The Photomorphogenic Transcription Factor PpHY5 Regulates Anthocyanin Accumulation in Response to UVA and UVB Irradiation.

Yun Zhao,Rong Jin,Kui Lin-Wang,Changqing Zhu,Andrew C Allan,Ting Min,Changjie Xu,Miaojin Chen,Hongxun Wang

doi:10.3389/fpls.2020.603178

Abstract

Red coloration contributes to fruit quality and is determined by anthocyanin content in peach (Prunus persica). Our previous study illustrated that anthocyanin accumulation is strongly regulated by light, and the effect of induction differs according to light quality. Here we showed that both ultraviolet-A (UVA) and ultraviolet-B (UVB) irradiation promoted anthocyanin biosynthesis in “Hujingmilu” peach fruit, and a combination of UVA and UVB had additional effects. The expression of anthocyanin biosynthesis and light signaling related genes, including transcription factor genes and light signaling elements, were induced following UV irradiation as early as 6 h post-treatment, earlier than apparent change in coloration which occurred at 72 h. To investigate the molecular mechanisms for UVA- and UVB-induced anthocyanin accumulation, the genes encoding ELONGATED HYPOCOTYL 5 (HY5), CONSTITUTIVE PHOTOMORPHOGENIC1 (COP1), Cryptochrome (CRY), and UV RESISTANCE LOCUS 8 (UVR8) in peach were isolated and characterized through functional complementation in corresponding Arabidopsis (Arabidopsis thaliana) mutants. PpHY5 and PpCOP1.1 restored hypocotyl length and anthocyanin content in Arabidopsis mutants under white light; while PpCRY1 and PpUVR8.1 restored AtHY5 expression in Arabidopsis mutants in response to UV irradiation. Arabidopsis PpHY5/hy5 transgenic lines accumulated higher amounts of anthocyanin under UV supplementation (compared with weak white light only), especially when UVA and UVB were applied together. These data indicated that PpHY5, acting as AtHY5 counterpart, was a vital regulator in UVA and UVB signaling pathway. In peach, the expression of PpHY5 was up-regulated by UVA and UVB, and PpHY5 positively regulated both its own transcription by interacting with an E-box in its own promoter, and the transcription of the downstream anthocyanin biosynthetic genes chalcone synthase 1 (PpCHS1), chalcone synthase 2 (PpCHS2), and dihydroflavonol 4-reductase (PpDFR1) as well as the transcription factor gene PpMYB10.1. In summary, functional evidence supports the role of PpHY5 in UVA and UVB light transduction pathway controlling anthocyanin biosynthesis. In peach this is via up-regulation of expression of genes encoding biosynthetic enzymes, as well as the transcription factor PpMYB10.1 and PpHY5 itself.

Highlights

Anthocyanins, a group of secondary metabolites known as flavonoid compounds, are important water-soluble pigments widely distributed in plants where they perform a multitude of biological functions such as protecting against a variety of abiotic stresses [ultraviolet (UV) radiation, nutrient deficiency, low temperature, drought, etc.], attracting pollinators and seed dispersers, and defense against pathogens and herbivores (Schaefer et al, 2004; Gould et al, 2010)
For hypocotyl length and anthocyanin accumulation assays, seeds of wild type (WT), above-mentioned mutants as well as transgenic lines obtained in this study were sterilized and germinated on Murashige and Skoog plates supplemented with 0.6% agar and 1% sucrose, and subjected to a chilling treatment at 4◦C for 2 days in the dark
The highest anthocyanin content was detected in fruit under UVA + UVB treatment, reaching 3.47 mg/100gFW at 72 h (2–3 fold higher than UVA or UVB) and 11.59 mg/100gFW at 144 h (3-6 fold higher than UVA or UVB), respectively (Figure 1B), which was consistent with the visual appearance

Summary

Introduction

Anthocyanins, a group of secondary metabolites known as flavonoid compounds, are important water-soluble pigments widely distributed in plants where they perform a multitude of biological functions such as protecting against a variety of abiotic stresses [ultraviolet (UV) radiation, nutrient deficiency, low temperature, drought, etc.], attracting pollinators and seed dispersers, and defense against pathogens and herbivores (Schaefer et al, 2004; Gould et al, 2010). They are recognized to have potential human health benefits in aspects such as prevention from cancer and heart disease (Tsuda, 2012; Zhang et al, 2015). In peach (Prunus persica), several relevant transcription factors (PpMYB10s, PpbHLH3, and PpWD40-1) have been functionally confirmed to control anthocyanin biosynthesis (Ravaglia et al, 2013; Rahim et al, 2014; Uematsu et al, 2014; Zhou et al, 2014, 2018; Tuan et al, 2015)

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