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Quercus suber is a monoecious oak tree with accentuated protandry: in late winter, unisexual male flowers emerge adjacent to the swollen buds, whereas unisexual female flowers emerge in the axils of newly formed leaves formed during spring (4\u20138\u00a0weeks after male flowering). Here, a phylogenetic profiling has led to the identification of cork oak homologs of key floral regulatory genes. The role of these cork oak homologs during flower development was identified with functional studies in Arabidopsis thaliana. The expression profile throughout the year of flower regulators (inducers and repressors), in leaves and buds, suggests that the development of male and female flowers may be preceded by separated induction events. Female flowers are most likely induced during the vegetative flush occurring in spring, whereas male flowers may be induced in early summer. Male flowers stay enclosed within the pre-dormant buds, but complete their development before the vegetative flush of the following year, displaying a long period of anthesis that spans the dormant period. Our results portray a genetic mechanism that may explain similar reproductive habits in other monoecious tree species.<\/jats:p>","DOI":"10.1093\/treephys\/tpaa061","type":"journal-article","created":{"date-parts":[[2020,4,30]],"date-time":"2020-04-30T15:11:27Z","timestamp":1588259487000},"page":"1260-1276","source":"Crossref","is-referenced-by-count":12,"title":["Unisexual flower initiation in the monoecious\n                    <i>Quercus suber<\/i>\n                    L.: a molecular approach"],"prefix":"10.1093","volume":"40","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3798-3154","authenticated-orcid":false,"given":"R\u00f3mulo","family":"Sobral","sequence":"first","affiliation":[{"name":"Biosystems and Integrative Sciences Institute (BioISI), Plant Functional Biology Centre, University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal"}]},{"given":"Helena Gomes","family":"Silva","sequence":"additional","affiliation":[{"name":"Biosystems and Integrative Sciences Institute (BioISI), Plant Functional Biology Centre, University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal"}]},{"given":"Sara","family":"Laranjeira","sequence":"additional","affiliation":[{"name":"Biosystems and Integrative Sciences Institute (BioISI), Plant Functional Biology Centre, University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal"}]},{"given":"Joana","family":"Magalh\u00e3es","sequence":"additional","affiliation":[{"name":"Biosystems and Integrative Sciences Institute (BioISI), Plant Functional Biology Centre, University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal"}]},{"given":"Lu\u00eds","family":"Andrade","sequence":"additional","affiliation":[{"name":"Biosystems and Integrative Sciences Institute (BioISI), Plant Functional Biology Centre, University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal"}]},{"given":"Ana Teresa","family":"Alhinho","sequence":"additional","affiliation":[{"name":"Biosystems and Integrative Sciences Institute (BioISI), Plant Functional Biology Centre, University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9032-5690","authenticated-orcid":false,"given":"Maria Manuela Ribeiro","family":"Costa","sequence":"additional","affiliation":[{"name":"Biosystems and Integrative Sciences Institute (BioISI), Plant Functional Biology Centre, University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal"}]}],"member":"286","published-online":{"date-parts":[[2020,5,5]]},"reference":[{"key":"2021050500063755000_ref1","doi-asserted-by":"crossref","first-page":"1052","DOI":"10.1126\/science.1115983","article-title":"FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex","volume":"309","author":"Abe","year":"2005","journal-title":"Science"},{"key":"2021050500063755000_ref2","doi-asserted-by":"crossref","first-page":"717","DOI":"10.1016\/j.cub.2014.02.037","article-title":"A tree ortholog of APETALA1 mediates photoperiodic control of seasonal growth","volume":"24","author":"Azeez","year":"2014","journal-title":"Curr Biol"},{"key":"2021050500063755000_ref3","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1007\/BF02772582","article-title":"An improved method for high-quality RNA isolation from needles of adult maritime pine trees","volume":"21","author":"Azevedo","year":"2003","journal-title":"Plant Mol Biol Report"},{"key":"2021050500063755000_ref4","doi-asserted-by":"crossref","first-page":"699","DOI":"10.1111\/j.1469-8137.2007.02202.x","article-title":"Mating patterns and pollen dispersal in a heterodichogamous tree, Juglans mandshurica (Juglandaceae)","volume":"176","author":"Bai","year":"2007","journal-title":"New Phytol"},{"key":"2021050500063755000_ref5","doi-asserted-by":"crossref","first-page":"464","DOI":"10.1016\/S1055-7903(03)00207-0","article-title":"The major clades of MADS-box genes and their role in the development and evolution of flowering plants","volume":"29","author":"Becker","year":"2003","journal-title":"Mol Phylogenet Evol"},{"key":"2021050500063755000_ref6","doi-asserted-by":"crossref","first-page":"3835","DOI":"10.1242\/dev.124.19.3835","article-title":"LEAFY expression and flower initiation in Arabidopsis","volume":"124","author":"Bl\u00e1zquez","year":"1997","journal-title":"Development"},{"key":"2021050500063755000_ref7","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1007\/s004970050162","article-title":"Sexual reproduction in the cork oak (Quercus suber L.). 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The progamic phase","volume":"11","author":"Boavida","year":"1999","journal-title":"Sex Plant Reprod"},{"key":"2021050500063755000_ref8","doi-asserted-by":"crossref","first-page":"1040","DOI":"10.1126\/science.1126038","article-title":"CO\/FT regulatory module controls timing of flowering and seasonal growth cessation in trees","volume":"312","author":"B\u00f6hlenius","year":"2006","journal-title":"Science"},{"key":"2021050500063755000_ref10","first-page":"37","article-title":"Genes directing flower development in Arabidopsis","volume":"1","author":"Bowman","year":"1989","journal-title":"Plant Cell"},{"key":"2021050500063755000_ref9","doi-asserted-by":"crossref","first-page":"721","DOI":"10.1242\/dev.119.3.721","article-title":"Control of flower development in Arabidopsis thaliana by APETALA1 and interacting genes","volume":"119","author":"Bowman","year":"1993","journal-title":"Development"},{"key":"2021050500063755000_ref11","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1007\/BF02670468","article-title":"A simple and efficient method for isolating RNA from pine trees","volume":"11","author":"Chang","year":"1993","journal-title":"Plant Mol Biol Report"},{"key":"2021050500063755000_ref12","doi-asserted-by":"crossref","first-page":"735","DOI":"10.1046\/j.1365-313x.1998.00343.x","article-title":"Floral dip: a simplified method for agrobacterium-mediated transformation of Arabidopsis thaliana","volume":"16","author":"Clough","year":"1998","journal-title":"Plant J"},{"key":"2021050500063755000_ref13","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1038\/353031a0","article-title":"The war of the whorls: genetic interactions controlling flower development","volume":"353","author":"Coen","year":"1991","journal-title":"Nature"},{"key":"2021050500063755000_ref14","doi-asserted-by":"crossref","first-page":"723","DOI":"10.1111\/j.1469-8137.2006.01721.x","article-title":"Transcriptome analysis of bud burst in sessile oak (Quercus petraea)","volume":"170","author":"Derory","year":"2006","journal-title":"New Phytol"},{"key":"2021050500063755000_ref15","doi-asserted-by":"crossref","first-page":"577","DOI":"10.1007\/s11103-013-0026-3","article-title":"Induction of endodormancy in crown buds of leafy spurge (Euphorbia esula L.) implicates a role for ethylene and cross-talk between photoperiod and temperature","volume":"81","author":"Do\u011framac\u0131","year":"2013","journal-title":"Plant Mol Biol"},{"key":"2021050500063755000_ref16","doi-asserted-by":"crossref","first-page":"114","DOI":"10.1051\/forest:19930710","article-title":"Ecological aspects of the floral phenology of the cork-oak (Q. suber L): why do annual and biennial biotypes appear?","volume":"50","author":"Elena-Rossello","year":"1993","journal-title":"Ann For Sci"},{"key":"2021050500063755000_ref17","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1007\/s11248-005-6632-3","article-title":"Ectopic expression of an FT homolog from citrus confers an early flowering phenotype on trifoliate orange (Poncirus trifoliata L. 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spurge","volume":"73","author":"Horvath","year":"2010","journal-title":"Plant Mol Biol"},{"key":"2021050500063755000_ref27","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fpls.2015.00989","article-title":"Extensive transcriptome changes during natural onset and release of vegetative bud dormancy in Populus","volume":"6","author":"Howe","year":"2015","journal-title":"Front Plant Sci"},{"key":"2021050500063755000_ref29","doi-asserted-by":"crossref","first-page":"1846","DOI":"10.1105\/tpc.106.041038","article-title":"Poplar FT2 shortens the juvenile phase and promotes seasonal flowering","volume":"18","author":"Hsu","year":"2006","journal-title":"Plant Cell"},{"key":"2021050500063755000_ref28","doi-asserted-by":"crossref","first-page":"10756","DOI":"10.1073\/pnas.1104713108","article-title":"FLOWERING LOCUS T duplication coordinates reproductive and vegetative growth in perennial poplar","volume":"108","author":"Hsu","year":"2011","journal-title":"Proc Natl Acad Sci 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Bot"},{"key":"2021050500063755000_ref33","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1186\/1471-2229-10-25","article-title":"Identification of genes associated with growth cessation and bud dormancy entrance using a dormancy-incapable tree mutant","volume":"10","author":"Jim\u00e9nez","year":"2010","journal-title":"BMC Plant Biol"},{"key":"2021050500063755000_ref34","doi-asserted-by":"crossref","first-page":"e1002361","DOI":"10.1371\/journal.pgen.1002361","article-title":"Short day-mediated cessation of growth requires the downregulation of AINTEGUMENTALIKE1 transcription factor in hybrid aspen","volume":"7","author":"Karlberg","year":"2011","journal-title":"PLoS Genet"},{"key":"2021050500063755000_ref35","doi-asserted-by":"crossref","first-page":"792","DOI":"10.1104\/pp.113.224139","article-title":"FLOWERING LOCUS T\/TERMINAL FLOWER1-like genes affect growth rhythm and bud set in Norway spruce","volume":"163","author":"Karlgren","year":"2013","journal-title":"Plant Physiol"},{"key":"2021050500063755000_ref36","doi-asserted-by":"crossref","first-page":"1962","DOI":"10.1002\/j.1537-2197.1985.tb08470.x","article-title":"Reproductive morphology of Quercus (Fagaceae)","volume":"72","author":"Kaul","year":"1985","journal-title":"Am J Bot"},{"key":"2021050500063755000_ref37","doi-asserted-by":"crossref","first-page":"2490","DOI":"10.1093\/jxb\/eraa057","article-title":"Genetic and molecular basis of floral induction in Arabidopsis thaliana","volume":"71","author":"Kinoshita","year":"2020","journal-title":"J Exp Bot"},{"key":"2021050500063755000_ref38","doi-asserted-by":"crossref","first-page":"808","DOI":"10.1111\/pbi.12431","article-title":"FT overexpression induces precocious flowering and normal reproductive development in eucalyptus","volume":"14","author":"Klocko","year":"2016","journal-title":"Plant Biotechnol 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Batsch] have distinct seasonal and photoperiodic expression patterns","volume":"60","author":"Li","year":"2009","journal-title":"J Exp Bot"},{"key":"2021050500063755000_ref45","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1007\/s11103-010-9660-1","article-title":"PtSVP, an SVP homolog from trifoliate orange (Poncirus trifoliata L. 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Dire\u00e7ao Geral dos Servi\u00e7os Florestais e Aqu\u00edcolas Lisbon, Portugal","author":"Natividade","year":"1950"},{"key":"2021050500063755000_ref55","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1038\/nrg2931","article-title":"Forest tree genomics: growing resources and applications","volume":"12","author":"Neale","year":"2011","journal-title":"Nat Rev Genet"},{"key":"2021050500063755000_ref56","doi-asserted-by":"crossref","first-page":"3915","DOI":"10.1093\/jxb\/erm246","article-title":"Increased CiFT abundance in the stem correlates with floral induction by low temperature in Satsuma mandarin (Citrus unshiu Marc)","volume":"58","author":"Nishikawa","year":"2007","journal-title":"J Exp Bot"},{"key":"2021050500063755000_ref57","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1007\/BF00197868","article-title":"Phenological and growth patterns of the Mediterranean oak Quercus suber L","volume":"9","author":"Oliveira","year":"1994","journal-title":"Trees"},{"key":"2021050500063755000_ref58","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1038\/26903","article-title":"A genetic framework for floral patterning","volume":"395","author":"Parcy","year":"1998","journal-title":"Nature"},{"key":"2021050500063755000_ref59","doi-asserted-by":"crossref","first-page":"200","DOI":"10.1038\/35012103","article-title":"B and C floral organ identity functions require SEPALLATA MADS-box genes","volume":"405","author":"Pelaz","year":"2000","journal-title":"Nature"},{"key":"2021050500063755000_ref60","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1038\/85719","article-title":"Constitutive expression of Arabidopsis LEAFY or APETALA1 genes in citrus reduces their generation time","volume":"19","author":"Pe\u00f1a","year":"2001","journal-title":"Nat 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Res","author":"Shuhart","year":"1927"},{"key":"2021050500063755000_ref79","doi-asserted-by":"crossref","first-page":"10368","DOI":"10.1038\/s41598-017-10732-0","article-title":"Role of floral organ identity genes in the development of unisexual flowers of Quercus suber L","volume":"7","author":"Sobral","year":"2017","journal-title":"Sci Rep"},{"key":"2021050500063755000_ref80","doi-asserted-by":"crossref","first-page":"1116","DOI":"10.1038\/35074138","article-title":"CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis","volume":"410","author":"Su\u00e1rez-L\u00f3pez","year":"2001","journal-title":"Nature"},{"key":"2021050500063755000_ref81","doi-asserted-by":"crossref","first-page":"549","DOI":"10.1111\/j.1365-313X.2012.04919.x","article-title":"Genome-wide identification of SOC1 and SVP targets during the floral transition in Arabidopsis","volume":"70","author":"Tao","year":"2012","journal-title":"Plant 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photoperiodic growth control and adaptive response pathways","volume":"112","author":"Tylewicz","year":"2015","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021050500063755000_ref86","first-page":"93","article-title":"Phenological phases of Quercus suber L. flowering","volume":"3","author":"Varela","year":"1996","journal-title":"For Genet"},{"key":"2021050500063755000_ref87","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1186\/1471-2229-11-72","article-title":"Identification and characterization of flowering genes in kiwifruit: sequence conservation and role in kiwifruit flower development","volume":"11","author":"Varkonyi-Gasic","year":"2011","journal-title":"BMC Plant Biol"},{"key":"2021050500063755000_ref88","doi-asserted-by":"crossref","first-page":"1539","DOI":"10.1093\/jxb\/erx044","article-title":"Three FT and multiple CEN and BFT genes regulate maturity, flowering, and vegetative phenology in 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Et Zucc (Lauraceae)","volume":"31","author":"Watanabe","year":"2016","journal-title":"Plant Spec Biol"},{"key":"2021050500063755000_ref94","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1038\/377495a0","article-title":"A developmental switch sufficient for flower initiation in diverse plants","volume":"377","author":"Weigel","year":"1995","journal-title":"Nature"},{"key":"2021050500063755000_ref95","doi-asserted-by":"crossref","first-page":"529","DOI":"10.2307\/2479045","article-title":"Pollination experiments with anonas","volume":"37","author":"Wester","year":"1910","journal-title":"Bull Torrey Bot Club"},{"key":"2021050500063755000_ref96","doi-asserted-by":"crossref","first-page":"1056","DOI":"10.1126\/science.1114358","article-title":"Integration of spatial and temporal information during floral induction in Arabidopsis","volume":"309","author":"Wigge","year":"2005","journal-title":"Science"},{"key":"2021050500063755000_ref97","doi-asserted-by":"crossref","first-page":"430","DOI":"10.1016\/j.devcel.2011.03.019","article-title":"LEAFY target genes reveal floral regulatory logic, cis motifs, and a link to biotic stimulus response","volume":"20","author":"Winter","year":"2011","journal-title":"Dev Cell"},{"key":"2021050500063755000_ref98","first-page":"1049","article-title":"The development of the pecan nut from flower to maturity","volume-title":"J Agric Res","author":"Woodroof","year":"1927"},{"key":"2021050500063755000_ref100","doi-asserted-by":"crossref","first-page":"3539","DOI":"10.1242\/dev.02521","article-title":"Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target 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