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Elucidation of the biological role of linker histone (H1) and heterochromatin protein 1 (HP1) in mammals has been difficult owing to the existence of a least 11 distinct H1 and three HP1 subtypes in mice.  Caenorhabditis elegans  possesses two HP1 homologues (HPL-1 and HPL-2) and eight H1 variants. Remarkably, one of eight H1 variants, HIS-24, is important for  C. elegans  development. Therefore we decided to analyse in parallel the transcriptional profiles of HIS-24, HPL-1/-2 deficient animals, and their phenotype, since  hpl-1 ,  hpl-2 , and  his-24  deficient nematodes are viable. Global transcriptional analysis of the double and triple mutants revealed that HPL proteins and HIS-24 play gene-specific roles, rather than a general repressive function. We showed that HIS-24 acts synergistically with HPL to allow normal reproduction, somatic gonad development, and vulval cell fate decision. Furthermore, the  hpl-2 ;  his-24  double mutant animals displayed abnormal development of the male tail and ectopic expression of  C. elegans  HOM-C/Hox genes ( egl-5  and  mab-5 ), which are involved in the developmental patterning of male mating structures. We found that HPL-2 and the methylated form of HIS-24 specifically interact with the histone H3 K27 region in the trimethylated state, and HIS-24 associates with the  egl-5  and  mab-5  genes. Our results establish the interplay between HPL-1/-2 and HIS-24 proteins in the regulation of positional identity in  C. elegans  males.

Transcriptional Repression of Hox Genes by C. elegans HP1/HPL and H1/HIS-24