The protein–protein interaction landscape of transcription factors during gynoecium development in Arabidopsis
Flowers are composed of organs whose identity is defined by the combinatorial activity of transcription factors (TFs). The interactions between MADS-box TFs and protein complex formation have been schematized in the floral quartet model of flower development. The gynoecium is the flower’s female rep...
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Veröffentlicht in: | Molecular plant 2023-01, Vol.16 (1), p.260-278 |
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creator | Herrera-Ubaldo, Humberto Campos, Sergio E. López-Gómez, Pablo Luna-García, Valentín Zúñiga-Mayo, Víctor M. Armas-Caballero, Gerardo E. González-Aguilera, Karla L. DeLuna, Alexander Marsch-Martínez, Nayelli Espinosa-Soto, Carlos de Folter, Stefan |
description | Flowers are composed of organs whose identity is defined by the combinatorial activity of transcription factors (TFs). The interactions between MADS-box TFs and protein complex formation have been schematized in the floral quartet model of flower development. The gynoecium is the flower’s female reproductive part, crucial for fruit and seed production and, hence, for reproductive success. After the establishment of carpel identity, many tissues arise to form a mature gynoecium. TFs have been described as regulators of gynoecium development, and some interactions and complexes have been identified. However, broad knowledge about the interactions among these TFs and their participation during development remains scarce. In this study, we used a systems biology approach to understand the formation of a complex reproductive unit—as the gynoecium—by mapping binary interactions between well-characterized TFs. We analyzed almost 4500 combinations and detected more than 250 protein–protein interactions (PPIs), resulting in a process-specific interaction map. Topological analyses suggest hidden functions and novel roles for many TFs. In addition, we observed a close relationship between TFs involved in auxin and cytokinin-signaling pathways and other TFs. Furthermore, we analyzed the network by combining PPI data, expression, and genetic data, which helped us to dissect it into several dynamic spatio-temporal subnetworks related to gynoecium development processes. Finally, we generated an extended PPI network that predicts new players in gynoecium development. Taken together, all these results serve as a valuable resource for the plant community.
Protein–protein interactions (PPIs) guide gynoecium development. This study identifies 263 unique PPIs among transcription factors, resulting in a process-specific interaction map. Several dynamic spatio-temporal subnetworks related to gynoecium development processes are also reported. |
doi_str_mv | 10.1016/j.molp.2022.09.004 |
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Protein–protein interactions (PPIs) guide gynoecium development. This study identifies 263 unique PPIs among transcription factors, resulting in a process-specific interaction map. Several dynamic spatio-temporal subnetworks related to gynoecium development processes are also reported.</description><identifier>ISSN: 1674-2052</identifier><identifier>EISSN: 1752-9867</identifier><identifier>DOI: 10.1016/j.molp.2022.09.004</identifier><identifier>PMID: 36088536</identifier><language>eng</language><publisher>England: Elsevier Inc</publisher><subject>Arabidopsis ; Arabidopsis - metabolism ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; auxins ; Cell Communication ; females ; flowering ; flowers ; Flowers - metabolism ; fruits ; Gene Expression Regulation, Plant ; gynoecium ; gynoecium development ; Indoleacetic Acids - metabolism ; interactome ; networks ; plant communities ; protein-protein interactions ; reproductive success ; topology ; transcription factors ; Transcription Factors - genetics ; Transcription Factors - metabolism</subject><ispartof>Molecular plant, 2023-01, Vol.16 (1), p.260-278</ispartof><rights>2022 The Author</rights><rights>Copyright © 2022 The Author. Published by Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c433t-65505f9af49fd282953f4d5160f677dddcb322273750bc5c56f7492b50824d453</citedby><cites>FETCH-LOGICAL-c433t-65505f9af49fd282953f4d5160f677dddcb322273750bc5c56f7492b50824d453</cites><orcidid>0000-0003-4363-7274</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36088536$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Herrera-Ubaldo, Humberto</creatorcontrib><creatorcontrib>Campos, Sergio E.</creatorcontrib><creatorcontrib>López-Gómez, Pablo</creatorcontrib><creatorcontrib>Luna-García, Valentín</creatorcontrib><creatorcontrib>Zúñiga-Mayo, Víctor M.</creatorcontrib><creatorcontrib>Armas-Caballero, Gerardo E.</creatorcontrib><creatorcontrib>González-Aguilera, Karla L.</creatorcontrib><creatorcontrib>DeLuna, Alexander</creatorcontrib><creatorcontrib>Marsch-Martínez, Nayelli</creatorcontrib><creatorcontrib>Espinosa-Soto, Carlos</creatorcontrib><creatorcontrib>de Folter, Stefan</creatorcontrib><title>The protein–protein interaction landscape of transcription factors during gynoecium development in Arabidopsis</title><title>Molecular plant</title><addtitle>Mol Plant</addtitle><description>Flowers are composed of organs whose identity is defined by the combinatorial activity of transcription factors (TFs). The interactions between MADS-box TFs and protein complex formation have been schematized in the floral quartet model of flower development. The gynoecium is the flower’s female reproductive part, crucial for fruit and seed production and, hence, for reproductive success. After the establishment of carpel identity, many tissues arise to form a mature gynoecium. TFs have been described as regulators of gynoecium development, and some interactions and complexes have been identified. However, broad knowledge about the interactions among these TFs and their participation during development remains scarce. In this study, we used a systems biology approach to understand the formation of a complex reproductive unit—as the gynoecium—by mapping binary interactions between well-characterized TFs. We analyzed almost 4500 combinations and detected more than 250 protein–protein interactions (PPIs), resulting in a process-specific interaction map. Topological analyses suggest hidden functions and novel roles for many TFs. In addition, we observed a close relationship between TFs involved in auxin and cytokinin-signaling pathways and other TFs. Furthermore, we analyzed the network by combining PPI data, expression, and genetic data, which helped us to dissect it into several dynamic spatio-temporal subnetworks related to gynoecium development processes. Finally, we generated an extended PPI network that predicts new players in gynoecium development. Taken together, all these results serve as a valuable resource for the plant community.
Protein–protein interactions (PPIs) guide gynoecium development. This study identifies 263 unique PPIs among transcription factors, resulting in a process-specific interaction map. Several dynamic spatio-temporal subnetworks related to gynoecium development processes are also reported.</description><subject>Arabidopsis</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>auxins</subject><subject>Cell Communication</subject><subject>females</subject><subject>flowering</subject><subject>flowers</subject><subject>Flowers - metabolism</subject><subject>fruits</subject><subject>Gene Expression Regulation, Plant</subject><subject>gynoecium</subject><subject>gynoecium development</subject><subject>Indoleacetic Acids - metabolism</subject><subject>interactome</subject><subject>networks</subject><subject>plant communities</subject><subject>protein-protein interactions</subject><subject>reproductive success</subject><subject>topology</subject><subject>transcription factors</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><issn>1674-2052</issn><issn>1752-9867</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkcFu1TAQRS1UREvLD7BAWXaTYI9jO5HYVBVQpEps2rWV2OPip8QOdlKpO_6hf8iX4Md7sESsfCWfudLMIeQtow2jTL7fNXOclgYoQEP7htL2BTljSkDdd1KdlCxVWwMVcEpe57yjVNJO8lfklJfQCS7PyHL3DaslxRV9-Pnj-ZgqH1ZMg1l9DNU0BJvNsGAVXbWmIWST_PL7yxUkplzZLfnwUD08hYjGb3Nl8RGnuMwY1tJVXaVh9DYu2ecL8tINU8Y3x_ec3H_6eHd9U99-_fzl-uq2Ni3nay2FoML1g2t7Z6GDXnDXWsEkdVIpa60ZOQAorgQdjTBCOtX2MAraQWtbwc_J5aG3rPR9w7zq2WeDU9kG45Y1KOCMAhPwHyiDTkAPrKBwQE2KOSd0ekl-HtKTZlTvpeid3kvReyma9rpIKUPvjv3bOKP9O_LHQgE-HAAsB3n0mHQ2HoNB6xOaVdvo_9X_C9YSoDs</recordid><startdate>20230102</startdate><enddate>20230102</enddate><creator>Herrera-Ubaldo, Humberto</creator><creator>Campos, Sergio E.</creator><creator>López-Gómez, Pablo</creator><creator>Luna-García, Valentín</creator><creator>Zúñiga-Mayo, Víctor M.</creator><creator>Armas-Caballero, Gerardo E.</creator><creator>González-Aguilera, Karla L.</creator><creator>DeLuna, Alexander</creator><creator>Marsch-Martínez, Nayelli</creator><creator>Espinosa-Soto, Carlos</creator><creator>de Folter, Stefan</creator><general>Elsevier Inc</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>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0003-4363-7274</orcidid></search><sort><creationdate>20230102</creationdate><title>The protein–protein interaction landscape of transcription factors during gynoecium development in Arabidopsis</title><author>Herrera-Ubaldo, Humberto ; Campos, Sergio E. ; López-Gómez, Pablo ; Luna-García, Valentín ; Zúñiga-Mayo, Víctor M. ; Armas-Caballero, Gerardo E. ; González-Aguilera, Karla L. ; DeLuna, Alexander ; Marsch-Martínez, Nayelli ; Espinosa-Soto, Carlos ; de Folter, Stefan</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c433t-65505f9af49fd282953f4d5160f677dddcb322273750bc5c56f7492b50824d453</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Arabidopsis</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>auxins</topic><topic>Cell Communication</topic><topic>females</topic><topic>flowering</topic><topic>flowers</topic><topic>Flowers - metabolism</topic><topic>fruits</topic><topic>Gene Expression Regulation, Plant</topic><topic>gynoecium</topic><topic>gynoecium development</topic><topic>Indoleacetic Acids - metabolism</topic><topic>interactome</topic><topic>networks</topic><topic>plant communities</topic><topic>protein-protein interactions</topic><topic>reproductive success</topic><topic>topology</topic><topic>transcription factors</topic><topic>Transcription Factors - genetics</topic><topic>Transcription Factors - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Herrera-Ubaldo, Humberto</creatorcontrib><creatorcontrib>Campos, Sergio E.</creatorcontrib><creatorcontrib>López-Gómez, Pablo</creatorcontrib><creatorcontrib>Luna-García, Valentín</creatorcontrib><creatorcontrib>Zúñiga-Mayo, Víctor M.</creatorcontrib><creatorcontrib>Armas-Caballero, Gerardo E.</creatorcontrib><creatorcontrib>González-Aguilera, Karla L.</creatorcontrib><creatorcontrib>DeLuna, Alexander</creatorcontrib><creatorcontrib>Marsch-Martínez, Nayelli</creatorcontrib><creatorcontrib>Espinosa-Soto, Carlos</creatorcontrib><creatorcontrib>de Folter, Stefan</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>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Molecular plant</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Herrera-Ubaldo, Humberto</au><au>Campos, Sergio E.</au><au>López-Gómez, Pablo</au><au>Luna-García, Valentín</au><au>Zúñiga-Mayo, Víctor M.</au><au>Armas-Caballero, Gerardo E.</au><au>González-Aguilera, Karla L.</au><au>DeLuna, Alexander</au><au>Marsch-Martínez, Nayelli</au><au>Espinosa-Soto, Carlos</au><au>de Folter, Stefan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The protein–protein interaction landscape of transcription factors during gynoecium development in Arabidopsis</atitle><jtitle>Molecular plant</jtitle><addtitle>Mol Plant</addtitle><date>2023-01-02</date><risdate>2023</risdate><volume>16</volume><issue>1</issue><spage>260</spage><epage>278</epage><pages>260-278</pages><issn>1674-2052</issn><eissn>1752-9867</eissn><abstract>Flowers are composed of organs whose identity is defined by the combinatorial activity of transcription factors (TFs). The interactions between MADS-box TFs and protein complex formation have been schematized in the floral quartet model of flower development. The gynoecium is the flower’s female reproductive part, crucial for fruit and seed production and, hence, for reproductive success. After the establishment of carpel identity, many tissues arise to form a mature gynoecium. TFs have been described as regulators of gynoecium development, and some interactions and complexes have been identified. However, broad knowledge about the interactions among these TFs and their participation during development remains scarce. In this study, we used a systems biology approach to understand the formation of a complex reproductive unit—as the gynoecium—by mapping binary interactions between well-characterized TFs. We analyzed almost 4500 combinations and detected more than 250 protein–protein interactions (PPIs), resulting in a process-specific interaction map. Topological analyses suggest hidden functions and novel roles for many TFs. In addition, we observed a close relationship between TFs involved in auxin and cytokinin-signaling pathways and other TFs. Furthermore, we analyzed the network by combining PPI data, expression, and genetic data, which helped us to dissect it into several dynamic spatio-temporal subnetworks related to gynoecium development processes. Finally, we generated an extended PPI network that predicts new players in gynoecium development. Taken together, all these results serve as a valuable resource for the plant community.
Protein–protein interactions (PPIs) guide gynoecium development. This study identifies 263 unique PPIs among transcription factors, resulting in a process-specific interaction map. Several dynamic spatio-temporal subnetworks related to gynoecium development processes are also reported.</abstract><cop>England</cop><pub>Elsevier Inc</pub><pmid>36088536</pmid><doi>10.1016/j.molp.2022.09.004</doi><tpages>19</tpages><orcidid>https://orcid.org/0000-0003-4363-7274</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Arabidopsis Arabidopsis - metabolism Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism auxins Cell Communication females flowering flowers Flowers - metabolism fruits Gene Expression Regulation, Plant gynoecium gynoecium development Indoleacetic Acids - metabolism interactome networks plant communities protein-protein interactions reproductive success topology transcription factors Transcription Factors - genetics Transcription Factors - metabolism |
title | The protein–protein interaction landscape of transcription factors during gynoecium development in Arabidopsis |
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