Complex pigment evolution in the Caryophyllales

Carotenoids and flavonoids including anthocyanins are the predominant pigments in flowering plants, where they play important roles in pollination, seed dispersal, protection against stress and signalling. In certain families within the Pentapetalae order Caryophyllales, an unusual class of pigments, known as betalains, replaces the more common anthocyanins. This isolated occurrence of betalains in the Caryophyllales has stimulated over half a century of debate and experimentation. Numerous hypotheses have been suggested to explain the phylogenetically restricted occurrence of betalains and their apparent mutual exclusion with anthocyanins. In this review, we evaluate these hypotheses in the face of a changing interpretation of Caryophyllales phylogeny and new comparative genetic data. Phylogenetic analyses expose substantial gaps in our knowledge of the early evolution of pigments in the Caryophyllales and suggest pigmentation to be much more labile than previously recognized. Reconstructions of character evolution imply multiple switches from betalain to anthocyanin pigmentation, but also allow for possible multiple origins of betalains. Comparative genetic studies propose possible mechanisms underlying switches between pigment types and suggest that transcriptional down-regulation of late-acting enzymes is responsible for a loss of anthocyanins. Given these insights from molecular phylogenetics and comparative genetics, we discuss outstanding questions and define key goals for future research.