Tomato transcriptional repressor SlBES1.8 influences shoot apical meristem development by inhibiting the DNA binding ability of SlWUS
SUMMARY As the reservoir of pluripotent stem cells, the shoot apical meristem (SAM) is responsible for the production of aboveground plant organs including flower and fruit. The stem cell pool is dramatically influenced by a conserved negative feedback circuit between WUSCHEL (WUS) and CLAVATA (CLV)...
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| Veröffentlicht in: | The Plant journal : for cell and molecular biology 2022-04, Vol.110 (2), p.482-498 |
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| creator | Su, Deding Wen, Ling Xiang, Wei Shi, Yuan Lu, Wang Liu, Yudong Xian, Zhiqiang Li, Zhengguo |
| description | SUMMARY
As the reservoir of pluripotent stem cells, the shoot apical meristem (SAM) is responsible for the production of aboveground plant organs including flower and fruit. The stem cell pool is dramatically influenced by a conserved negative feedback circuit between WUSCHEL (WUS) and CLAVATA (CLV). Numerous studies have focused on the functional mechanism of WUS in maintaining SAM development over the past few years, while the co‐regulators of WUS remain to be discovered. Here, we identified a tomato (Solanum lycopersicum) BES1 transcription factor, SlBES1.8, that is specifically expressed in the SAM and flower and functions as a transcriptional repressor. Overexpression of SlBES1.8 resulted in enlarged SAM and extra floral organs in tomato, which eventually led to the formation of pepper‐like fruit with increased soluble sugar and organic acid contents. Direct regulatory effects of SlBES1.8 on the CLV–WUS signaling cascade were not observed; instead, protein–protein interaction between SlBES1.8 and SlWUS was confirmed and the crucial interaction domains were identified. As a result, this heterodimerization significantly repressed the transcriptional regulation ability of SlWUS by inhibiting SlWUS binding to the promoter fragments of CLV3 and downstream genes. Taken together, our findings suggest that SlBES1.8 serves as a novel co‐regulator of SlWUS to influence the development of the SAM.
Significance Statement
The development of plant shoot apical meristems (SAMs) is accurately controlled by WUSCHEL (WUS), while the co‐regulators of WUS still need to be discovered. We identified a tomato (Solanum lycopersicum) transcriptional repressor, SlBES1.8, and found that it can interact with WUS and inhibit WUS–DNA binding to enlarge SAM size, which further results in an increase of floral organ numbers and changes in fruit shape. Thus, SlBES1.8 is a novel co‐regulator of WUS, contributing to the regulation of SAM development. |
| doi_str_mv | 10.1111/tpj.15683 |
| format | Article |
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As the reservoir of pluripotent stem cells, the shoot apical meristem (SAM) is responsible for the production of aboveground plant organs including flower and fruit. The stem cell pool is dramatically influenced by a conserved negative feedback circuit between WUSCHEL (WUS) and CLAVATA (CLV). Numerous studies have focused on the functional mechanism of WUS in maintaining SAM development over the past few years, while the co‐regulators of WUS remain to be discovered. Here, we identified a tomato (Solanum lycopersicum) BES1 transcription factor, SlBES1.8, that is specifically expressed in the SAM and flower and functions as a transcriptional repressor. Overexpression of SlBES1.8 resulted in enlarged SAM and extra floral organs in tomato, which eventually led to the formation of pepper‐like fruit with increased soluble sugar and organic acid contents. Direct regulatory effects of SlBES1.8 on the CLV–WUS signaling cascade were not observed; instead, protein–protein interaction between SlBES1.8 and SlWUS was confirmed and the crucial interaction domains were identified. As a result, this heterodimerization significantly repressed the transcriptional regulation ability of SlWUS by inhibiting SlWUS binding to the promoter fragments of CLV3 and downstream genes. Taken together, our findings suggest that SlBES1.8 serves as a novel co‐regulator of SlWUS to influence the development of the SAM.
Significance Statement
The development of plant shoot apical meristems (SAMs) is accurately controlled by WUSCHEL (WUS), while the co‐regulators of WUS still need to be discovered. We identified a tomato (Solanum lycopersicum) transcriptional repressor, SlBES1.8, and found that it can interact with WUS and inhibit WUS–DNA binding to enlarge SAM size, which further results in an increase of floral organ numbers and changes in fruit shape. Thus, SlBES1.8 is a novel co‐regulator of WUS, contributing to the regulation of SAM development.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/tpj.15683</identifier><identifier>PMID: 35076967</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Arabidopsis Proteins - metabolism ; BES1 transcription factor ; Binding ; DNA - metabolism ; Feedback circuits ; Flowers ; fruit shape ; Fruits ; Gene Expression Regulation, Plant ; Gene regulation ; heterodimerization ; Homeodomain Proteins - genetics ; Lycopersicon esculentum - genetics ; Meristem - metabolism ; Meristems ; Negative feedback ; Organic acids ; Organs ; Plant Shoots - metabolism ; Pluripotency ; Proteins ; shoot apical meristem (SAM) ; Solanum lycopersicum ; Stem cells ; tomato (Solanum lycopersicum) ; Tomatoes ; Transcription Factors - metabolism ; WUSCHEL (WUS)</subject><ispartof>The Plant journal : for cell and molecular biology, 2022-04, Vol.110 (2), p.482-498</ispartof><rights>2022 Society for Experimental Biology and John Wiley & Sons Ltd</rights><rights>Copyright © 2022 John Wiley & Sons Ltd and the Society for Experimental Biology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><orcidid>0000-0001-7019-2560</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.15683$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Ftpj.15683$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1416,1432,27915,27916,45565,45566,46400,46824</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35076967$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Su, Deding</creatorcontrib><creatorcontrib>Wen, Ling</creatorcontrib><creatorcontrib>Xiang, Wei</creatorcontrib><creatorcontrib>Shi, Yuan</creatorcontrib><creatorcontrib>Lu, Wang</creatorcontrib><creatorcontrib>Liu, Yudong</creatorcontrib><creatorcontrib>Xian, Zhiqiang</creatorcontrib><creatorcontrib>Li, Zhengguo</creatorcontrib><title>Tomato transcriptional repressor SlBES1.8 influences shoot apical meristem development by inhibiting the DNA binding ability of SlWUS</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>SUMMARY
As the reservoir of pluripotent stem cells, the shoot apical meristem (SAM) is responsible for the production of aboveground plant organs including flower and fruit. The stem cell pool is dramatically influenced by a conserved negative feedback circuit between WUSCHEL (WUS) and CLAVATA (CLV). Numerous studies have focused on the functional mechanism of WUS in maintaining SAM development over the past few years, while the co‐regulators of WUS remain to be discovered. Here, we identified a tomato (Solanum lycopersicum) BES1 transcription factor, SlBES1.8, that is specifically expressed in the SAM and flower and functions as a transcriptional repressor. Overexpression of SlBES1.8 resulted in enlarged SAM and extra floral organs in tomato, which eventually led to the formation of pepper‐like fruit with increased soluble sugar and organic acid contents. Direct regulatory effects of SlBES1.8 on the CLV–WUS signaling cascade were not observed; instead, protein–protein interaction between SlBES1.8 and SlWUS was confirmed and the crucial interaction domains were identified. As a result, this heterodimerization significantly repressed the transcriptional regulation ability of SlWUS by inhibiting SlWUS binding to the promoter fragments of CLV3 and downstream genes. Taken together, our findings suggest that SlBES1.8 serves as a novel co‐regulator of SlWUS to influence the development of the SAM.
Significance Statement
The development of plant shoot apical meristems (SAMs) is accurately controlled by WUSCHEL (WUS), while the co‐regulators of WUS still need to be discovered. We identified a tomato (Solanum lycopersicum) transcriptional repressor, SlBES1.8, and found that it can interact with WUS and inhibit WUS–DNA binding to enlarge SAM size, which further results in an increase of floral organ numbers and changes in fruit shape. Thus, SlBES1.8 is a novel co‐regulator of WUS, contributing to the regulation of SAM development.</description><subject>Arabidopsis Proteins - metabolism</subject><subject>BES1 transcription factor</subject><subject>Binding</subject><subject>DNA - metabolism</subject><subject>Feedback circuits</subject><subject>Flowers</subject><subject>fruit shape</subject><subject>Fruits</subject><subject>Gene Expression Regulation, Plant</subject><subject>Gene regulation</subject><subject>heterodimerization</subject><subject>Homeodomain Proteins - genetics</subject><subject>Lycopersicon esculentum - genetics</subject><subject>Meristem - metabolism</subject><subject>Meristems</subject><subject>Negative feedback</subject><subject>Organic acids</subject><subject>Organs</subject><subject>Plant Shoots - metabolism</subject><subject>Pluripotency</subject><subject>Proteins</subject><subject>shoot apical meristem (SAM)</subject><subject>Solanum lycopersicum</subject><subject>Stem cells</subject><subject>tomato (Solanum lycopersicum)</subject><subject>Tomatoes</subject><subject>Transcription Factors - metabolism</subject><subject>WUSCHEL (WUS)</subject><issn>0960-7412</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpd0c1u1DAQB3ALgehSOPACyBIXLtl6YsdJjqW0fKgCpN0KbpEdT1ivnDjYDtU-AO-Nty0c8GU8mp_mMH9CXgJbQ35nad6voZINf0RWwGVVcODfH5MVayUragHlCXkW454xqLkUT8kJr1gtW1mvyO-tH1XyNAU1xT7YOVk_KUcDzgFj9IFu3NvLDawbaqfBLTj1GGnceZ-omm2f6YjBxoQjNfgLnZ9HnBLVh-x3Vttkpx807ZC--3xOtZ3MsVfaOpsO1A95_bebzXPyZFAu4ouHekpuri63Fx-K6y_vP16cXxczB8GLpuZa9SVq1uPAFZSg-3pgIGRpBFMtCMXrysDQmLaRBkyW2mhjFAzCKMlPyZv7vXPwPxeMqRtt7NE5NaFfYlfKspSSQdtm-vo_uvdLyKc5qqoCIRhvsnr1oBY9ounmYEcVDt3fA2dwdg9urcPDvzmw7phcl5Pr7pLrtl8_3X34HxGXjNw</recordid><startdate>202204</startdate><enddate>202204</enddate><creator>Su, Deding</creator><creator>Wen, Ling</creator><creator>Xiang, Wei</creator><creator>Shi, Yuan</creator><creator>Lu, Wang</creator><creator>Liu, Yudong</creator><creator>Xian, Zhiqiang</creator><creator>Li, Zhengguo</creator><general>Blackwell Publishing Ltd</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</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><orcidid>https://orcid.org/0000-0001-7019-2560</orcidid></search><sort><creationdate>202204</creationdate><title>Tomato transcriptional repressor SlBES1.8 influences shoot apical meristem development by inhibiting the DNA binding ability of SlWUS</title><author>Su, Deding ; Wen, Ling ; Xiang, Wei ; Shi, Yuan ; Lu, Wang ; Liu, Yudong ; Xian, Zhiqiang ; Li, Zhengguo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-p3143-873bac2eb0cef3a121bc7f01462d40a914a375d1f8d986d1deb0bdbdda1f4da63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Arabidopsis Proteins - metabolism</topic><topic>BES1 transcription factor</topic><topic>Binding</topic><topic>DNA - metabolism</topic><topic>Feedback circuits</topic><topic>Flowers</topic><topic>fruit shape</topic><topic>Fruits</topic><topic>Gene Expression Regulation, Plant</topic><topic>Gene regulation</topic><topic>heterodimerization</topic><topic>Homeodomain Proteins - genetics</topic><topic>Lycopersicon esculentum - genetics</topic><topic>Meristem - metabolism</topic><topic>Meristems</topic><topic>Negative feedback</topic><topic>Organic acids</topic><topic>Organs</topic><topic>Plant Shoots - metabolism</topic><topic>Pluripotency</topic><topic>Proteins</topic><topic>shoot apical meristem (SAM)</topic><topic>Solanum lycopersicum</topic><topic>Stem cells</topic><topic>tomato (Solanum lycopersicum)</topic><topic>Tomatoes</topic><topic>Transcription Factors - metabolism</topic><topic>WUSCHEL (WUS)</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Su, Deding</creatorcontrib><creatorcontrib>Wen, Ling</creatorcontrib><creatorcontrib>Xiang, Wei</creatorcontrib><creatorcontrib>Shi, Yuan</creatorcontrib><creatorcontrib>Lu, Wang</creatorcontrib><creatorcontrib>Liu, Yudong</creatorcontrib><creatorcontrib>Xian, Zhiqiang</creatorcontrib><creatorcontrib>Li, Zhengguo</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</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><jtitle>The Plant journal : for cell and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Su, Deding</au><au>Wen, Ling</au><au>Xiang, Wei</au><au>Shi, Yuan</au><au>Lu, Wang</au><au>Liu, Yudong</au><au>Xian, Zhiqiang</au><au>Li, Zhengguo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Tomato transcriptional repressor SlBES1.8 influences shoot apical meristem development by inhibiting the DNA binding ability of SlWUS</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2022-04</date><risdate>2022</risdate><volume>110</volume><issue>2</issue><spage>482</spage><epage>498</epage><pages>482-498</pages><issn>0960-7412</issn><eissn>1365-313X</eissn><abstract>SUMMARY
As the reservoir of pluripotent stem cells, the shoot apical meristem (SAM) is responsible for the production of aboveground plant organs including flower and fruit. The stem cell pool is dramatically influenced by a conserved negative feedback circuit between WUSCHEL (WUS) and CLAVATA (CLV). Numerous studies have focused on the functional mechanism of WUS in maintaining SAM development over the past few years, while the co‐regulators of WUS remain to be discovered. Here, we identified a tomato (Solanum lycopersicum) BES1 transcription factor, SlBES1.8, that is specifically expressed in the SAM and flower and functions as a transcriptional repressor. Overexpression of SlBES1.8 resulted in enlarged SAM and extra floral organs in tomato, which eventually led to the formation of pepper‐like fruit with increased soluble sugar and organic acid contents. Direct regulatory effects of SlBES1.8 on the CLV–WUS signaling cascade were not observed; instead, protein–protein interaction between SlBES1.8 and SlWUS was confirmed and the crucial interaction domains were identified. As a result, this heterodimerization significantly repressed the transcriptional regulation ability of SlWUS by inhibiting SlWUS binding to the promoter fragments of CLV3 and downstream genes. Taken together, our findings suggest that SlBES1.8 serves as a novel co‐regulator of SlWUS to influence the development of the SAM.
Significance Statement
The development of plant shoot apical meristems (SAMs) is accurately controlled by WUSCHEL (WUS), while the co‐regulators of WUS still need to be discovered. We identified a tomato (Solanum lycopersicum) transcriptional repressor, SlBES1.8, and found that it can interact with WUS and inhibit WUS–DNA binding to enlarge SAM size, which further results in an increase of floral organ numbers and changes in fruit shape. Thus, SlBES1.8 is a novel co‐regulator of WUS, contributing to the regulation of SAM development.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>35076967</pmid><doi>10.1111/tpj.15683</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0001-7019-2560</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Arabidopsis Proteins - metabolism BES1 transcription factor Binding DNA - metabolism Feedback circuits Flowers fruit shape Fruits Gene Expression Regulation, Plant Gene regulation heterodimerization Homeodomain Proteins - genetics Lycopersicon esculentum - genetics Meristem - metabolism Meristems Negative feedback Organic acids Organs Plant Shoots - metabolism Pluripotency Proteins shoot apical meristem (SAM) Solanum lycopersicum Stem cells tomato (Solanum lycopersicum) Tomatoes Transcription Factors - metabolism WUSCHEL (WUS) |
| title | Tomato transcriptional repressor SlBES1.8 influences shoot apical meristem development by inhibiting the DNA binding ability of SlWUS |
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