Sox9 Expression in Amniotes: Species-Specific Differences in the Formation of Digits

Abstract

In tetrapods the digit pattern has evolved to adapt to distinct locomotive strategies. The number of digits varies between species or even between hindlimb and forelimb within the same species. These facts illustrate the plasticity of embryonic limb autopods. Sox9 is a precocious marker of skeletal differentiation of limb mesenchymal cells. Its pattern of expression in the developing limb has been widely studied and reflects the activity of signaling cascades responsible for skeletogenesis. In this assay we stress previously overlooked differences in the pattern of expression of Sox9 in limbs of avian, mouse and turtle embryos which may reflect signaling differences associated with distinct limb skeletal morphologies observed in these species. Furthermore, we show that Sox9 gene expression is higher and maintained in the interdigital region in species with webbed digits in comparison with free digit animals.

The missing segment of the autopod 1st ray: new insights from a morphometric study of the human hand

“…The studied differences support mechanisms of skeletal diversification based on a combination of a distinct distribution of finely tuned signals by the regulatory genes responsible for growth (Montero et al. ).…”

“…Hence, the analysis of phylogenetically related but phenotypically different species has provided important clues accounting for limb morphogenesis and the autopod development in particular (Moore et al 2015). The studied differences support mechanisms of skeletal diversification based on a combination of a distinct distribution of finely tuned signals by the regulatory genes responsible for growth (Montero et al 2017).…”

“…; Montero et al. ) and may explain how digits differ in morphology. Hence, the analysis of phylogenetically related but phenotypically different species has provided important clues accounting for limb morphogenesis and the autopod development in particular (Moore et al.…”

“…The variability of the vertebrate autopod has so far raises unanswered questions, similar to that of the human 1st ray, such as digit loss, developmental variability and the origin of the avian hand (Vargas & Fallon, 2005;Bever et al 2011;Young et al 2011). Subtle Sox9 expression differences have been shown to be consistent with heterochrony detected in the stages of chondrification (Richardson et al 2009;Montero et al 2017) and may explain how digits differ in morphology. Hence, the analysis of phylogenetically related but phenotypically different species has provided important clues accounting for limb morphogenesis and the autopod development in particular (Moore et al 2015).…”

Early limb patterning in the direct‐developing salamander Plethodon cinereus revealed by sox9 and col2a1

“…Sox9 is an HMG‐box‐containing transcription factor that can reveal the initial differentiation of pre‐chondrocytes before they form extracellular matrix (Chimal‐Monroy et al, ; Welten, Verbeek, Meijer, & Richardson, ; Kerney & Hanken, ; Kerney, Gross, & Hanken, ; Lorda‐Diez, Montero, Diaz‐Mendoza, Garcia‐Porrera, & Hurle, ; Hayashi et al, ). In situ hybridizations detecting sox9 mRNA are a consistently useful technique for analyzing early skeletal patterning (de Bakker et al, ; Guimond et al, ; Kerney & Hanken, ; Kerney et al, ; Kumar et al, ; Montero et al, ). The gene for type‐II collagen, col2a1 , is a direct target of Sox9 transcriptional activation in the chondrocyte lineage of amniotes and amphibians (Bell et al, ; Kerney, Hall, & Hanken, ; Lefebvre, Huang, Harley, Goodfellow, & de Crombrugghe, ; Ng et al, ).…”