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Cytoplasmic Polyadenylation Element Binding (CPEB) proteins are translational regulators that can either activate or repress translation depending on the target mRNA and the specific biological context. There are two CPEB subfamilies and most animals have one or more genes from each.  Drosophila  has a single CPEB gene,  orb  and  orb2 , from each subfamily.  orb  expression is only detected at high levels in the germline and has critical functions in oogenesis but not spermatogenesis. By contrast,  orb2  is broadly expressed in the soma; and previous studies have revealed important functions in asymmetric cell division, viability, motor function, learning, and memory. Here we show that  orb2  is also expressed in the adult male germline and that it has essential functions in programming the progression of spermatogenesis from meiosis through differentiation. Like the translational regulators  boule (bol)  and  off-schedule (ofs) ,  orb2  is required for meiosis and  orb2  mutant spermatocytes undergo a prolonged arrest during the meiotic G2-M transition. However,  orb2  differs from  boule  and  off-schedule  in that this arrest occurs at a later step in meiotic progression after the synthesis of the meiotic regulator  twine .  orb2  is also required for the orderly differentiation of the spermatids after meiosis is complete. The differentiation defects in  orb2  mutants include abnormal elongation of the spermatid flagellar axonemes, a failure in individualization and improper post-meiotic gene expression. Amongst the  orb2  differentiation targets are  orb  and two other mRNAs, which are transcribed post-meiotically and localized to the tip of the flagellar axonemes. Additionally, analysis of a partial loss of function  orb2  mutant suggests that the  orb2  differentiation phenotypes are independent of the earlier arrest in meiosis.

The CPEB Protein Orb2 Has Multiple Functions during Spermatogenesis in Drosophila melanogaster