Abstract

The evolution of amniotes has involved major molecular innovations in the epidermis. In particular, distinct structural proteins that undergo covalent cross-linking during cornification of keratinocytes facilitate the formation of mechanically resilient superficial cell layers and help to limit water loss to the environment. Special modes of cornification generate amniote-specific skin appendages such as claws, feathers, and hair. In mammals, many protein substrates of cornification are encoded by a cluster of genes, termed the epidermal differentiation complex (EDC). To provide a basis for hypotheses about the evolution of cornification proteins, we screened for homologs of the EDC in non-mammalian vertebrates. By comparative genomics, de novo gene prediction and gene expression analyses, we show that, in contrast to fish and amphibians, the chicken and the green anole lizard have EDC homologs comprising genes that are specifically expressed in the epidermis and in skin appendages. Our data suggest that an important component of the cornified protein envelope of mammalian keratinocytes, that is, loricrin, has originated in a common ancestor of modern amniotes, perhaps during the acquisition of a fully terrestrial lifestyle. Moreover, we provide evidence that the sauropsid-specific beta-keratins have evolved as a subclass of EDC genes. Based on the comprehensive characterization of the arrangement, exon–intron structures and conserved sequence elements of EDC genes, we propose new scenarios for the evolutionary origin of epidermal barrier proteins via fusion of neighboring S100A and peptidoglycan recognition protein genes, subsequent loss of exons and highly divergent sequence evolution.

Highlights

  • Adaptations of the epidermis played key roles in the evolution of vertebrates that colonized the land in the lower Carboniferous (Chuong et al 2002)

  • The results of this study demonstrate that mammals and sauropsids have an epidermal differentiation complex (EDC), implying that the EDC was already present in their last common ancestor

  • S100A genes and peptidoglycan recognition proteins (PGLYRPs) genes were found, indicating that the EDC originated after the divergence of amniotes from these clades of vertebrates

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Summary

Introduction

Adaptations of the epidermis played key roles in the evolution of vertebrates that colonized the land in the lower Carboniferous (Chuong et al 2002). The evolution of an efficient protection against cutaneous water loss was a crucial event in the transition of amniotes to a fully terrestrial lifestyle (Alibardi 2003; Maderson 2003; Madison 2003). Later, evolutionary innovations such as hair, mammary glands, and feathers, all of which represent modifications of the epidermis with contributions of the underlying mesenchyme (Wu et al 2004), were the defining events in the appearance of mammals and birds, respectively. The most abundant proteins in the mammalian cornified envelope are involucrin, small proline-rich proteins (SPRRs), S100A proteins and loricrin, with the latter reportedly making up approximately 70% of total proteins (Rice and Green 1977, 1979; Steinert and Marekov 1995; Robinson et al 1997; Kalinin et al 2002)

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