Genetic dissection of the planarian reproductive system through characterization of Schmidtea mediterranea CPEB homologs

•Characterization CPEB1 and CPEB2 expression and function in Schmidtea mediterranea.•Neuronal CPEB2 drives planarian reproductive maturation non-autonomously.•Transcriptomic analysis of germline and somatic reproductive structures in S. mediterranea.•Identification of genes required for germline development and capsule formation.

Cytoplasmic polyadenylation is a mechanism of mRNA regulation prevalent in metazoan germ cells; it is largely dependent on Cytoplasmic Polyadenylation Element Binding proteins (CPEBs). Two CPEB homologs were identified in the planarian Schmidtea mediterranea. Smed-CPEB1 is expressed in ovaries and yolk glands of sexually mature planarians, and required for oocyte and yolk gland development. In contrast, Smed-CPEB2 is expressed in the testes and the central nervous system; its function is required for spermatogenesis as well as non-autonomously for development of ovaries and accessory reproductive organs. Transcriptome analysis of CPEB knockdown animals uncovered a comprehensive collection of molecular markers for reproductive structures in S. mediterranea, including ovaries, testes, yolk glands, and the copulatory apparatus. Analysis by RNA interference revealed contributions for a dozen of these genes during oogenesis, spermatogenesis, or capsule formation. We also present evidence suggesting that Smed-CPEB2 promotes translation of Neuropeptide Y-8, a prohormone required for planarian sexual maturation. These findings provide mechanistic insight into potentially conserved processes of germ cell development, as well as events involved in capsule deposition by flatworms.

Graphical abstractNeuronal Smed-CPEB2 expression (gray box) drives maturation of the planarian reproductive system non-autonomously (dashed lines). Expression of additional genes in the ovaries (pink), testes (blue), and yolk glands (yellow) is required for development and function of oocytes, sperm, and yolk cells, respectively.Download high-res image (350KB)Download full-size image