TERMINAL FLOWER‐1/CENTRORADIALIS inhibits tuberisation via protein interaction with the tuberigen activation complex
SUMMARY Potato tuber formation is a secondary developmental programme by which cells in the subapical stolon region divide and radially expand to further differentiate into starch‐accumulating parenchyma. Although some details of the molecular pathway that signals tuberisation are known, important g...
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creator | Zhang, Xing Campbell, Raymond Ducreux, Laurence J. M. Morris, Jennifer Hedley, Pete E. Mellado‐Ortega, Elena Roberts, Alison G. Stephens, Jennifer Bryan, Glenn J. Torrance, Lesley Chapman, Sean N. Prat, Salomé Taylor, Mark A. |
description | SUMMARY
Potato tuber formation is a secondary developmental programme by which cells in the subapical stolon region divide and radially expand to further differentiate into starch‐accumulating parenchyma. Although some details of the molecular pathway that signals tuberisation are known, important gaps in our knowledge persist. Here, the role of a member of the TERMINAL FLOWER 1/CENTRORADIALIS gene family (termed StCEN) in the negative control of tuberisation is demonstrated for what is thought to be the first time. It is shown that reduced expression of StCEN accelerates tuber formation whereas transgenic lines overexpressing this gene display delayed tuberisation and reduced tuber yield. Protein–protein interaction studies (yeast two‐hybrid and bimolecular fluorescence complementation) demonstrate that StCEN binds components of the recently described tuberigen activation complex. Using transient transactivation assays, we show that the StSP6A tuberisation signal is an activation target of the tuberigen activation complex, and that co‐expression of StCEN blocks activation of the StSP6A gene by StFD‐Like‐1. Transcriptomic analysis of transgenic lines misexpressing StCEN identifies early transcriptional events in tuber formation. These results demonstrate that StCEN suppresses tuberisation by directly antagonising the function of StSP6A in stolons, identifying StCEN as a breeding marker to improve tuber initiation and yield through the selection of genotypes with reduced StCEN expression.
Significance Statement
Understanding the mechanism of tuber initiation in potato provides a key route to increasing productivity of a crop that is essential for food security. We demonstrate that a member of the potato phosphatidylethanolamine‐binding protein gene family (StCEN) is a key component in the regulation of tuberisation that acts via interaction with the tuberigen activation complex to regulate early tuberisation transcriptional changes. |
doi_str_mv | 10.1111/tpj.14898 |
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Potato tuber formation is a secondary developmental programme by which cells in the subapical stolon region divide and radially expand to further differentiate into starch‐accumulating parenchyma. Although some details of the molecular pathway that signals tuberisation are known, important gaps in our knowledge persist. Here, the role of a member of the TERMINAL FLOWER 1/CENTRORADIALIS gene family (termed StCEN) in the negative control of tuberisation is demonstrated for what is thought to be the first time. It is shown that reduced expression of StCEN accelerates tuber formation whereas transgenic lines overexpressing this gene display delayed tuberisation and reduced tuber yield. Protein–protein interaction studies (yeast two‐hybrid and bimolecular fluorescence complementation) demonstrate that StCEN binds components of the recently described tuberigen activation complex. Using transient transactivation assays, we show that the StSP6A tuberisation signal is an activation target of the tuberigen activation complex, and that co‐expression of StCEN blocks activation of the StSP6A gene by StFD‐Like‐1. Transcriptomic analysis of transgenic lines misexpressing StCEN identifies early transcriptional events in tuber formation. These results demonstrate that StCEN suppresses tuberisation by directly antagonising the function of StSP6A in stolons, identifying StCEN as a breeding marker to improve tuber initiation and yield through the selection of genotypes with reduced StCEN expression.
Significance Statement
Understanding the mechanism of tuber initiation in potato provides a key route to increasing productivity of a crop that is essential for food security. We demonstrate that a member of the potato phosphatidylethanolamine‐binding protein gene family (StCEN) is a key component in the regulation of tuberisation that acts via interaction with the tuberigen activation complex to regulate early tuberisation transcriptional changes.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/tpj.14898</identifier><identifier>PMID: 32593210</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>CENTRORADIALIS gene ; Complementation ; Flowers ; Fluorescence ; Genes, Plant ; Genotypes ; Original ; Parenchyma ; Plant Proteins - metabolism ; Plant Proteins - physiology ; Plant Tubers - growth & development ; Plant Tubers - metabolism ; Plants, Genetically Modified ; Potatoes ; Proteins ; protein–protein interaction ; Solanum tuberosum (potato) ; Solanum tuberosum - growth & development ; Solanum tuberosum - metabolism ; Starch ; TERMINAL FLOWER 1/CENTRORADIALIS ; Transcription ; Transcriptome ; tuberigen complex ; tuberisation ; Yeasts</subject><ispartof>The Plant journal : for cell and molecular biology, 2020-09, Vol.103 (6), p.2263-2278</ispartof><rights>2020 The Authors. published by Society for Experimental Biology and John Wiley & Sons Ltd</rights><rights>2020 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.</rights><rights>2020. This article is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4438-4b12dbc7c0fa99351b1a8d14b3d353026b925dac9575cfd5ef891e52b90410c43</citedby><cites>FETCH-LOGICAL-c4438-4b12dbc7c0fa99351b1a8d14b3d353026b925dac9575cfd5ef891e52b90410c43</cites><orcidid>0000-0001-9724-915X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Ftpj.14898$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Ftpj.14898$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,1411,1427,27901,27902,45550,45551,46384,46808</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32593210$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhang, Xing</creatorcontrib><creatorcontrib>Campbell, Raymond</creatorcontrib><creatorcontrib>Ducreux, Laurence J. M.</creatorcontrib><creatorcontrib>Morris, Jennifer</creatorcontrib><creatorcontrib>Hedley, Pete E.</creatorcontrib><creatorcontrib>Mellado‐Ortega, Elena</creatorcontrib><creatorcontrib>Roberts, Alison G.</creatorcontrib><creatorcontrib>Stephens, Jennifer</creatorcontrib><creatorcontrib>Bryan, Glenn J.</creatorcontrib><creatorcontrib>Torrance, Lesley</creatorcontrib><creatorcontrib>Chapman, Sean N.</creatorcontrib><creatorcontrib>Prat, Salomé</creatorcontrib><creatorcontrib>Taylor, Mark A.</creatorcontrib><title>TERMINAL FLOWER‐1/CENTRORADIALIS inhibits tuberisation via protein interaction with the tuberigen activation complex</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>SUMMARY
Potato tuber formation is a secondary developmental programme by which cells in the subapical stolon region divide and radially expand to further differentiate into starch‐accumulating parenchyma. Although some details of the molecular pathway that signals tuberisation are known, important gaps in our knowledge persist. Here, the role of a member of the TERMINAL FLOWER 1/CENTRORADIALIS gene family (termed StCEN) in the negative control of tuberisation is demonstrated for what is thought to be the first time. It is shown that reduced expression of StCEN accelerates tuber formation whereas transgenic lines overexpressing this gene display delayed tuberisation and reduced tuber yield. Protein–protein interaction studies (yeast two‐hybrid and bimolecular fluorescence complementation) demonstrate that StCEN binds components of the recently described tuberigen activation complex. Using transient transactivation assays, we show that the StSP6A tuberisation signal is an activation target of the tuberigen activation complex, and that co‐expression of StCEN blocks activation of the StSP6A gene by StFD‐Like‐1. Transcriptomic analysis of transgenic lines misexpressing StCEN identifies early transcriptional events in tuber formation. These results demonstrate that StCEN suppresses tuberisation by directly antagonising the function of StSP6A in stolons, identifying StCEN as a breeding marker to improve tuber initiation and yield through the selection of genotypes with reduced StCEN expression.
Significance Statement
Understanding the mechanism of tuber initiation in potato provides a key route to increasing productivity of a crop that is essential for food security. We demonstrate that a member of the potato phosphatidylethanolamine‐binding protein gene family (StCEN) is a key component in the regulation of tuberisation that acts via interaction with the tuberigen activation complex to regulate early tuberisation transcriptional changes.</description><subject>CENTRORADIALIS gene</subject><subject>Complementation</subject><subject>Flowers</subject><subject>Fluorescence</subject><subject>Genes, Plant</subject><subject>Genotypes</subject><subject>Original</subject><subject>Parenchyma</subject><subject>Plant Proteins - metabolism</subject><subject>Plant Proteins - physiology</subject><subject>Plant Tubers - growth & development</subject><subject>Plant Tubers - metabolism</subject><subject>Plants, Genetically Modified</subject><subject>Potatoes</subject><subject>Proteins</subject><subject>protein–protein interaction</subject><subject>Solanum tuberosum (potato)</subject><subject>Solanum tuberosum - growth & development</subject><subject>Solanum tuberosum - metabolism</subject><subject>Starch</subject><subject>TERMINAL FLOWER 1/CENTRORADIALIS</subject><subject>Transcription</subject><subject>Transcriptome</subject><subject>tuberigen complex</subject><subject>tuberisation</subject><subject>Yeasts</subject><issn>0960-7412</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><recordid>eNp1kc-O0zAQhy0EYrsLB14AReICh2w9_tPEF6SqdKEobFEpgpvlOM7WVZoE2-nu3ngEnpEnId2UFSDhiyXP508z80PoGeBz6M84tNtzYKlIH6AR0AmPKdCvD9EIiwmOEwbkBJ16v8UYEjphj9EJJVxQAniE9uv56sPicppFF9nyy3z18_sPGM_ml-vVcjV9s5hmi0-RrTc2t8FHocuNs14F29TR3qqodU0wtu6JYJzSd-_XNmyisDFH-srU0aGyH37pZtdW5uYJelSqypunx_sMfb6Yr2fv4mz5djGbZrFmjKYxy4EUuU40LpUQlEMOKi2A5bSgnGIyyQXhhdKCJ1yXBTdlKsBwkgvMAGtGz9Drwdt2-c4U2tTBqUq2zu6Uu5WNsvLvSm038qrZy4QzTNlB8PIocM23zvggd9ZrU1WqNk3nJWGQAkn6Jffoi3_QbdO5uh-vpxjhgAU5UK8GSrvGe2fK-2YAy0Oask9T3qXZs8__7P6e_B1fD4wH4NpW5vb_Jrn--H5Q_gIE5qqO</recordid><startdate>202009</startdate><enddate>202009</enddate><creator>Zhang, Xing</creator><creator>Campbell, Raymond</creator><creator>Ducreux, Laurence J. M.</creator><creator>Morris, Jennifer</creator><creator>Hedley, Pete E.</creator><creator>Mellado‐Ortega, Elena</creator><creator>Roberts, Alison G.</creator><creator>Stephens, Jennifer</creator><creator>Bryan, Glenn J.</creator><creator>Torrance, Lesley</creator><creator>Chapman, Sean N.</creator><creator>Prat, Salomé</creator><creator>Taylor, Mark A.</creator><general>Blackwell Publishing Ltd</general><general>John Wiley and Sons Inc</general><scope>24P</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>7QO</scope><scope>7QP</scope><scope>7QR</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-9724-915X</orcidid></search><sort><creationdate>202009</creationdate><title>TERMINAL FLOWER‐1/CENTRORADIALIS inhibits tuberisation via protein interaction with the tuberigen activation complex</title><author>Zhang, Xing ; Campbell, Raymond ; Ducreux, Laurence J. M. ; Morris, Jennifer ; Hedley, Pete E. ; Mellado‐Ortega, Elena ; Roberts, Alison G. ; Stephens, Jennifer ; Bryan, Glenn J. ; Torrance, Lesley ; Chapman, Sean N. ; Prat, Salomé ; Taylor, Mark A.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4438-4b12dbc7c0fa99351b1a8d14b3d353026b925dac9575cfd5ef891e52b90410c43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>CENTRORADIALIS gene</topic><topic>Complementation</topic><topic>Flowers</topic><topic>Fluorescence</topic><topic>Genes, Plant</topic><topic>Genotypes</topic><topic>Original</topic><topic>Parenchyma</topic><topic>Plant Proteins - metabolism</topic><topic>Plant Proteins - physiology</topic><topic>Plant Tubers - growth & development</topic><topic>Plant Tubers - metabolism</topic><topic>Plants, Genetically Modified</topic><topic>Potatoes</topic><topic>Proteins</topic><topic>protein–protein interaction</topic><topic>Solanum tuberosum (potato)</topic><topic>Solanum tuberosum - growth & development</topic><topic>Solanum tuberosum - metabolism</topic><topic>Starch</topic><topic>TERMINAL FLOWER 1/CENTRORADIALIS</topic><topic>Transcription</topic><topic>Transcriptome</topic><topic>tuberigen complex</topic><topic>tuberisation</topic><topic>Yeasts</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhang, Xing</creatorcontrib><creatorcontrib>Campbell, Raymond</creatorcontrib><creatorcontrib>Ducreux, Laurence J. M.</creatorcontrib><creatorcontrib>Morris, Jennifer</creatorcontrib><creatorcontrib>Hedley, Pete E.</creatorcontrib><creatorcontrib>Mellado‐Ortega, Elena</creatorcontrib><creatorcontrib>Roberts, Alison G.</creatorcontrib><creatorcontrib>Stephens, Jennifer</creatorcontrib><creatorcontrib>Bryan, Glenn J.</creatorcontrib><creatorcontrib>Torrance, Lesley</creatorcontrib><creatorcontrib>Chapman, Sean N.</creatorcontrib><creatorcontrib>Prat, Salomé</creatorcontrib><creatorcontrib>Taylor, Mark A.</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Plant journal : for cell and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhang, Xing</au><au>Campbell, Raymond</au><au>Ducreux, Laurence J. M.</au><au>Morris, Jennifer</au><au>Hedley, Pete E.</au><au>Mellado‐Ortega, Elena</au><au>Roberts, Alison G.</au><au>Stephens, Jennifer</au><au>Bryan, Glenn J.</au><au>Torrance, Lesley</au><au>Chapman, Sean N.</au><au>Prat, Salomé</au><au>Taylor, Mark A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>TERMINAL FLOWER‐1/CENTRORADIALIS inhibits tuberisation via protein interaction with the tuberigen activation complex</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2020-09</date><risdate>2020</risdate><volume>103</volume><issue>6</issue><spage>2263</spage><epage>2278</epage><pages>2263-2278</pages><issn>0960-7412</issn><eissn>1365-313X</eissn><abstract>SUMMARY
Potato tuber formation is a secondary developmental programme by which cells in the subapical stolon region divide and radially expand to further differentiate into starch‐accumulating parenchyma. Although some details of the molecular pathway that signals tuberisation are known, important gaps in our knowledge persist. Here, the role of a member of the TERMINAL FLOWER 1/CENTRORADIALIS gene family (termed StCEN) in the negative control of tuberisation is demonstrated for what is thought to be the first time. It is shown that reduced expression of StCEN accelerates tuber formation whereas transgenic lines overexpressing this gene display delayed tuberisation and reduced tuber yield. Protein–protein interaction studies (yeast two‐hybrid and bimolecular fluorescence complementation) demonstrate that StCEN binds components of the recently described tuberigen activation complex. Using transient transactivation assays, we show that the StSP6A tuberisation signal is an activation target of the tuberigen activation complex, and that co‐expression of StCEN blocks activation of the StSP6A gene by StFD‐Like‐1. Transcriptomic analysis of transgenic lines misexpressing StCEN identifies early transcriptional events in tuber formation. These results demonstrate that StCEN suppresses tuberisation by directly antagonising the function of StSP6A in stolons, identifying StCEN as a breeding marker to improve tuber initiation and yield through the selection of genotypes with reduced StCEN expression.
Significance Statement
Understanding the mechanism of tuber initiation in potato provides a key route to increasing productivity of a crop that is essential for food security. We demonstrate that a member of the potato phosphatidylethanolamine‐binding protein gene family (StCEN) is a key component in the regulation of tuberisation that acts via interaction with the tuberigen activation complex to regulate early tuberisation transcriptional changes.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>32593210</pmid><doi>10.1111/tpj.14898</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0001-9724-915X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | CENTRORADIALIS gene Complementation Flowers Fluorescence Genes, Plant Genotypes Original Parenchyma Plant Proteins - metabolism Plant Proteins - physiology Plant Tubers - growth & development Plant Tubers - metabolism Plants, Genetically Modified Potatoes Proteins protein–protein interaction Solanum tuberosum (potato) Solanum tuberosum - growth & development Solanum tuberosum - metabolism Starch TERMINAL FLOWER 1/CENTRORADIALIS Transcription Transcriptome tuberigen complex tuberisation Yeasts |
title | TERMINAL FLOWER‐1/CENTRORADIALIS inhibits tuberisation via protein interaction with the tuberigen activation complex |
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