Recent advances on the regulation of anthocyanin synthesis in reproductive organs

Abstract

Anthocyanins represent the major red, purple, violet and blue pigments in many flowers and fruits. They attract pollinators and seed dispersers and defend plants against abiotic and biotic stresses. Anthocyanins are produced by a specific branch of the flavonoid pathway, which is differently regulated in monocot and dicot species. In the monocot maize, the anthocyanin biosynthesis genes are activated as a single unit by a ternary complex of MYB-bHLH-WD40 transcription factors (MBW complex). In the dicot Arabidopsis, anthocyanin biosynthesis genes can be divided in two subgroups: early biosynthesis genes (EBGs) are activated by co-activator independent R2R3-MYB transcription factors, whereas late biosynthesis genes (LBGs) require an MBW complex. In addition to this, a complex regulatory network of positive and negative feedback mechanisms controlling anthocyanin synthesis in Arabidopsis has been described. Recent studies have broadened our understanding of the regulation of anthocyanin synthesis in flowers and fruits, indicating that a regulatory system based on the cooperation of MYB, bHLH and WD40 proteins that control floral and fruit pigmentation is common to many dicot species.

Introduction

Anthocyanins are the major red, purple, violet and blue pigments admired in many flowers and fruits. The recruitment of pollinators is a well-known physiological function of anthocyanin pigments in flowers. Bumble bees have a preference for pink or violet flowers, whereas hummingbirds, which see colours in very much the same way as humans, prefer red flowers [1]. Anthocyanins are also crucial in attracting seed dispersers. As the seeds complete their development inside fruits, the flesh sweetens and becomes purple or red that signals to birds and other animals to collect food. Besides providing pigmentation in flowers and fruits, anthocyanins also have key roles in protection against UV radiation and cold temperatures [2], [3], response to drought stress [4] and in defense against microbial agents [5].

Anthocyanin synthesis is the most studied secondary metabolic pathway in plants. Genetic and molecular studies aimed at understanding its regulation have led to key scientific breakthroughs, such as the discovery of transposable elements [6] and of the epigenetic phenomena of paramutation and silencing of duplicated genes in maize [7], [8], the discovery of cosuppression in petunia [9] and of the first plant transcription factor in maize [10]. Most of our knowledge about transcriptional regulation in plants has initially come from studies of the regulation of anthocyanin biosynthesis in the monocot maize. Since then, the regulation of this pathway has been extended to several other species, particularly dicots. Transcription factors are regulatory proteins that modulate the expression of specific groups of genes through sequence-specific DNA binding and protein–protein interactions with the general transcription machinery, chromatin remodelling proteins and/or other transcription factors. They can act as activators or repressors of gene expression, mediating either an increase or a decrease in transcript level of target genes. Transcription factors are classified into families primarily on the basis of their conserved DNA binding domain. In Arabidopsis, more than 200 genes encoding transcription factors representing about 60 protein families have been identified [11]. The transcriptional regulators for anthocyanin biosynthesis, which activate the structural genes, include members of protein families containing R2R3-MYB domains, bHLH (basic helix–loop–helix) domains and conserved WD40 repeats. Combinations of the R2R3-MYB, bHLH and WD40 transcription factors and their interactions determine the set of biosynthesis genes to be expressed [12], [13].

Here, we review recent advances in understanding the regulation of anthocyanin biosynthesis in plants, with particular emphasis on transcription factors controlling anthocyanin synthesis in reproductive organs.