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The transcription factor SlHY5 regulates the ripening of tomato fruit at both the transcriptional and translational levels.

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.

SUBMITTER: Wang W

PROVIDER: S-EPMC8012583 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Abscisic acid (ABA) regulates plant development and adaptation to environmental conditions. The ABA biosynthesis pathway in plants has been thoroughly elucidated; however, very few transcription factors directly regulating the expression of ABA biosynthetic genes have been identified. Here we show that the tomato (Solanum lycopersicum) zinc finger transcription factor SlZFP2, which is mainly expressed in developing fruits and axillary buds, negatively regulates ABA biosynthesis. Overexpression of SlZFP2 resulted in multiple phenotypic changes, including more branches, early flowering, delayed fruit ripening, lighter seeds and faster seed germination, whereas gene silencing by RNA interference (RNAi) caused poor fruit set and inhibited seed germination. Gene expression analysis showed that SlZFP2 represses ABA biosynthesis mainly through downregulation of the ABA biosynthetic genes SITIENS (SIT), FLACCA (FLC) and aldehyde oxidase SlAO1. SlZFP2 delays the onset of ripening through suppression of the ripening regulator COLORLESS NON-RIPENING (CNR). Using bacterial one hybrid screening and a selected amplification and binding assay we identified the (A/T)(G/C)TT repeat as the core binding sequence of SlZFP2. We further identified a large number of tomato genes containing putative SlZFP2 binding sites in their promoter regions. Chromatin immunoprecipitation and electrophoretic mobility shift assays demonstrated that SIT, FLC and SlAO1 are direct targets of SlZFP2 through binding to their promoter regions. We propose that SlZFP2 represents a novel negative regulator for fine tuning ABA biosynthesis during fruit development and provides a potentially valuable tool for dissecting the role of ABA in fruit ripening.To gain further insight on transcriptome changes regulated by SlZFP2, we sequenced a representative SlZFP2 RNAi line in LA1589 background and its nontransgenic sibling (WT) on a Miseq platform. The RNAi line 207 showed defected fruit set and ABA biosynthesis were chosen for profiling gene expression via RNA sequencing. Its nontransgenic sibling was served as controls. Three biological replicates were conducted.

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The transcription factor SlHY5 regulates the ripening of tomato fruit at both the transcriptional and translational levels.

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