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Genetic Basis of Differential Heat Resistance between Two Species of Congeneric Freshwater Snails: Insights from Quantitative Proteomics and Base Substitution Rate Analysis
We compared the heat tolerance, proteomic responses to heat stress, and adaptive sequence divergence in the invasive snail Pomacea canaliculata and its noninvasive congener Pomacea diffusa. The LT 50 of P. canaliculata was significantly higher than that of P. diffusa. More than 3350 proteins were id...
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Published in: | Journal of proteome research 2015-10, Vol.14 (10), p.4296-4308 |
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description | We compared the heat tolerance, proteomic responses to heat stress, and adaptive sequence divergence in the invasive snail Pomacea canaliculata and its noninvasive congener Pomacea diffusa. The LT 50 of P. canaliculata was significantly higher than that of P. diffusa. More than 3350 proteins were identified from the hepatopancreas of the snails exposed to acute and chronic thermal stress using iTRAQ-coupled mass spectrometry. Acute exposure (3 h exposure at 37 °C with 25 °C as control) resulted in similar numbers (27 in P. canaliculata and 23 in P. diffusa) of differentially expressed proteins in the two species. Chronic exposure (3 weeks of exposure at 35 °C with 25 °C as control) caused differential expression of more proteins (58 in P. canaliculata and 118 in P. diffusa), with many of them related to restoration of damaged molecules, ubiquitinating dysfunctional molecules, and utilization of energy reserves in both species; but only in P. diffusa was there a shift from carbohydrate to lipid catabolism. Analysis of orthologous genes encoding the differentially expressed proteins revealed two genes having clear evidence of positive selection (Ka/Ks > 1) and seven candidates for more detailed analysis of positive selection (Ka/Ks between 0.5 and 1). These nine genes are related to energy metabolism, cellular oxidative homeostasis, signaling, and binding processes. Overall, the proteomic and base substitution rate analyses indicate genetic basis of differential resistance to heat stress between the two species, and such differences could affect their further range expansion in a warming climate. |
doi_str_mv | 10.1021/acs.jproteome.5b00462 |
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C ; Qiu, Jian-Wen</creator><creatorcontrib>Mu, Huawei ; Sun, Jin ; Fang, Ling ; Luan, Tiangang ; Williams, Gray A ; Cheung, Siu Gin ; Wong, Chris K. C ; Qiu, Jian-Wen</creatorcontrib><description>We compared the heat tolerance, proteomic responses to heat stress, and adaptive sequence divergence in the invasive snail Pomacea canaliculata and its noninvasive congener Pomacea diffusa. The LT 50 of P. canaliculata was significantly higher than that of P. diffusa. More than 3350 proteins were identified from the hepatopancreas of the snails exposed to acute and chronic thermal stress using iTRAQ-coupled mass spectrometry. Acute exposure (3 h exposure at 37 °C with 25 °C as control) resulted in similar numbers (27 in P. canaliculata and 23 in P. diffusa) of differentially expressed proteins in the two species. Chronic exposure (3 weeks of exposure at 35 °C with 25 °C as control) caused differential expression of more proteins (58 in P. canaliculata and 118 in P. diffusa), with many of them related to restoration of damaged molecules, ubiquitinating dysfunctional molecules, and utilization of energy reserves in both species; but only in P. diffusa was there a shift from carbohydrate to lipid catabolism. Analysis of orthologous genes encoding the differentially expressed proteins revealed two genes having clear evidence of positive selection (Ka/Ks > 1) and seven candidates for more detailed analysis of positive selection (Ka/Ks between 0.5 and 1). These nine genes are related to energy metabolism, cellular oxidative homeostasis, signaling, and binding processes. Overall, the proteomic and base substitution rate analyses indicate genetic basis of differential resistance to heat stress between the two species, and such differences could affect their further range expansion in a warming climate.</description><identifier>ISSN: 1535-3893</identifier><identifier>EISSN: 1535-3907</identifier><identifier>DOI: 10.1021/acs.jproteome.5b00462</identifier><identifier>PMID: 26290311</identifier><language>eng</language><publisher>United States: American Chemical Society</publisher><subject>Adaptation, Physiological - genetics ; Animals ; Carbohydrate Metabolism - genetics ; Chromatography, Liquid ; Energy Metabolism - genetics ; Fresh Water ; Gene Expression Profiling ; Gene Expression Regulation ; Hepatopancreas - chemistry ; Hepatopancreas - metabolism ; Hot Temperature ; Lipid Metabolism - genetics ; Molecular Sequence Annotation ; Mutation ; Peptides - analysis ; Proteolysis ; Proteome - genetics ; Proteome - isolation & purification ; Proteome - metabolism ; Snails - chemistry ; Snails - genetics ; Snails - metabolism ; Species Specificity ; Staining and Labeling ; Stress, Physiological - genetics ; Synteny ; Tandem Mass Spectrometry ; Trypsin - chemistry</subject><ispartof>Journal of proteome research, 2015-10, Vol.14 (10), p.4296-4308</ispartof><rights>Copyright © 2015 American Chemical Society</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-a351t-62dce7c8b5e3c0896cde58bbc6304fc58e49d1b1702e004ff8d69933106d1eda3</citedby><cites>FETCH-LOGICAL-a351t-62dce7c8b5e3c0896cde58bbc6304fc58e49d1b1702e004ff8d69933106d1eda3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26290311$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Mu, Huawei</creatorcontrib><creatorcontrib>Sun, Jin</creatorcontrib><creatorcontrib>Fang, Ling</creatorcontrib><creatorcontrib>Luan, Tiangang</creatorcontrib><creatorcontrib>Williams, Gray A</creatorcontrib><creatorcontrib>Cheung, Siu Gin</creatorcontrib><creatorcontrib>Wong, Chris K. C</creatorcontrib><creatorcontrib>Qiu, Jian-Wen</creatorcontrib><title>Genetic Basis of Differential Heat Resistance between Two Species of Congeneric Freshwater Snails: Insights from Quantitative Proteomics and Base Substitution Rate Analysis</title><title>Journal of proteome research</title><addtitle>J. Proteome Res</addtitle><description>We compared the heat tolerance, proteomic responses to heat stress, and adaptive sequence divergence in the invasive snail Pomacea canaliculata and its noninvasive congener Pomacea diffusa. The LT 50 of P. canaliculata was significantly higher than that of P. diffusa. More than 3350 proteins were identified from the hepatopancreas of the snails exposed to acute and chronic thermal stress using iTRAQ-coupled mass spectrometry. Acute exposure (3 h exposure at 37 °C with 25 °C as control) resulted in similar numbers (27 in P. canaliculata and 23 in P. diffusa) of differentially expressed proteins in the two species. Chronic exposure (3 weeks of exposure at 35 °C with 25 °C as control) caused differential expression of more proteins (58 in P. canaliculata and 118 in P. diffusa), with many of them related to restoration of damaged molecules, ubiquitinating dysfunctional molecules, and utilization of energy reserves in both species; but only in P. diffusa was there a shift from carbohydrate to lipid catabolism. Analysis of orthologous genes encoding the differentially expressed proteins revealed two genes having clear evidence of positive selection (Ka/Ks > 1) and seven candidates for more detailed analysis of positive selection (Ka/Ks between 0.5 and 1). These nine genes are related to energy metabolism, cellular oxidative homeostasis, signaling, and binding processes. Overall, the proteomic and base substitution rate analyses indicate genetic basis of differential resistance to heat stress between the two species, and such differences could affect their further range expansion in a warming climate.</description><subject>Adaptation, Physiological - genetics</subject><subject>Animals</subject><subject>Carbohydrate Metabolism - genetics</subject><subject>Chromatography, Liquid</subject><subject>Energy Metabolism - genetics</subject><subject>Fresh Water</subject><subject>Gene Expression Profiling</subject><subject>Gene Expression Regulation</subject><subject>Hepatopancreas - chemistry</subject><subject>Hepatopancreas - metabolism</subject><subject>Hot Temperature</subject><subject>Lipid Metabolism - genetics</subject><subject>Molecular Sequence Annotation</subject><subject>Mutation</subject><subject>Peptides - analysis</subject><subject>Proteolysis</subject><subject>Proteome - genetics</subject><subject>Proteome - isolation & purification</subject><subject>Proteome - metabolism</subject><subject>Snails - chemistry</subject><subject>Snails - genetics</subject><subject>Snails - metabolism</subject><subject>Species Specificity</subject><subject>Staining and Labeling</subject><subject>Stress, Physiological - genetics</subject><subject>Synteny</subject><subject>Tandem Mass Spectrometry</subject><subject>Trypsin - chemistry</subject><issn>1535-3893</issn><issn>1535-3907</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><recordid>eNqFkctuFDEQRa0IlBf5BFAt2cxgt8f9YBcG8pAiAZlk3XK7y4mjbntwuRnln_jIOJlJtqxsyfceV93L2EfB54IX4os2NH9Yx5AwjDhXHeeLsthjh0JJNZMNr9693utGHrAjogfOhaq43GcHRVk0XApxyP6do8fkDHzT5AiChe_OWozok9MDXKBOcI35KWlvEDpMG0QPN5sAqzUahy-eZfB3mRMz5ywi3W90wggrr91AX-HSk7u7TwQ2hhF-Tzqzk07uL8Kv7QLOEGjfPw-BsJo6yoIpueDhOpPg1OvhMc_wgb23eiA82Z3H7Pbsx83yYnb18_xyeXo101KJNCuL3mBl6k6hNLxuStOjqrvOlJIvrFE1LppedKLiBebYrK37smmkFLzsBfZaHrPPW27O98-ElNrRkcFh0B7DRK2oRN1kteJZqrZSEwNRRNuuoxt1fGwFb5-LanNR7VtR7a6o7Pu0-2LqRuzfXK_NZIHYCl78YYo5A_oP9AmMM6fi</recordid><startdate>20151002</startdate><enddate>20151002</enddate><creator>Mu, Huawei</creator><creator>Sun, Jin</creator><creator>Fang, Ling</creator><creator>Luan, Tiangang</creator><creator>Williams, Gray A</creator><creator>Cheung, Siu Gin</creator><creator>Wong, Chris K. 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C ; Qiu, Jian-Wen</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a351t-62dce7c8b5e3c0896cde58bbc6304fc58e49d1b1702e004ff8d69933106d1eda3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Adaptation, Physiological - genetics</topic><topic>Animals</topic><topic>Carbohydrate Metabolism - genetics</topic><topic>Chromatography, Liquid</topic><topic>Energy Metabolism - genetics</topic><topic>Fresh Water</topic><topic>Gene Expression Profiling</topic><topic>Gene Expression Regulation</topic><topic>Hepatopancreas - chemistry</topic><topic>Hepatopancreas - metabolism</topic><topic>Hot Temperature</topic><topic>Lipid Metabolism - genetics</topic><topic>Molecular Sequence Annotation</topic><topic>Mutation</topic><topic>Peptides - analysis</topic><topic>Proteolysis</topic><topic>Proteome - genetics</topic><topic>Proteome - isolation & purification</topic><topic>Proteome - metabolism</topic><topic>Snails - chemistry</topic><topic>Snails - genetics</topic><topic>Snails - metabolism</topic><topic>Species Specificity</topic><topic>Staining and Labeling</topic><topic>Stress, Physiological - genetics</topic><topic>Synteny</topic><topic>Tandem Mass Spectrometry</topic><topic>Trypsin - chemistry</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Mu, Huawei</creatorcontrib><creatorcontrib>Sun, Jin</creatorcontrib><creatorcontrib>Fang, Ling</creatorcontrib><creatorcontrib>Luan, Tiangang</creatorcontrib><creatorcontrib>Williams, Gray A</creatorcontrib><creatorcontrib>Cheung, Siu Gin</creatorcontrib><creatorcontrib>Wong, Chris K. C</creatorcontrib><creatorcontrib>Qiu, Jian-Wen</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 proteome research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Mu, Huawei</au><au>Sun, Jin</au><au>Fang, Ling</au><au>Luan, Tiangang</au><au>Williams, Gray A</au><au>Cheung, Siu Gin</au><au>Wong, Chris K. C</au><au>Qiu, Jian-Wen</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genetic Basis of Differential Heat Resistance between Two Species of Congeneric Freshwater Snails: Insights from Quantitative Proteomics and Base Substitution Rate Analysis</atitle><jtitle>Journal of proteome research</jtitle><addtitle>J. Proteome Res</addtitle><date>2015-10-02</date><risdate>2015</risdate><volume>14</volume><issue>10</issue><spage>4296</spage><epage>4308</epage><pages>4296-4308</pages><issn>1535-3893</issn><eissn>1535-3907</eissn><abstract>We compared the heat tolerance, proteomic responses to heat stress, and adaptive sequence divergence in the invasive snail Pomacea canaliculata and its noninvasive congener Pomacea diffusa. The LT 50 of P. canaliculata was significantly higher than that of P. diffusa. More than 3350 proteins were identified from the hepatopancreas of the snails exposed to acute and chronic thermal stress using iTRAQ-coupled mass spectrometry. Acute exposure (3 h exposure at 37 °C with 25 °C as control) resulted in similar numbers (27 in P. canaliculata and 23 in P. diffusa) of differentially expressed proteins in the two species. Chronic exposure (3 weeks of exposure at 35 °C with 25 °C as control) caused differential expression of more proteins (58 in P. canaliculata and 118 in P. diffusa), with many of them related to restoration of damaged molecules, ubiquitinating dysfunctional molecules, and utilization of energy reserves in both species; but only in P. diffusa was there a shift from carbohydrate to lipid catabolism. Analysis of orthologous genes encoding the differentially expressed proteins revealed two genes having clear evidence of positive selection (Ka/Ks > 1) and seven candidates for more detailed analysis of positive selection (Ka/Ks between 0.5 and 1). These nine genes are related to energy metabolism, cellular oxidative homeostasis, signaling, and binding processes. Overall, the proteomic and base substitution rate analyses indicate genetic basis of differential resistance to heat stress between the two species, and such differences could affect their further range expansion in a warming climate.</abstract><cop>United States</cop><pub>American Chemical Society</pub><pmid>26290311</pmid><doi>10.1021/acs.jproteome.5b00462</doi><tpages>13</tpages></addata></record> |
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subjects | Adaptation, Physiological - genetics Animals Carbohydrate Metabolism - genetics Chromatography, Liquid Energy Metabolism - genetics Fresh Water Gene Expression Profiling Gene Expression Regulation Hepatopancreas - chemistry Hepatopancreas - metabolism Hot Temperature Lipid Metabolism - genetics Molecular Sequence Annotation Mutation Peptides - analysis Proteolysis Proteome - genetics Proteome - isolation & purification Proteome - metabolism Snails - chemistry Snails - genetics Snails - metabolism Species Specificity Staining and Labeling Stress, Physiological - genetics Synteny Tandem Mass Spectrometry Trypsin - chemistry |
title | Genetic Basis of Differential Heat Resistance between Two Species of Congeneric Freshwater Snails: Insights from Quantitative Proteomics and Base Substitution Rate Analysis |
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