The H3K27me3 demethylase REF6 promotes leaf senescence through directly activating major senescence regulatory and functional genes in Arabidopsis.

Publisher: Public Library of Science Country of Publication: United States NLM ID: 101239074 Publication Model: eCollection Cited Medium: Internet ISSN: 1553-7404 (Electronic) Linking ISSN: 15537390 NLM ISO Abbreviation: PLoS Genet Subsets: MEDLINE

Original Publication: San Francisco, CA : Public Library of Science, c2005-

Arabidopsis/*genetics ; Arabidopsis/*metabolism ; Arabidopsis Proteins/*genetics ; Arabidopsis Proteins/*metabolism ; Jumonji Domain-Containing Histone Demethylases/*genetics ; Jumonji Domain-Containing Histone Demethylases/*metabolism ; Transcription Factors/*genetics ; Transcription Factors/*metabolism; Arabidopsis/growth & development ; Binding Sites/genetics ; Chlorophyll/metabolism ; Chloroplast Proteins/genetics ; Chloroplast Proteins/metabolism ; Epigenesis, Genetic ; Gene Expression Regulation, Developmental ; Gene Expression Regulation, Plant ; Genes, Plant ; Genes, Regulator ; Models, Genetic ; Plant Leaves/genetics ; Plant Leaves/growth & development ; Plant Leaves/metabolism ; Plants, Genetically Modified ; Promoter Regions, Genetic

The roles of histone demethylation in the regulation of plant flowering, disease resistance, rhythmical response, and seed germination have been elucidated recently; however, how histone demethylation affects leaf senescence remains largely unclear. In this study, we exploited yeast one-hybrid (Y1H) to screen for the upstream regulators of NONYELLOWING1 (NYE1), and identified RELATIVE OF EARLY FLOWERING6 (REF6), a histone H3 lysine 27 tri-methylation (H3K27me3) demethylase, as a putative binding protein of NYE1 promoter. By in vivo and in vitro analyses, we demonstrated that REF6 directly binds to the motif CTCGYTY in NYE1/2 promoters through its zinc finger domain and positively regulates their expression. Loss-of-function of REF6 delayed chlorophyll (Chl) degradation, whereas overexpression of REF6 accelerated Chl degradation. Subsequently, we revealed that REF6 positively regulates the general senescence process by directly up-regulating ETHYLENE INSENSITIVE 2 (EIN2), ORESARA1 (ORE1), NAC-LIKE, ACTIVATED BY AP3/PI (NAP), PYRUVATE ORTHOPHOSPHATE DIKINASE (PPDK), PHYTOALEXIN DEFICIENT 4 (PAD4), LIPOXYGENASE 1 (LOX1), NAC DOMAIN CONTAINING PROTEIN 3 (AtNAC3), and NAC TRANSCRIPTION FACTOR-LIKE 9 (NTL9), the key regulatory and functional genes predominantly involved in the regulation of developmental leaf senescence. Importantly, loss-of-function of REF6 increased H3K27me3 levels at all the target Senescence associated genes (SAGs). We therefore conclusively demonstrate that H3K27me3 methylation represents an epigenetic mechanism prohibiting the premature transcriptional activation of key developmentally up-regulated senescence regulatory as well as functional genes in Arabidopsis.
Competing Interests: The authors have declared that no competing interests exist.

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0 (Arabidopsis Proteins)
0 (Chloroplast Proteins)
0 (REF6 protein, Arabidopsis)
0 (SGR1 protein, Arabidopsis)
0 (SGR2 protein, Arabidopsis)
0 (Transcription Factors)
1406-65-1 (Chlorophyll)
EC 1.14.11.- (Jumonji Domain-Containing Histone Demethylases)

Date Created: 20190411 Date Completed: 20190508 Latest Revision: 20220410

20240104

PMC6457497

10.1371/journal.pgen.1008068

30969965