The Histone H3K4 Demethylase JMJ16 Represses Leaf Senescence in Arabidopsis

Abstract

Leaf senescence is governed by a complex regulatory network involving the dynamic reprogramming of gene expression. Age-dependent induction of senescence-associated genes (SAGs) is associated with increased levels of trimethylation of histone H3 at Lys4 (H3K4me3), but the regulatory mechanism remains elusive. Here, we found that JMJ16, an Arabidopsis (Arabidopsis thaliana) JmjC-domain containing protein, is a specific H3K4 demethylase that negatively regulates leaf senescence through its enzymatic activity. Genome-wide analysis revealed a widespread coordinated upregulation of gene expression and hypermethylation of H3K4me3 at JMJ16 binding genes associated with leaf senescence in the loss-offunction jmj16 mutant as compared with the wild type. Genetic analysis indicated that JMJ16 negatively regulates leaf senescence, at least partly through repressing the expression of positive regulators of leaf senescence, WRKY53 and SAG201. JMJ16 associates with WRKY53 and SAG201 and represses their precocious expression in mature leaves by reducing H3K4me3 levels at these loci. The protein abundance of JMJ16 gradually decreases during aging, which is correlated with increased H3K4me3 levels at WRKY53 and SAG201, suggesting that the age-dependent downregulation of JMJ16 is required for the precise transcriptional activation of SAGs during leaf senescence. Thus, JMJ16 is an important regulator of leaf senescence that demethylates H3K4 at SAGs in an age-dependent manner.

Integrated Genome-Scale Analysis Identifies Novel Genes and Networks Underlying Senescence in Maize

“…The role of epigenetic mechanisms, specifically histone Lys methylation, in stay-green is another important finding of this analysis. In Arabidopsis, histone demethylase activity of a JmjC domain-containing protein JMJ16 is responsible for suppression of age-dependent senescence (Liu et al, 2019). Coexpression network analysis of stay-green also provided some very intriguing insights.…”

Genetic Network between Leaf Senescence and Plant Immunity: Crucial Regulatory Nodes and New Insights

“…JMJ16 is a JmjC domain-containing protein and it is a specific H3K4 demethylase in Arabidopsis. The expression of two positive regulators of leaf senescence, WRKY53 and SAG201, is repressed by JMJ16 in an age-dependent manner through reducing H3K4me3 levels at these loci [82]. The jmj16 mutants display an early senescence phenotype, suggesting that JMJ16 is an important epigenetic regulator of leaf senescence via demethylating H3K4 at SAGs in an age-dependent manner.…”

Arabidopsis WRKY53, a Node of Multi-Layer Regulation in the Network of Senescence

“…While cytosine methylation directly on the DNA remains unchanged and overall very low during onset and progression of senescence in the WRKY53 promoter [65], di-and tri-methylation of HISTONE3 (H3K4me2 and H3K4me3) in the promoter region of WRKY53 increases and makes the DNA more accessible for transcription [66,67]. In contrast, the JmjC-domain containing protein JMJ16, which is a specific H3K4 demethylase, negatively regulates leaf senescence at least partly through repressing the expression of WRKY53 [68]. This suggests that the accessibility of the chromatin at the WRKY53 promoter region can be driven back and forth, most likely to adjust WRKY53 expression and senescence induction to environmental conditions.…”