title: Lineage-specific gene radiations underlie the evolution of novel betalain pigmentation in Caryophyllales.
abstract: Betalain pigments are unique to the Caryophyllales and structurally and biosynthetically distinct from anthocyanins. Two key enzymes within the betalain synthesis pathway have been identified: 4,5-dioxygenase (DODA) that catalyzes the formation of betalamic acid and CYP76AD1, a cytochrome P450 gene that catalyzes the formation of cyclo-DOPA. We performed phylogenetic analyses to reveal the evolutionary history of the DODA and CYP76AD1 lineages and in the context of an ancestral reconstruction of pigment states we explored the evolution of these genes in relation to the complex evolution of pigments in Caryophylalles. Duplications within the CYP76AD1 and DODA lineages arose just before the origin of betalain pigmentation in the core Caryophyllales. The duplications gave rise to DODA-α and CYP76AD1-α isoforms that appear specific to betalain synthesis. Both betalain-specific isoforms were then lost or downregulated in the anthocyanic Molluginaceae and Caryophyllaceae. Our findings suggest a single origin of the betalain synthesis pathway, with neofunctionalization following gene duplications in the CYP76AD1 and DODA lineages. Loss of DODA-α and CYP76AD1-α in anthocyanic taxa suggests that betalain pigmentation has been lost twice in Caryophyllales, and exclusion of betalain pigments from anthocyanic taxa is mediated through gene loss or downregulation. [Correction added after online publication 13 May 2015: in the last two paragraphs of the Summary the gene name CYP761A was changed to CYP76AD1.].
authors.affiliation: Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, UK.
authors.forename: Samuel F
authors.initials: SF
authors.lastname: Brockington
authors.affiliation: Department of Ecology & Evolutionary Biology, University of Michigan, 830 North University Avenue, Ann Arbor, MI, 48109-1048, USA.
authors.forename: Ya
authors.initials: Y
authors.lastname: Yang
authors.affiliation: Departamento de Bioquímica y Biología Molecular A, Unidad Docente de Biología, Facultad de Veterinaria, Regional Campus of International Excellence 'Campus Mare Nostrum', Universidad de Murcia, E-30100, Espinardo, Murcia, Spain.
authors.forename: Fernando
authors.initials: F
authors.lastname: Gandia-Herrero
authors.affiliation: Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, UK.
authors.forename: Sarah
authors.initials: S
authors.lastname: Covshoff
authors.affiliation: Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, UK.
authors.forename: Julian M
authors.initials: JM
authors.lastname: Hibberd
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks Street, Toronto, ON, M5S 3B2, Canada.
authors.forename: Rowan F
authors.initials: RF
authors.lastname: Sage
authors.affiliation: Department of Biological Sciences, University of Alberta, Edmonton, AB, T6G 2E9, Canada.|Department of Medicine, University of Alberta, Edmonton, AB, T6G 2E1, Canada.|BGI-Shenzhen, Beishan Industrial Zone, Yantian District, Shenzhen, 518083, China.
authors.forename: Gane K S
authors.initials: GK
authors.lastname: Wong
authors.affiliation: Department of Biology, Oberlin College, 119 Woodland St, Oberlin, OH, 44074-1097, USA.
authors.forename: Michael J
authors.initials: MJ
authors.lastname: Moore
authors.affiliation: Department of Ecology & Evolutionary Biology, University of Michigan, 830 North University Avenue, Ann Arbor, MI, 48109-1048, USA.
authors.forename: Stephen A
authors.initials: SA
authors.lastname: Smith
mesh_terms: D050858:Betalains / Q000096:biosynthesis / Q000737:chemistry / Q000378:metabolism*; D053898:Biosynthetic Pathways / Q000235:genetics; D029748:Caryophyllaceae / Q000235:genetics*; D003577:Cytochrome P-450 Enzyme System / Q000235:genetics; D019143:Evolution, Molecular; D017343:Genes, Plant; D016013:Likelihood Functions; D008969:Molecular Sequence Data; D010802:Phylogeny; D010858:Pigmentation / Q000235:genetics
chemical_list: D050858:Betalains; D003577:Cytochrome P-450 Enzyme System
keywords: Caryophyllales; anthocyanin; betalains; lineage-specific genes; pigmentation; taxonomically restricted genes