{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T02:53:24Z","timestamp":1790823204905,"version":"4.1.0"},"reference-count":51,"publisher":"Oxford University Press (OUP)","issue":"2","license":[{"start":{"date-parts":[[2020,2,18]],"date-time":"2020-02-18T00:00:00Z","timestamp":1581984000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"name":"Department of Organismic and Evolutionary Biology, Harvard University"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2020,7,24]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:sec><jats:title>Background and Aims<\/jats:title><jats:p>The ranunculid model system Aquilegia is notable for the presence of a fifth type of floral organ, the staminode, which appears to be the result of sterilization and modification of the two innermost whorls of stamens. Previous studies have found that the genetic basis for the identity of this new organ is the result of sub- and neofunctionalization of floral organ identity gene paralogues; however, we do not know the extent of developmental and molecular divergence between stamens and staminodes.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>We used histological techniques to describe the development of the Aquilegia coerulea \u2018Origami\u2019 staminode relative to the stamen filament. These results have been compared with four other Aquilegia species and the closely related genera Urophysa and Semiaquilegia. As a complement, RNA sequencing has been conducted at two developmental stages to investigate the molecular divergence of the stamen filaments and staminodes in A. coerulea \u2018Origami\u2019.<\/jats:p><\/jats:sec><jats:sec><jats:title>Key Results<\/jats:title><jats:p>Our developmental study has revealed novel features of staminode development, most notably a physical interaction along the lateral margin of adjacent organs that appears to mediate their adhesion. In addition, patterns of abaxial\/adaxial differentiation are observed in staminodes but not stamen filaments, including asymmetric lignification of the adaxial epidermis in the staminodes. The comparative transcriptomics are consistent with the observed lignification of staminodes and indicate that stamen filaments are radialized due to overexpression of adaxial identity, while the staminodes are expanded due to the balanced presence of abaxial identity.<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusions<\/jats:title><jats:p>These findings suggest a model in which the novel staminode identity programme interacts with the abaxial\/adaxial identity pathways to produce two whorls of laterally expanded organs that are highly differentiated along their abaxial\/adaxial axis. While the ecological function of Aquilegia staminodes remains to be determined, these data are consistent with a role in protecting the early carpels from herbivory and\/or pathogens.<\/jats:p><\/jats:sec>","DOI":"10.1093\/aob\/mcaa029","type":"journal-article","created":{"date-parts":[[2020,2,17]],"date-time":"2020-02-17T20:13:49Z","timestamp":1581970429000},"page":"231-243","source":"Crossref","is-referenced-by-count":16,"title":["Developmental and molecular characterization of novel staminodes in Aquilegia"],"prefix":"10.1093","volume":"126","author":[{"given":"Clara","family":"Meaders","sequence":"first","affiliation":[{"name":"Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA"},{"name":"Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ya","family":"Min","sequence":"additional","affiliation":[{"name":"Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katherine J","family":"Freedberg","sequence":"additional","affiliation":[{"name":"Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA"},{"name":"Tufts University School of Medicine, Boston, MA, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elena","family":"Kramer","sequence":"additional","affiliation":[{"name":"Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2020,2,18]]},"reference":[{"key":"2020072410564589600_CIT0001","doi-asserted-by":"crossref","first-page":"6194","DOI":"10.1038\/srep06194","article-title":"Co-option of the polarity gene network shapes filament morphology in angiosperms","volume":"4","author":"de Almeida","year":"2014","journal-title":"Scientific Reports"},{"key":"2020072410564589600_CIT0003","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1093\/bioinformatics\/btu638","article-title":"HTSeq \u2013 a Python framework to work with high-throughput sequencing data","volume":"31","author":"Anders","year":"2015","journal-title":"Bioinformatics"},{"key":"2020072410564589600_CIT0004","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1186\/2041-9139-2-4","article-title":"The control of flowering time in the lower eudicot Aquilegia formosa","volume":"2","author":"Ballerini","year":"2011","journal-title":"EvoDevo"},{"key":"2020072410564589600_CIT0005","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/S0074-7696(08)61609-5","article-title":"Lignification in plant cell walls","volume":"176","author":"Barcelo","year":"1997","journal-title":"International Review of Cytology"},{"key":"2020072410564589600_CIT0006","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1007\/s00606-009-0243-z","article-title":"Extended phylogeny of Aquilegia: the biogeographical and ecological patterns of two simultaneous but contrasting radiations","volume":"284","author":"Bastida","year":"2010","journal-title":"Plant Systematics and Evolution"},{"key":"2020072410564589600_CIT0007","volume-title":"Buttercups, waterlilies, and their relatives: (the order Ranales) in British Columbia","author":"Brayshaw","year":"1989"},{"key":"2020072410564589600_CIT0008","doi-asserted-by":"crossref","first-page":"145","DOI":"10.2307\/4107428","article-title":"A revision of Isopyrum (Ranunculaceae) and its nearer allies","volume":"5","author":"Drummond","year":"1920","journal-title":"Bulletin of Miscellaneous Information (Royal Botanic Gardens, Kew)"},{"key":"2020072410564589600_CIT0009","volume-title":"Diversity and evolutionary biology of tropical flowers","author":"Endress","year":"1994"},{"key":"2020072410564589600_CIT0010","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1016\/j.ode.2005.09.005","article-title":"Elaborate petals and staminodes in eudicots: diversity, function, and evolution","volume":"6","author":"Endress","year":"2006","journal-title":"Organisms Diversity and Evolution"},{"key":"2020072410564589600_CIT0011","doi-asserted-by":"crossref","first-page":"1251","DOI":"10.1016\/S0960-9822(01)00392-X","article-title":"Establishment of polarity in lateral organs of plants","volume":"11","author":"Eshed","year":"2001","journal-title":"Current Biology"},{"key":"2020072410564589600_CIT0013","doi-asserted-by":"crossref","first-page":"1\u201318","DOI":"10.1002\/dvg.22728","article-title":"Adaxial\u2013abaxial polarity: the developmental basis of leaf shape diversity","volume":"52","author":"Fukushima","year":"2014","journal-title":"Genesis"},{"key":"2020072410564589600_CIT0014","doi-asserted-by":"crossref","DOI":"10.5962\/bhl.title.127448","volume-title":"Versuch die metamorphose der pflanzen zu erklaren","author":"Goethe","year":"1790"},{"key":"2020072410564589600_CIT0015","doi-asserted-by":"crossref","first-page":"5129","DOI":"10.1073\/pnas.91.11.5129","article-title":"Columbines \u2013 a geographically widespread species flock","volume":"91","author":"Hodges","year":"1994","journal-title":"Proceedings of the National Academy of Sciences, USA"},{"key":"2020072410564589600_CIT0017","doi-asserted-by":"crossref","first-page":"222","DOI":"10.1016\/j.cell.2016.05.002","article-title":"Morphomechanical innovation drives explosive seed dispersal","volume":"166","author":"Hofhuis","year":"2016","journal-title":"Cell"},{"key":"2020072410564589600_CIT0018","doi-asserted-by":"crossref","first-page":"617","DOI":"10.1016\/S0076-6879(05)95032-5","article-title":"Methods for studying the evolution of plant reproductive structures: comparative gene expression techniques","volume":"395","author":"Kramer","year":"2005","journal-title":"Methods in Enzymology"},{"key":"2020072410564589600_CIT0019","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1016\/bs.ctdb.2018.11.015","article-title":"Plus \u00e7a change, plus c\u2019est la m\u00eame chose: the developmental evolution of flowers","volume":"131","author":"Kramer","year":"2019","journal-title":"Current Topics in Developmental Biology"},{"key":"2020072410564589600_CIT0020","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1086\/344694","article-title":"Complex patterns of gene duplication in the APETALA3 and PISTILLATA lineages of the Ranunculaceae","volume":"164","author":"Kramer","year":"2003","journal-title":"International Journal of Plant Science"},{"key":"2020072410564589600_CIT0021","doi-asserted-by":"crossref","first-page":"750","DOI":"10.1105\/tpc.107.050385","article-title":"Elaboration of B gene function to include the identity of novel floral organs in the lower eudicot Aquilegia (Ranunculaceae)","volume":"19","author":"Kramer","year":"2007","journal-title":"The Plant Cell"},{"key":"2020072410564589600_CIT0022","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1046\/j.1365-313X.2003.01824.x","article-title":"Isolation and characterization of the Arabidopsis organ fusion gene HOTHEAD","volume":"35","author":"Krolikowski","year":"2003","journal-title":"The Plant Journal"},{"key":"2020072410564589600_CIT0023","doi-asserted-by":"crossref","first-page":"2947","DOI":"10.1093\/bioinformatics\/btm404","article-title":"Clustal W and clustal X version 2.0","volume":"23","author":"Larkin","year":"2007","journal-title":"Bioinformatics"},{"key":"2020072410564589600_CIT0024","doi-asserted-by":"crossref","first-page":"5021","DOI":"10.1242\/dev.02067","article-title":"Recruitment of CRABS CLAW to promote nectary development within the eudicot clade","volume":"132","author":"Lee","year":"2005","journal-title":"Development"},{"key":"2020072410564589600_CIT0025","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1016\/j.semcdb.2009.11.019","article-title":"The ABC model and the diversification of floral organ identity","volume":"21","author":"Litt","year":"2010","journal-title":"Seminars in Cell and Developmental Biology"},{"key":"2020072410564589600_CIT0026","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1016\/S0092-8674(00)81523-8","article-title":"Control of organ asymmetry in flowers of Antirrhinum","volume":"99","author":"Luo","year":"1999","journal-title":"Cell"},{"key":"2020072410564589600_CIT0027","doi-asserted-by":"crossref","first-page":"D183","DOI":"10.1093\/nar\/gkw1138","article-title":"PANTHER version 11: expanded annotation data from Gene Ontology and Reactome pathways, and data analysis tool enhancements","volume":"45","author":"Mi","year":"2016","journal-title":"Nucleic Acids Research"},{"key":"2020072410564589600_CIT0028","doi-asserted-by":"crossref","first-page":"358","DOI":"10.3389\/fpls.2014.00358","article-title":"The role of the secondary cell wall in plant resistance to pathogens","volume":"5","author":"Miedes","year":"2014","journal-title":"Frontiers in Plant Science"},{"key":"2020072410564589600_CIT0029","doi-asserted-by":"crossref","DOI":"10.1145\/2016741.2016785","article-title":"The CIPRES science gateway: a community resource for phylogenetic analyses","volume-title":"TG \u201811: Proceedings of the 2011 TeraGrid Conference: Extreme Digital Discovery","author":"Miller","year":"2011"},{"key":"2020072410564589600_CIT0030","doi-asserted-by":"crossref","first-page":"536","DOI":"10.1111\/nph.14282","article-title":"The Aquilegia JAGGED homolog promotes proliferation of adaxial cell types in both leaves and stems","volume":"216","author":"Min","year":"2017","journal-title":"New Phytologist"},{"key":"2020072410564589600_CIT0031","doi-asserted-by":"crossref","first-page":"114","DOI":"10.1016\/j.pbi.2016.10.010","article-title":"Cells, walls, and endless forms","volume":"34","author":"Monniaux","year":"2016","journal-title":"Current Opinion in Plant Biology"},{"key":"2020072410564589600_CIT0032","first-page":"1","article-title":"Aquilegia: the cultivated and wild columbines","volume":"7","author":"Munz","year":"1946","journal-title":"Gentes Herbarium"},{"key":"2020072410564589600_CIT0033","doi-asserted-by":"crossref","first-page":"368","DOI":"10.1007\/BF01248568","article-title":"Polychromatic staining of plant cell walls by toluidine blue O","volume":"59","author":"O\u2019Brien","year":"1964","journal-title":"Protoplasma"},{"key":"2020072410564589600_CIT0034","doi-asserted-by":"crossref","first-page":"1773","DOI":"10.1104\/pp.109.143388","article-title":"The Arabidopsis DCR encoding a soluble BAHD acyltransferase is required for cutin polyester formation and seed hydration properties","volume":"151","author":"Panikashvili","year":"2009","journal-title":"Plant Physiology"},{"key":"2020072410564589600_CIT0035","doi-asserted-by":"crossref","first-page":"1640","DOI":"10.1098\/rspb.2011.1873","article-title":"Evolution of spur-length diversity in Aquilegia petals is achieved solely through cell-shape anisotropy","volume":"279","author":"Puzey","year":"2012","journal-title":"Proceedings of the Royal Society B: Biological Science"},{"key":"2020072410564589600_CIT0036","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1007\/s00606-010-0399-6","article-title":"Floral development of Dichocarpum, Thalictrum, and Aquilegia (Thalictroideae, Ranunculaceae)","volume":"292","author":"Ren","year":"2011","journal-title":"Plant Systematics and Evolution"},{"key":"2020072410564589600_CIT0037","doi-asserted-by":"crossref","first-page":"529","DOI":"10.1186\/s12859-017-1934-z","article-title":"ImageJ2: ImageJ for the next generation of scientific image data","volume":"18","author":"Rueden","year":"2017","journal-title":"BMC Bioinformatics"},{"key":"2020072410564589600_CIT0038","volume-title":"Plant microtechnique and microscopy","author":"Ruzin","year":"1999"},{"key":"2020072410564589600_CIT0039","doi-asserted-by":"crossref","first-page":"949","DOI":"10.1111\/nph.12078","article-title":"Sub- and neofunctionalization of APETALA3 paralogs have contributed to the evolution of novel floral organ identity in Aquilegia (columbine, Ranunculaceae)","volume":"197","author":"Sharma","year":"2013","journal-title":"New Phytologist"},{"key":"2020072410564589600_CIT0040","doi-asserted-by":"crossref","first-page":"870","DOI":"10.1111\/j.1469-8137.2011.03744.x","article-title":"Petal-specific subfunctionalization of an APETALA3 paralog in the Ranunculales and its implications for petal evolution","volume":"190","author":"Sharma","year":"2011","journal-title":"New Phytologist"},{"key":"2020072410564589600_CIT0041","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/j.pbi.2013.10.006","article-title":"Understanding the development and evolution of novel floral form in Aquilegia","volume":"17","author":"Sharma","year":"2014","journal-title":"Current Opinion in Plant Biology"},{"key":"2020072410564589600_CIT0042","doi-asserted-by":"crossref","first-page":"4117","DOI":"10.1242\/dev.126.18.4117","article-title":"Members of the YABBY gene family specify abaxial cell fate in Arabidopsis","volume":"126","author":"Siegfried","year":"1999","journal-title":"Development"},{"key":"2020072410564589600_CIT0043","doi-asserted-by":"crossref","first-page":"1312","DOI":"10.1093\/bioinformatics\/btu033","article-title":"RAxML Version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies","volume":"30","author":"Stamatakis","year":"2014","journal-title":"Bioinformatics"},{"key":"2020072410564589600_CIT0044","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1007\/s00438-017-1392-3","article-title":"RNA-Seq analysis reveals the distinctive adaxial\u2013abaxial polarity in the asymmetric one-theca stamen of Canna indica","volume":"293","author":"Tian","year":"2018","journal-title":"Molecular Genetics and Genomics"},{"key":"2020072410564589600_CIT0045","doi-asserted-by":"crossref","first-page":"1452","DOI":"10.1105\/tpc.110.075291","article-title":"Distinct regulation of adaxial\u2013abaxial polarity in anther patterning in rice","volume":"22","author":"Toriba","year":"2010","journal-title":"The Plant Cell"},{"key":"2020072410564589600_CIT0046","doi-asserted-by":"crossref","first-page":"430","DOI":"10.4161\/psb.6.3.14494","article-title":"Common and distinct mechanisms underlying the establishment of adaxial and abaxial polarity in stamen and leaf development","volume":"6","author":"Toriba","year":"2011","journal-title":"Plant Signaling and Behavior"},{"key":"2020072410564589600_CIT0047","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1046\/j.1525-142x.2001.003002109.x","article-title":"Developmental system drift and flexibility in evolutionary trajectories","volume":"3","author":"True","year":"2001","journal-title":"Evolution and Development"},{"key":"2020072410564589600_CIT0048","doi-asserted-by":"crossref","first-page":"557","DOI":"10.1086\/429848","article-title":"Floral ontogeny of Aquilegia, Semiaquilegia, and Isopyrum (Ranunculaceae)","volume":"166","author":"Tucker","year":"2005","journal-title":"International Journal of Plant Science"},{"key":"2020072410564589600_CIT0049","doi-asserted-by":"crossref","first-page":"2143","DOI":"10.1242\/dev.121.7.2143","article-title":"PHANTASTICA \u2013 a gene required for dorsoventrality of leaves in Antirrhinum majus","volume":"121","author":"Waites","year":"1995","journal-title":"Development"},{"key":"2020072410564589600_CIT0050","doi-asserted-by":"crossref","first-page":"1367","DOI":"10.2307\/2656866","article-title":"The evolution of staminodes in angiosperms: patterns of stamen reduction, loss, and functional re-invention","volume":"87","author":"Walker-Larsen","year":"2000","journal-title":"American Journal of Botant"},{"key":"2020072410564589600_CIT0051","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1104\/pp.113.222737","article-title":"The formation and function of plant cuticles","volume":"163","author":"Yeats","year":"2013","journal-title":"Plant Physiology"},{"key":"2020072410564589600_CIT0052","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1016\/j.ympev.2019.02.024","article-title":"Chloroplast genomic data provide new and robust insights into the phylogeny and evolution of the Ranunculaceae","volume":"135","author":"Zhai","year":"2019","journal-title":"Molecular Phylogenetics and Evolution"},{"key":"2020072410564589600_CIT0053","doi-asserted-by":"crossref","first-page":"5074","DOI":"10.1073\/pnas.1219690110","article-title":"Disruption of the petal identity gene APETALA3-3 is highly correlated with loss of petals within the buttercup family (Ranunculaceae)","volume":"110","author":"Zhang","year":"2013","journal-title":"Proceedings of the National Acadamy of Sciences, USA"},{"key":"2020072410564589600_CIT0054","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1139\/cjb-2015-0232","article-title":"Floral organogenesis in Urophysa rockii, a rediscovered endangered and rare species of Ranunculaceae","volume":"94","author":"Zhao","year":"2016","journal-title":"Botany"}],"container-title":["Annals of Botany"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/aob\/advance-article-pdf\/doi\/10.1093\/aob\/mcaa029\/32517378\/mcaa029.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/aob\/article-pdf\/126\/2\/231\/33529029\/mcaa029.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/aob\/article-pdf\/126\/2\/231\/33529029\/mcaa029.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,10,15]],"date-time":"2022-10-15T20:17:48Z","timestamp":1665865068000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/aob\/article\/126\/2\/231\/5739953"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,2,18]]},"references-count":51,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2020,2,18]]},"published-print":{"date-parts":[[2020,7,24]]}},"URL":"https:\/\/doi.org\/10.1093\/aob\/mcaa029","relation":{},"ISSN":["0305-7364","1095-8290"],"issn-type":[{"value":"0305-7364","type":"print"},{"value":"1095-8290","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2020,8,1]]},"published":{"date-parts":[[2020,2,18]]}}}