HIS-24 Linker Histone and SIR-2.1 Deacetylase Induce H3K27me3 in the Caenorhabditis elegans Germ Line

Abstract

HIS-24 linker histone and SIR-2.1 deacetylase are involved in chromatin silencing in Caenorhabditis elegans. Depletion of SIR-2.1 results in cytoplasmic retention of HIS-24 in oocytes. However, the molecular working mechanisms of HIS-24 and SIR-2.1 are unclear. We show here a synergistic function of SIR-2.1 and HIS-24 that are together essential for maintenance of the H3K27me3 mark in the germ line of C. elegans. We demonstrate the synthetic effects of the two factors on brood size, embryogenesis, and fertility. SIR-2.1 and HIS-24 associate with the subtelomeric regions but apparently do not interact directly. We report that SIR-2.1 deacetylates H3K9 at subtelomeric regions and suggest that deacetylation of H3K9 is a prerequisite for H3K27 methylation. In turn, we found that HIS-24 specifically interacts with the histone H3 K27 region, when unmodified or in the trimethylated state. Overall, our data indicate that SIR-2.1 and HIS-24 contribute to the propagation of a specialized chromatin state at the subtelomeric regions and elsewhere in the genome.

ACKNOWLEDGMENTS

We thank Kathy Gelato for critically reading of the manuscript; Szabolcs Sörös for kindly providing the HP1β plasmid; Bettina Meier (Dundee, United Kingdom) for Southern blot analysis; and Anton Gartner, Sebastian Greiss, and B. Meier (Dundee, United Kingdom) for helpful discussions. We are grateful to T. Jenuwein (Vienna, Austria) for the anti-H3K27me3 antibodies, A. Gartner (Dundee, United Kingdom) for anti-SIR-2.1 antibodies, and F. Palladino (Lyon, France) for anti-HPL-2 antibodies. Several, C. elegans strains used in the present study were obtained from the Caenorhabditis Genetics Center, which is funded by the National Institutes of Health National Center for Research Resources.

This study was supported by the Max Planck Society (W.F.) and the German National Funding Agency (JE 505/1-1 and JE 505/1-2 [M.J.-B.]).