Composition And Function Of COMPASS Complexes In Arabidopsis Thaliana

Histone H3 lysine K4(H3K4)methylation is considered as an important epigenetic mark in eukaryotes.Complex of proteins associated with Set1(COMPASS)is the only H3K4 methyltransferase complex found in the Saccharomyces cerevisiae.As species evolve,the variety and quantity of the COMPASS complexes have increased in higher eukaryotes.The COMPASS complexes which contain the Trithorax-type histone H3K4 methyltransferase are widely involved in multiple biological processes including embryonic development and tumorigenesis.The catalytic activities of histone methyltransferase and the gene targeting specificity of these complexes are regulated by other subunits.Thus,studying the compositions of the COMPASS complexes has been providing important clues for understanding the mechanism underlying the regulation of the catalytic activity and targeting specificity of these complexes.The COMPASS complexes have been identified and characterized in yeast,fruit fly,and humans.Although the homologous proteins of Trithorax and the conserved core components of COMPASS have been reported to be involved in plant growth and development,flowering regulation,and stress responses,the plant COMPASS complexes have not been identified yet.The compositions of the COMPASS complexes are still unknown in plants.In this study,three types of COMPASS complexes were identified in Arabidopsis thaliana by using affinity purification in combination with mass spectrometry,which contain ATX1-ATX5,the Arabidopsis homologs of Trithorax.We named the three types of COMPASS complexes ATX1/2-COMPASS ?,ATX3-COMPASS ?,and ATX4/5-COMPASS ?.Each type of the COMPASS complex includes three core components of COMPASS complex and a unique JmjC domain-containing Histone H3 lysine K9(H3K9)demethylase family protein.Analyses of phenotypes,transcriptome sequencing,and H3K4me3 ChIP-seq demonstrated that the functions of different COMPASS complexes in plant growth and development and transcriptional regulation were partially redundant.The lethality of atx1/2/3/4/5 homozygous mutants proved that three types of COMPASS complexes were essential for plant growth and reproduction.Our studies revealed that ATX1/2 and ATX4/5 not only mediate the transcription of NRPE1,which encodes a core component of the RNA-directed DNA methylation pathway,but also mediate the transcription of the DNA demethylases genes ROS1,DML2,and DML3,thereby regulating DNA methylation in Arabidopsis.The study also identified the Arabidopsis INO80 chromatin remodeling complex,and discovered a plant-specific ATX4/5-COMPASS-INO80 complex.In the plant-specific complex,JMJ24 plays critical roles in linking the ATX4/5-COMPASS and INO80 complexes as well as in maintaining the stability of ATX4/5 histone methyltransferases.Analyses of phenotypes,transcriptome sequencing,and H3K4me3 ChIP-seq showed that ATX4/5-COMPASS ? and the N-terminal binding proteins of INO80 have similar functions in plant growth and development and gene expression regulation.ATX4/5-COMPASS ? and INO80 coordinately promoted the expressions of their common targeting genes.This study filled the knowledge gaps of the compositions of COMPASS complex and INO80 complex in plants,and will lay foundations for studying the assembly,the catalytic activity,and the tareting specificity of the COMPASS complexes in the future.This study revealed that the ATX proteins not only possess important regulatory functions in the processes of growth and development in plants but also play key roles in maintaining the whole-genome DNA methylation status.The discovery of the plant-specific ATX4/5-COMPASS-INO80 complex may offer new directions for investigating the coordination of chromatin remodeling and H3K4 methylations.