TY - JOUR
T1 - Germline X chromosomes exhibit contrasting patterns of histone H3 methylation in Caenorhabditis elegans
AU - Reuben, Melanie
AU - Lin, Rueyling
N1 - Funding Information:
We thank C. David Allis, Leon Avery, Scott Cameron, Dennis Mckearin, Eric Olson, Scott Robertson, and Jim Waddle for critical reading of the manuscript. Special thanks to C. David Allis for sharing unpublished information and unpublished reagents before they were commercially available. We appreciate Brian Strahl for his initial efforts in performing the in vitro HMTase assay. We thank Jim Richardson and the histology core at UT Southwestern Medical Center for mouse sectioning and staging of testis tubules. We also thank Tim Schedl for strain BS3128 and the C. elegans Genome Consortium for all other strains described in this study. This work is supported by an NIH ROI grant (HD37933).
PY - 2002/5/1
Y1 - 2002/5/1
N2 - In mammals, one of the two somatic X chromosomes in the female is inactivated, thereby equalizing X chromosome-derived transcription in the two sexes, a process known as dosage compensation. In the germline, however, the situation is quite different. Both X chromosomes are transcriptionally active during female oogenesis, whereas the X and Y chromosomes are transcriptionally silent during male spermatogenesis. Previous studies suggest that Caenorhabditis elegans germline X chromosomes might have different transcriptional activity in the two sexes in a manner similar to that in mammals. Using antibodies specific to H3 methylated at either lysine 4 or lysine 9, we show that the pattern of site-specific H3 methylation is different between X chromosomes and autosomes as well as between germline X chromosomes from the two sexes in C. elegans. We show that the pachytene germline X chromosomes in both sexes lack Me(K4)H3 when compared with autosomes, consistent with their being transcriptionally inactive. This transcriptional inactivity of germline X chromosomes is apparently transient in hermaphrodites because both X chromosomes stain brightly for Me(K4)H3 after germ nuclei exit pachytene. The male single X chromosome, on the other hand, remains devoid of Me(K4)H3 staining throughout the germline. Instead, the male germline X chromosome exhibits a high level of Me(K9)H3 that is not detected on any other chromosomes in either sex, consistent with stable silencing of this chromosome. Using mutants defective in the sex determination pathway, we show that X-chromosomal Me(K9)H3 staining is determined by the sexual phenotype, and not karyotype, of the animal. We detect a similar high level of Me(K9)H3 in male mouse XY bodies, suggesting an evolutionarily conserved mechanism for silencing the X chromosome specifically in the male germline.
AB - In mammals, one of the two somatic X chromosomes in the female is inactivated, thereby equalizing X chromosome-derived transcription in the two sexes, a process known as dosage compensation. In the germline, however, the situation is quite different. Both X chromosomes are transcriptionally active during female oogenesis, whereas the X and Y chromosomes are transcriptionally silent during male spermatogenesis. Previous studies suggest that Caenorhabditis elegans germline X chromosomes might have different transcriptional activity in the two sexes in a manner similar to that in mammals. Using antibodies specific to H3 methylated at either lysine 4 or lysine 9, we show that the pattern of site-specific H3 methylation is different between X chromosomes and autosomes as well as between germline X chromosomes from the two sexes in C. elegans. We show that the pachytene germline X chromosomes in both sexes lack Me(K4)H3 when compared with autosomes, consistent with their being transcriptionally inactive. This transcriptional inactivity of germline X chromosomes is apparently transient in hermaphrodites because both X chromosomes stain brightly for Me(K4)H3 after germ nuclei exit pachytene. The male single X chromosome, on the other hand, remains devoid of Me(K4)H3 staining throughout the germline. Instead, the male germline X chromosome exhibits a high level of Me(K9)H3 that is not detected on any other chromosomes in either sex, consistent with stable silencing of this chromosome. Using mutants defective in the sex determination pathway, we show that X-chromosomal Me(K9)H3 staining is determined by the sexual phenotype, and not karyotype, of the animal. We detect a similar high level of Me(K9)H3 in male mouse XY bodies, suggesting an evolutionarily conserved mechanism for silencing the X chromosome specifically in the male germline.
KW - C. elegans
KW - Germline
KW - Histone
KW - Methylation
KW - Telomere
KW - X chromosome
KW - XY body
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U2 - 10.1006/dbio.2002.0634
DO - 10.1006/dbio.2002.0634
M3 - Article
C2 - 11969256
AN - SCOPUS:0036570006
SN - 0012-1606
VL - 245
SP - 71
EP - 82
JO - Developmental Biology
JF - Developmental Biology
IS - 1
ER -