The evolution of flavonoid biosynthesis

Abstract

The flavonoid pathway is characteristic of land plants and a central biosynthetic component enabling life in a terrestrial environment. Flavonoids provide tolerance to both abiotic and biotic stresses and facilitate beneficial relationships, such as signalling to symbiont microorganisms, or attracting pollinators and seed dispersal agents. The biosynthetic pathway shows great diversity across species, resulting principally from repeated biosynthetic gene duplication and neofunctionalization events during evolution. Such events may reflect a selection for new flavonoid structures with novel functions that enable occupancy of varied ecological niches. However, the biochemical and genetic diversity of the pathway also likely resulted from evolution along parallel trends across land plant lineages, producing variant compounds with similar biological functions. Analyses of the wide range of whole-plant genome sequences now available, particularly for archegoniate plants, have enabled proposals on which genes were ancestral to land plants and which arose within the land plant lineages. In this review, we discuss the emerging proposals for how the flavonoid pathway may have evolved and diversified. This article is part of the theme issue 'The evolution of plant metabolism'.

Keywords: convergent evolution; neofunctionalization; phenylpropanoid; transcription.

Figure 1.

Proposed evolutionary developments of the flavonoid pathway. The biosynthetic pathway to some of the major flavonoid types is shown on the right. The known occurrence of these flavonoids in land plant lineages is indicated by the coloured circles. The currently proposed relationships of the major land plant lineages are indicated by the tree diagram. Superimposed as boxes on the tree are some of the flavonoid biosynthetic and regulatory genes associated with the flavonoid types produced in each lineage, with the box colour indicating possible gene gains or losses. Darker green outline and fill indicate a gene gain for which there is reasonable genetic and/or enzymatic evidence. Light green indicates a gene gain that may be inferred from the biosynthetic activities required to produce the types of flavonoid present. The positioning of these in the evolutionary tree is generally speculative. Blue indicates a group of several biosynthetic genes (which may or may not have been characterized). Red indicates a gene loss. The gene order within each individual branch is not meant to imply the order in which the genes arose. Gene abbreviations not given in the text are: DFR, DIHYDROFLAVONOL 4-REDUCTASE; FNR, FLAVANONE 4-REDUCTASE; ANR, ANTHOCYANIDIN REDUCTASE; FGTs, FLAVONOID O-GLYCOSYLTRANSFERASES; A3GT, ANTHOCYANIDIN 3-O-GLUCOSYLTRANSFERASE; A5GT, ANTHOCYANIDIN 5-O-GLUCOSYLTRANSFERASE; AUR, auronidin biosynthesis; SPH, sphagnorubin biosynthesis; IsoFlav, isoflavonoid biosynthesis; MYB and bHLH, R2R3MYB and bHLH transcription factors activating flavonoid biosynthetic genes.

Figure 2.

Gene numbers across land plants for enzyme families important in flavonoid metabolism. Gene numbers were compared in 14 plant species representing the major lineages of streptophytes: streptophyte algae (Klebsormidium nitens), mosses (Physcomitrium patens and Ceratodon purpureus), hornworts (Anthoceros agrestis), liverworts (Marchantia polymorpha and Ricciocarpos natans), lycophytes (Selaginella moellendorffii and Diphasiastrum complanatum), ferns (Azolla filiculoides and Ceratopteris richardii), gymnosperms (Thuja plicata and Picea abies) and angiosperms (Arabidopsis thaliana and Oryza sativa). Enzyme abbreviations are: PKS, POLYKETIDE SYNTHASE; NED, NAD-DEPENDENT EPIMERASE/DEHYDRATASE; 2OGD, 2-OXOGLUTARATE-DEPENDENT DIOXYGENASE; AKR, ALDO–KETO REDUCTASE; CYP450, CYTOCHROME P450; DIR, DIRIGENT PROTEIN; PKC, POLYKETIDE CYCLASE; PR10, PATHOGEN-RELATED 10; PPO, POLYPHENOL OXIDASE; BAHD, BAHD ACYLTRANSFERASE; GST, GLUTATHIONE-S-TRANSFERASE; UGT, URIDINE DIPHOSPHATE-DEPENDENT GLYCOSIDE : GLYCOSYLTRANSFERASE genes containing the plant secondary product glycosyltransferase-box motif; and ABC, ATP-BINDING CASSETTE TRANSPORTER. Sources: BLAST searches for specific PFAM domains using publicly available genomes. Colours in heatmap are based on Z-scores of the number of genes within each enzyme family.