Chromatin state dynamics of autosomes and the B chromosome during spermatogenesis in Pseudococcus viburni

The mealybug Pseudococcus viburni is a plant-feeding insect with a non-Mendelian genetic system known as paternal genome elimination (PGE). In PGE, males eliminate their paternally inherited chromosomes during meiosis, transmitting only the maternal genome to the next generation. This involves genome-wide imprinting, where paternal chromosomes are heterochromatinised in embryogenesis and throughout adulthood. In this species, a non-essential B chromosome can escape paternal genome elimination, thereby enhancing its transmission rate to the next generation. Previous studies show that the B chromosome escapes elimination by changing its chromatin compaction during meiosis to resemble that of maternal chromosomes. Although the exact mechanism underlying this change is poorly understood. Here we investigated histone methylation and acetylation modifications, as well as the Heterochromatin Protein 1 (HP1), to characterise differences between maternal, paternal and B chromosomes during male meiosis of P. viburni. Maternal and paternal chromosomes show distinct histone modification patterns, with marks associated with euchromatin present on maternal chromosomes and marks associated with heterochromatin present on paternal chromosomes. We then identified key histone modification changes that coincide with chromatin remodelling of the B chromosome, which allows it to segregate with maternal chromosomes. In addition, we showed that these chromatin modifications occur regardless of the parental origin of the B chromosome. Overall, our findings support the role of histone modifications for proper chromosome segregation during meiosis in mealybugs and provide insight into the mechanisms by which the B chromosome exploits PGE for its preferential transmission.