The Papaver Self-Incompatibility Pollen S-Determinant, PrpS, Functions in Arabidopsis thaliana

Many angiosperms use specific interactions between pollen and pistil proteins as “self” recognition and/or rejection mechanisms to prevent self-fertilization. Self-incompatibility (SI) is encoded by a multiallelic S locus, comprising pollen and pistil S-determinants [1, 2]. In Papaver rhoeas, cognat...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Current biology 2012-01, Vol.22 (2), p.154-159
Hauptverfasser: de Graaf, Barend H.J., Vatovec, Sabina, Juárez-Díaz, Javier Andrés, Chai, Lijun, Kooblall, Kreepa, Wilkins, Katie A., Zou, Huawen, Forbes, Thomas, Franklin, F. Christopher H., Franklin-Tong, Vernonica E.
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 159
container_issue 2
container_start_page 154
container_title Current biology
container_volume 22
creator de Graaf, Barend H.J.
Vatovec, Sabina
Juárez-Díaz, Javier Andrés
Chai, Lijun
Kooblall, Kreepa
Wilkins, Katie A.
Zou, Huawen
Forbes, Thomas
Franklin, F. Christopher H.
Franklin-Tong, Vernonica E.
description Many angiosperms use specific interactions between pollen and pistil proteins as “self” recognition and/or rejection mechanisms to prevent self-fertilization. Self-incompatibility (SI) is encoded by a multiallelic S locus, comprising pollen and pistil S-determinants [1, 2]. In Papaver rhoeas, cognate pistil and pollen S-determinants, PrpS, a pollen-expressed transmembrane protein, and PrsS, a pistil-expressed secreted protein [3, 4], interact to trigger a Ca2+-dependent signaling network [5–10], resulting in inhibition of pollen tube growth, cytoskeletal alterations [11–13], and programmed cell death (PCD) [14, 15] in incompatible pollen. We introduced the PrpS gene into Arabidopsis thaliana, a self-compatible model plant. Exposing transgenic A. thaliana pollen to recombinant Papaver PrsS protein triggered remarkably similar responses to those observed in incompatible Papaver pollen: S-specific inhibition and hallmark features of Papaver SI [11–15]. Our findings demonstrate that Papaver PrpS is functional in a species with no SI system that diverged ∼140 million years ago [16]. This suggests that the Papaver SI system uses cellular targets that are, perhaps, common to all eudicots and that endogenous signaling components can be recruited to elicit a response that most likely never operated in this species. This will be of interest to biologists interested in the evolution of signaling networks in higher plants. ► PrpS, a Papaver SI determinant, functions in Arabidopsis thaliana pollen ► A “self” interaction with PrsS reveals Papaver SI hallmark features in A. thaliana ► The first evidence for transfamily functionality of an SI system (>140 my apart) ► Evidence of recruitment of signaling components for novel SI function
doi_str_mv 10.1016/j.cub.2011.12.006
format Article
fullrecord <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_3695568</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><els_id>S0960982211013790</els_id><sourcerecordid>918579686</sourcerecordid><originalsourceid>FETCH-LOGICAL-c474t-5e4752ced9b285bd473ada3fbe8d8094af0486301ce9d5cf2e3900a936b6a5783</originalsourceid><addsrcrecordid>eNp9kUFv1DAQhS0EosvCD-ACuXFpwtiJHVtISFWhUKkSK217xXKcSderxA52slL_PVltqeDCaQ7z5s3T-wh5S6GgQMXHfWHnpmBAaUFZASCekRWVtcqhqvhzsgIlIFeSsTPyKqU9AGVSiZfkjDEGijO1Ij9vd5htzGgOGLMt9l1-7W0YRjO5xvVuesg2oe_RZ9v8C04YB-eNn86zTRy359nV7O3kgk-Z89lFNI1rw5hcyqad6Z3x5jV50Zk-4ZvHuSZ3V19vL7_nNz--XV9e3OS2qqsp51jVnFlsVcMkb9qqLk1ryq5B2UpQlemgkqIEalG13HYMSwVgVCkaYXgtyzX5fPId52bA1qKfoun1GN1g4oMOxul_N97t9H046FIozsXR4MOjQQy_ZkyTHlyy2PfGY5iTVlTyWoklxJrQk9LGkFLE7ukLBX3Eovd6waKPWDRlesGy3Lz7O97TxR8Oi-D9SdCZoM19dEnfbRcHDgCl5Esfa_LppMClxoPDqJN16JfOXEQ76Ta4_wT4DUJJqGY</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>918579686</pqid></control><display><type>article</type><title>The Papaver Self-Incompatibility Pollen S-Determinant, PrpS, Functions in Arabidopsis thaliana</title><source>MEDLINE</source><source>Cell Press Free Archives</source><source>Elsevier ScienceDirect Journals</source><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><creator>de Graaf, Barend H.J. ; Vatovec, Sabina ; Juárez-Díaz, Javier Andrés ; Chai, Lijun ; Kooblall, Kreepa ; Wilkins, Katie A. ; Zou, Huawen ; Forbes, Thomas ; Franklin, F. Christopher H. ; Franklin-Tong, Vernonica E.</creator><creatorcontrib>de Graaf, Barend H.J. ; Vatovec, Sabina ; Juárez-Díaz, Javier Andrés ; Chai, Lijun ; Kooblall, Kreepa ; Wilkins, Katie A. ; Zou, Huawen ; Forbes, Thomas ; Franklin, F. Christopher H. ; Franklin-Tong, Vernonica E.</creatorcontrib><description>Many angiosperms use specific interactions between pollen and pistil proteins as “self” recognition and/or rejection mechanisms to prevent self-fertilization. Self-incompatibility (SI) is encoded by a multiallelic S locus, comprising pollen and pistil S-determinants [1, 2]. In Papaver rhoeas, cognate pistil and pollen S-determinants, PrpS, a pollen-expressed transmembrane protein, and PrsS, a pistil-expressed secreted protein [3, 4], interact to trigger a Ca2+-dependent signaling network [5–10], resulting in inhibition of pollen tube growth, cytoskeletal alterations [11–13], and programmed cell death (PCD) [14, 15] in incompatible pollen. We introduced the PrpS gene into Arabidopsis thaliana, a self-compatible model plant. Exposing transgenic A. thaliana pollen to recombinant Papaver PrsS protein triggered remarkably similar responses to those observed in incompatible Papaver pollen: S-specific inhibition and hallmark features of Papaver SI [11–15]. Our findings demonstrate that Papaver PrpS is functional in a species with no SI system that diverged ∼140 million years ago [16]. This suggests that the Papaver SI system uses cellular targets that are, perhaps, common to all eudicots and that endogenous signaling components can be recruited to elicit a response that most likely never operated in this species. This will be of interest to biologists interested in the evolution of signaling networks in higher plants. ► PrpS, a Papaver SI determinant, functions in Arabidopsis thaliana pollen ► A “self” interaction with PrsS reveals Papaver SI hallmark features in A. thaliana ► The first evidence for transfamily functionality of an SI system (&gt;140 my apart) ► Evidence of recruitment of signaling components for novel SI function</description><identifier>ISSN: 0960-9822</identifier><identifier>EISSN: 1879-0445</identifier><identifier>DOI: 10.1016/j.cub.2011.12.006</identifier><identifier>PMID: 22209529</identifier><language>eng</language><publisher>England: Elsevier Inc</publisher><subject>Actins - metabolism ; apoptosis ; Arabidopsis - physiology ; Arabidopsis thaliana ; biologists ; Caspase 3 - metabolism ; Cell Death ; cytoskeleton ; evolution ; genes ; genetically modified organisms ; loci ; Papaver - genetics ; Papaver rhoeas ; Peptide Hydrolases - metabolism ; pistil ; Plant Proteins - metabolism ; pollen ; Pollen - metabolism ; pollen tubes ; proteins ; Self-Incompatibility in Flowering Plants - genetics ; selfing</subject><ispartof>Current biology, 2012-01, Vol.22 (2), p.154-159</ispartof><rights>2012 Elsevier Ltd</rights><rights>Copyright © 2012 Elsevier Ltd. All rights reserved.</rights><rights>2012 ELL &amp; Excerpta Medica. 2012 Elsevier Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c474t-5e4752ced9b285bd473ada3fbe8d8094af0486301ce9d5cf2e3900a936b6a5783</citedby><cites>FETCH-LOGICAL-c474t-5e4752ced9b285bd473ada3fbe8d8094af0486301ce9d5cf2e3900a936b6a5783</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0960982211013790$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22209529$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>de Graaf, Barend H.J.</creatorcontrib><creatorcontrib>Vatovec, Sabina</creatorcontrib><creatorcontrib>Juárez-Díaz, Javier Andrés</creatorcontrib><creatorcontrib>Chai, Lijun</creatorcontrib><creatorcontrib>Kooblall, Kreepa</creatorcontrib><creatorcontrib>Wilkins, Katie A.</creatorcontrib><creatorcontrib>Zou, Huawen</creatorcontrib><creatorcontrib>Forbes, Thomas</creatorcontrib><creatorcontrib>Franklin, F. Christopher H.</creatorcontrib><creatorcontrib>Franklin-Tong, Vernonica E.</creatorcontrib><title>The Papaver Self-Incompatibility Pollen S-Determinant, PrpS, Functions in Arabidopsis thaliana</title><title>Current biology</title><addtitle>Curr Biol</addtitle><description>Many angiosperms use specific interactions between pollen and pistil proteins as “self” recognition and/or rejection mechanisms to prevent self-fertilization. Self-incompatibility (SI) is encoded by a multiallelic S locus, comprising pollen and pistil S-determinants [1, 2]. In Papaver rhoeas, cognate pistil and pollen S-determinants, PrpS, a pollen-expressed transmembrane protein, and PrsS, a pistil-expressed secreted protein [3, 4], interact to trigger a Ca2+-dependent signaling network [5–10], resulting in inhibition of pollen tube growth, cytoskeletal alterations [11–13], and programmed cell death (PCD) [14, 15] in incompatible pollen. We introduced the PrpS gene into Arabidopsis thaliana, a self-compatible model plant. Exposing transgenic A. thaliana pollen to recombinant Papaver PrsS protein triggered remarkably similar responses to those observed in incompatible Papaver pollen: S-specific inhibition and hallmark features of Papaver SI [11–15]. Our findings demonstrate that Papaver PrpS is functional in a species with no SI system that diverged ∼140 million years ago [16]. This suggests that the Papaver SI system uses cellular targets that are, perhaps, common to all eudicots and that endogenous signaling components can be recruited to elicit a response that most likely never operated in this species. This will be of interest to biologists interested in the evolution of signaling networks in higher plants. ► PrpS, a Papaver SI determinant, functions in Arabidopsis thaliana pollen ► A “self” interaction with PrsS reveals Papaver SI hallmark features in A. thaliana ► The first evidence for transfamily functionality of an SI system (&gt;140 my apart) ► Evidence of recruitment of signaling components for novel SI function</description><subject>Actins - metabolism</subject><subject>apoptosis</subject><subject>Arabidopsis - physiology</subject><subject>Arabidopsis thaliana</subject><subject>biologists</subject><subject>Caspase 3 - metabolism</subject><subject>Cell Death</subject><subject>cytoskeleton</subject><subject>evolution</subject><subject>genes</subject><subject>genetically modified organisms</subject><subject>loci</subject><subject>Papaver - genetics</subject><subject>Papaver rhoeas</subject><subject>Peptide Hydrolases - metabolism</subject><subject>pistil</subject><subject>Plant Proteins - metabolism</subject><subject>pollen</subject><subject>Pollen - metabolism</subject><subject>pollen tubes</subject><subject>proteins</subject><subject>Self-Incompatibility in Flowering Plants - genetics</subject><subject>selfing</subject><issn>0960-9822</issn><issn>1879-0445</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kUFv1DAQhS0EosvCD-ACuXFpwtiJHVtISFWhUKkSK217xXKcSderxA52slL_PVltqeDCaQ7z5s3T-wh5S6GgQMXHfWHnpmBAaUFZASCekRWVtcqhqvhzsgIlIFeSsTPyKqU9AGVSiZfkjDEGijO1Ij9vd5htzGgOGLMt9l1-7W0YRjO5xvVuesg2oe_RZ9v8C04YB-eNn86zTRy359nV7O3kgk-Z89lFNI1rw5hcyqad6Z3x5jV50Zk-4ZvHuSZ3V19vL7_nNz--XV9e3OS2qqsp51jVnFlsVcMkb9qqLk1ryq5B2UpQlemgkqIEalG13HYMSwVgVCkaYXgtyzX5fPId52bA1qKfoun1GN1g4oMOxul_N97t9H046FIozsXR4MOjQQy_ZkyTHlyy2PfGY5iTVlTyWoklxJrQk9LGkFLE7ukLBX3Eovd6waKPWDRlesGy3Lz7O97TxR8Oi-D9SdCZoM19dEnfbRcHDgCl5Esfa_LppMClxoPDqJN16JfOXEQ76Ta4_wT4DUJJqGY</recordid><startdate>20120124</startdate><enddate>20120124</enddate><creator>de Graaf, Barend H.J.</creator><creator>Vatovec, Sabina</creator><creator>Juárez-Díaz, Javier Andrés</creator><creator>Chai, Lijun</creator><creator>Kooblall, Kreepa</creator><creator>Wilkins, Katie A.</creator><creator>Zou, Huawen</creator><creator>Forbes, Thomas</creator><creator>Franklin, F. Christopher H.</creator><creator>Franklin-Tong, Vernonica E.</creator><general>Elsevier Inc</general><general>Cell Press</general><scope>6I.</scope><scope>AAFTH</scope><scope>FBQ</scope><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>5PM</scope></search><sort><creationdate>20120124</creationdate><title>The Papaver Self-Incompatibility Pollen S-Determinant, PrpS, Functions in Arabidopsis thaliana</title><author>de Graaf, Barend H.J. ; Vatovec, Sabina ; Juárez-Díaz, Javier Andrés ; Chai, Lijun ; Kooblall, Kreepa ; Wilkins, Katie A. ; Zou, Huawen ; Forbes, Thomas ; Franklin, F. Christopher H. ; Franklin-Tong, Vernonica E.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c474t-5e4752ced9b285bd473ada3fbe8d8094af0486301ce9d5cf2e3900a936b6a5783</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Actins - metabolism</topic><topic>apoptosis</topic><topic>Arabidopsis - physiology</topic><topic>Arabidopsis thaliana</topic><topic>biologists</topic><topic>Caspase 3 - metabolism</topic><topic>Cell Death</topic><topic>cytoskeleton</topic><topic>evolution</topic><topic>genes</topic><topic>genetically modified organisms</topic><topic>loci</topic><topic>Papaver - genetics</topic><topic>Papaver rhoeas</topic><topic>Peptide Hydrolases - metabolism</topic><topic>pistil</topic><topic>Plant Proteins - metabolism</topic><topic>pollen</topic><topic>Pollen - metabolism</topic><topic>pollen tubes</topic><topic>proteins</topic><topic>Self-Incompatibility in Flowering Plants - genetics</topic><topic>selfing</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>de Graaf, Barend H.J.</creatorcontrib><creatorcontrib>Vatovec, Sabina</creatorcontrib><creatorcontrib>Juárez-Díaz, Javier Andrés</creatorcontrib><creatorcontrib>Chai, Lijun</creatorcontrib><creatorcontrib>Kooblall, Kreepa</creatorcontrib><creatorcontrib>Wilkins, Katie A.</creatorcontrib><creatorcontrib>Zou, Huawen</creatorcontrib><creatorcontrib>Forbes, Thomas</creatorcontrib><creatorcontrib>Franklin, F. Christopher H.</creatorcontrib><creatorcontrib>Franklin-Tong, Vernonica E.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>AGRIS</collection><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>PubMed Central (Full Participant titles)</collection><jtitle>Current biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>de Graaf, Barend H.J.</au><au>Vatovec, Sabina</au><au>Juárez-Díaz, Javier Andrés</au><au>Chai, Lijun</au><au>Kooblall, Kreepa</au><au>Wilkins, Katie A.</au><au>Zou, Huawen</au><au>Forbes, Thomas</au><au>Franklin, F. Christopher H.</au><au>Franklin-Tong, Vernonica E.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The Papaver Self-Incompatibility Pollen S-Determinant, PrpS, Functions in Arabidopsis thaliana</atitle><jtitle>Current biology</jtitle><addtitle>Curr Biol</addtitle><date>2012-01-24</date><risdate>2012</risdate><volume>22</volume><issue>2</issue><spage>154</spage><epage>159</epage><pages>154-159</pages><issn>0960-9822</issn><eissn>1879-0445</eissn><abstract>Many angiosperms use specific interactions between pollen and pistil proteins as “self” recognition and/or rejection mechanisms to prevent self-fertilization. Self-incompatibility (SI) is encoded by a multiallelic S locus, comprising pollen and pistil S-determinants [1, 2]. In Papaver rhoeas, cognate pistil and pollen S-determinants, PrpS, a pollen-expressed transmembrane protein, and PrsS, a pistil-expressed secreted protein [3, 4], interact to trigger a Ca2+-dependent signaling network [5–10], resulting in inhibition of pollen tube growth, cytoskeletal alterations [11–13], and programmed cell death (PCD) [14, 15] in incompatible pollen. We introduced the PrpS gene into Arabidopsis thaliana, a self-compatible model plant. Exposing transgenic A. thaliana pollen to recombinant Papaver PrsS protein triggered remarkably similar responses to those observed in incompatible Papaver pollen: S-specific inhibition and hallmark features of Papaver SI [11–15]. Our findings demonstrate that Papaver PrpS is functional in a species with no SI system that diverged ∼140 million years ago [16]. This suggests that the Papaver SI system uses cellular targets that are, perhaps, common to all eudicots and that endogenous signaling components can be recruited to elicit a response that most likely never operated in this species. This will be of interest to biologists interested in the evolution of signaling networks in higher plants. ► PrpS, a Papaver SI determinant, functions in Arabidopsis thaliana pollen ► A “self” interaction with PrsS reveals Papaver SI hallmark features in A. thaliana ► The first evidence for transfamily functionality of an SI system (&gt;140 my apart) ► Evidence of recruitment of signaling components for novel SI function</abstract><cop>England</cop><pub>Elsevier Inc</pub><pmid>22209529</pmid><doi>10.1016/j.cub.2011.12.006</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 0960-9822
ispartof Current biology, 2012-01, Vol.22 (2), p.154-159
issn 0960-9822
1879-0445
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_3695568
source MEDLINE; Cell Press Free Archives; Elsevier ScienceDirect Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals
subjects Actins - metabolism
apoptosis
Arabidopsis - physiology
Arabidopsis thaliana
biologists
Caspase 3 - metabolism
Cell Death
cytoskeleton
evolution
genes
genetically modified organisms
loci
Papaver - genetics
Papaver rhoeas
Peptide Hydrolases - metabolism
pistil
Plant Proteins - metabolism
pollen
Pollen - metabolism
pollen tubes
proteins
Self-Incompatibility in Flowering Plants - genetics
selfing
title The Papaver Self-Incompatibility Pollen S-Determinant, PrpS, Functions in Arabidopsis thaliana
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-05T12%3A39%3A02IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=The%20Papaver%20Self-Incompatibility%20Pollen%20S-Determinant,%20PrpS,%20Functions%20in%20Arabidopsis%20thaliana&rft.jtitle=Current%20biology&rft.au=de%C2%A0Graaf,%20Barend%C2%A0H.J.&rft.date=2012-01-24&rft.volume=22&rft.issue=2&rft.spage=154&rft.epage=159&rft.pages=154-159&rft.issn=0960-9822&rft.eissn=1879-0445&rft_id=info:doi/10.1016/j.cub.2011.12.006&rft_dat=%3Cproquest_pubme%3E918579686%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=918579686&rft_id=info:pmid/22209529&rft_els_id=S0960982211013790&rfr_iscdi=true