Studying evolution of the primary body axis in vivo and in vitro

Abstract

The metazoan body plan is established during early embryogenesis via collective cell rearrangements and evolutionarily conserved gene networks, as part of a process commonly referred to as gastrulation. While substantial progress has been achieved in terms of characterizing the embryonic development of several model organisms, underlying principles of many early patterning processes nevertheless remain enigmatic. Despite the diversity of (pre-)gastrulating embryo and adult body shapes across the animal kingdom, the body axes, which are arguably the most fundamental features, generally remain identical between phyla. Recently there has been a renewed appreciation of ex vivo and in vitro embryo-like systems to model early embryonic patterning events. Here, we briefly review key examples and propose that similarities in morphogenesis and associated gene expression dynamics may reveal an evolutionarily conserved developmental mode as well as provide further insights into the role of external or extraembryonic cues in shaping the early embryo. In summary, we argue that embryo-like systems can be employed to inform previously uncharted aspects of animal body plan evolution as well as associated patterning rules.

Sculpting with stem cells: how models of embryo development take shape

“…Interestingly, these models do more reliably mimic the architecture of the pre- and peri-implantation embryo, but (at present) cannot further develop into the later developmental stages modelled by gastruloids. This might be due to constrained development in the co-culture setting, which is absent in the culture of stembryos of the gastruloid ‘family’ ( Anlas and Trivedi, 2021 ).…”

“…an in vivo -like body plan with an axial neural tube flanked by bilateral rows of somites), the stembryo may not necessarily employ the same developmental mode to reach this state. In contrast, stembryos may engage parallel but distinct modes that, nevertheless, ultimately converge on the same body plan ( Anlas and Trivedi, 2021 ). Employment of different developmental trajectories to reach a similar morphological state has been observed in Nematostella vectensis dissociation-reaggregation experiments, whereby aggregates of dissociated gastrula cells use an alternative developmental mode normally reserved for distantly related members of the same phylum ( Kirillova et al, 2018 ).…”

Polarity Events in the Drosophila melanogaster Oocyte

“…A subclass of metazoans, called bilaterians, define two body axes during embryonic development, the anterior-posterior (AP) axis being the first and the dorsal-ventral (DV) axis following as second symmetry break ( Kimelman and Martin, 2012 ; Anlas and Trivedi, 2021 ). For most species the AP axis defines head and tail.…”

Organoid-based single-cell spatiotemporal gene expression landscape of human embryonic development and hematopoiesis

“…Stem-cell-derived embryos reconstitute the developmental process and cell-cell interactions. Previous studies have modeled human and mouse embryonic development from pluripotent stem cells or directly used primary embryos (Aguilera-Castrejon et al, 2021; Alsinet et al, 2022; Anlas and Trivedi, 2021; Atkins et al, 2022; Ávila-González et al, 2022; Decembrini et al, 2020; Diaz-Cuadros et al, 2020; Lancaster et al, 2013; Mackinlay et al, 2021; Matsuda et al, 2020; Minn et al, 2020; Morgani et al, 2018; Saykali et al, 2019; Shahbazi et al, 2016; Simunovic et al, 2022; Tamaoki et al, 2021). Synthetic embryos recapitulated gastrulation and organogenesis by assembling pluripotent stem cells and their extraembryonic derivatives (Amadei et al, 2022; Harrison et al, 2017).…”