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Molecular and Cellular Biology, March 2007, p. 2229-2239, Vol. 27, No. 6
0270-7306/07/$08.00+0     doi:10.1128/MCB.01713-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Linker Histone HIS-24 (H1.1) Cytoplasmic Retention Promotes Germ Line Development and Influences Histone H3 Methylation in Caenorhabditis elegans

Max Planck Institute for Biophysical Chemistry, Laboratory of Chromatin Biochemistry, Am Fassberg 11, D-37077 Göttingen, Germany,¹ Institute for Biology 3, Bioinformatics and Molecular Genetics, Fakultät für Biologie, Albert Ludwigs University, Schänzlestr. 1, D-79104 Freiburg, Germany²

Received 11 September 2006/ Returned for modification 22 October 2006/ Accepted 18 December 2006

RNA interference with one of the eight Caenorhabditis elegans linker histone genes triggers desilencing of a repetitive transgene and developmental defects in the hermaphrodite germ line. These characteristics are similar to the phenotype of the C. elegans Polycomb group genes mes-2, mes-3, mes-4, and mes-6 (M. A. Jedrusik and E. Schulze, Development 128:1069-1080, 2001; I. Korf, Y. Fan, and S. Strome, Development 125:2469-2478, 1998). These Polycomb group proteins contribute to germ line-specific chromatin modifications. Using a his-24 deletion mutant and an isoform-specific antibody, we characterized the role of his-24 in C. elegans germ line development. We describe an unexpected cytoplasmic retention of HIS-24 in peculiar granular structures. This phenomenon is confined to the developing germ lines of both sexes. It is strictly dependent on the activities of the chromatin-modifying genes mes-2, mes-3, mes-4, and mes-6, as well as on the C. elegans sirtuin gene sir-2.1. A temperature shift experiment with a mes-3(ts) mutant revealed that mes gene activity is required in a time window ranging from L3 to the early L4 stage before the onset of meiosis. We find that the his-24(ok1024) mutant germ line is characterized by an increased level of the activating H3K4 methylation mark concomitant with a decrease of the repressive H3K9 methylation. In the germ line of his-24(ok1024) mes-3(bn35) double mutant animals, the repressive H3K27 methylation is more reduced than in the respective mes single mutant. These observations distinguish his-24 as an unusual element in the developmental regulation of germ line chromatin structure in C. elegans.

Published ahead of print on 8 January 2007.