Negative Regulation of Anthocyanin Biosynthesis in Arabidopsis by a miR156-Targeted SPL Transcription Factor

Jin-Ying Gou,Detlef Weigel,Chang-Jun Liu,Felipe F Felippes,Jia-Wei Wang

doi:10.1105/tpc.111.084525

Abstract

Flavonoids are synthesized through an important metabolic pathway that leads to the production of diverse secondary metabolites, including anthocyanins, flavonols, flavones, and proanthocyanidins. Anthocyanins and flavonols are derived from Phe and share common precursors, dihydroflavonols, which are substrates for both flavonol synthase and dihydroflavonol 4-reductase. In the stems of Arabidopsis thaliana, anthocyanins accumulate in an acropetal manner, with the highest level at the junction between rosette and stem. We show here that this accumulation pattern is under the regulation of miR156-targeted SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) genes, which are deeply conserved and known to have important roles in regulating phase change and flowering. Increased miR156 activity promotes accumulation of anthocyanins, whereas reduced miR156 activity results in high levels of flavonols. We further provide evidence that at least one of the miR156 targets, SPL9, negatively regulates anthocyanin accumulation by directly preventing expression of anthocyanin biosynthetic genes through destabilization of a MYB-bHLH-WD40 transcriptional activation complex. Our results reveal a direct link between the transition to flowering and secondary metabolism and provide a potential target for manipulation of anthocyanin and flavonol content in plants.

Highlights

Flavonoids are major plant phenylpropanoid metabolites found throughout the plant kingdom, including the model species Arabidopsis thaliana
We propose a model for how metabolic flux through the branched flavonoid biosynthetic pathway is affected by miR156-regulated
Expression of SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) gradually increases along the growing stem because miR156 levels decline as the plant progresses during development (Wu and Poethig, 2006; Wang et al, 2009; Wu et al, 2009)

Summary

Introduction

Flavonoids are major plant phenylpropanoid metabolites found throughout the plant kingdom, including the model species Arabidopsis thaliana. These diphenylchroman compounds play vital roles in growth and development by providing plants with red, blue, and purple pigments that protect against UV radiation, attract pollinators and other beneficial organisms, or mediate plant–microbe interactions (Buer et al, 2010). The most common flavonols in Arabidopsis are kaempferol glycosides, with quercetin glycoside levels increasing after exposure to UV radiation (Veit and Pauli, 1999) Another group of flavonoids are anthocyanins that accumulate in variable amounts in Arabidopsis leaves and stems, depending on light level and nutrition (Holton and Cornish, 1995). The glycosylated and acylated cyanidin derivatives constitute the major anthocyanins present in the leaves and stems of mature Arabidopsis plants (Bloor and Abrahams, 2002)

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