Land plant-specific H3K27 methyltransferases ATXR5 and ATXR6 control plant development and stress responses

Histone modifications are critical for transcriptional regulation. A notable genetic innovation in land plants is the emergence of histone lysine methyltransferases ATXR5/6, which specifically catalyze the repressive histone H3 lysine 27 monomethylation (H3K27me1). Current knowledge of ATXR5/6 function is largely based on Arabidopsis studies using a weak atxr5;atxr6 hypomorphic mutant, in which ATXR6 is still partially expressed and defects are primarily observed in heterochromatin. However, the significance for land plants to evolve these enzymes remains unclear. In this study, we generate strong atxr5;atxr6 mutants with further reduced ATXR6 expression in Arabidopsis to explore the broader roles of ATXR5/6. Our results show that ATXR5/6 are essential for plant reproductive development and play a critical role in supporting normal plant growth by repressing the transcription of stress responsive genes. In addition, ATXR5/6 are necessary for maintaining H3K27 trimethylation (H3K27me3), likely by providing H3K27me1 as a substrate for further methylation. We also demonstrate that the function of ATXR5/6 in regulating development and responsive genes is conserved in the monocot rice. Our findings suggest that land plants evolved ATXR5/6 not only to maintain heterochromatin, but also to regulate development and environmental responses, providing new insights into the functional significance of ATXR5/6 in land plants.