Conserved and distinct roles of H3K27me3 demethylases regulating flowering time in Brassica rapa

Abstract

Epigenetic regulation is necessary for optimal organism development and preservation of gene expression profiles in the cell. In plants, the trimethylation of histone H3 lysine 27 (H3K27me3) is a silencing epigenetic mark relevant for developmental transitions like flowering. The floral transition is a key agronomic trait; however, the epigenetic mechanisms of flowering time regulation in crops remain poorly understood. Here we study the Jumonji H3K27me3 demethylases BraA.REF6 and BraA.ELF6 in Brassica rapa. Phenotypic characterization of novel mutant lines and genome-wide H3K27me3 chromatin immunoprecipitation and transcriptomic analyses indicated that BraA.REF6 plays a greater role than BraA.ELF6 in fine-tuning H3K27me3 levels. In addition, we found that braA.elf6 mutants were early flowering due to high H3K27me3 levels at B. rapa homologs of the floral repressor FLC. Unlike mutations in Arabidopsis thaliana, braA.ref6 mutants were late flowering without altering the expression of B. rapa FLC genes. Remarkably, we found that BraA.REF6 regulated a number of gibberellic acid (GA) biosynthetic genes, including a homolog of GA1, and that GA-treatment complemented the late flowering mutant phenotype. This study increases our understanding of the epigenetic regulation of flowering time in B. rapa, highlighting conserved and distinct regulatory mechanisms between model and crop species.

Brassica rapa CURLY LEAF is a major H3K27 methyltransferase regulating flowering time

“…In A. thaliana, the expression of many floral regulatory genes is controlled by H3K27me3 methylation (Baile et al 2022 ; Vijayanathan et al 2022 ). We have also observed a similar scenario in B. rapa (Payá-Milans et al 2019 ; Poza-Viejo et al 2022 ) . Thus, we decided to characterize the flowering time of the braA.clf-1 mutant.…”

“…The braA.clf-1 plants used in our genomic experiments were grown in parallel and collected together with the plant materials described in Poza-Viejo et al 2022 . We used primary leaves of B. rapa plants grown for 14 days collected at the end of the light period (Zeitgeber time ZT16).…”

“…Transcriptomic and epigenomic data were analyzed using our previously described analytical workflow (Payá-Milans et al 2019 ; Poza-Viejo et al 2022 ) at the Supercomputing Galician Centre (CESGA) high-throughput computing server. The specific code can be found at https://github.com/mpaya/epigenomics_scripts .…”

“…Recent advances in B. rapa epigenomics have provided valuable insights into the regulatory mechanisms governing gene expression in this important crop species. For example, the repressive histone modification H3K27me3 has been proposed to play a key role in the regulation of the floral transition (Payá-Milans et al 2019 ; Poza-Viejo et al 2022 ). Furthermore, there is a distinct distribution of H3K36me3 and H3K27me3 among homoeologous paired genes, which has been proposed to lead to variations in gene-expression levels or tissue specificity (Mehraj et al 2021 ).…”

Epigenetics and its role in effecting agronomical traits

“…BraA.REF6 is more important than BraA.ELF6 10.3389/fpls.2022.925688 in regulating H3K27me3 levels. In braA.ref6 mutants, the expression of FLC genes remains unchanged and there is a delay in flowering, while in braA.elf6 mutants, H3K27me3 levels are high at FLC, leading to early flowering (Poza-Viejo et al, 2022). Through an epigenetic change of upstream FLC components, BrcuHAC1 may influence the bolting and flowering time (Si et al, 2021).…”