{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T04:30:34Z","timestamp":1790742634894,"version":"4.1.0"},"reference-count":53,"publisher":"Public Library of Science (PLoS)","issue":"1","license":[{"start":{"date-parts":[[2026,1,23]],"date-time":"2026-01-23T00:00:00Z","timestamp":1769126400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["IOS 1931114"],"award-info":[{"award-number":["IOS 1931114"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["IOS 2526475"],"award-info":[{"award-number":["IOS 2526475"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000057","name":"National Institute of General Medical Sciences","doi-asserted-by":"publisher","award":["R01GM157611"],"award-info":[{"award-number":["R01GM157611"]}],"id":[{"id":"10.13039\/100000057","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosbiology.org"],"crossmark-restriction":false},"short-container-title":["PLoS Biol"],"abstract":"<jats:p>\n                    Land plants alternate between generations of asexual sporophytes and sexual gametophytes. Unlike seed plants, ferns produce free-living gametophytes that grow independently from their sporophytes. Gametophytes of the model fern\n                    <jats:italic>Ceratopteris<\/jats:italic>\n                    exist in two sex types: hermaphrodites and males. Hermaphrodites maintain meristems and secrete the pheromone antheridiogen, inducing undecided gametophytes to become males. In the absence of antheridiogen, males exhibit developmental plasticity and dynamic cell fate specification by initiating de novo meristems to convert into hermaphrodites. Despite its essential role, the molecular signals governing this process remain unclear. Here, we show that local auxin biosynthesis, dynamically regulated during sex-type conversion, establishes new auxin maxima that are critical for specifying and promoting the proliferation of the meristem progenitor cell (MPC) lineage, ultimately enabling the de novo formation of a multicellular meristem from a single MPC. Time-lapse imaging revealed that upon antheridiogen removal, auxin signaling is specifically activated at the initial site of proliferation in\n                    <jats:italic>Ceratopteris<\/jats:italic>\n                    males, triggering new meristem formation. This auxin signaling subsequently becomes concentrated at the center of the proliferating meristem, aligning with localized auxin biosynthesis and the emergence of the meristem notch. Computationally reconstrued lineage maps further showed that chemical inhibition of CrTAA1 abolishes these dynamic auxin patterns, blocking MPC lineage initiation and its subsequent proliferation. Furthermore, genetic knockout of\n                    <jats:italic>CrTAA1<\/jats:italic>\n                    via CRISPR-Cas9 phenocopies the effects of chemical inhibition, preventing new meristem formation and disrupting male-to-hermaphrodite conversion. Together, these findings uncover a molecular mechanism underlying sex-type conversion in land plants and highlight the pivotal role of de novo auxin biosynthesis in orchestrating cell fate and proliferation during meristem formation.\n                  <\/jats:p>","DOI":"10.1371\/journal.pbio.3003592","type":"journal-article","created":{"date-parts":[[2026,1,23]],"date-time":"2026-01-23T18:43:23Z","timestamp":1769193803000},"page":"e3003592","update-policy":"https:\/\/doi.org\/10.1371\/journal.pbio.corrections_policy","source":"Crossref","is-referenced-by-count":4,"title":["Dynamic auxin maxima regulate male-to-hermaphrodite conversion and de novo meristem formation in the fern Ceratopteris gametophytes"],"prefix":"10.1371","volume":"24","author":[{"given":"Dinh Nhan","family":"Lai","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xi","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chong","family":"Xie","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ting","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"An","family":"Yan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xing","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4105-5174","authenticated-orcid":true,"given":"Yun","family":"Zhou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2026,1,23]]},"reference":[{"key":"pbio.3003592.ref001","first-page":"972","article-title":"Ferns: the missing link in shoot evolution and development","volume":"6","author":"ARG Plackett","year":"2015","journal-title":"Front Plant Sci"},{"key":"pbio.3003592.ref002","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1146\/annurev.arplant.50.1.163","article-title":"Gametophyte development in ferns","volume":"50","author":"JA Banks","year":"1999","journal-title":"Annu Rev Plant Physiol Plant Mol Biol"},{"issue":"8","key":"pbio.3003592.ref003","doi-asserted-by":"crossref","first-page":"1304","DOI":"10.1002\/j.1537-2197.1987.tb08743.x","article-title":"Ceratopteris richardii: applications for experimental plant biology","volume":"74","author":"LG Hickok","year":"1987","journal-title":"Am J Bot"},{"issue":"1","key":"pbio.3003592.ref004","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1016\/j.ydbio.2019.08.017","article-title":"An ontogenetic framework for functional studies in the model fern Ceratopteris richardii","volume":"457","author":"SJ Conway","year":"2020","journal-title":"Dev Biol"},{"issue":"4","key":"pbio.3003592.ref005","doi-asserted-by":"crossref","first-page":"522","DOI":"10.1086\/297135","article-title":"The programming of sexual phenotype in the homosporous fern Ceratopteris richardii","volume":"154","author":"JA Banks","year":"1993","journal-title":"Int J Plant Sci"},{"issue":"3","key":"pbio.3003592.ref006","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1086\/297255","article-title":"The biology of the fern Ceratopteris and its use as a model system","volume":"156","author":"LG Hickok","year":"1995","journal-title":"Int J Plant Sci"},{"issue":"2","key":"pbio.3003592.ref007","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1893\/0005-3155(2007)78[58:COMGTH]2.0.CO;2","article-title":"Conversion of male gametophytes to hermaphrodites in the fern Ceratopteris richardii","volume":"78","author":"DJ Cheruiyot","year":"2007","journal-title":"BIOS"},{"issue":"1","key":"pbio.3003592.ref008","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1016\/S1369-5266(98)80130-1","article-title":"Sex determination in plants","volume":"1","author":"C Juarez","year":"1998","journal-title":"Curr Opin Plant Biol"},{"issue":"3","key":"pbio.3003592.ref009","doi-asserted-by":"crossref","DOI":"10.1242\/dev.204411","article-title":"Single cell-derived multicellular meristem: insights into male-to-hermaphrodite conversion and de novo meristem formation in Ceratopteris","volume":"152","author":"X Yang","year":"2025","journal-title":"Development"},{"key":"pbio.3003592.ref010","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1146\/annurev-arplant-042809-112308","article-title":"Auxin biosynthesis and its role in plant development","volume":"61","author":"Y Zhao","year":"2010","journal-title":"Annu Rev Plant Biol"},{"issue":"5","key":"pbio.3003592.ref011","doi-asserted-by":"crossref","first-page":"1410","DOI":"10.1093\/plcell\/koae054","article-title":"An auxin research odyssey: 1989-2023","volume":"36","author":"JD Cohen","year":"2024","journal-title":"Plant Cell"},{"issue":"5","key":"pbio.3003592.ref012","doi-asserted-by":"crossref","first-page":"661","DOI":"10.1016\/S0092-8674(02)00656-6","article-title":"AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis","volume":"108","author":"J Friml","year":"2002","journal-title":"Cell"},{"issue":"6964","key":"pbio.3003592.ref013","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1038\/nature02081","article-title":"Regulation of phyllotaxis by polar auxin transport","volume":"426","author":"D Reinhardt","year":"2003","journal-title":"Nature"},{"issue":"8","key":"pbio.3003592.ref014","doi-asserted-by":"crossref","first-page":"1015","DOI":"10.1101\/gad.1402406","article-title":"Control of leaf vascular patterning by polar auxin transport","volume":"20","author":"E Scarpella","year":"2006","journal-title":"Genes Dev"},{"issue":"6","key":"pbio.3003592.ref015","doi-asserted-by":"crossref","first-page":"1005","DOI":"10.1016\/j.cell.2009.03.001","article-title":"Auxin: a trigger for change in plant development","volume":"136","author":"S Vanneste","year":"2009","journal-title":"Cell"},{"issue":"1","key":"pbio.3003592.ref016","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1104\/pp.17.00765","article-title":"Auxin signaling","volume":"176","author":"O Leyser","year":"2018","journal-title":"Plant Physiol"},{"issue":"1","key":"pbio.3003592.ref017","doi-asserted-by":"crossref","first-page":"164","DOI":"10.1016\/j.cell.2008.01.049","article-title":"Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants","volume":"133","author":"Y Tao","year":"2008","journal-title":"Cell"},{"issue":"1","key":"pbio.3003592.ref018","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/j.cell.2008.01.047","article-title":"TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development","volume":"133","author":"AN Stepanova","year":"2008","journal-title":"Cell"},{"issue":"1","key":"pbio.3003592.ref019","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1104\/pp.109.138859","article-title":"The TRANSPORT INHIBITOR RESPONSE2 gene is required for auxin synthesis and diverse aspects of plant development","volume":"151","author":"M Yamada","year":"2009","journal-title":"Plant Physiol"},{"issue":"45","key":"pbio.3003592.ref020","doi-asserted-by":"crossref","first-page":"18518","DOI":"10.1073\/pnas.1108436108","article-title":"Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASES OF ARABIDOPSIS and YUCCAs in Arabidopsis","volume":"108","author":"C Won","year":"2011","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"45","key":"pbio.3003592.ref021","doi-asserted-by":"crossref","first-page":"18512","DOI":"10.1073\/pnas.1108434108","article-title":"The main auxin biosynthesis pathway in Arabidopsis","volume":"108","author":"K Mashiguchi","year":"2011","journal-title":"Proc Natl Acad Sci USA"},{"issue":"9","key":"pbio.3003592.ref022","doi-asserted-by":"crossref","first-page":"2541","DOI":"10.1093\/jxb\/ert080","article-title":"Auxin biosynthesis and storage forms","volume":"64","author":"DA Korasick","year":"2013","journal-title":"J Exp Bot"},{"issue":"6","key":"pbio.3003592.ref023","doi-asserted-by":"crossref","first-page":"1072","DOI":"10.1093\/pcp\/pcu039","article-title":"Auxin overproduction in shoots cannot rescue auxin deficiencies in Arabidopsis roots","volume":"55","author":"Q Chen","year":"2014","journal-title":"Plant Cell Physiol"},{"issue":"8","key":"pbio.3003592.ref024","doi-asserted-by":"crossref","first-page":"1020","DOI":"10.1038\/s41477-020-0737-9","article-title":"Local auxin biosynthesis is required for root regeneration after wounding","volume":"6","author":"R Matosevich","year":"2020","journal-title":"Nat Plants"},{"issue":"23","key":"pbio.3003592.ref025","doi-asserted-by":"crossref","DOI":"10.1242\/dev.202014","article-title":"Local auxin biosynthesis promotes shoot patterning and stem cell differentiation in Arabidopsis shoot apex","volume":"150","author":"S Yadav","year":"2023","journal-title":"Development"},{"issue":"5935","key":"pbio.3003592.ref026","doi-asserted-by":"crossref","first-page":"1684","DOI":"10.1126\/science.1167324","article-title":"Auxin-dependent patterning and gamete specification in the Arabidopsis female gametophyte","volume":"324","author":"GC Pagnussat","year":"2009","journal-title":"Science"},{"issue":"3","key":"pbio.3003592.ref027","doi-asserted-by":"crossref","first-page":"1406","DOI":"10.1104\/pp.113.214023","article-title":"The MOSS Physcomitrella patens reproductive organ development is highly organized, affected by the two SHI\/STY genes and by the level of active auxin in the SHI\/STY expression domain","volume":"162","author":"K Landberg","year":"2013","journal-title":"Plant Physiol"},{"issue":"1","key":"pbio.3003592.ref028","doi-asserted-by":"crossref","first-page":"1125","DOI":"10.1038\/s41467-017-01252-6","article-title":"Fine-tuning of auxin homeostasis governs the transition from floral stem cell maintenance to gynoecium formation","volume":"8","author":"N Yamaguchi","year":"2017","journal-title":"Nat Commun"},{"issue":"22","key":"pbio.3003592.ref029","doi-asserted-by":"crossref","DOI":"10.1073\/pnas.2101492118","article-title":"Auxin guides germ-cell specification in Arabidopsis anthers","volume":"118","author":"Y Zheng","year":"2021","journal-title":"Proc Natl Acad Sci USA"},{"issue":"3","key":"pbio.3003592.ref030","doi-asserted-by":"crossref","DOI":"10.1016\/j.devcel.2018.09.022","article-title":"Local auxin biosynthesis is a key regulator of plant development","volume":"47","author":"J Brumos","year":"2018","journal-title":"Dev Cell"},{"issue":"6","key":"pbio.3003592.ref031","doi-asserted-by":"crossref","first-page":"1650","DOI":"10.1105\/tpc.15.00065","article-title":"Auxin produced by the indole-3-pyruvic acid pathway regulates development and gemmae dormancy in the liverwort Marchantia polymorpha","volume":"27","author":"DM Eklund","year":"2015","journal-title":"Plant Cell"},{"issue":"2","key":"pbio.3003592.ref032","doi-asserted-by":"crossref","first-page":"845","DOI":"10.1111\/nph.16914","article-title":"Studies of moss reproductive development indicate that auxin biosynthesis in apical stem cells may constitute an ancestral function for focal growth control","volume":"229","author":"K Landberg","year":"2020","journal-title":"New Phytologist"},{"issue":"10","key":"pbio.3003592.ref033","doi-asserted-by":"crossref","first-page":"1642","DOI":"10.1093\/pcp\/pcx095","article-title":"The roles of the sole activator-type auxin response factor in pattern formation of Marchantia polymorpha","volume":"58","author":"H Kato","year":"2017","journal-title":"Plant Cell Physiol"},{"issue":"5","key":"pbio.3003592.ref034","doi-asserted-by":"crossref","DOI":"10.1016\/j.cub.2018.01.063","article-title":"The interrelationships of land plants and the nature of the ancestral embryophyte","volume":"28","author":"MN Puttick","year":"2018","journal-title":"Curr Biol"},{"issue":"19","key":"pbio.3003592.ref035","article-title":"The evolutionary emergence of land plants","volume":"31","author":"PCJ Donoghue","year":"2021","journal-title":"Curr Biol"},{"issue":"1","key":"pbio.3003592.ref036","doi-asserted-by":"crossref","first-page":"23","DOI":"10.3103\/S0095452720010089","article-title":"Endogenous phytohormones of fern Polystichum aculeatum (L.) roth gametophytes at different stages of morphogenesis in vitro culture","volume":"54","author":"IV Kosakivska","year":"2020","journal-title":"Cytol Genet"},{"issue":"12","key":"pbio.3003592.ref037","doi-asserted-by":"crossref","first-page":"2709","DOI":"10.3390\/plants10122709","article-title":"Involvement of auxin biosynthesis and transport in the antheridium and prothalli formation in Lygodium japonicum","volume":"10","author":"N Ohishi","year":"2021","journal-title":"Plants"},{"issue":"20","key":"pbio.3003592.ref038","doi-asserted-by":"crossref","DOI":"10.1242\/dev.203026","article-title":"Analysis of auxin responses in the fern Ceratopteris richardii identifies the developmental phase as a major determinant for response properties","volume":"151","author":"S Woudenberg","year":"2024","journal-title":"Development"},{"issue":"21","key":"pbio.3003592.ref039","doi-asserted-by":"crossref","first-page":"15832","DOI":"10.3390\/ijms242115832","article-title":"Auxin involvement in Ceratopteris gametophyte meristem regeneration","volume":"24","author":"KA Withers","year":"2023","journal-title":"IJMS"},{"issue":"11","key":"pbio.3003592.ref040","first-page":"1963","article-title":"Aux\/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements","volume":"9","author":"T Ulmasov","year":"1997","journal-title":"Plant Cell"},{"issue":"3","key":"pbio.3003592.ref041","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1038\/nmeth.3279","article-title":"Reporters for sensitive and quantitative measurement of auxin response","volume":"12","author":"C-Y Liao","year":"2015","journal-title":"Nat Methods"},{"issue":"15","key":"pbio.3003592.ref042","doi-asserted-by":"crossref","DOI":"10.1016\/j.cub.2024.06.064","article-title":"A conserved GRAS-domain transcriptional regulator links meristem indeterminacy to sex determination in Ceratopteris gametophytes","volume":"34","author":"Y Geng","year":"2024","journal-title":"Curr Biol"},{"issue":"11","key":"pbio.3003592.ref043","doi-asserted-by":"crossref","first-page":"3944","DOI":"10.1105\/tpc.111.089029","article-title":"A small-molecule screen identifies L-kynurenine as a competitive inhibitor of TAA1\/TAR activity in ethylene-directed auxin biosynthesis and root growth in Arabidopsis","volume":"23","author":"W He","year":"2011","journal-title":"Plant Cell"},{"issue":"1","key":"pbio.3003592.ref044","doi-asserted-by":"crossref","first-page":"650","DOI":"10.1038\/s42003-022-03627-y","article-title":"Positional cues and cell division dynamics drive meristem development and archegonium formation in Ceratopteris gametophytes","volume":"5","author":"Y Geng","year":"2022","journal-title":"Commun Biol"},{"issue":"6","key":"pbio.3003592.ref045","doi-asserted-by":"crossref","DOI":"10.15252\/embj.2022113018","article-title":"The birth of a giant: evolutionary insights into the origin of auxin responses in plants","volume":"42","author":"VP Carrillo-Carrasco","year":"2023","journal-title":"EMBO J"},{"issue":"15","key":"pbio.3003592.ref046","doi-asserted-by":"crossref","first-page":"4005","DOI":"10.1073\/pnas.1616387114","article-title":"Symplastic communication spatially directs local auxin biosynthesis to maintain root stem cell niche in Arabidopsis","volume":"114","author":"Y Liu","year":"2017","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"5","key":"pbio.3003592.ref047","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pgen.1005084","article-title":"Auxin-mediated transcriptional system with a minimal set of components is critical for morphogenesis through the life cycle in Marchantia polymorpha","volume":"11","author":"H Kato","year":"2015","journal-title":"PLoS Genet"},{"issue":"3","key":"pbio.3003592.ref048","doi-asserted-by":"crossref","first-page":"2125","DOI":"10.1111\/pce.15286","article-title":"Functions and regulation of HAM family genes in meristems during gametophyte and sporophyte generations","volume":"48","author":"Y Geng","year":"2025","journal-title":"Plant Cell Environ"},{"issue":"3","key":"pbio.3003592.ref049","doi-asserted-by":"crossref","first-page":"352","DOI":"10.1111\/tpj.12399","article-title":"Yucasin is a potent inhibitor of YUCCA , a key enzyme in auxin biosynthesis","volume":"77","author":"T Nishimura","year":"2014","journal-title":"Plant J"},{"issue":"1","key":"pbio.3003592.ref050","doi-asserted-by":"crossref","DOI":"10.1038\/s41598-017-14332-w","article-title":"Yucasin DF, a potent and persistent inhibitor of auxin biosynthesis in plants","volume":"7","author":"S Tsugafune","year":"2017","journal-title":"Sci Rep"},{"issue":"9","key":"pbio.3003592.ref051","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0162169","article-title":"Genome-wide assessment of efficiency and specificity in CRISPR\/Cas9 mediated multiple site targeting in Arabidopsis","volume":"11","author":"BA Peterson","year":"2016","journal-title":"PLoS One"},{"issue":"1","key":"pbio.3003592.ref052","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1111\/tpj.15784","article-title":"Cell growth dynamics in two types of apical meristems in fern gametophytes","volume":"111","author":"X Wu","year":"2022","journal-title":"Plant J"},{"key":"pbio.3003592.ref053","article-title":"InterPro in 2017-beyond protein family and domain annotations","volume":"45","author":"RD Finn","year":"2017","journal-title":"Nucleic Acids Res"}],"container-title":["PLOS Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pbio.3003592","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,1,23]],"date-time":"2026-01-23T18:43:35Z","timestamp":1769193815000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pbio.3003592"}},"subtitle":[],"editor":[{"given":"Mark","family":"Estelle","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2026,1,23]]},"references-count":53,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2026,1,23]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pbio.3003592","relation":{},"ISSN":["1545-7885"],"issn-type":[{"value":"1545-7885","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,1,23]]}}}