The evolution of betalain biosynthesis in Caryophyllales

• Published in: The New phytologist Vol. 224; no. 1; pp. 71 - 85
• Main Authors: Timoneda, Alfonso, Feng, Tao, Sheehan, Hester, Walker-Hale, Nathanael, Pucker, Boas, Lopez-Nieves, Samuel, Guo, Rui, Brockington, Samuel
• Format: Journal Article
• Language: English
• Published: England Wiley 01.10.2019; Wiley Subscription Services, Inc
• Subjects: anthocyanin; Anthocyanins; betalain; betalains; Betalains - biosynthesis; Betalains - chemistry; biochemical pathways; Biological Evolution; Biology; Biosynthesis; Biosynthetic Pathways; Caryophyllales; Caryophyllales - genetics; Caryophyllales - metabolism; Chemical synthesis; Chromophores; Colour; Evolution; Evolutionary genetics; Genes; Genetics; Metabolism; Phenylalanine; Phylogenetics; Phylogeny; Pigmentation; Pigmentation - genetics; Pigments; Regulators; synthetic biology; Tansley review; Transcription; transcription factors; Tyrosine; pigmentation; anthocyanin; tyrosine; betalain; caryophyllales
• ISSN: 0028-646X; 1469-8137; 1469-8137
• DOI: 10.1111/nph.15980

Within the angiosperm order Caryophyllales, an unusual class of pigments known as betalains can replace the otherwise ubiquitous anthocyanins. In contrast to the phenylalanine-derived anthocyanins, betalains are tyrosine-derived pigments which contain the chromophore betalamic acid. The origin of betalain pigments within Caryophyllales and their mutual exclusion with anthocyanin pigments have been the subject of considerable research. In recent years, numerous discoveries, accelerated by -omic scale data, phylogenetics and synthetic biology, have shed light on the evolution of the betalain biosynthetic pathway in Caryophyllales. These advances include the elucidation of the biosynthetic steps in the betalain pathway, identification of transcriptional regulators of betalain synthesis, resolution of the phylogenetic history of key genes, and insight into a role for modulation of primary metabolism in betalain synthesis. Here we review how molecular genetics have advanced our understanding of the betalain biosynthetic pathway, and discuss the impact of phylogenetics in revealing its evolutionary history. In light of these insights, weexplore our new understanding of the origin of betalains, the mutual exclusion of betalains and anthocyanins, and the homoplastic distribution of betalain pigmentation within Caryophyllales. We conclude with a speculative conceptual model for the stepwise emergence of betalain pigmentation.