Comparative Genomics Identifies Epidermal Proteins Associated with the Evolution of the Turtle Shell

Abstract

The evolution of reptiles, birds, and mammals was associated with the origin of unique integumentary structures. Studies on lizards, chicken, and humans have suggested that the evolution of major structural proteins of the outermost, cornified layers of the epidermis was driven by the diversification of a gene cluster called Epidermal Differentiation Complex (EDC). Turtles have evolved unique defense mechanisms that depend on mechanically resilient modifications of the epidermis. To investigate whether the evolution of the integument in these reptiles was associated with specific adaptations of the sequences and expression patterns of EDC-related genes, we utilized newly available genome sequences to determine the epidermal differentiation gene complement of turtles. The EDC of the western painted turtle (Chrysemys picta bellii) comprises more than 100 genes, including at least 48 genes that encode proteins referred to as beta-keratins or corneous beta-proteins. Several EDC proteins have evolved cysteine/proline contents beyond 50% of total amino acid residues. Comparative genomics suggests that distinct subfamilies of EDC genes have been expanded and partly translocated to loci outside of the EDC in turtles. Gene expression analysis in the European pond turtle (Emys orbicularis) showed that EDC genes are differentially expressed in the skin of the various body sites and that a subset of beta-keratin genes within the EDC as well as those located outside of the EDC are expressed predominantly in the shell. Our findings give strong support to the hypothesis that the evolutionary innovation of the turtle shell involved specific molecular adaptations of epidermal differentiation.

Identification and comparative analysis of the epidermal differentiation complex in snakes

“…The EDCs of the Burmese python ( Python bivittatus ) and the king cobra ( Ophiophagus hannah ) were defined as the genomic regions flanked by S100A genes, like in other amniotes3033. The gene complement of the EDC of these snakes was identified by tBLASTn searches using EDC-encoded proteins of A. carolinensis , chicken and humans as queries and by de novo prediction of genes in an iterative process, as described previously33.…”

“…Based on the dermatologically relevant characterization of human epidermal barrier genes, we have screened non-mammalian tetrapods for homologs of a gene cluster known as the Epidermal Differentiation Complex (EDC)3031323334. Genes encoding S100 fused-type proteins (SFTPs), which are homologous to a subgroup of mammalian EDC genes35, were found in amphibians34, and more complex gene clusters homologous to the mammalian EDC were identified in the chicken3032, in the green anole lizard ( Anolis carolinensis )30 and in turtles33.…”

Filaggrin has evolved from an “S100 fused‐type protein” (SFTP) gene present in a common ancestor of amphibians and mammals

“…[11][12][13] Our recent studies have suggested that SFTPs originated prior to the diversification of amniotes (mammals, reptiles and birds). [14][15][16] However, the evolutionary origin of SFTPs has remained uncertain because of incomplete genome data of the next relatives of amniotes, the amphibians. Here, we performed a comparative genomics study to infer the time of origin of SFTPs and to estimate when sequence elements of SFTPs, such as the carboxy-terminal motif implicated in binding keratin filaments, [14,17] have evolved.…”

Microscopic and immunohistochemical analyses of the claw of the nesting dinosaur, Citipati osmolskae

“…Alpha-keratins [5] are widely distributed across all vertebrates, consistent with an early evolutionary origin and comprise an alpha-helical central rod, producing a 10 nm intermediate filament [6]. Beta-keratins (or 'corneous beta-proteins' [7][8][9][10]) are insoluble, rigid, fibrous, structural proteins distinct from alpha-keratins in composition and structure. They are expressed only in reptiles and birds (sauropsids) [11][12][13], suggesting that this gene family originated after the divergence of sauropsids from other vertebrates [5,[14][15][16].…”