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A Ceratopteris EXCESS MICROSPOROCYTES1 suppresses reproductive transition in the fern vegetative leaves
Land plant sexual reproduction involves the transition of cells from somatic to reproductive identity during post-embryonic development. In Arabidopsis, the leucine-rich repeat receptor-like kinase EXCESS MICROSPOROCYTES1 (EXS/EMS1) restricts the number of sporogenous cells during the transition fro...
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Published in: | Plant science (Limerick) 2023-10, Vol.335, p.111812-111812, Article 111812 |
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creator | Withers, Kelley Falls, Kevin Youngstrom, Christopher Nguyen, Tommy Dewald, Anika Yarvis, Rebekah M. Simons, Gabriel P. Flanagan, Robert Bui, Linh T. Irish, Erin Cheng, Chi-Lien |
description | Land plant sexual reproduction involves the transition of cells from somatic to reproductive identity during post-embryonic development. In Arabidopsis, the leucine-rich repeat receptor-like kinase EXCESS MICROSPOROCYTES1 (EXS/EMS1) restricts the number of sporogenous cells during the transition from diploid tissue to haploid spore production by promoting the formation of the tapetum cell layer within the anther. Although all land plants studied contain EMS1 genes, its function is unknown beyond a few angiosperms. In the model fern Ceratopteris (Ceratopteris richardii), we discovered an EMS1 homolog (CrEMS1) that functions to suppress formation of reproductive structures on vegetative leaves of the fern sporophyte, a role not found in angiosperms. Suppression of CrEMS1 by RNAi did not affect sporogenesis on reproductive leaves but did affect antheridium production of the fern gametophyte. Expression patterns of CrEMS1 across developmental stages suggest threshold levels of CrEMS1 control the specification of reproductive organs during both generations of the fern. Additional EMS1 homologs present in the fern genome suggest a dynamic role of EMS1 receptors in the evolution of reproductive development in vascular plants.
•A Ceratopteris EMS1 gene suppresses vegetative leaves to become reproductive.•Knocking down the fern EMS1 does not affect sporangium development in sporophylls.•Knocking down EMS1 affects the number of antheridia in the gametophyte generation. |
doi_str_mv | 10.1016/j.plantsci.2023.111812 |
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•A Ceratopteris EMS1 gene suppresses vegetative leaves to become reproductive.•Knocking down the fern EMS1 does not affect sporangium development in sporophylls.•Knocking down EMS1 affects the number of antheridia in the gametophyte generation.</description><identifier>ISSN: 0168-9452</identifier><identifier>EISSN: 1873-2259</identifier><identifier>DOI: 10.1016/j.plantsci.2023.111812</identifier><identifier>PMID: 37532002</identifier><language>eng</language><publisher>Ireland: Elsevier B.V</publisher><subject>antheridium ; Arabidopsis ; Ceratopteris ; Ceratopteris richardii ; diploidy ; EMS1 ; evolution ; ferns and fern allies ; gametophyte ; gametophytes ; genome ; haploidy ; reproductive transition ; sexual reproduction ; sporangium ; spores ; sporophytes ; sporulation</subject><ispartof>Plant science (Limerick), 2023-10, Vol.335, p.111812-111812, Article 111812</ispartof><rights>2023 Elsevier B.V.</rights><rights>Copyright © 2023 Elsevier B.V. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c449t-d7e1f92668f7f448b8fa8fde59903c5a620788672fe7b90f9567c6ee085f30083</citedby><cites>FETCH-LOGICAL-c449t-d7e1f92668f7f448b8fa8fde59903c5a620788672fe7b90f9567c6ee085f30083</cites><orcidid>0000-0003-3188-047X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27900,27901</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37532002$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Withers, Kelley</creatorcontrib><creatorcontrib>Falls, Kevin</creatorcontrib><creatorcontrib>Youngstrom, Christopher</creatorcontrib><creatorcontrib>Nguyen, Tommy</creatorcontrib><creatorcontrib>Dewald, Anika</creatorcontrib><creatorcontrib>Yarvis, Rebekah M.</creatorcontrib><creatorcontrib>Simons, Gabriel P.</creatorcontrib><creatorcontrib>Flanagan, Robert</creatorcontrib><creatorcontrib>Bui, Linh T.</creatorcontrib><creatorcontrib>Irish, Erin</creatorcontrib><creatorcontrib>Cheng, Chi-Lien</creatorcontrib><title>A Ceratopteris EXCESS MICROSPOROCYTES1 suppresses reproductive transition in the fern vegetative leaves</title><title>Plant science (Limerick)</title><addtitle>Plant Sci</addtitle><description>Land plant sexual reproduction involves the transition of cells from somatic to reproductive identity during post-embryonic development. In Arabidopsis, the leucine-rich repeat receptor-like kinase EXCESS MICROSPOROCYTES1 (EXS/EMS1) restricts the number of sporogenous cells during the transition from diploid tissue to haploid spore production by promoting the formation of the tapetum cell layer within the anther. Although all land plants studied contain EMS1 genes, its function is unknown beyond a few angiosperms. In the model fern Ceratopteris (Ceratopteris richardii), we discovered an EMS1 homolog (CrEMS1) that functions to suppress formation of reproductive structures on vegetative leaves of the fern sporophyte, a role not found in angiosperms. Suppression of CrEMS1 by RNAi did not affect sporogenesis on reproductive leaves but did affect antheridium production of the fern gametophyte. Expression patterns of CrEMS1 across developmental stages suggest threshold levels of CrEMS1 control the specification of reproductive organs during both generations of the fern. Additional EMS1 homologs present in the fern genome suggest a dynamic role of EMS1 receptors in the evolution of reproductive development in vascular plants.
•A Ceratopteris EMS1 gene suppresses vegetative leaves to become reproductive.•Knocking down the fern EMS1 does not affect sporangium development in sporophylls.•Knocking down EMS1 affects the number of antheridia in the gametophyte generation.</description><subject>antheridium</subject><subject>Arabidopsis</subject><subject>Ceratopteris</subject><subject>Ceratopteris richardii</subject><subject>diploidy</subject><subject>EMS1</subject><subject>evolution</subject><subject>ferns and fern allies</subject><subject>gametophyte</subject><subject>gametophytes</subject><subject>genome</subject><subject>haploidy</subject><subject>reproductive transition</subject><subject>sexual reproduction</subject><subject>sporangium</subject><subject>spores</subject><subject>sporophytes</subject><subject>sporulation</subject><issn>0168-9452</issn><issn>1873-2259</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><recordid>eNqFkU1rGzEQhkVoiZ2Pv2B07GVdfaw-9tawuG0gxSVOoD0JWTtyZOzdraQ19N93HTu95jQMPO_MMA9CM0rmlFD5eTvvd7bNyYU5I4zPKaWasgs0pVrxgjFRfUDTEdRFVQo2QVcpbQkhTAh1iSZcCc7Gboo2d7iGaHPXZ4gh4cWverFa4R_39eNy9XP5uKx_Py1WFKeh7yOkBAlH6GPXDC6HA-AcbZtCDl2LQ4vzC2APscUH2EC2r8QO7AHSDfro7S7B7bleo-evi6f6e_Gw_HZf3z0UriyrXDQKqK-YlNorX5Z6rb3VvgFRVYQ7YSUjSmupmAe1roivhFROAhAtPCdE82v06TR3vPHPACmbfUgOduOzoBuS4VSUVEpO30eZLoUUSqojKk-oi11KEbzpY9jb-NdQYo4-zNa8-TBHH-bkYwzOzjuG9R6a_7E3ASPw5QTA-JRDgGjGEdA6aEIEl03Thfd2_ANg_55n</recordid><startdate>20231001</startdate><enddate>20231001</enddate><creator>Withers, Kelley</creator><creator>Falls, Kevin</creator><creator>Youngstrom, Christopher</creator><creator>Nguyen, Tommy</creator><creator>Dewald, Anika</creator><creator>Yarvis, Rebekah M.</creator><creator>Simons, Gabriel P.</creator><creator>Flanagan, Robert</creator><creator>Bui, Linh T.</creator><creator>Irish, Erin</creator><creator>Cheng, Chi-Lien</creator><general>Elsevier B.V</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0003-3188-047X</orcidid></search><sort><creationdate>20231001</creationdate><title>A Ceratopteris EXCESS MICROSPOROCYTES1 suppresses reproductive transition in the fern vegetative leaves</title><author>Withers, Kelley ; Falls, Kevin ; Youngstrom, Christopher ; Nguyen, Tommy ; Dewald, Anika ; Yarvis, Rebekah M. ; Simons, Gabriel P. ; Flanagan, Robert ; Bui, Linh T. ; Irish, Erin ; Cheng, Chi-Lien</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c449t-d7e1f92668f7f448b8fa8fde59903c5a620788672fe7b90f9567c6ee085f30083</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>antheridium</topic><topic>Arabidopsis</topic><topic>Ceratopteris</topic><topic>Ceratopteris richardii</topic><topic>diploidy</topic><topic>EMS1</topic><topic>evolution</topic><topic>ferns and fern allies</topic><topic>gametophyte</topic><topic>gametophytes</topic><topic>genome</topic><topic>haploidy</topic><topic>reproductive transition</topic><topic>sexual reproduction</topic><topic>sporangium</topic><topic>spores</topic><topic>sporophytes</topic><topic>sporulation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Withers, Kelley</creatorcontrib><creatorcontrib>Falls, Kevin</creatorcontrib><creatorcontrib>Youngstrom, Christopher</creatorcontrib><creatorcontrib>Nguyen, Tommy</creatorcontrib><creatorcontrib>Dewald, Anika</creatorcontrib><creatorcontrib>Yarvis, Rebekah M.</creatorcontrib><creatorcontrib>Simons, Gabriel P.</creatorcontrib><creatorcontrib>Flanagan, Robert</creatorcontrib><creatorcontrib>Bui, Linh T.</creatorcontrib><creatorcontrib>Irish, Erin</creatorcontrib><creatorcontrib>Cheng, Chi-Lien</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Plant science (Limerick)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Withers, Kelley</au><au>Falls, Kevin</au><au>Youngstrom, Christopher</au><au>Nguyen, Tommy</au><au>Dewald, Anika</au><au>Yarvis, Rebekah M.</au><au>Simons, Gabriel P.</au><au>Flanagan, Robert</au><au>Bui, Linh T.</au><au>Irish, Erin</au><au>Cheng, Chi-Lien</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A Ceratopteris EXCESS MICROSPOROCYTES1 suppresses reproductive transition in the fern vegetative leaves</atitle><jtitle>Plant science (Limerick)</jtitle><addtitle>Plant Sci</addtitle><date>2023-10-01</date><risdate>2023</risdate><volume>335</volume><spage>111812</spage><epage>111812</epage><pages>111812-111812</pages><artnum>111812</artnum><issn>0168-9452</issn><eissn>1873-2259</eissn><abstract>Land plant sexual reproduction involves the transition of cells from somatic to reproductive identity during post-embryonic development. In Arabidopsis, the leucine-rich repeat receptor-like kinase EXCESS MICROSPOROCYTES1 (EXS/EMS1) restricts the number of sporogenous cells during the transition from diploid tissue to haploid spore production by promoting the formation of the tapetum cell layer within the anther. Although all land plants studied contain EMS1 genes, its function is unknown beyond a few angiosperms. In the model fern Ceratopteris (Ceratopteris richardii), we discovered an EMS1 homolog (CrEMS1) that functions to suppress formation of reproductive structures on vegetative leaves of the fern sporophyte, a role not found in angiosperms. Suppression of CrEMS1 by RNAi did not affect sporogenesis on reproductive leaves but did affect antheridium production of the fern gametophyte. Expression patterns of CrEMS1 across developmental stages suggest threshold levels of CrEMS1 control the specification of reproductive organs during both generations of the fern. Additional EMS1 homologs present in the fern genome suggest a dynamic role of EMS1 receptors in the evolution of reproductive development in vascular plants.
•A Ceratopteris EMS1 gene suppresses vegetative leaves to become reproductive.•Knocking down the fern EMS1 does not affect sporangium development in sporophylls.•Knocking down EMS1 affects the number of antheridia in the gametophyte generation.</abstract><cop>Ireland</cop><pub>Elsevier B.V</pub><pmid>37532002</pmid><doi>10.1016/j.plantsci.2023.111812</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0003-3188-047X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | antheridium Arabidopsis Ceratopteris Ceratopteris richardii diploidy EMS1 evolution ferns and fern allies gametophyte gametophytes genome haploidy reproductive transition sexual reproduction sporangium spores sporophytes sporulation |
title | A Ceratopteris EXCESS MICROSPOROCYTES1 suppresses reproductive transition in the fern vegetative leaves |
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