Muscle cell-type diversification is driven by bHLH transcription factor expansion and extensive effector gene duplications

Abstract

Animals are typically composed of hundreds of different cell types, yet mechanisms underlying the emergence of new cell types remain unclear. Here we address the origin and diversification of muscle cells in the non-bilaterian, diploblastic sea anemone Nematostella vectensis. We discern two fast and two slow-contracting muscle cell populations, which differ by extensive sets of paralogous structural protein genes. We find that the regulatory gene set of the slow cnidarian muscles is remarkably similar to the bilaterian cardiac muscle, while the two fast muscles differ substantially from each other in terms of transcription factor profiles, though driving the same set of structural protein genes and having similar physiological characteristics. We show that anthozoan-specific paralogs of Paraxis/Twist/Hand-related bHLH transcription factors are involved in the formation of fast and slow muscles. Our data suggest that the subsequent recruitment of an entire effector gene set from the inner cell layer into the neural ectoderm contributes to the evolution of a novel muscle cell type. Thus, we conclude that extensive transcription factor gene duplications and co-option of effector modules act as an evolutionary mechanism underlying cell type diversification during metazoan evolution.

Nanos2+cells give rise to germline and somatic lineages in the sea anemoneNematostella vectensis

“…To assess the consequences of the nanos2 -/- mutation on the cell type composition of the animal, we carried out single-cell RNA sequencing of an individual nanos2 -/- mutant 2-month-old juvenile polyp. We integrated the nanos2 -/- mutant cell transcriptomes with the available wildtype adult tissue catalog (14,43), newly mapped to the updated genome and transcriptome models (44). We find that the nanos2 -/- mutant exhibits no differences in the overall cell type diversity (Fig.…”