The genetic basis of pollinator adaptation in a sexually deceptive orchid
In plants, pollinator adaptation is considered to be a major driving force for floral diversification and speciation. However, the genetic basis of pollinator adaptation is poorly understood. The orchid genus Ophrys mimics its pollinators' mating signals and is pollinated by male insects during...
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| creator | Xu, Shuqing Schlüter, Philipp M Grossniklaus, Ueli Schiestl, Florian P |
| description | In plants, pollinator adaptation is considered to be a major driving force for floral diversification and speciation. However, the genetic basis of pollinator adaptation is poorly understood. The orchid genus Ophrys mimics its pollinators' mating signals and is pollinated by male insects during mating attempts. In many species of this genus, chemical mimicry of the pollinators' pheromones, especially of alkenes with different double-bond positions, plays a key role for specific pollinator attraction. Thus, different alkenes produced in different species are probably a consequence of pollinator adaptation. In this study, we identify genes that are likely involved in alkene biosynthesis, encoding stearoyl-acyl carrier protein (ACP) desaturases (SAD), in three closely related Ophrys species, O. garganica, O. sphegodes, and O. exaltata. Combining floral odor and gene expression analyses, two SAD homologs (SAD1/2) showed significant association with the production of (Z)-9- and (Z)-12-alkenes that were abundant in O. garganica and O. sphegodes, supporting previous biochemical data. In contrast, two other newly identified homologs (SAD5/6) were significantly associated with (Z)-7-alkenes that were highly abundant only in O. exaltata. Both molecular evolutionary analyses and pollinator preference tests suggest that the alkenes associated with SAD1/2 and SAD5/6 are under pollinator-mediated divergent selection among species. The expression patterns of these genes in F₁ hybrids indicate that species-specific expression differences in SAD1/2 are likely due to cis-regulation, while changes in SAD5/6 are likely due to trans-regulation. Taken together, we report a genetic mechanism for pollinator-mediated divergent selection that drives adaptive changes in floral alkene biosynthesis involved in reproductive isolation among Ophrys species. |
| doi_str_mv | 10.1371/journal.pgen.1002889 |
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However, the genetic basis of pollinator adaptation is poorly understood. The orchid genus Ophrys mimics its pollinators' mating signals and is pollinated by male insects during mating attempts. In many species of this genus, chemical mimicry of the pollinators' pheromones, especially of alkenes with different double-bond positions, plays a key role for specific pollinator attraction. Thus, different alkenes produced in different species are probably a consequence of pollinator adaptation. In this study, we identify genes that are likely involved in alkene biosynthesis, encoding stearoyl-acyl carrier protein (ACP) desaturases (SAD), in three closely related Ophrys species, O. garganica, O. sphegodes, and O. exaltata. Combining floral odor and gene expression analyses, two SAD homologs (SAD1/2) showed significant association with the production of (Z)-9- and (Z)-12-alkenes that were abundant in O. garganica and O. sphegodes, supporting previous biochemical data. In contrast, two other newly identified homologs (SAD5/6) were significantly associated with (Z)-7-alkenes that were highly abundant only in O. exaltata. Both molecular evolutionary analyses and pollinator preference tests suggest that the alkenes associated with SAD1/2 and SAD5/6 are under pollinator-mediated divergent selection among species. The expression patterns of these genes in F₁ hybrids indicate that species-specific expression differences in SAD1/2 are likely due to cis-regulation, while changes in SAD5/6 are likely due to trans-regulation. Taken together, we report a genetic mechanism for pollinator-mediated divergent selection that drives adaptive changes in floral alkene biosynthesis involved in reproductive isolation among Ophrys species.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1002889</identifier><identifier>PMID: 22916031</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adaptation ; Adaptation, Physiological ; Alkenes - isolation & purification ; Animal reproduction ; Animals ; Behavior ; Biological Evolution ; Biology ; Biosynthesis ; Chemical ecology ; Colleges & universities ; Flowers - classification ; Flowers - physiology ; Gene Expression ; Genetic aspects ; Genetic engineering ; Hybridization, Genetic ; Insecta - physiology ; Isoenzymes - genetics ; Isoenzymes - metabolism ; Male ; Mixed Function Oxygenases - genetics ; Mixed Function Oxygenases - metabolism ; Molecular Mimicry ; Mutation ; Odorants ; Odors ; Orchidaceae - classification ; Orchidaceae - physiology ; Orchids ; Pheromones ; Phylogeny ; Physiological aspects ; Plant genetics ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plant reproduction ; Pollination ; Pollination - physiology ; Reproduction ; Reproductive Isolation ; Sex Attractants - biosynthesis ; Sex Attractants - genetics ; Sex Attractants - isolation & purification ; Sexual Behavior, Animal ; Species Specificity</subject><ispartof>PLoS genetics, 2012-08, Vol.8 (8), p.e1002889-e1002889</ispartof><rights>COPYRIGHT 2012 Public Library of Science</rights><rights>Xu 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: Xu S, Schlüter PM, Grossniklaus U, Schiestl FP (2012) The Genetic Basis of Pollinator Adaptation in a Sexually Deceptive Orchid. PLoS Genet 8(8): e1002889. doi:10.1371/journal.pgen.1002889</rights><rights>2012 Xu et al 2012 Xu et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c792t-971a19d9f42c347b2bc328de289a56e7506c5f520f5714a7fdcce52cbb09ba213</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3420943/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3420943/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2100,2926,23865,27923,27924,53790,53792,79371,79372</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22916031$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Schnable, Patrick S.</contributor><creatorcontrib>Xu, Shuqing</creatorcontrib><creatorcontrib>Schlüter, Philipp M</creatorcontrib><creatorcontrib>Grossniklaus, Ueli</creatorcontrib><creatorcontrib>Schiestl, Florian P</creatorcontrib><title>The genetic basis of pollinator adaptation in a sexually deceptive orchid</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>In plants, pollinator adaptation is considered to be a major driving force for floral diversification and speciation. However, the genetic basis of pollinator adaptation is poorly understood. The orchid genus Ophrys mimics its pollinators' mating signals and is pollinated by male insects during mating attempts. In many species of this genus, chemical mimicry of the pollinators' pheromones, especially of alkenes with different double-bond positions, plays a key role for specific pollinator attraction. Thus, different alkenes produced in different species are probably a consequence of pollinator adaptation. In this study, we identify genes that are likely involved in alkene biosynthesis, encoding stearoyl-acyl carrier protein (ACP) desaturases (SAD), in three closely related Ophrys species, O. garganica, O. sphegodes, and O. exaltata. Combining floral odor and gene expression analyses, two SAD homologs (SAD1/2) showed significant association with the production of (Z)-9- and (Z)-12-alkenes that were abundant in O. garganica and O. sphegodes, supporting previous biochemical data. In contrast, two other newly identified homologs (SAD5/6) were significantly associated with (Z)-7-alkenes that were highly abundant only in O. exaltata. Both molecular evolutionary analyses and pollinator preference tests suggest that the alkenes associated with SAD1/2 and SAD5/6 are under pollinator-mediated divergent selection among species. The expression patterns of these genes in F₁ hybrids indicate that species-specific expression differences in SAD1/2 are likely due to cis-regulation, while changes in SAD5/6 are likely due to trans-regulation. Taken together, we report a genetic mechanism for pollinator-mediated divergent selection that drives adaptive changes in floral alkene biosynthesis involved in reproductive isolation among Ophrys species.</description><subject>Adaptation</subject><subject>Adaptation, Physiological</subject><subject>Alkenes - isolation & purification</subject><subject>Animal reproduction</subject><subject>Animals</subject><subject>Behavior</subject><subject>Biological Evolution</subject><subject>Biology</subject><subject>Biosynthesis</subject><subject>Chemical ecology</subject><subject>Colleges & universities</subject><subject>Flowers - classification</subject><subject>Flowers - physiology</subject><subject>Gene Expression</subject><subject>Genetic aspects</subject><subject>Genetic engineering</subject><subject>Hybridization, Genetic</subject><subject>Insecta - physiology</subject><subject>Isoenzymes - genetics</subject><subject>Isoenzymes - metabolism</subject><subject>Male</subject><subject>Mixed Function Oxygenases - genetics</subject><subject>Mixed Function Oxygenases - metabolism</subject><subject>Molecular Mimicry</subject><subject>Mutation</subject><subject>Odorants</subject><subject>Odors</subject><subject>Orchidaceae - classification</subject><subject>Orchidaceae - physiology</subject><subject>Orchids</subject><subject>Pheromones</subject><subject>Phylogeny</subject><subject>Physiological aspects</subject><subject>Plant genetics</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plant reproduction</subject><subject>Pollination</subject><subject>Pollination - physiology</subject><subject>Reproduction</subject><subject>Reproductive Isolation</subject><subject>Sex Attractants - biosynthesis</subject><subject>Sex Attractants - genetics</subject><subject>Sex Attractants - isolation & purification</subject><subject>Sexual Behavior, Animal</subject><subject>Species Specificity</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</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>eNqVk01v1DAQhiMEoqXwDxBEQkJw2MWfSXxBqio-VqqoBIWrNXEmu1554zROqvbf47BptUE9gHywNX7mHc-MJ0leUrKkPKcftn7oGnDLdo3NkhLCikI9So6plHyRCyIeH5yPkmchbAnhslD50-SIMUUzwulxsrrcYBoVsLcmLSHYkPo6bb1ztoHedylU0PbQW9-ktkkhDXgzgHO3aYUG295eY-o7s7HV8-RJDS7gi2k_SX5-_nR59nVxfvFldXZ6vjC5Yv1C5RSoqlQtmOEiL1lpOCsqZIUCmWEuSWZkLRmpZU4F5HVlDEpmypKoEhjlJ8nrvW7rfNBTFYKmnHJJheQqEqs9UXnY6razO-hutQer_xh8t9bQxXwdallylRVZUXLMhIKiRFKJGJMZwoucYdT6OEUbyh1WBpu-AzcTnd80dqPX_lpzwYgSPAq8mwQ6fzVg6PXOBoPOQYN-iO-OTaFEFDyL6Ju_0Iezm6g1xARsU_sY14yi-pSTiGScjGGXD1BxVbizxjdY22ifObyfOUSmx5t-DUMIevXj-3-w3_6dvfg1Z98esBsE12-Cd8P4-8IcFHvQdD6EDuv7hlCix-m4q5wep0NP0xHdXh02897pbhz4b0H2B7I</recordid><startdate>20120801</startdate><enddate>20120801</enddate><creator>Xu, Shuqing</creator><creator>Schlüter, Philipp M</creator><creator>Grossniklaus, Ueli</creator><creator>Schiestl, Florian P</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>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</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>CCPQU</scope><scope>DWQXO</scope><scope>FR3</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>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20120801</creationdate><title>The genetic basis of pollinator adaptation in a sexually deceptive orchid</title><author>Xu, Shuqing ; Schlüter, Philipp M ; Grossniklaus, Ueli ; Schiestl, Florian P</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c792t-971a19d9f42c347b2bc328de289a56e7506c5f520f5714a7fdcce52cbb09ba213</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Adaptation</topic><topic>Adaptation, Physiological</topic><topic>Alkenes - isolation & purification</topic><topic>Animal reproduction</topic><topic>Animals</topic><topic>Behavior</topic><topic>Biological Evolution</topic><topic>Biology</topic><topic>Biosynthesis</topic><topic>Chemical ecology</topic><topic>Colleges & universities</topic><topic>Flowers - classification</topic><topic>Flowers - physiology</topic><topic>Gene Expression</topic><topic>Genetic aspects</topic><topic>Genetic engineering</topic><topic>Hybridization, Genetic</topic><topic>Insecta - physiology</topic><topic>Isoenzymes - genetics</topic><topic>Isoenzymes - metabolism</topic><topic>Male</topic><topic>Mixed Function Oxygenases - genetics</topic><topic>Mixed Function Oxygenases - metabolism</topic><topic>Molecular Mimicry</topic><topic>Mutation</topic><topic>Odorants</topic><topic>Odors</topic><topic>Orchidaceae - classification</topic><topic>Orchidaceae - physiology</topic><topic>Orchids</topic><topic>Pheromones</topic><topic>Phylogeny</topic><topic>Physiological aspects</topic><topic>Plant genetics</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plant reproduction</topic><topic>Pollination</topic><topic>Pollination - physiology</topic><topic>Reproduction</topic><topic>Reproductive Isolation</topic><topic>Sex Attractants - biosynthesis</topic><topic>Sex Attractants - genetics</topic><topic>Sex Attractants - isolation & purification</topic><topic>Sexual Behavior, Animal</topic><topic>Species Specificity</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Xu, Shuqing</creatorcontrib><creatorcontrib>Schlüter, Philipp M</creatorcontrib><creatorcontrib>Grossniklaus, Ueli</creatorcontrib><creatorcontrib>Schiestl, Florian P</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Xu, Shuqing</au><au>Schlüter, Philipp M</au><au>Grossniklaus, Ueli</au><au>Schiestl, Florian P</au><au>Schnable, Patrick S.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The genetic basis of pollinator adaptation in a sexually deceptive orchid</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2012-08-01</date><risdate>2012</risdate><volume>8</volume><issue>8</issue><spage>e1002889</spage><epage>e1002889</epage><pages>e1002889-e1002889</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>In plants, pollinator adaptation is considered to be a major driving force for floral diversification and speciation. However, the genetic basis of pollinator adaptation is poorly understood. The orchid genus Ophrys mimics its pollinators' mating signals and is pollinated by male insects during mating attempts. In many species of this genus, chemical mimicry of the pollinators' pheromones, especially of alkenes with different double-bond positions, plays a key role for specific pollinator attraction. Thus, different alkenes produced in different species are probably a consequence of pollinator adaptation. In this study, we identify genes that are likely involved in alkene biosynthesis, encoding stearoyl-acyl carrier protein (ACP) desaturases (SAD), in three closely related Ophrys species, O. garganica, O. sphegodes, and O. exaltata. Combining floral odor and gene expression analyses, two SAD homologs (SAD1/2) showed significant association with the production of (Z)-9- and (Z)-12-alkenes that were abundant in O. garganica and O. sphegodes, supporting previous biochemical data. In contrast, two other newly identified homologs (SAD5/6) were significantly associated with (Z)-7-alkenes that were highly abundant only in O. exaltata. Both molecular evolutionary analyses and pollinator preference tests suggest that the alkenes associated with SAD1/2 and SAD5/6 are under pollinator-mediated divergent selection among species. The expression patterns of these genes in F₁ hybrids indicate that species-specific expression differences in SAD1/2 are likely due to cis-regulation, while changes in SAD5/6 are likely due to trans-regulation. Taken together, we report a genetic mechanism for pollinator-mediated divergent selection that drives adaptive changes in floral alkene biosynthesis involved in reproductive isolation among Ophrys species.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>22916031</pmid><doi>10.1371/journal.pgen.1002889</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Adaptation Adaptation, Physiological Alkenes - isolation & purification Animal reproduction Animals Behavior Biological Evolution Biology Biosynthesis Chemical ecology Colleges & universities Flowers - classification Flowers - physiology Gene Expression Genetic aspects Genetic engineering Hybridization, Genetic Insecta - physiology Isoenzymes - genetics Isoenzymes - metabolism Male Mixed Function Oxygenases - genetics Mixed Function Oxygenases - metabolism Molecular Mimicry Mutation Odorants Odors Orchidaceae - classification Orchidaceae - physiology Orchids Pheromones Phylogeny Physiological aspects Plant genetics Plant Proteins - genetics Plant Proteins - metabolism Plant reproduction Pollination Pollination - physiology Reproduction Reproductive Isolation Sex Attractants - biosynthesis Sex Attractants - genetics Sex Attractants - isolation & purification Sexual Behavior, Animal Species Specificity |
| title | The genetic basis of pollinator adaptation in a sexually deceptive orchid |
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