Association of zygotic piRNAs derived from paternal P elements with hybrid dysgenesis in Drosophila melanogaster

Keiko Tsuji Wakisaka, Kenji Ichiyanagi, Seiko Ohno, Masanobu Itoh

P -element transposition in the genome causes P-M hybrid dysgenesis inDrosophila melanogaster. Maternally deposited piRNAs suppressP-element transposition in the progeny, linking them to P-M phenotypes; however, the role of zygotic piRNAs derived from paternalPelements is poorly understood. To elucidate the molecular basis ofP-element suppression by zygotic factors, we investigated the genomic constitution andP-element piRNA production derived from fathers. As a result, we characterized males of naturally derived Q, M' and P strains, which show different capacities for theP-element mobilizations introduced after hybridizations with M-strain females. The amounts of piRNAs produced in ovaries of F1 hybrids varied among the strains and were influenced by the characteristics of the piRNA clusters that harbored thePelements. Importantly, while both the Q- and M'-strain fathers restrict theP-element mobilization in ovaries of their daughters, the Q-strain fathers supported the production of the highest piRNA expression in the ovaries of their daughters, and the M' strain carriesKPelements in transcriptionally active regions directing the highest expression ofKPelements in their daughters. Interestingly, the zygoticP-element piRNAs, but not theKPelement mRNA, contributed to the variations inPtransposition immunity in the granddaughters. The piRNA-cluster-embeddedPelements and the transcriptionally activeKPelements from the paternal genome are both important suppressors ofPelement activities that are co-inherited by the progeny. Expression levels of theP-element piRNA andKP-element mRNA vary among F1 progeny due to the constitution of the paternal genome, and are involved in phenotypic variation in the subsequent generation.