The tolerance to hypoxia is defined by a time-sensitive response of the gene regulatory network in sea urchin embryos

Abstract

Deoxygenation, the reduction of oxygen level in the oceans induced by global warming and anthropogenic disturbances, is a major threat to marine life. Acute diurnal changes in oxygen levels could be especially harmful to vertebrate and sea urchin embryos that utilize endogenous hypoxia gradients to drive morphogenetic events during normal development. Here we show that the tolerance to hypoxic conditions changes between different developmental stages of the sea urchin embryo, due to the structure of the gene regulatory network (GRN). Specifically, Nodal signaling, bone morphogenetic protein (BMP) and the vascular endothelial growth factor (VEGF) pathways, are strongly disturbed by hypoxia during early embryogenesis, but are largely unaffected by hypoxia applied after dorsal-ventral axis formation. These pathways regulate hypoxia-induced vascularization in vertebrates which could suggest that they are a part of an evolutionary conserved program that uses hypoxia to drive morphogenesis. We propose that the structure of the GRN, that includes positive and negative feedback and feedforward loops, increases its resilience to changes of the initial hypoxia gradients and could help the embryos tolerate transient hypoxic conditions.

microRNA-1 represses signaling pathway components to impact embryonic structures derived from all three germ layers

“…Thus, although the change in Vegf3 expression domain may be due to miR-1’s direct suppression, our results indicate that the expression of Vegf3 in the ventral-dorsal axis may be a result of miR-1’s direct regulation of Nodal . Additionally, a previous study has shown that a loss of Bmp2/4 resulted in the position of the PMC ring to shift towards the animal pole and a radialized the embryo (Angerer et al, 2000; Layous, 2020). Interestingly, in miR-1 mimic-injected gastrulae, we observed mispatterned PMCs that migrated near the animal pole (Fig.…”

“…Both Nodal and Bmp2/4 signaling pattern the PMCs by restricting Vegf3 expression to the two lateral ectodermal domains and posterior ventral corners where the PMC clusters reside to form the skeletal rudiments within the border ectoderm-dorsal ventral margin (BE-DVM) intersection (Fig. 12A) (Duboc et al, 2010; McIntyre et al, 2013; Layous, 2020). In the ventral ectoderm, Nodal activates the expression of itself, Not1, Bmp2/4 and Vegf3 at 8-9 hpf in the ventral ectoderm (Lapraz et al, 2009; Li et al, 2012).…”

“…Nodal activation of Not1 restricts Vegf3 expression to the two lateral ectodermal domains. BE-DVM intersection is where the PMC clusters reside to form the skeletal rudiments (Duboc et al, 2010; McIntyre et al, 2013; Layous, 2020). (B) miR-1 directly suppresses transcripts (orange) such as Ets1/2, Tbr and Notch which are downstream of miR-31 target , Pmar1 (purple).…”

“…This study identifies novel functions of miR-1, by identifying its direct targets and revealing miR-1 as a multifunctional miRNA that regulates structures derived from all three germ layers in a developing embryo. where the PMC clusters reside to form the skeletal rudiments (Duboc et al, 2010;McIntyre et al, 2013;Layous, 2020). (B) miR-1 directly suppresses transcripts (orange) such as Ets1/2, Tbr and Notch which are downstream of miR-31 target, Pmar1 (purple).…”

Two Benthic Diatoms, Nanofrustulum shiloi and Striatella unipunctata, Encapsulated in Alginate Beads, Influence the Reproductive Efficiency of Paracentrotus lividus by Modulating the Gene Expression

“…In addition, S. unipunctata was able to increase the relative expression of the VEGF gene (Figure 7b), which is demonstrated to be involved in sea urchin spiculogenesis [50]. However, recent data on sea urchin gene regulatory networks (GRN) reported that hypoxia-induced stress is able to perturb the expression of HIF1A, nodal and VEGF pathways, inducing severe effects on the structure of larval skeletons [51]. This is also the case with our results, reporting a significant variation of these latter genes following diatom feeding, that might explain the anomalies in sea urchin plutei observed under light microscopy (Figure 1; see also Figure S3).…”