High Ambient Temperature Represses Anthocyanin Biosynthesis through Degradation of HY5.

Sara Kim,Inyup Paik,Jungmook Kim,Seulgi Lee,Jia-Ying Zhu,Geonhee Hwang,Thom Thi Nguyen,Eunkyoo Oh

doi:10.3389/fpls.2017.01787

Sara Kim, Inyup Paik + Show 6 more

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https://doi.org/10.3389/fpls.2017.01787

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Abstract

Anthocyanins are flavonoid compounds that protect plant tissues from many environmental stresses including high light irradiance, freezing temperatures, and pathogen infection. Regulation of anthocyanin biosynthesis is intimately associated with environmental changes to enhance plant survival under stressful environmental conditions. Various factors, such as UV, visible light, cold, osmotic stress, and pathogen infection, can induce anthocyanin biosynthesis. In contrast, high temperatures are known to reduce anthocyanin accumulation in many plant species, even drastically in the skin of fruits such as grape berries and apples. However, the mechanisms by which high temperatures regulate anthocyanin biosynthesis in Arabidopsis thaliana remain largely unknown. Here, we show that high ambient temperatures repress anthocyanin biosynthesis through the E3 ubiquitin ligase CONSTITUTIVE PHOTOMORPHOGENIC1 (COP1) and the positive regulator of anthocyanin biosynthesis ELONGATED HYPOCOTYL5 (HY5). We show that an increase in ambient temperature decreases expression of genes required in both the early and late steps of the anthocyanin biosynthesis pathway in Arabidopsis seedlings. As a result, seedlings grown at a high temperature (28°C) accumulate less anthocyanin pigment than those grown at a low temperature (17°C). We further show that high temperature induces the degradation of the HY5 protein in a COP1 activity-dependent manner. In agreement with this finding, anthocyanin biosynthesis and accumulation do not respond to ambient temperature changes in cop1 and hy5 mutant plants. The degradation of HY5 derepresses the expression of MYBL2, which partially mediates the high temperature repression of anthocyanin biosynthesis. Overall, our study demonstrates that high ambient temperatures repress anthocyanin biosynthesis through a COP1-HY5 signaling module.

Highlights

Anthocyanins are water-soluble pigments found throughout the plant kingdom and are derived from the flavonoid branch of the phenylpropanoid pathway
In the model plant Arabidopsis thaliana, the genes encoding anthocyanin biosynthesis enzymes are grouped into two classes: early biosynthetic genes [chalcone synthase (CHS), chalcone isomerase (CHI), flavanone 3-hydroxylase (F3H), and flavonoid 3 -hydroxylase (F3 H)], all of which are common to other flavonoids; and late biosynthetic genes [dihydroflavonol 4-reductase (DFR), leucoanthocyanidin oxygenase (LDOX), UDP-glucose flavonoid 3-O-glucosyltransferase (UF3GT), and anthocyanin acyltransferase (AAT)] that are specific to the anthocyanin pathway (Figure 1) (Tanaka et al, 2008)
We demonstrated that anthocyanin biosynthesis is repressed by an elevation in ambient temperature and that a CONSTITUTIVE PHOTOMORPHOGENIC1 (COP1)-HY5 signaling module mediates the hightemperature regulation of anthocyanin biosynthesis

Summary

Introduction

Anthocyanins are water-soluble pigments found throughout the plant kingdom and are derived from the flavonoid branch of the phenylpropanoid pathway. The anthocyanin biosynthesis pathway has been studied in numerous plant species and most of the genes involved in this process have been identified. Several transcription factors that regulate the expression of anthocyanin biosynthetic genes have been identified. The bHLH and MYB transcription factors form a ternary complex with the WD40 protein TTG1 to activate anthocyanin biosynthesis, the late biosynthetic steps (Zhang et al, 2003; Gonzalez et al, 2008). The small MYB protein MYBL2 negatively regulates anthocyanin biosynthesis by repressing the expression of the late biosynthetic genes DFR and LDOX (Dubos et al, 2008; Matsui et al, 2008)

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