{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,17]],"date-time":"2026-10-17T04:15:34Z","timestamp":1792210534600,"version":"4.4.0"},"reference-count":102,"publisher":"Oxford University Press (OUP)","issue":"10","license":[{"start":{"date-parts":[[2022,9,27]],"date-time":"2022-09-27T00:00:00Z","timestamp":1664236800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2022,10,7]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>How do separate sexes originate and evolve? Plants provide many opportunities to address this question as they have diverse mating systems and separate sexes (dioecy) that evolved many times independently. The classic \u201ctwo-factor\u201d model for evolution of separate sexes proposes that males and females can evolve from hermaphrodites via the spread of male and female sterility mutations that turn hermaphrodites into females and males, respectively. This widely accepted model was inspired by early genetic work in dioecious white campion (Silene latifolia) that revealed the presence of two sex-determining factors on the Y-chromosome, though the actual genes remained unknown. Here, we report identification and functional analysis of the putative sex-determining gene in S. latifolia, corresponding to the gynoecium suppression factor (GSF). We demonstrate that GSF likely corresponds to a Y-linked CLV3-like gene that is specifically expressed in early male flower buds and encodes the protein that suppresses gynoecium development in S. latifolia. Interestingly, GSFY has a dysfunctional X-linked homolog (GSFX) and their synonymous divergence (dS\u2009=\u200917.9%) is consistent with the age of sex chromosomes in this species. We propose that female development in S. latifolia is controlled via the WUSCHEL-CLAVATA feedback loop, with the X-linked WUSCHEL-like and Y-linked CLV3-like genes, respectively. Evolution of dioecy in the S. latifolia ancestor likely involved inclusion of ancestral GSFY into the nonrecombining region on the nascent Y-chromosome and GSFX loss of function, which resulted in disbalance of the WUSCHEL-CLAVATA feedback loop between the sexes and ensured gynoecium suppression in males.<\/jats:p>","DOI":"10.1093\/molbev\/msac195","type":"journal-article","created":{"date-parts":[[2022,9,27]],"date-time":"2022-09-27T21:13:17Z","timestamp":1664313197000},"source":"Crossref","is-referenced-by-count":36,"title":["A <i>CLAVATA3<\/i>-like Gene Acts as a Gynoecium Suppression Function in White Campion"],"prefix":"10.1093","volume":"39","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5876-7755","authenticated-orcid":false,"given":"Yusuke","family":"Kazama","sequence":"first","affiliation":[{"name":"Graduate School of Bioscience and Biotechnology, Fukui Prefectural University , 4-1-1 Kenjojima, Matsuoka, Eiheiji-cho , Japan"},{"name":"RIKEN Nishina Center , 2-1 Hirosawa, Wako, Saitama 351-0198 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Moe","family":"Kitoh","sequence":"additional","affiliation":[{"name":"Graduate School of Bioscience and Biotechnology, Fukui Prefectural University , 4-1-1 Kenjojima, Matsuoka, Eiheiji-cho , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Taiki","family":"Kobayashi","sequence":"additional","affiliation":[{"name":"Graduate School of Bioscience and Biotechnology, Fukui Prefectural University , 4-1-1 Kenjojima, Matsuoka, Eiheiji-cho , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kotaro","family":"Ishii","sequence":"additional","affiliation":[{"name":"RIKEN Nishina Center , 2-1 Hirosawa, Wako, Saitama 351-0198 , Japan"},{"name":"National Institutes for Quantum and Radiological Science and Technology , 4-9-1 Anagawa, Inage-ku, Chiba 263-8555 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marc","family":"Krasovec","sequence":"additional","affiliation":[{"name":"Department of Plant Sciences, University of Oxford , Oxford OX1 3RB , UK"},{"name":"Sorbonne Universit\u00e9, CNRS, UMR 7232 Biologie Int\u00e9grative des Organismes Marins (BIOM), Observatoire Oc\u00e9anologique , 66650 Banyuls-sur-Mer , France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yasuo","family":"Yasui","sequence":"additional","affiliation":[{"name":"Graduate School of Agriculture, Kyoto University, Kitashirakawa Oiwake-cho , Sakyo-ku, Kyoto 606-8502 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tomoko","family":"Abe","sequence":"additional","affiliation":[{"name":"RIKEN Nishina Center , 2-1 Hirosawa, Wako, Saitama 351-0198 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shigeyuki","family":"Kawano","sequence":"additional","affiliation":[{"name":"Department of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa, FSB-601 , 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8562 , Japan"},{"name":"Future Center Initiative, The University of Tokyo , 178-4-4 Wakashiba, Kashiwa, Chiba 277-0871 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dmitry A","family":"Filatov","sequence":"additional","affiliation":[{"name":"Department of Plant Sciences, University of Oxford , Oxford OX1 3RB , UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2022,9,27]]},"reference":[{"key":"2022101104063593000_msac195-B1","doi-asserted-by":"crossref","first-page":"780","DOI":"10.1105\/tpc.17.00787","article-title":"A Y-encoded suppressor of feminization arose via lineage-specific duplication of a cytokinin response regulator in kiwifruit","volume":"30","author":"Akagi","year":"2018","journal-title":"Plant Cell"},{"key":"2022101104063593000_msac195-B2","doi-asserted-by":"crossref","first-page":"646","DOI":"10.1126\/science.1257225","article-title":"Plant genetics. A Y-chromosome-encoded small RNA acts as a sex determinant in persimmons","volume":"346","author":"Akagi","year":"2014","journal-title":"Science"},{"key":"2022101104063593000_msac195-B3","doi-asserted-by":"crossref","first-page":"801","DOI":"10.1038\/s41477-019-0489-6","article-title":"Two Y-chromosome-encoded genes determine sex in kiwifruit","volume":"5","author":"Akagi","year":"2019","journal-title":"Nat Plants"},{"key":"2022101104063593000_msac195-B4","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1508\/cytologia.86.329","article-title":"Male\/female trade-off in hermaphroditic Y-chromosome deletion mutants of the dioecious plant Silene latifolia","volume":"86","author":"Aonuma","year":"2021","journal-title":"Cytologia (Tokyo)"},{"key":"2022101104063593000_msac195-B5","first-page":"217","article-title":"Sex determination in flowering plants: papaya as a model system","author":"Aryal","year":"2014","journal-title":"Plant 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