The Histone H3K27 Demethylase REF6 Is a Positive Regulator of Light-Initiated Seed Germination in Arabidopsis

Abstract

Seed germination is the first step in initiating a new life cycle in seed plants. Light is a major environmental factor affecting seed germination. Phytochrome B (phyB) is the primary photoreceptor promoting germination during the initial phase of imbibition. Post-translational histone methylation occurring at both lysine and arginine residues plays a crucial role in transcriptional regulation in plants. However, the role of histone lysine demethylation in light-initiated seed germination is not yet reported. Here, we identified that Relative of Early Flowering 6 (REF6)/Jumonji Domain-containing Protein 12 (JMJ12), a histone H3 lysine 27 (H3K27) demethylase, acts as a positive regulator of light-initiated seed germination. The loss of function of REF6 in Arabidopsis inhibits phyB-dependent seed germination. Genome-wide RNA-sequencing analysis revealed that REF6 regulates about half of the light-responsive transcriptome in imbibed seeds, including genes related to multiple hormonal signaling pathways and cellular processes. Phenotypic analyses indicated that REF6 not only regulates seed germination through GA (gibberellin) and ABA (abscisic acid) processes but also depends on the auxin signaling pathway. Furthermore, REF6 directly binds to and decreases the histone H3K27me3 levels of auxin-signaling- and cell-wall-loosening-related genes, leading to the activated expression of these genes in imbibed seeds. Taken together, our study identifies REF6 as the first histone lysine demethylase required for light-initiated seed germination. Our work also reveals the important role of REF6-mediated histone H3K27 demethylation in transcriptional reprogramming in the light-initiated seed germination process.

BRI1-mediated removal of seed coat H3K27me3 marks is a brassinosteroid-independent process

“…The three major H3K27me3 demethylases REF6, ELF6 and JMJ13 have been shown to be important for reproductive processes. REF6 was shown to be necessary for suppression of the seed dormancy (Chen et al, 2020), as well as for seed germination (Pan et al, 2023; Sato et al, 2021; Yahan Wang et al, 2023). ELF6 and JMJ13, on the other hand, have been shown to control carpel growth in an antagonistic matter (Keyzor et al, 2021).…”