Hepatocyte growth factor is crucial for development of the carapace in turtles

Abstract

Turtles are characterized by their shell, composed of a dorsal carapace and a ventral plastron. The carapace first appears as the turtle-specific carapacial ridge (CR) on the lateral aspect of the embryonic flank. Accompanying the acquisition of the shell, unlike in other amniotes, hypaxial muscles in turtle embryos appear as thin threads of fibrous tissue. To understand carapacial evolution from the perspective of muscle development, we compared the development of the muscle plate, the anlage of hypaxial muscles, between the Chinese soft-shelled turtle, Pelodiscus sinensis, and chicken embryos. We found that the ventrolateral lip (VLL) of the thoracic dermomyotome of P. sinensis delaminates early and produces sparse muscle plate in the lateral body wall. Expression patterns of the regulatory genes for myotome differentiation, such as Myf5, myogenin, Pax3, and Pax7 have been conserved among amniotes, including turtles. However, in P. sinensis embryos, the gene hepatocyte growth factor (HGF), encoding a regulatory factor for delamination of the dermomyotomal VLL, was uniquely expressed in sclerotome and the lateral body wall at the interlimb level. Implantation of COS-7 cells expressing a HGF antagonist into the turtle embryo inhibited CR formation. We conclude that the de novo expression of HGF in the turtle mesoderm would have played an innovative role resulting in the acquisition of the turtle-specific body plan.

Hatchlings of the Marine Turtle Lepidochelys olivacea Display Signs of Prenatal Stress at Emergence after Being Incubated in Man-Made Nests: A Preliminary Report

“…Hence, future experiments must evaluate whether MMN incubation decreases yolk and egg size and/or if it shifts their biochemical composition. It will be also useful to study expression and methylation patterns of genes that are involved in modulating fetal growth (e.g., hepatocyte growth factor; Kawashima-Ohya et al, 2011). In spite of these limitations, the differential effects (and the absence of them; e.g., carapace length) that MMN incubatory conditions had on various morphological parameters and on corticosterone serum levels still support the general inference of this work, namely, MNN promotes stress in turtle fetuses.…”

Comparative analysis of pleurodiran and cryptodiran turtle embryos depicts the molecular ground pattern of the turtle carapacial ridge

“…Accordingly, we found that b-catenin was specifically translocated into the nucleus of the CR ectodermal cells at stage TK14, when the CR is clearly visible (Kuraku et al, 2005); no equivalent expression patterns have been observed in non-turtle embryos. Although we had previously hypothesized that HGF/c-Met pathway might have had a role in the b-catenin translocation, Hgf is, while nearby, actually not expressed in the CR (Kawashima-Ohya et al, 2011, Nagashima et al, 2014. However, the distribution of the HGF protein and a putative role in the CR formation is unknown, and thus require further investigation.…”

The origin and loss of periodic patterning in the turtle shell

“…Recent studies of turtle development and paleontology (CebraThomas et al, 2005;Nagashima et al, 2007;Li et al, 2008;Moustakas, 2008;Sánchez-Villagra et al, 2009;Kawashima-Ohya et al, 2011;Kuratani et al, 2011;Hirasawa et al, 2013) have advanced our understanding of the evolutionary origin of turtles and the genetic and cellular interactions that regulate various aspects of bone development in the carapace. However, the genetic regulation of the origin and evolution of the epidermal scutes has not been addressed.…”