First Transcriptomic Insights into the Invertebrate Placental Analogue: Differential Gene Expression in Gonozooids of Crisiella producta (Bryozoa, Cyclostomatida).

AbstractPlacentotrophy, the most complex mode of nutrient transfer from a parental organism to developing embryos, has evolved multiple times among Metazoa, being a well-known example of convergent evolution. However, the molecular mechanisms underlying the development and physiology of placenta-like systems in invertebrates remain unknown. Phylum Bryozoa is an excellent model for studying the evolution of placentotrophy, since this reproductive strategy evolved repeatedly within this group. Cyclostome bryozoans are characterized by a unique syncytial/coenocytic placental analogue that nourishes polyembryonic progeny inside polymorphic zooids (gonozooids). Here, we provide transcriptomic analysis of the gonozooids in the cyclostome Crisiella producta. We generated a high-quality transcriptome assembly from reproducing colonies of C. producta and compared gene expression between feeding zooids and gonozooid developmental stages. Our analyses identified a core set of candidate transport proteins likely involved in nutrient delivery to progeny, as well as pronounced activation of extracellular matrix development and remodeling, consistent with ultrastructural data. Additionally, we tested the hypothesis of endocrine regulation in gonozooid development and revealed differential expression of insulin-like neuropeptides and the conserved nuclear receptor FTZ-F1. Together, these findings support the hypothesis that bryozoan placentotrophy is regulated by endocrine signaling, provide evidence for the transport function of the cyclostome placental analogue, and highlight the importance of the extracellular matrix in these processes.