SlJMJ7 orchestrates tomato fruit ripening via crosstalk between H3K4me3 and DML2‐mediated DNA demethylation

Abstract

The ripening of fleshy fruits is a unique developmental process that Arabidopsis and rice lack. This process is driven by hormones and transcription factors. However, the critical and early regulators of fruit ripening are still poorly understood.Here, we revealed that SlJMJ7, an H3K4 demethylase, is a critical negative regulator of fruit ripening in tomato.Combined genome-wide transcription, binding sites, histone H3K4me3 and DNA methylation analyses demonstrated that SlJMJ7 regulates a key group of ripening-related genes, including ethylene biosynthesis (ACS2, ACS4 and ACO6), transcriptional regulation (RIN and NOR) and DNA demethylation (DML2) genes, by H3K4me3 demethylation. Moreover, loss of SlJMJ7 function leads to increased H3K4me3 levels, which directly activates ripeningrelated genes, and to global DML2-mediated DNA hypomethylation in fruit, which indirectly prompts expression of ripening-related genes. Together, these effects lead to accelerated fruit ripening in sljmj7 mutant.Our findings demonstrate that SlJMJ7 acts as a master negative regulator of fruit ripening not only through direct removal of H3K4me3 from multiple key ripening-related factors, but also through crosstalk between histone and DNA demethylation. These findings reveal a novel crosstalk between histone methylation and DNA methylation to regulate gene expression in plant developmental processes.

Molecular and Genetic Events Determining the Softening of Fleshy Fruits: A Comprehensive Review

“…Overexpressing SlJMJ7 represses the expression of target genes by removing the H3K4me3 of genes related to cell wall modification ( CEL2 , XTH5 , EXP1 , XYL1 , PG2a , TBG4 and PL1 / 2 / 8 ), ETH biosynthesis-related genes ( ACS2/4/8 and ACO6 ) and transcriptional regulators ( RIN , NOR and CNR ). SlJMJ7 also directly represses SlDML2 expression by H3K4me3 demethylation during fruit ripening [ 22 ].…”

“…Epigenetic regulation including DNA methylation, histone methylation, and acetylation also is reported to be involved in the ripening and softening of many fruits [ 4 ]. DNA methylation is located in a cascade with histone methylation modifications [ 22 , 23 ]. In addition, there is increasing evidence that transcriptional factors (TFs), phytohormones, and epigenetic regulators work together to regulate cell wall metabolism during fruit softening [ 24 , 25 , 26 , 27 ].…”

Genome-wide analysis of histone acetyltransferase and histone deacetylase families and their expression in fruit development and ripening stage of pepper (Capsicum annuum)

“…Whether orthologous climacteric fruit ripening-related HDAC genes process conserved functions in pepper needs further research. As another important modification, histone methylation, and demethylation have been evidenced to play an important role in fruit ripening by modulating H3K27 to regulate ripening-related gene expression ( Li Z. et al, 2020 ; Ding et al, 2022 ); the exact function of histone methylation in pepper ripening also needs further study. In addition, fruit ripening along with genome-wide dynamic changes in DNA methylation has been identified in tomato ( Zhong et al, 2013 ), strawberry ( Cheng et al, 2018 ), and orange ( Huang et al, 2019 ), and whether DNA methylation is associated with pepper fruit ripening should be dissected in future.…”

Dynamic Network Biomarker Analysis Reveals the Critical Phase Transition of Fruit Ripening in Grapevine

“…There are some factors controlling fruit ripening, such as the external environment, a variety of hormones, and a complex regulatory network of many transcription factors. In future, refined molecular mechanisms need to be studied with the use of datasets with higher temporal and spatial resolution [ 55 , 56 ].…”