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Lineage‐specific gene radiations underlie the evolution of novel betalain pigmentation in Caryophyllales
Author(s) -
Brockington Samuel F.,
Yang Ya,
GandiaHerrero Fernando,
Covshoff Sarah,
Hibberd Julian M.,
Sage Rowan F.,
Wong Gane K. S.,
Moore Michael J.,
Smith Stephen A.
Publication year - 2015
Publication title -
new phytologist
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 3.742
H-Index - 244
eISSN - 1469-8137
pISSN - 0028-646X
DOI - 10.1111/nph.13441
Subject(s) - betalain , biology , genetics , neofunctionalization , botany , gene , phylogenetic tree , pigment , chemistry , organic chemistry
Summary 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 CYP 76 AD 1, a cytochrome P450 gene that catalyzes the formation of cyclo‐ DOPA . We performed phylogenetic analyses to reveal the evolutionary history of the DODA and CYP 76 AD 1 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 CYP 76 AD 1 and DODA lineages arose just before the origin of betalain pigmentation in the core Caryophyllales. The duplications gave rise to DODA ‐α and CYP 76 AD 1‐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 CYP 76 AD 1 and DODA lineages. Loss of DODA ‐α and CYP 76 AD 1‐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.]