Transcriptional control of flavonoid biosynthesis: a complex network of conserved regulators involved in multiple aspects of differentiation in Arabidopsis
Introduction
Secondary metabolism is an integral part of the developmental program of plants, and accumulation of secondary metabolites often marks the onset of developmental stages. In tomato, for example, production of the red pigment lycopene defines an important transition, known as the breaker stage, towards completion of fruit development. In Arabidopsis, several developmental milestones are reached when the accumulation of specific secondary metabolites occurs. For instance, proanthocyanidins or condensed tannins, which are derived from the flavonoid pathway, accumulate in the innermost layer of the developing seed coat after fertilization and until full seed maturity ([1, 2•]; Figure 1).
Although this association between plant differentiation and secondary metabolism has long been known, a picture of the molecular mechanisms that connect these two programs is starting to emerge. Much of our current understanding stems from work on flavonoid metabolism in Arabidopsis, a process that is intimately linked to specific cellular differentiation programs. This review covers some of the latest findings related to the regulation of flavonoid biosynthesis in Arabidopsis. It emphasizes the role played by a common set of transcription factors that control both this pathway and specific aspects of cellular differentiation, and discusses the importance of WD40 proteins in coordinating flavonoid regulation in Arabidopsis and other plant species.
Section snippets
Epidermal cell fate, seed-coat development and flavonoid biosynthesis are linked in Arabidopsis
The relationship between flavonoid metabolism and epidermal and seed differentiation in Arabidopsis first became apparent with the discovery of the transparent testa glabra1 (ttg1) mutants. These mutants typically produce few or no trichomes, have an aberrant pattern of root-hair initiation, and produce yellow seeds because of the absence of condensed tannins in the inner integument of their seed coat (Figure 1). The abnormal development of their seed coat also impairs mucilage production.
TTG1 is a common denominator in partially overlapping and redundant regulatory networks
The involvement of MYB and bHLH-type transcription factors in regulating epidermal and seed-coat cell fate was implied around 15 years ago with the identification of GLABROUS1 (GL1), which encodes a MYB-domain-containing protein [13, 14, 15], and in overexpression experiments involving RED [9]. Because of the effect of RED on anthocyanin production in plants and its role in maize, it was suspected that anthocyanin production in Arabidopsis would also be controlled by factors of the same class
TTG1-like proteins are functionally conserved
What is the role of TTG1 in modulating regulatory control by MYB and bHLH transcription factors? TTG1, a WD40-containing protein, interacts with the bHLH factors GL3, EGL3 and TT8 in yeast [22••, 25••]. It is also possible that this interacting ability extends to MYB transcription factors, although only interactions with TT2 have been demonstrated in yeast ([25••]; Figure 2). TTG1 is critical for productive bHLH–MYB interactions in planta, as suggested by the ttg1 mutant phenotype and by the
Several possible roles for TTG1-like regulators
The mode of action of TTG1 and its orthologs remains unclear. The extent of our knowledge is that these proteins interact with a variety of bHLH and MYB transcription factors, are expressed widely, and localize in the cytoplasm and in the nucleus [25••, 35, 36]. It is difficult to assign a putative mechanism of action for the regulation of TTG1 proteins solely on the basis of their sequence homology with other WD40 proteins. A sequence homology search using the TTG1 or the AN11 protein sequence
Conclusions
Understanding the specific role of TTG1 awaits further experimentation. However, it is increasingly clear that the control of transcription factors over secondary metabolism in plants occurs within complex regulatory networks that integrate metabolism and development. The focus of our collective attention is gradually shifting from identifying the transcription factors that are involved to defining the molecular nature of the relationship between secondary metabolism and cell differentiation.
References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
I would like to thank Phil Roberts for his help in preparing the figures, Meg Stark for her assistance with SEM, and Dr Loic Lepiniec for his useful comments on the manuscript.
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