Histone methylation readers MRG1/MRG2 interact with the transcription factor TCP14 to positively modulate cytokinin sensitivity in Arabidopsis

Cytokinins influence many aspects of plant growth and development. Although cytokinin biosynthesis and signaling have been well studied in planta, little is known about the regulatory effects of epigenetic modifications on the cytokinin response. Here, we reveal that mutations to Morf Related Gene (MRG) proteins MRG1/MRG2, which are readers of trimethylated histone H3 lysine 4 and lysine 36 (H3K4me3 and H3K36me3), result in cytokinin hyposensitivity during various developmental processes, including callus induction and root and seedling growth inhibition. Similar to the mrg1 mrg2 mutant, plants with a defective AtTCP14, which belongs to the TEOSINTE BRANCHED, CYCLOIDEA, AND PROLIFERATING CELL FACTOR (TCP) transcription factor family, are insensitive to cytokinin. Furthermore, the transcription of several genes related to cytokinin signaling pathway is altered. Specifically, the expression of Arabidopsis thalianaHISTIDINE-CONTAINING PHOSPHOTRANSMITTER PROTEIN 2 (AHP2) decreases significantly in the mrg1 mrg2 and tcp14-2 mutants. We also confirm the interaction between MRG2 and TCP14 in vitro and in vivo. Thus, MRG2 and TCP14 can be recruited to AHP2 after recognizing H3K4me3/H3K36me3 markers and promote the histone-4 lysine-5 acetylation to further enhance AHP2 expression. In summary, our research elucidate a previously unknown mechanism mediating the effects of MRG proteins on the magnitude of the cytokinin response.