Tombola, a tesmin/TSO1-family protein, regulates transcriptional activation in the Drosophila male germline and physically interacts with Always early

During male gametogenesis, a developmentally regulated and cell type-specific transcriptional programme is activated in primary spermatocytes to prepare for differentiation of sperm. The Drosophila aly-class meiotic-arrest loci (aly, comr, achi/vis and topi) are essential for activation of transcription of many differentiation-specific genes, and several genes important for meiotic cell cycle progression, thus linking meiotic divisions to cellular differentiation during spermatogenesis. Protein interaction studies suggest that the aly-class gene products form a chromatin-associated complex in primary spermatocytes. We identify, clone and characterise a new aly-class meiotic-arrest gene, tombola (tomb), which encodes a testis-specific CXC-domain protein that interacts with Aly. The tomb mutant phenotype is more like that of aly and comr mutants than that of achi/vis or topi mutants in terms of target gene profile and chromosome morphology. tomb encodes a chromatin-associated protein required for localisation of Aly and Comr, but not Topi, to chromatin Reciprocally, aly and comr, but not topi or achi/vis, are required to maintain the normal localisation of Tomb. tomb and aly might be components of a complex paralogous to the Drosophila dREAM/Myb-MuvB and C. elegans DRM transcriptional regulatory complexes.