Abstract
Germline-stem cells (GSCs) produce gametes and are thus true “immortal stem cells”. In Drosophila ovaries, GSCs divide asymmetrically to produce daughter GSCs and cystoblasts, and the latter differentiate into germline cysts. Here we show that the histone-lysine methyltransferase dSETDB1, located in pericentric heterochromatin, catalyzes H3-K9 trimethylation in GSCs and their immediate descendants. As germline cysts differentiate into egg chambers, the dSETDB1 function is gradually taken over by another H3-K9-specific methyltransferase, SU(VAR)3–9. Loss-of-function mutations in dsetdb1 or Su(var)3–9 abolish both H3K9me3 and heterochromatin protein-1 (HP1) signals from the anterior germarium and the developing egg chambers, respectively, and cause localization of H3K9me3 away from DNA-dense regions in most posterior germarium cells. These results indicate that dSETDB1 and SU(VAR)3–9 act together with distinct roles during oogenesis, with dsetdb1 being of particular importance due to its GSC-specific function and more severe mutant phenotype.
Highlights
Drosophila oogenesis is a complex developmental process involving the coordinated differentiation of germline and somatic cells, and begins with asymmetric division of a single germline stem cell (GSC) [1,2]
We found that dSETDB1, localized to pericentric heterochromatin in germ cells including the oocytes, is the only HKMTase that synthesizes trimethylated H3-K9 in the germ-cell lineages in the germarium, and this function is transferred to SU(VAR)3-9 in later oogenesis
We showed that dSETDB1 is the only HKMTase responsible for the synthesis of H3K9me3 signals in the inner germarium where GSCs and their early descendants are found
Summary
Drosophila oogenesis is a complex developmental process involving the coordinated differentiation of germline and somatic cells, and begins with asymmetric division of a single germline stem cell (GSC) [1,2]. This GSC is located at the tip of each ovariole in the germarium, which is a generative region that is divided into sub-regions such as region-1, -2a, -2b and -3. The germline cells, including the GSCs are the only population from which both parental epigenetic information and genetic information can be transferred to progeny. Germ-cell development is an excellent system to study how the epigenetic system involving DNA methylation and histone lysine methylation is erased, reestablished, and maintained in the germ cells at the genome-wide level
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