SlBBX20 interacts with the COP9 signalosome subunit SlCSN5-2 to regulate anthocyanin biosynthesis by activating SlDFR expression in tomato

Dan Luo,Chunli Zhang,Taotao Wang,Aihua Lin,Yongen Lu,Junhong Zhang,Zhibiao Ye,Wenhui Sun,Changxian Yang,Hanxia Li,Cheng Xiong,Ping He

doi:10.1038/s41438-021-00595-y

Dan Luo, Chunli Zhang + Show 10 more

Open Access

https://doi.org/10.1038/s41438-021-00595-y

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Abstract

Anthocyanins play vital roles in plant stress tolerance and growth regulation. Previously, we reported that the photomorphogenesis-related transcription factor SlBBX20 regulates anthocyanin accumulation in tomato. However, the underlying mechanism remains unclear. Here, we showed that SlBBX20 promotes anthocyanin biosynthesis by binding the promoter of the anthocyanin biosynthesis gene SlDFR, suggesting that SlBBX20 directly activates anthocyanin biosynthesis genes. Furthermore, we found by yeast two-hybrid screening that SlBBX20 interacts with the COP9 signalosome subunit SlCSN5-2, and the interaction was confirmed by bimolecular fluorescence complementation and coimmunoprecipitation assays. SlCSN5 gene silencing led to anthocyanin hyperaccumulation in the transgenic tomato calli and shoots, and SlCSN5-2 overexpression decreased anthocyanin accumulation, suggesting thSlCSN5-2 enhanced the ubiquitination of SlBBX20 and promoted the degradation of SlBBX20 in vivo. Consistently, silencing the SlCSN5-2 homolog in tobacco significantly increased the accumulation of the SlBBX20 protein. Since SlBBX20 is a vital regulator of photomorphogenesis, the SlBBX20-SlCSN5-2 module may represent a novel regulatory pathway in light-induced anthocyanin biosynthesis.

Highlights

Anthocyanins are pigments synthesized by the flavonoid pathway involved in the coloring of various organs, such as leaves, fruits, and flowers[1,2]
Atv is located on chromosome 7 and encodes the SlMYBATV protein, which negatively regulates the synthesis of anthocyanins
We found that the SlBBX20 protein is modified by the CRL4 E3 ubiquitin ligase to regulate the biosynthesis of carotenoids in tomato fruit[34]

Summary

Introduction

Anthocyanins are pigments synthesized by the flavonoid pathway involved in the coloring of various organs, such as leaves, fruits, and flowers[1,2]. Anthocyanins are the main pigments responsible for determining color in a broad variety of fruits. Aft and Atv are two important loci that regulate anthocyanin biosynthesis in tomato. The Aft gene from tomato was mapped to chromosome 10 and found to encode a SlAN2-like R2R3-MYB protein that promotes anthocyanin biosynthesis[9,10]. Atv is located on chromosome 7 and encodes the SlMYBATV protein, which negatively regulates the synthesis of anthocyanins. In addition to positively regulating anthocyanin biosynthesis, Aft was reported to directly activate SlMYBATV expression. SlMYBATV competes with Aft for interaction with the transcription factor SlJAF13, thereby downregulating the accumulation of anthocyanins in tomato fruit. Mutation of SlMYBATV results in the release of SlJAF13, which interacts with Aft, further

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