Transcriptome and Metabolic Profiling Provides Insights into Betalain Biosynthesis and Evolution in Mirabilis jalapa

Mol Plant. 2018 Jan 8;11(1):189-204. doi: 10.1016/j.molp.2017.12.002. Epub 2017 Dec 14.

Abstract

Betalains are tyrosine-derived pigments that occur solely in one plant order, the Caryophyllales, where they largely replace the anthocyanins in a mutually exclusive manner. In this study, we conducted multi-species transcriptome and metabolic profiling in Mirabilis jalapa and additional betalain-producing species to identify candidate genes possibly involved in betalain biosynthesis. Among the candidates identified, betalain-related cytochrome P450 and glucosyltransferase-type genes, which catalyze tyrosine hydroxylation or (hydroxy)cinnamoyl-glucose formation, respectively, were further functionally characterized. We detected the expression of genes in the flavonoid/anthocyanin biosynthetic pathways as well as their metabolite intermediates in betalain-accumulating M. jalapa flowers, and found that the anthocyanin-related gene ANTHOCYANIDIN SYNTHASE (MjANS) is highly expressed in the betalain-accumulating petals. However, it appears that MjANS contains a significant deletion in a region spanning the corresponding enzyme active site. These findings provide novel insights into betalain biosynthesis and a possible explanation for how anthocyanins have been lost in this plant species. Our study also implies a complex, non-uniform history for the loss of anthocyanin production across betalain producers, previously assumed to be strictly due to diminished expression of anthocyanin-related genes.

Keywords: anthocyanin; betalain; biosynthesis; caryophyllales; plant pigment; secondary metabolism.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anthocyanins / metabolism
  • Betalains / biosynthesis*
  • Betalains / metabolism
  • Caryophyllales / metabolism
  • Catalytic Domain / genetics
  • Catalytic Domain / physiology
  • Gene Expression Regulation, Plant / genetics
  • Gene Expression Regulation, Plant / physiology
  • Oxygenases / genetics
  • Oxygenases / metabolism
  • Transcriptome / genetics*

Substances

  • Anthocyanins
  • Betalains
  • Oxygenases
  • anthocyanidin synthase