Abstract
The adaptation of vertebrates to different environments was associated with changes in the molecular composition and regulation of epithelia. Whales and dolphins, together forming the clade cetaceans, have lost multiple epithelial keratins during or after their evolutionary transition from life on land to life in water. It is unknown whether the changes in keratins were accompanied by gain or loss of cytoskeletal adapter proteins of the plakin family. Here we investigated whether plakin proteins are conserved in cetaceans and other vertebrates. Comparative analysis of genome sequences showed conservation of dystonin, microtubule actin crosslinking factor 1 (MACF1), plectin, desmoplakin, periplakin and envoplakin in cetaceans. By contrast, EPPK1 (epiplakin) was disrupted by inactivating mutations in all cetaceans investigated. Orthologs of EPPK1 are present in bony and cartilaginous fishes and tetrapods, indicating an evolutionary origin of EPPK1 in a common ancestor of jawed vertebrates (Gnathostomes). In many vertebrates, EPPK1 is flanked by an as-yet uncharacterized gene that encodes protein domains homologous to the carboxy-terminal segment of MACF1. We conclude that epiplakin, unlike other plakins, was lost in cetaceans.
Highlights
A single e xon[23,26] and alternative splicing that generates many isoforms of other members of this gene family, does not occur in EPPK1
We show that epiplakin has undergone pseudogenization in cetaceans and, upon comparative genomics analysis of vertebrates, identify a previously uncharacterized plakin gene which is located besides EPPK1 in diverse species of fish and tetrapods and has been lost in a common ancestor of placental mammals
Genes encoding MACF1, dystonin (DST)/BPAG1, plectin, desmoplakin, envoplakin and periplakin were conserved in the blue whale (Balaenoptera musculus), a representative of baleen whales (Mysticeti), and in the bottlenose dolphin, a representative of toothed whales (Odontoceti), whereas only unusually short coding sequences of epiplakin could be identified in these cetaceans (Fig. 1A,B; Supplementary Table S1)
Summary
A single e xon[23,26] and alternative splicing that generates many isoforms of other members of this gene family, does not occur in EPPK1. The aim of the present study was to determine whether evolutionary adaptions of the cytoskeleton in the epidermis and other epithelia were associated with changes in plakin genes. We show that epiplakin has undergone pseudogenization in cetaceans and, upon comparative genomics analysis of vertebrates, identify a previously uncharacterized plakin gene which is located besides EPPK1 in diverse species of fish and tetrapods and has been lost in a common ancestor of placental mammals
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