Modular co-option of cardiopharyngeal genes during non-embryonic myogenesis

Abstract

Background In chordates, cardiac and body muscles arise from different embryonic origins. In addition, myogenesis can be triggered in adult organisms, during asexual development or regeneration. In non-vertebrate chordates like ascidians, muscles originate from embryonic precursors regulated by a conserved set of genes that orchestrate cell behavior and dynamics during development. In colonial ascidians, besides embryogenesis and metamorphosis, an adult can propagate asexually via blastogenesis, skipping embryo and larval stages, and form anew the adult body, including the complete body musculature. Results To investigate the cellular origin and mechanisms that trigger non-embryonic myogenesis, we followed the expression of ascidian myogenic genes during Botryllus schlosseri blastogenesis and reconstructed the dynamics of muscle precursors. Based on the expression dynamics of Tbx1/10 , Ebf, Mrf, Myh3 for body wall and of FoxF, Tbx1/10, Nk4, Myh2 for heart development, we show that the embryonic factors regulating myogenesis are only partially co-opted in blastogenesis, and that markers for muscle precursors are expressed in two separate domains: the dorsal tube and the ventral mesenchyma. Conclusions Regardless of the developmental pathway, non-embryonic myogenesis shares a similar molecular and anatomical setup as embryonic myogenesis, but implements a co-option and loss of molecular modules. We then propose that the cellular precursors contributing to heart and body muscles may have different origins and may be coordinated by different developmental pathways. Electronic supplementary material The online version of this article (10.1186/s13227-019-0116-7) contains supplementary material, which is available to authorized users.

Novel budding mode in Polyandrocarpa zorritensis: a model for comparative studies on asexual development and whole body regeneration

“…Studies of two different NED modes in Botryllus schlosseri , peribranchial and vascular budding, show that the double vesicle stage exhibits the first spatial segregation of cell fate domains, notably for ectodermal and endodermal identities [33–35]. During vasal budding, the tissue differentiation and the organogenesis also start from the double vesicle stage, wherein organ primordia appears as foldings of the inner vesicle [10].…”

Regulation and evolution of muscle development in tunicates

“…In contrast, the heart appears to derive from an invagination of the peribranchial epithelium (endoderm) [79, 247]. Recent molecular analysis of body wall muscle and heart development during Botryllus blastogenesis further confirmed this uncoupling of cardiopharyngeal fates and lineages, suggesting that different parts of the embryonic CPhM regulatory network have been partially co-opted in different blastozooid lineages [263].…”

The eventful history of nonembryonic development in tunicates

“…Once again, further morphological descriptions of the budding tissues and clarification of the deepest nodes of the tunicate phylogeny are needed (Tsagkogeorga et al, 2009). (Prünster et al, 2018(Prünster et al, , 2019Ricci, Cabrera, et al, 2016;Ricci, Chourasia, et al 2016;Tiozzo et al, 2005). The redeployment of embryonic developmental programs during asexual development and regeneration is not a novel idea in the literature.…”