{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,1]],"date-time":"2026-09-01T14:48:18Z","timestamp":1788274098972,"version":"build-2803163510"},"reference-count":52,"publisher":"Oxford University Press (OUP)","license":[{"start":{"date-parts":[[2022,1,20]],"date-time":"2022-01-20T00:00:00Z","timestamp":1642636800000},"content-version":"vor","delay-in-days":19,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2022,1,5]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Morphological, genic and epigenetic differences often exist in separate sexes of dioecious and trioecious plants. However, the connections and relationships among them in different breeding systems are still unclear. Papaya has three sex types, which is genetically determined and epigenetically regulated, and was chosen as a model to study sex differentiation. Bisulfite sequencing of genomic DNA extracted from early-stage flowers revealed sex-specific genomic methylation landscapes and seasonally methylome reprogramming processes in dioecious and gynodioecious papaya grown in spring and summer. Extensive methylation of sex-determining region (SDR) was the distinguishing epigenetic characteristics of nascent XY sex chromosomes in papaya. Seasonal methylome reprogramming of early-stage flowers in both dioecy and gynodioecy systems were detected, resulting from transcriptional expression pattern alterations of methylation-modification-related and chromatin-remodeling-related genes, particularly from those genes involved in active demethylation. Genes involved in phytohormone signal transduction pathway in male flowers have played an important role in the formation of male-specific characteristics. These findings enhanced the understanding of the genetic and epigenetic contributions to sex differentiation and the complexity of sex chromosome evolution in trioecious plants.<\/jats:p>","DOI":"10.1093\/hr\/uhab065","type":"journal-article","created":{"date-parts":[[2022,1,20]],"date-time":"2022-01-20T07:23:30Z","timestamp":1642663410000},"source":"Crossref","is-referenced-by-count":19,"title":["Methylation related genes affect sex differentiation in dioecious and gynodioecious papaya"],"prefix":"10.1093","volume":"9","author":[{"given":"Ping","family":"Zhou","sequence":"first","affiliation":[{"name":"Fujian Academy of Agricultural Sciences Fruit Research Institute\uff0c \uff0cFuzhou 350013\uff0cFujian, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaodan","family":"Zhang","sequence":"additional","affiliation":[{"name":"University of Illinois at Urbana-Champaign Department of Plant Biology, , Urbana, IL 61801, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xinyi","family":"Ma","sequence":"additional","affiliation":[{"name":"Fujian Agriculture and Forestry University FAFU and UIUC Joint Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, , Fuzhou 350002, Fujian, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jingjing","family":"Yue","sequence":"additional","affiliation":[{"name":"Fujian Agriculture and Forestry University FAFU and UIUC Joint Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, , Fuzhou 350002, Fujian, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhenyang","family":"Liao","sequence":"additional","affiliation":[{"name":"Fujian Agriculture and Forestry University FAFU and UIUC Joint Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, , Fuzhou 350002, Fujian, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ray","family":"Ming","sequence":"additional","affiliation":[{"name":"University of Illinois at Urbana-Champaign Department of Plant Biology, , Urbana, IL 61801, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2022,1,20]]},"reference":[{"key":"2022092909515043400_ref1","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/j.bbagrm.2016.07.014","article-title":"Gene-regulatory networks controlling inflorescence and flower development in Arabidopsis thaliana","volume":"1860","author":"Wils","year":"2017","journal-title":"Biochim Biophys Acta Gene Regul Mech"},{"key":"2022092909515043400_ref2","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1016\/bs.ctdb.2018.11.007","article-title":"Molecular regulation of flower development","volume":"131","author":"Thomson","year":"2019","journal-title":"Curr Top Dev Biol"},{"key":"2022092909515043400_ref3","doi-asserted-by":"crossref","first-page":"485","DOI":"10.1146\/annurev-arplant-042110-103914","article-title":"Sex chromosomes in land plants","volume":"62","author":"Ming","year":"2011","journal-title":"Annu Rev Plant Biol"},{"key":"2022092909515043400_ref4","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1016\/S1360-1385(97)01012-1","article-title":"Genetics of sex determination in flowering plants","volume":"2","author":"Lebel-Hardenack","year":"1997","journal-title":"Trends Plant Sci"},{"key":"2022092909515043400_ref5","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1016\/j.plantsci.2013.10.018","article-title":"Sex determination in flowering plants: papaya as a model system","volume":"217-218","author":"Aryal","year":"2014","journal-title":"Plant Sci"},{"key":"2022092909515043400_ref6","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1016\/j.plantsci.2015.03.019","article-title":"The genomics of plant sex chromosomes","volume":"236","author":"Vyskot","year":"2015","journal-title":"Plant Sci"},{"key":"2022092909515043400_ref7","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s11295-016-1055-2","article-title":"Transcriptome analysis of the male-to-hermaphrodite sex reversal induced by low temperature in papaya","volume":"12","author":"Lin","year":"2016","journal-title":"Tree Genet Genomes"},{"key":"2022092909515043400_ref8","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1038\/s41438-019-0205-8","article-title":"Auxin regulation involved in gynoecium morphogenesis of papaya flowers","volume":"6","author":"Zhou","year":"2019","journal-title":"Hortic Res"},{"key":"2022092909515043400_ref9","doi-asserted-by":"crossref","first-page":"13710","DOI":"10.1073\/pnas.1207833109","article-title":"Sequencing papaya X and Yh chromosomes reveals molecular basis of incipient sex chromosome evolution","volume":"109","author":"Wang","year":"2012","journal-title":"Proc Natl Acad Sci"},{"key":"2022092909515043400_ref10","first-page":"524","article-title":"Origin and domestication of papaya Yh chromosome","volume":"25","author":"VanBuren","year":"2015","journal-title":"Genome Biol"},{"key":"2022092909515043400_ref11","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1590\/S1984-70332011000200001","article-title":"Seasonal and genetic influences on sex expression in a backcrossed segregating papaya population","volume":"11","author":"Ramos","year":"2011","journal-title":"Crop Breed Applied Biotechnol"},{"key":"2022092909515043400_ref12","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1590\/1984-70332018v18n1a2","article-title":"Estimation of genetic parameters for flower anomalies in papaya","volume":"18","author":"Damasceno Junior","year":"2018","journal-title":"Crop Breed Applied Biotechnol"},{"key":"2022092909515043400_ref13","doi-asserted-by":"crossref","DOI":"10.1590\/1678-4499.20180197","article-title":"Quantification of f loral abnormalities in a population generated from sexual polymorphism aiming at recurrent selection in papaya","volume":"78","author":"Moreira","year":"2019","journal-title":"Bragantia"},{"key":"2022092909515043400_ref14","doi-asserted-by":"crossref","first-page":"1393","DOI":"10.1007\/s00299-012-1255-7","article-title":"Sex-specific DNA methylation and gene expression in andromonoecious poplar","volume":"31","author":"Song","year":"2012","journal-title":"Plant Cell Rep"},{"key":"2022092909515043400_ref15","doi-asserted-by":"crossref","first-page":"45388","DOI":"10.1038\/srep45388","article-title":"Sexual epigenetics: gender-specific methylation of a gene in the sex determining region of Populus balsamifera","volume":"7","author":"Br\u00e4utigam","year":"2017","journal-title":"Sci Rep"},{"key":"2022092909515043400_ref16","doi-asserted-by":"crossref","first-page":"630","DOI":"10.1038\/s41477-020-0672-9","article-title":"A single gene underlies the dynamic evolution of poplar sex determination","volume":"6","author":"M\u00fcller","year":"2020","journal-title":"Nature Plants"},{"key":"2022092909515043400_ref17","doi-asserted-by":"crossref","first-page":"968","DOI":"10.1093\/molbev\/msaa261","article-title":"A general model to explain repeated turnovers of sex determination in the Salicaceae","volume":"38","author":"Yang","year":"2020","journal-title":"Mol Biol Evol"},{"key":"2022092909515043400_ref18","doi-asserted-by":"crossref","first-page":"5893","DOI":"10.1038\/s41467-020-19559-2","article-title":"Evidences for a role of two Y-specific genes in sex determination in Populus deltoides","volume":"11","author":"Xue","year":"2020","journal-title":"Nat Commun"},{"key":"2022092909515043400_ref19","doi-asserted-by":"crossref","first-page":"540","DOI":"10.1186\/s12864-018-4936-y","article-title":"DNA methylation and genetic degeneration of the Y chromosome in the dioecious plant Silene latifolia","volume":"19","author":"Rodr\u00edguez Lorenzo","year":"2018","journal-title":"BMC Genomics"},{"key":"2022092909515043400_ref20","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1007\/s00425-019-03182-7","article-title":"The distribution of epigenetic histone marks differs between the X and Y chromosomes in Silene latifolia","volume":"250","author":"Ba\u010dovsk\u00fd","year":"2019","journal-title":"Planta"},{"key":"2022092909515043400_ref21","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1038\/s41438-020-0298-0","article-title":"DNA methylome and transcriptome landscapes revealed differential characteristics of dioecious flowers in papaya","volume":"7","author":"Zhou","year":"2020","journal-title":"Hortic Res"},{"key":"2022092909515043400_ref22","doi-asserted-by":"crossref","first-page":"D1176","DOI":"10.1093\/nar\/gkt1000","article-title":"P-MITE: a database for plant miniature inverted-repeat transposable elements","volume":"42","author":"Chen","year":"2014","journal-title":"Nucleic Acids Res"},{"key":"2022092909515043400_ref23","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1093\/database\/baw078","article-title":"DPTEdb, an integrative database of transposable elements in dioecious plants","volume":"2016","author":"Li","year":"2016","journal-title":"Database"},{"key":"2022092909515043400_ref24","doi-asserted-by":"crossref","first-page":"4683","DOI":"10.3390\/ijms20194683","article-title":"Active DNA demethylation in plants","volume":"20","author":"Parrilla-Doblas","year":"2019","journal-title":"Int J Mol Sci"},{"key":"2022092909515043400_ref25","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1002\/cbf.3183","article-title":"DNA methylation dynamics in plants and mammals: overview of regulation and dysregulation","volume":"34","author":"Elhamamsy","year":"2016","journal-title":"Cell Biochem Funct"},{"key":"2022092909515043400_ref26","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1038\/s41580-018-0016-z","article-title":"Dynamics and function of DNA methylation in plants","volume":"19","author":"Zhang","year":"2018","journal-title":"Nat Rev Mol Cell Biol"},{"key":"2022092909515043400_ref27","doi-asserted-by":"crossref","first-page":"743","DOI":"10.1042\/EBC20190032","article-title":"Establishment, maintenance, and biological roles of non-CG methylation in plants","volume":"63","author":"Kenchanmane Raju","year":"2019","journal-title":"Essays Biochem"},{"key":"2022092909515043400_ref28","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1007\/s12374-017-0410-7","article-title":"Functional analyses of PtROS1-RNAi in poplars and evaluation of its effect on DNA methylation","volume":"61","author":"Movahedi","year":"2018","journal-title":"J Plant Biol"},{"key":"2022092909515043400_ref29","doi-asserted-by":"crossref","first-page":"11327","DOI":"10.1073\/pnas.1806304115","article-title":"Mutations in the DNA demethylase OsROS1 result in a thickened aleurone and improved nutritional value in rice grains","volume":"115","author":"Liu","year":"2018","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2022092909515043400_ref30","doi-asserted-by":"crossref","first-page":"971","DOI":"10.1016\/j.molcel.2015.01.009","article-title":"The methyl-CpG-binding protein MBD7 facilitates active DNA demethylation to limit DNA hyper-methylation and transcriptional gene silencing","volume":"57","author":"Lang","year":"2015","journal-title":"Mol Cell"},{"key":"2022092909515043400_ref31","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1186\/s12870-019-1670-9","article-title":"High-resolution DNA methylome reveals that demethylation enhances adaptability to continuous cropping comprehensive stress in soybean","volume":"19","author":"Liang","year":"2019","journal-title":"BMC Plant Biol"},{"key":"2022092909515043400_ref32","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1007\/s11103-013-0108-2","article-title":"Sexual dimorphic floral development in dioecious plants revealed by transcriptome, phytohormone, and DNA methylation analysis in Populus tomentosa","volume":"83","author":"Song","year":"2013","journal-title":"Plant Mol Biol"},{"key":"2022092909515043400_ref33","doi-asserted-by":"crossref","first-page":"16641","DOI":"10.1073\/pnas.1906023116","article-title":"Histone acetylation recruits the SWR1 complex to regulate active DNA demethylation in Arabidopsis","volume":"116","author":"Nie","year":"2019","journal-title":"Proc Natl Acad Sci"},{"key":"2022092909515043400_ref34","doi-asserted-by":"crossref","first-page":"7773","DOI":"10.1038\/s41598-018-25963-y","article-title":"Auxin decreases chromatin accessibility through the TIR1\/AFBs auxin signaling pathway in proliferative cells","volume":"8","author":"Hasegawa","year":"2018","journal-title":"Sci Rep"},{"key":"2022092909515043400_ref35","doi-asserted-by":"crossref","first-page":"1085","DOI":"10.1093\/aob\/mcy130","article-title":"Sex and the flower - developmental aspects of sex chromosome evolution","volume":"122","author":"Hobza","year":"2018","journal-title":"Ann Bot"},{"key":"2022092909515043400_ref36","doi-asserted-by":"crossref","first-page":"1938","DOI":"10.1101\/gr.078808.108","article-title":"DNA methylation and heterochromatinization in the male-specific region of the primitive Y chromosome of papaya","volume":"18","author":"Zhang","year":"2008","journal-title":"Genome Res"},{"key":"2022092909515043400_ref37","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1007\/s00438-007-0243-z","article-title":"Chromosomal location and gene paucity of the male specific region on papaya Y chromosome","volume":"278","author":"Yu","year":"2007","journal-title":"Mol Gen Genomics"},{"key":"2022092909515043400_ref38","doi-asserted-by":"crossref","first-page":"413","DOI":"10.1534\/genetics.114.173021","article-title":"Evidence for emergence of sex-determining gene(s) in a Centromeric region in Vasconcellea parviflora","volume":"199","author":"Iovene","year":"2015","journal-title":"Genetics"},{"key":"2022092909515043400_ref39","doi-asserted-by":"crossref","first-page":"3593","DOI":"10.1242\/dev.011510","article-title":"The HECATE genes regulate female reproductive tract development in Arabidopsis thaliana","volume":"134","author":"Gremski","year":"2007","journal-title":"Development"},{"key":"2022092909515043400_ref40","doi-asserted-by":"crossref","first-page":"6836","DOI":"10.1038\/s41598-018-25017-3","article-title":"Conserved and novel responses to cytokinin treatments during flower and fruit development in Brassica napus and Arabidopsis thaliana","volume":"8","author":"Zu\u00f1iga-Mayo","year":"2018","journal-title":"Sci Rep"},{"key":"2022092909515043400_ref41","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pgen.1002506","article-title":"A regulatory network for coordinated flower maturation","volume":"8","author":"Reeves","year":"2012","journal-title":"PLoS Genet"},{"key":"2022092909515043400_ref42","doi-asserted-by":"crossref","first-page":"901","DOI":"10.1186\/s12864-015-2182-0","article-title":"Genome-wide identification and characterization of auxin response factor (ARF) family genes related to flower and fruit development in papaya (Carica papaya L.)","volume":"16","author":"Liu","year":"2015","journal-title":"BMC Genomics"},{"key":"2022092909515043400_ref43","doi-asserted-by":"crossref","first-page":"10576","DOI":"10.1073\/pnas.1904143116","article-title":"Peroxisomal \u03b2-oxidation regulates histone acetylation and DNA methylation in Arabidopsis","volume":"116","author":"Wang","year":"2019","journal-title":"Proc Natl Acad Sci"},{"key":"2022092909515043400_ref44","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1038\/s41438-021-00633-9","article-title":"DNA methylation is involved in sexual differentiation and sex chromosome evolution in the dioecious plant garden asparagus","volume":"8","author":"Li","year":"2021","journal-title":"Hortic Res"},{"key":"2022092909515043400_ref45","first-page":"36","article-title":"Transgenic papaya in Hawaii and beyond","volume":"7","author":"Gonsalves","year":"2004","journal-title":"AgBioforum"},{"key":"2022092909515043400_ref46","first-page":"115","volume-title":"Hawaii\u2019s Transgenic Papaya Story 1978\u20132012: A Personal Account in Genetics and Genomics of Papaya","author":"Gonsalves","year":"2014"},{"key":"2022092909515043400_ref47","doi-asserted-by":"crossref","first-page":"3893","DOI":"10.3390\/v6103893","article-title":"Development and validation of a multiplex reverse transcription PCR assay for simultaneous detection of three papaya viruses","volume":"6","author":"Tuo","year":"2014","journal-title":"Viruses"},{"key":"2022092909515043400_ref48","doi-asserted-by":"crossref","first-page":"1571","DOI":"10.1093\/bioinformatics\/btr167","article-title":"Bismark: a flexible aligner and methylation caller for bisulfite-Seq applications","volume":"27","author":"Krueger","year":"2011","journal-title":"Bioinformatics"},{"key":"2022092909515043400_ref49","doi-asserted-by":"crossref","first-page":"R87","DOI":"10.1186\/gb-2012-13-10-r87","article-title":"methylKit: a comprehensive R package for the analysis of genome-wide DNA methylation profiles","volume":"13","author":"Akalin","year":"2012","journal-title":"Genome Biol"},{"key":"2022092909515043400_ref50","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1093\/bioinformatics\/bts635","article-title":"STAR: ultrafast universal RNA-seq aligner","volume":"29","author":"Dobin","year":"2012","journal-title":"Bioinformatics"},{"key":"2022092909515043400_ref51","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1038\/nbt.2450","article-title":"Differential analysis of gene regulation at transcript resolution with RNA-seq","volume":"31","author":"Trapnell","year":"2013","journal-title":"Nat Biotechnol"},{"key":"2022092909515043400_ref52","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1186\/1471-2105-9-559","article-title":"WGCNA: an R package for weighted correlation network analysis","volume":"9","author":"Langfelder","year":"2008","journal-title":"BMC Bioinform"}],"container-title":["Horticulture Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/hr\/advance-article-pdf\/doi\/10.1093\/hr\/uhab065\/42244425\/uhab065.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/hr\/article-pdf\/doi\/10.1093\/hr\/uhab065\/46167967\/uhab065.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/hr\/article-pdf\/doi\/10.1093\/hr\/uhab065\/46167967\/uhab065.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,9,29]],"date-time":"2022-09-29T10:00:44Z","timestamp":1664445644000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/hr\/article\/doi\/10.1093\/hr\/uhab065\/6511819"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022]]},"references-count":52,"URL":"https:\/\/doi.org\/10.1093\/hr\/uhab065","relation":{},"ISSN":["2052-7276"],"issn-type":[{"value":"2052-7276","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2022]]},"published":{"date-parts":[[2022]]},"article-number":"uhab065"}}