Conserved regulatory state expression controlled by divergent developmental gene regulatory networks in echinoids

Abstract

Evolution of the animal body plan is driven by changes in developmental gene regulatory networks (GRNs), but how networks change to control novel developmental phenotypes remains, in most cases, unresolved. Here, we address GRN evolution by comparing the endomesoderm GRN in two echinoid sea urchins, Strongylocentrotus purpuratus and Eucidaris tribuloides, with at least 268 million years of independent evolution. We first analyzed the expression of twelve transcription factors and signaling molecules of the S. purpuratus GRN in E. tribuloides embryos, showing that orthologous regulatory genes are expressed in corresponding endomesodermal cell fates in the two species. However, perturbation of regulatory genes revealed that important regulatory circuits of the S. purpuratus GRN are significantly different in E. tribuloides. For example, mesodermal Delta/Notch signaling controls exclusion of alternative cell fates in E. tribuloides but controls mesoderm induction and activation of a positive feedback circuit in S. purpuratus. These results indicate that the architecture of the sea urchin endomesoderm GRN evolved by extensive gain and loss of regulatory interactions between a conserved set of regulatory factors that control endomesodermal cell fate specification.

FGF signaling induces mesoderm in members of Spiralia

“…Different circuitries of GRNs orchestrating the formation of homologous mesodermal derivatives have been described in some animals and support the idea that the evolution of GRNs is mainly based on the developmental regulatory demands of each network Erkenbrack, 2016;Erkenbrack et al, 2018;Hinman and Davidson, 2007). Therefore, alterations in GRN circuitries do not necessarily reflect convergent evolution of the resulting tissues (Davidson and Erwin, 2006;Peter, 2020), but can also be a product of developmental system drift (True and Haag, 2001).…”

Evolution of abbreviated development inHeliocidaris erythrogrammadramatically re-wired the highly conserved sea urchin developmental gene regulatory network to decouple signaling center function from ultimate fate

“…We found both similarities and striking differences between the two GRNs. Our observation of a Delta signaling input into alx1 and hesC in H. erythrogramma resembles the cidaroid GRN [49,51]; however, while cidaroids deploy Tbr in NSM such as pigment cells [51,52] H. erythrogramma does not show localized tbr expression in any mesenchyme cells. Finally, while some elements appear to be conserved from the ancestral endomesodermal GRN rather than the SM-GRN, such as Wnt and Delta control of ets1/2 transcription, other connections, such as Wnt signaling activation of hesC appear to be H. erythrogramma novelties.…”

“…We also examined and excluded the hypothesis that H. erythrogramma ’s GRN is similar to the modified GRN activated in a planktotroph embryo experimentally depleted of SM cells, the replacement SM-GRN [47,48]. Instead, we found evidence that while many gene linkages remain intact, the H. erythrogramma GRN has several novel features, as well as features that resemble non-euechinoid urchins’ GRN [49-52]. Our results indicate a surprising degree of lability in the early developmental GRN associated with the evolution of lecithotrophy in H. erythrogramma .…”

Stepping From Modeling Cancer Plasticity to the Philosophy of Cancer

“…Could this hypothesis be tested by evaluation of coherence in the expression of transcription factors responsible for the differentiations of mandatorily compatible tissues at different stages of their differentiations? This could rely on the investigation of intercellular communication means regulating GRNs in different cells, as described in Peter and Davidson ( 2017 ) and Erkenbrack et al ( 2018 ).…”