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.]

Draft genome sequence of an inbred line ofChenopodium quinoa, an allotetraploid crop with great environmental adaptability and outstanding nutritional properties

“…Some cytochrome P450 genes were also expanded in the quinoa genome. Two of these were annotated as cytochrome P450 71A1 and 76AD1, which play a role in the polyphenol- and betalain-biosynthesis pathway, respectively 76 , 77 . Expansion and subsequent functional differentiation of these genes might be related to quinoa having a high protein content and abundant secondary metabolites.…”

Proteomic Analysis of Hylocereus polyrhizus Reveals Metabolic Pathway Changes

“…CYP76AD, a novel cytochrome P450 enzyme, catalyzes oxidation of L-DOPA for the formation of cyclo-DOPA in B. vulgaris [47], A. hypochondriacus [38] and M. jalapa [48]. In addition, CYP76AD and DOD have also been considered as key genes involved in betalain biosynthesis based on phylogenetic analysis [49,50]. GTs are the key enzyme in betalain biosynthetic pathway to make the pigments stable and diversified.…”

Evolution of Gene Duplication in Plants

“…Note that determining whether neofunctionalization has taken place requires knowledge of gene functions prior to duplication. Some examples where neofunctionalization after duplication has likely contributed to duplicate retention include MADS box transcription factors involved in the evolution of novel floral structures (He and Saedler, 2005;Hu et al, 2015b;Zhang et al, 2015), 4,5-dioxygenase and cytochrome P450 genes that contribute to pigment variation in Caryophyllales (Brockington et al, 2015), and the recruitment of duplicated primary metabolite genes into specialized metabolite pathways (Durbin et al, 2000). At the gene expression level, it is estimated that approximately 10% of Arabidopsis duplicate genes have gained a novel response to stress conditions (Zou et al, 2009b), although it remains to be determined whether these novel responses are adaptive or not.…”