Protamine lacking piscine spermatozoa are transcriptionally active

Transcriptional quiescence of post-meiotic spermatozoa associated with protamine-mediated chromatin condensation is widely recognized in animals. How sperm acquire the extratesticular maturational competence to move and fertilize the egg is therefore thought to occur via non-transcriptional mechanisms. Here, using transcriptional profiling during spermatozoon differentiation in a fish that does not condense chromatin with protamines, we uncover spatially distinct roles of the GnRH receptor and PDGF signaling pathways between the somatic epithelia of the extratesticular ducts and the maturing spermatozoa. In vitro induction and inhibition experiments demonstrate that the endocrine signaling pathways are conserved in different lineages of fish and activate de novo transcription of spermatozoon genes required for the acquisition of full motility. These experiments further confirmed that mitochondrial translation is important for sperm maturation in anamniotes as in amniotes, but that transcriptional quiescence of post-meiotic spermatozoa is not a pan vertebrate phenomenon. On the contrary, the data show that the identified signal transduction pathways between the soma and the sperm upregulate effector genes essential for maturational competence and male fertility.