Establishing a paternal chromosome identity in the Drosophila male germline

In many animals, mature sperm chromatin is organized with sperm-specific chromosomal proteins known as protamines. Complete or partial elimination of nucleosomes occur during the histone-to-protamine transition, a complex chromatin reorganization process that takes place during spermiogenesis, the differentiation of post-meiotic spermatids. Although protamines are generally thought to play a critical role in sperm chromatin compaction, their actual function remains mysterious. Through the analysis of a rare Drosophila paternal effect mutant named paternal loss (pal), we have discovered that the removal of histones in insect sperm is critical to maintain the epigenetic identity of paternal chromosomes at fertilization. Sperm from pal mutant males aberrantly retain H3-H4 tetrasomes without affecting their ability to fertilize eggs. However, at fertilization, pal chromosomes are mistaken for maternal chromosomes and engage into a deleterious pseudo-meiotic division, leading to the sporadic loss of paternal chromosomes in the early embryo. I will also present our unpublished characterization of a new paternal effect mutant with a pal-like phenotype and discuss our findings in the context of sperm chromatin evolution in animals.