Abstract
BackgroundClassical cadherins are a metazoan-specific family of homophilic cell-cell adhesion molecules that regulate morphogenesis. Type I and type IV cadherins in this family function at adherens junctions in the major epithelial tissues of vertebrates and insects, respectively, but they have distinct, relatively simple domain organizations that are thought to have evolved by independent reductive changes from an ancestral type III cadherin, which is larger than derived paralogs and has a complicated domain organization. Although both type III and type IV cadherins have been identified in hexapods and branchiopods, the process by which the type IV cadherin evolved is still largely unclear.ResultsThrough an analysis of arthropod genome sequences, we found that the only classical cadherin encoded in chelicerate genomes was the type III cadherin and that the two type III cadherin genes found in the spider Parasteatoda tepidariorum genome exhibited a complex yet ancestral exon-intron organization in arthropods. Genomic and transcriptomic data from branchiopod, copepod, isopod, amphipod, and decapod crustaceans led us to redefine the type IV cadherin category, which we separated into type IVa and type IVb, which displayed a similar domain organization, except type IVb cadherins have a larger number of extracellular cadherin (EC) domains than do type IVa cadherins (nine versus seven). We also showed that type IVa cadherin genes occurred in the hexapod, branchiopod, and copepod genomes whereas only type IVb cadherin genes were present in malacostracans. Furthermore, comparative characterization of the type IVb cadherins suggested that the presence of two extra EC domains in their N-terminal regions represented primitive characteristics. In addition, we identified an evolutionary loss of two highly conserved cysteine residues among the type IVa cadherins of insects.ConclusionsWe provide a genomic perspective of the evolution of classical cadherins among bilaterians, with a focus on the Arthropoda, and suggest that following the divergence of early arthropods, the precursor of the insect type IV cadherin evolved through stepwise reductive changes from the ancestral type III state. In addition, the complementary distributions of polarized genomic characters related to type IVa/IVb cadherins may have implications for our interpretations of pancrustacean phylogeny.
Highlights
Classical cadherins are a metazoan-specific family of homophilic cell-cell adhesion molecules that regulate morphogenesis
Type IV cadherins are characterized by their shared domain organization, which includes seven extracellular cadherin (EC) domains, followed by the non-chordate classical cadherin (NC), cysteine-rich EGF-like (CE), and laminin-G (LG) domains [25], and they have been identified in insects, non-insect hexapods and branchiopod crustaceans [15]
We investigated both genomic and transcriptomic classical cadherin-encoding sequences from a wide range of arthropod and non-arthropod bilaterians, including chelicerates, a myriapod, and several non-branchiopod crustaceans, to determine whether type IV cadherin genes evolved from type III cadherin genes before, during, or after the early divergence of arthropods, and whether type IV cadherins arose from the type III state abruptly or through an intermediate state
Summary
Classical cadherins are a metazoan-specific family of homophilic cell-cell adhesion molecules that regulate morphogenesis. Type I and type IV cadherins in this family function at adherens junctions in the major epithelial tissues of vertebrates and insects, respectively, but they have distinct, relatively simple domain organizations that are thought to have evolved by independent reductive changes from an ancestral type III cadherin, which is larger than derived paralogs and has a complicated domain organization. Both type III and type IV cadherins have been identified in hexapods and branchiopods, the process by which the type IV cadherin evolved is still largely unclear. Up to 17 EC domains have been observed in the classical cadherins of bilaterians, 25 or more have been reported in the classical cadherinencoding genes of non-bilaterian metazoans [2, 17]
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