ReviewRecent advances on the regulation of anthocyanin synthesis in reproductive organs
Highlights
► Anthocyanins are the final products of a specific branch of the flavonoid pathway. ► In maize, anthocyanin biosynthetic genes are activated by an MBW complex. ► In Arabidopsis, EBGs are activated by MYB TFs and LBGs by an MBW complex. ► In Arabidopsis, positive/negative feedback mechanisms control anthocyanin synthesis. ► Flower/fruit pigmentation is controlled by an MBW complex in 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.
Section snippets
The anthocyanin regulatory system
Anthocyanins are produced by a specific branch of the flavonoid pathway. Flavonoid biosynthesis genes are highly conserved at the structural and functional level among species and are organized in different branches, leading to the production of different flavonoids, e.g. hydroxycinnamic acids, isoflavones, flavonols, phlobaphenes, pro-anthocyanidins and anthocyanins (Fig. 1). Some branches are species-specific, such as the phlobaphenes branch in maize, whereas others are almost ubiquitous,
Flowers
A regulatory system based on the cooperation between MYB and bHLH proteins that controls floral pigmentation is common in many dicotyledonous species (Table 2; [46], [47], [48], [49], [50], [51], [52], [53]), but only in petunia and, to a lesser extent, in morning glory has an MBW complex and a regulatory network similar to that of Arabidopsis been identified.
Anthocyanin synthesis in petunia petals and anthers is controlled by two different ternary MBW complexes, composed by the WD40 AN11 and
Enhancing anthocyanin content in food
There is an increasing interest in functional foods and in particular in foods rich in antioxidants, such as anthocyanins. The identification of transcription factors controlling their biosynthesis in crop plants offers the possibility of improving the existing commercial varieties and rendering them functional foods. Depending on the species, modern crop improvement consists of two main approaches: marker-assisted breeding and metabolic engineering.
Concluding remarks
There is an increasing interest in developing anthocyanin-rich functional foods. To this purpose, the identification of transcription factors and a better understanding of the regulatory network controlling anthocyanin biosynthesis in crop plants is a crucial prerequisite. Beside the structural and functional conservation of anthocyanin biosynthesis genes among species, recent studies highlighted that in many flowering plants and horticultural crops the anthocyanin pathway is also controlled by
Acknowledgment
KP dedicates this review to the loving memory of her sister Anna Petroni, who passed away on March 12, 2010, for giving her an unforgettable example of life and faith. This work was supported by the European Union FP7 ATHENA collaborative project (Grant Agreement 245121) and FP6 FLORA project (FOODCT-01730).
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