Abstract

Light plays a critical role in plant growth and development, but the mechanisms through which light regulates fruit ripening and nutritional quality in horticultural crops remain largely unknown. Here, we found that ELONGATED HYPOCOTYL 5 (HY5), a master regulator in the light signaling pathway, is required for normal fruit ripening in tomato (Solanum lycopersicum). Loss of function of tomato HY5 (SlHY5) impairs pigment accumulation and ethylene biosynthesis. Transcriptome profiling identified 2948 differentially expressed genes, which included 1424 downregulated and 1524 upregulated genes, in the Slhy5 mutants. In addition, genes involved in carotenoid and anthocyanin biosynthesis and ethylene signaling were revealed as direct targets of SlHY5 by chromatin immunoprecipitation. Surprisingly, the expression of a large proportion of genes encoding ribosomal proteins was downregulated in the Slhy5 mutants, and this downregulation pattern was accompanied by a decrease in the abundance of ribosomal proteins. Further analysis demonstrated that SlHY5 affected the translation efficiency of numerous ripening-related genes. These data indicate that SlHY5 regulates fruit ripening both at the transcriptional level by targeting specific molecular pathways and at the translational level by affecting the protein translation machinery. Our findings unravel the regulatory mechanisms of SlHY5 in controlling fruit ripening and nutritional quality and uncover the multifaceted regulation of gene expression by transcription factors.

Highlights

  • Light serves as a source of energy for plant photosynthesis, and represents an important cue that regulates plant growth and development, including seed germination[1], seedling growth[2], flowering[3], and eventually senescence[4]

  • A transcriptome analysis coupled with chromatin immunoprecipitation (ChIP) indicated that SlHY5 directly bound to promoters of genes involved in carotenoid and anthocyanin biosynthesis, and genes associated with ethylene generation

  • HYPOCOTYL 5 (HY5) was first identified in Arabidopsis as a transcriptional regulator with a basic leucine zipper (bZIP) motif[9]

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Summary

Introduction

Light serves as a source of energy for plant photosynthesis, and represents an important cue that regulates plant growth and development, including seed germination[1], seedling growth[2], flowering[3], and eventually senescence[4]. 20–35% of plant genes display massive transcriptional reprogramming under light[7]. Several transcription factors, such as PHYTOCHROME-INTERACTING FACTORs (PIFs) and ELONGATED HYPOCOTYL 5 (HY5), which exhibit antagonistic actions, have been identified as the key components in the light signaling pathway[8]. PIFs belong to the family of basic helix-loop-helix transcription factors, whereas HY5 is a member of the basic leucine zipper (bZIP) transcription factor family[9,10]. The stability of both PIFs and HY5 is regulated by CONSTITUTIVE

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