topic>Animals</topic><topic>Antennae</topic><topic>Binding</topic><topic>Biology and Life Sciences</topic><topic>Capsicum</topic><topic>Capsicum annuum</topic><topic>Chemoreception</topic><topic>Diseases</topic><topic>Flowers & plants</topic><topic>Fluorescence</topic><topic>Frankliniella intonsa</topic><topic>Genes</topic><topic>Health aspects</topic><topic>Hex-3-enal</topic><topic>Host plants</topic><topic>Infection</topic><topic>Infections</topic><topic>Influence</topic><topic>Insects</topic><topic>Ligands</topic><topic>Medicine and Health Sciences</topic><topic>Molecular docking</topic><topic>Molecular Docking Simulation</topic><topic>Odors</topic><topic>Peppers</topic><topic>Physical Sciences</topic><topic>Plant Viruses</topic><topic>Plant-pathogen relationships</topic><topic>Protein binding</topic><topic>Proteins</topic><topic>Research and Analysis Methods</topic><topic>Residues</topic><topic>Signal transduction</topic><topic>Site-directed mutagenesis</topic><topic>Solanum lycopersicum</topic><topic>Statistical significance</topic><topic>Sweet peppers</topic><topic>Three dimensional models</topic><topic>Thrips</topic><topic>Thysanoptera - 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Vector-borne viral infections induce changes in plant volatiles, which render infected plants more attractive to insect vectors. However, the detailed mechanisms underlying the olfactory responses of insect vectors induced by the volatiles produced by virus-infected plants are poorly understood. Here, we show that volatiles emitted by pepper (Capsicum annuum) plants infected with tomato zonate spot virus (TZSV), particularly the volatile cis-3-hexenal, which is recognized by chemosensory protein 1 of the thrips Frankliniella intonsa (FintCSP1), are more attractive to F. intonsa than the volatiles emitted by non-infected pepper plants. FintCSP1 is highly abundant in the antenna of F. intonsa. Silencing of FintCSP1 significantly decreased electroantennogram responses of F. intonsa antennae to cis-3-hexenal and impaired thrips' responses to TZSV-infected pepper plants and cis-3-hexenal, as assessed using a Y-tube olfactometer. Three-dimensional model predictions indicated that FintCSP1 consists of seven α-helixes and two disulfide bridges. Molecular docking analysis suggested that cis-3-hexenal is positioned deep inside the binding pocket of FintCSP1 and binds to residues of the protein. We combined site-directed mutagenesis and fluorescence binding assays and identified three hydrophilic residues, Lys26, Thr28, and Glu67, of FintCSP1 as being critical for cis-3-hexenal binding. Furthermore, CSP of F. occidentalis (FoccCSP) is also a key olfactory protein involved in modulating the behaviour of F. occidentalis to TZSV-infected pepper. This study revealed the specific binding characteristics of CSPs to cis-3-hexenal and confirmed the general hypothesis that virus infections induce changes in host volatiles, which can be recognized by the olfactory proteins of the insect vector to enhance vector attraction and this may facilitate viral spread and transmission.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>37155712</pmid><doi>10.1371/journal.ppat.1011380</doi><tpages>e1011380</tpages><orcidid>https://orcid.org/0000-0002-3441-9155</orcidid><orcidid>https://orcid.org/0000-0003-4110-2698</orcidid><oa>free_for_read</oa></addata></record> |
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| recordid | cdi_plos_journals_2826806077 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central Open Access; Public Library of Science (PLoS); PubMed Central |
| subjects | Allelochemicals Analysis Animals Antennae Binding Biology and Life Sciences Capsicum Capsicum annuum Chemoreception Diseases Flowers & plants Fluorescence Frankliniella intonsa Genes Health aspects Hex-3-enal Host plants Infection Infections Influence Insects Ligands Medicine and Health Sciences Molecular docking Molecular Docking Simulation Odors Peppers Physical Sciences Plant Viruses Plant-pathogen relationships Protein binding Proteins Research and Analysis Methods Residues Signal transduction Site-directed mutagenesis Solanum lycopersicum Statistical significance Sweet peppers Three dimensional models Thrips Thysanoptera - physiology Tomatoes Vectors Vegetables Viral proteins Virus diseases Viruses VOCs Volatile organic compounds Volatiles Winter |
| title | Chemosensory protein regulates the behavioural response of Frankliniella intonsa and Frankliniella occidentalis to tomato zonate spot virus-Infected pepper (Capsicum annuum) |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-21T03%3A08%3A38IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Chemosensory%20protein%20regulates%20the%20behavioural%20response%20of%20Frankliniella%20intonsa%20and%20Frankliniella%20occidentalis%20to%20tomato%20zonate%20spot%20virus-Infected%20pepper%20(Capsicum%20annuum)&rft.jtitle=PLoS%20pathogens&rft.au=Li,%20Heng&rft.date=2023-05-01&rft.volume=19&rft.issue=5&rft.spage=e1011380&rft.epage=e1011380&rft.pages=e1011380-e1011380&rft.issn=1553-7374&rft.eissn=1553-7374&rft_id=info:doi/10.1371/journal.ppat.1011380&rft_dat=%3Cgale_plos_%3EA751605380%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2826806077&rft_id=info:pmid/37155712&rft_galeid=A751605380&rft_doaj_id=oai_doaj_org_article_c97710b62c8b41c592375fa9b3ee1646&rfr_iscdi=true |