Dynamic chromatin regulatory programs of sucrose and citric acid metabolism during fruit ripening in Citrus

TL;DR

This study explores how citrus fruits ripen by examining changes in chromatin and gene activity, revealing key regulators of sugar and acid metabolism.

Contribution

The study identifies a regulatory cascade involving ABA, CrbZIP5b, and CrHSFA6B that controls citrus fruit ripening.

Findings

A transcriptional regulatory network involving 52 key transcription factors was constructed for citrus ripening.

CrHSFA6B and CrbZIP5b regulate genes involved in sucrose and citric acid metabolism during ripening.

Abscisic acid (ABA) plays a central role in modulating citrus fruit ripening processes.

Abstract

Fruit ripening is a complex, tightly regulated process that affects fruit flavor, nutritional value, and shelf life. Citrus is a typical non-climacteric fruit, as citrus fruits ripen independently of ethylene. However, the precise regulatory mechanism underlying this process remains to be elucidated. To dissect the epigenetic and transcriptional basis of citrus ripening, we performed integrative analyses of genome-wide histone modifications (H3K27ac, H3K4me3, and H3K27me3), chromatin accessibility, and transcriptome profiles throughout fruit ripening in Citrus reticulata. We constructed a transcriptional regulatory network encompassing 52 key transcription factors that orchestrate citrus fruit ripening. Further, we identified the key role of abscisic acid (ABA) in modulating sucrose and citric acid metabolism and uncovered the underlying transcriptional and epigenetic regulatory network during fruit ripening in C. reticulata. The findings demonstrate that CrHSFA6B and CrbZIP5b interact with the promoters of CrACO1 (Aconitase 1) and CrACO3 and CrSPSF1 (Sucrose Phosphate Synthase F1), regulating their expression to affect the sucrose and citric acid metabolism and fruit ripening. This study provides insights into the epigenomic dynamics of citrus fruit ripening and identifies a putative regulatory cascade centered on ABA, CrbZIP5b, and CrHSFA6B that modulates key processes in citrus ripening.

A transcriptional regulatory network of the citrus ripening process is established based on the histone modifications, chromatin accessibility, and transcriptome profiles. Two transcription factors activate sucrose biosynthesis and citric acid degradation genes for turning the fruit from sour to sweet.

Graphical AbstractFor image description, please refer to the figure legend and surrounding text.

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