Immune response and survival of Circulifer haematoceps to Spiroplasma citri infection requires expression of the gene hexamerin
Spiroplasma citri is a cell wall-less bacterium that infects plants. It is transmitted by the leafhopper Circulifer haematoceps, which hosts this bacterium in the haemocel and insect tissues. Bacterial factors involved in spiroplasma colonization of the insect host have been identified, but the immu...
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creator | Eliautout, Rémi Dubrana, Marie-Pierre Vincent-Monégat, Carole Vallier, Agnès Braquart-Varnier, Christine Poirié, Marylène Saillard, Colette Heddi, Abdelaziz Arricau-Bouvery, Nathalie |
description | Spiroplasma citri is a cell wall-less bacterium that infects plants. It is transmitted by the leafhopper Circulifer haematoceps, which hosts this bacterium in the haemocel and insect tissues. Bacterial factors involved in spiroplasma colonization of the insect host have been identified, but the immune response of the leafhopper to S. citri infection remains unknown. In this study, we showed that C. haematoceps activates both humoral and cellular immune responses when challenged with bacteria. When infected by S. citri, C. haematoceps displayed a specific immune response, evidenced by activation of phagocytosis and upregulation of a gene encoding the protein hexamerin. S. citri infection also resulted in decreased phenoloxidase-like activity. Inhibition of hexamerin by RNA interference resulted in a significant reduction in phenoloxidase-like activity and increased mortality of infected leafhoppers. Therefore, the gene hexamerin is involved in S. citri control by interfering with insect phenoloxidase activity.
•Spiroplasma citri induced a specific immune response compared to Escherichia coli and Micrococcus luteus.•Activation of phagocytosis is observed in Circulifer haematoceps after S. citri infection.•S. citri promotes a continuous phenoloxydase activity decrease in insect hemolymph.•We succeed in using RNA interference to inhibit the transcription of hexamerin gene.•Hexamerin is required for full PO activity and insect surviving to S. citri infection. |
doi_str_mv | 10.1016/j.dci.2015.08.007 |
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•Spiroplasma citri induced a specific immune response compared to Escherichia coli and Micrococcus luteus.•Activation of phagocytosis is observed in Circulifer haematoceps after S. citri infection.•S. citri promotes a continuous phenoloxydase activity decrease in insect hemolymph.•We succeed in using RNA interference to inhibit the transcription of hexamerin gene.•Hexamerin is required for full PO activity and insect surviving to S. citri infection.</description><identifier>ISSN: 0145-305X</identifier><identifier>EISSN: 1879-0089</identifier><identifier>DOI: 10.1016/j.dci.2015.08.007</identifier><identifier>PMID: 26279217</identifier><language>eng</language><publisher>United States: Elsevier Ltd</publisher><subject>Animals ; Biodiversity and Ecology ; Environmental Sciences ; Gene Knockdown Techniques ; Gram-Negative Bacterial Infections - immunology ; Hemiptera - genetics ; Hemiptera - immunology ; Hemiptera - microbiology ; Hemipteran innate immunity ; Hexamerin ; Immune cells ; Insect Proteins - biosynthesis ; Insect Proteins - immunology ; Insect Vectors - immunology ; Insect Vectors - microbiology ; Phenoloxidase activity ; Polymerase Chain Reaction ; RNAi ; Spiroplasma ; Spiroplasma citri - immunology</subject><ispartof>Developmental and comparative immunology, 2016-01, Vol.54 (1), p.7-19</ispartof><rights>2015 Elsevier Ltd</rights><rights>Copyright © 2015 Elsevier Ltd. All rights reserved.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c453t-49aea077c879069b7e7a898500c592e565cf1baa4c0f6152ac79bad01d4d360c3</citedby><cites>FETCH-LOGICAL-c453t-49aea077c879069b7e7a898500c592e565cf1baa4c0f6152ac79bad01d4d360c3</cites><orcidid>0000-0001-9505-4834 ; 0000-0001-6398-7832 ; 0000-0001-6377-5573 ; 0000-0002-3349-6925</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.dci.2015.08.007$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>230,315,781,785,886,3551,27929,27930,46000</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26279217$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01204859$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Eliautout, Rémi</creatorcontrib><creatorcontrib>Dubrana, Marie-Pierre</creatorcontrib><creatorcontrib>Vincent-Monégat, Carole</creatorcontrib><creatorcontrib>Vallier, Agnès</creatorcontrib><creatorcontrib>Braquart-Varnier, Christine</creatorcontrib><creatorcontrib>Poirié, Marylène</creatorcontrib><creatorcontrib>Saillard, Colette</creatorcontrib><creatorcontrib>Heddi, Abdelaziz</creatorcontrib><creatorcontrib>Arricau-Bouvery, Nathalie</creatorcontrib><title>Immune response and survival of Circulifer haematoceps to Spiroplasma citri infection requires expression of the gene hexamerin</title><title>Developmental and comparative immunology</title><addtitle>Dev Comp Immunol</addtitle><description>Spiroplasma citri is a cell wall-less bacterium that infects plants. It is transmitted by the leafhopper Circulifer haematoceps, which hosts this bacterium in the haemocel and insect tissues. Bacterial factors involved in spiroplasma colonization of the insect host have been identified, but the immune response of the leafhopper to S. citri infection remains unknown. In this study, we showed that C. haematoceps activates both humoral and cellular immune responses when challenged with bacteria. When infected by S. citri, C. haematoceps displayed a specific immune response, evidenced by activation of phagocytosis and upregulation of a gene encoding the protein hexamerin. S. citri infection also resulted in decreased phenoloxidase-like activity. Inhibition of hexamerin by RNA interference resulted in a significant reduction in phenoloxidase-like activity and increased mortality of infected leafhoppers. Therefore, the gene hexamerin is involved in S. citri control by interfering with insect phenoloxidase activity.
•Spiroplasma citri induced a specific immune response compared to Escherichia coli and Micrococcus luteus.•Activation of phagocytosis is observed in Circulifer haematoceps after S. citri infection.•S. citri promotes a continuous phenoloxydase activity decrease in insect hemolymph.•We succeed in using RNA interference to inhibit the transcription of hexamerin gene.•Hexamerin is required for full PO activity and insect surviving to S. citri infection.</description><subject>Animals</subject><subject>Biodiversity and Ecology</subject><subject>Environmental Sciences</subject><subject>Gene Knockdown Techniques</subject><subject>Gram-Negative Bacterial Infections - immunology</subject><subject>Hemiptera - genetics</subject><subject>Hemiptera - immunology</subject><subject>Hemiptera - microbiology</subject><subject>Hemipteran innate immunity</subject><subject>Hexamerin</subject><subject>Immune cells</subject><subject>Insect Proteins - biosynthesis</subject><subject>Insect Proteins - immunology</subject><subject>Insect Vectors - immunology</subject><subject>Insect Vectors - microbiology</subject><subject>Phenoloxidase activity</subject><subject>Polymerase Chain Reaction</subject><subject>RNAi</subject><subject>Spiroplasma</subject><subject>Spiroplasma citri - immunology</subject><issn>0145-305X</issn><issn>1879-0089</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kcFq3DAQhkVpaLZpH6CXomN7sDuyLcuip7CkTWChh6TQm5iVx10ttuVI9pKe-urRskmO0WVg-OYTMz9jnwTkAkT9bZ-31uUFCJlDkwOoN2wlGqUzgEa_ZSsQlcxKkH_O2fsY95BeI-AdOy_qQulCqBX7fzMMy0g8UJz8GInj2PK4hIM7YM99x9cu2KV3HQW-Qxpw9pamyGfPbycX_NRjHJBbNwfH3diRnZ0fk-5-ccnJ6WFKJR57STbviP-l9N2OHnCg4MYP7KzDPtLHp3rBfv-4ultfZ5tfP2_Wl5vMVrKcs0ojIShl03ZQ660ihY1uJICVuiBZS9uJLWJloauFLNAqvcUWRFu1ZQ22vGBfT94d9mYKbsDwz3h05vpyY449EAVUjdQHkdgvJ3YK_n6hOJvBRUt9jyP5JRqhCl3KshR1QsUJtcHHGKh7cQswx4zM3qSMzDEjA41JGaWZz0_6ZTtQ-zLxHEoCvp8ASgc5OAomWkejpTad1M6m9e4V_SMYVqOg</recordid><startdate>20160101</startdate><enddate>20160101</enddate><creator>Eliautout, Rémi</creator><creator>Dubrana, Marie-Pierre</creator><creator>Vincent-Monégat, Carole</creator><creator>Vallier, Agnès</creator><creator>Braquart-Varnier, Christine</creator><creator>Poirié, Marylène</creator><creator>Saillard, Colette</creator><creator>Heddi, Abdelaziz</creator><creator>Arricau-Bouvery, Nathalie</creator><general>Elsevier Ltd</general><general>Elsevier</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><scope>1XC</scope><orcidid>https://orcid.org/0000-0001-9505-4834</orcidid><orcidid>https://orcid.org/0000-0001-6398-7832</orcidid><orcidid>https://orcid.org/0000-0001-6377-5573</orcidid><orcidid>https://orcid.org/0000-0002-3349-6925</orcidid></search><sort><creationdate>20160101</creationdate><title>Immune response and survival of Circulifer haematoceps to Spiroplasma citri infection requires expression of the gene hexamerin</title><author>Eliautout, Rémi ; Dubrana, Marie-Pierre ; Vincent-Monégat, Carole ; Vallier, Agnès ; Braquart-Varnier, Christine ; Poirié, Marylène ; Saillard, Colette ; Heddi, Abdelaziz ; Arricau-Bouvery, Nathalie</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c453t-49aea077c879069b7e7a898500c592e565cf1baa4c0f6152ac79bad01d4d360c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Animals</topic><topic>Biodiversity and Ecology</topic><topic>Environmental Sciences</topic><topic>Gene Knockdown Techniques</topic><topic>Gram-Negative Bacterial Infections - immunology</topic><topic>Hemiptera - genetics</topic><topic>Hemiptera - immunology</topic><topic>Hemiptera - microbiology</topic><topic>Hemipteran innate immunity</topic><topic>Hexamerin</topic><topic>Immune cells</topic><topic>Insect Proteins - biosynthesis</topic><topic>Insect Proteins - immunology</topic><topic>Insect Vectors - immunology</topic><topic>Insect Vectors - microbiology</topic><topic>Phenoloxidase activity</topic><topic>Polymerase Chain Reaction</topic><topic>RNAi</topic><topic>Spiroplasma</topic><topic>Spiroplasma citri - immunology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Eliautout, Rémi</creatorcontrib><creatorcontrib>Dubrana, Marie-Pierre</creatorcontrib><creatorcontrib>Vincent-Monégat, Carole</creatorcontrib><creatorcontrib>Vallier, Agnès</creatorcontrib><creatorcontrib>Braquart-Varnier, Christine</creatorcontrib><creatorcontrib>Poirié, Marylène</creatorcontrib><creatorcontrib>Saillard, Colette</creatorcontrib><creatorcontrib>Heddi, Abdelaziz</creatorcontrib><creatorcontrib>Arricau-Bouvery, Nathalie</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><collection>Hyper Article en Ligne (HAL)</collection><jtitle>Developmental and comparative immunology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Eliautout, Rémi</au><au>Dubrana, Marie-Pierre</au><au>Vincent-Monégat, Carole</au><au>Vallier, Agnès</au><au>Braquart-Varnier, Christine</au><au>Poirié, Marylène</au><au>Saillard, Colette</au><au>Heddi, Abdelaziz</au><au>Arricau-Bouvery, Nathalie</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Immune response and survival of Circulifer haematoceps to Spiroplasma citri infection requires expression of the gene hexamerin</atitle><jtitle>Developmental and comparative immunology</jtitle><addtitle>Dev Comp Immunol</addtitle><date>2016-01-01</date><risdate>2016</risdate><volume>54</volume><issue>1</issue><spage>7</spage><epage>19</epage><pages>7-19</pages><issn>0145-305X</issn><eissn>1879-0089</eissn><abstract>Spiroplasma citri is a cell wall-less bacterium that infects plants. It is transmitted by the leafhopper Circulifer haematoceps, which hosts this bacterium in the haemocel and insect tissues. Bacterial factors involved in spiroplasma colonization of the insect host have been identified, but the immune response of the leafhopper to S. citri infection remains unknown. In this study, we showed that C. haematoceps activates both humoral and cellular immune responses when challenged with bacteria. When infected by S. citri, C. haematoceps displayed a specific immune response, evidenced by activation of phagocytosis and upregulation of a gene encoding the protein hexamerin. S. citri infection also resulted in decreased phenoloxidase-like activity. Inhibition of hexamerin by RNA interference resulted in a significant reduction in phenoloxidase-like activity and increased mortality of infected leafhoppers. Therefore, the gene hexamerin is involved in S. citri control by interfering with insect phenoloxidase activity.
•Spiroplasma citri induced a specific immune response compared to Escherichia coli and Micrococcus luteus.•Activation of phagocytosis is observed in Circulifer haematoceps after S. citri infection.•S. citri promotes a continuous phenoloxydase activity decrease in insect hemolymph.•We succeed in using RNA interference to inhibit the transcription of hexamerin gene.•Hexamerin is required for full PO activity and insect surviving to S. citri infection.</abstract><cop>United States</cop><pub>Elsevier Ltd</pub><pmid>26279217</pmid><doi>10.1016/j.dci.2015.08.007</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0001-9505-4834</orcidid><orcidid>https://orcid.org/0000-0001-6398-7832</orcidid><orcidid>https://orcid.org/0000-0001-6377-5573</orcidid><orcidid>https://orcid.org/0000-0002-3349-6925</orcidid></addata></record> |
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subjects | Animals Biodiversity and Ecology Environmental Sciences Gene Knockdown Techniques Gram-Negative Bacterial Infections - immunology Hemiptera - genetics Hemiptera - immunology Hemiptera - microbiology Hemipteran innate immunity Hexamerin Immune cells Insect Proteins - biosynthesis Insect Proteins - immunology Insect Vectors - immunology Insect Vectors - microbiology Phenoloxidase activity Polymerase Chain Reaction RNAi Spiroplasma Spiroplasma citri - immunology |
title | Immune response and survival of Circulifer haematoceps to Spiroplasma citri infection requires expression of the gene hexamerin |
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