Sasaki Mizuki, Akiyama-Oda Yasuko, Oda Hiroki
Laboratory of Evolutionary Cell and Developmental Biology, JT Biohistory Research Hall, 1-1 Murasaki-cho, Takatsuki, 569-1125, Osaka, Japan.
Current address: Department of Parasitology, Asahikawa Medical University, 2-1-1-1 Midorigaoka-higashi, Asahikawa, 078-8510, Hokkaido, Japan.
BMC Evol Biol. 2017 Jun 17;17(1):142. doi: 10.1186/s12862-017-0991-2.
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. 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.
Through 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.
We 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.
经典钙黏蛋白是后生动物特有的一类同源性细胞间黏附分子，可调节形态发生。该家族中的I型和IV型钙黏蛋白分别在脊椎动物和昆虫的主要上皮组织的黏着连接中发挥作用，但它们具有独特且相对简单的结构域组织，据认为是由祖先的III型钙黏蛋白通过独立的简化变化进化而来，III型钙黏蛋白比衍生的旁系同源物更大，且具有复杂的结构域组织。尽管在六足动物和鳃足动物中都已鉴定出III型和IV型钙黏蛋白，但IV型钙黏蛋白的进化过程仍 largely不清楚。
通过对节肢动物基因组序列的分析，我们发现螯肢动物基因组中编码的唯一经典钙黏蛋白是III型钙黏蛋白，并且在蜘蛛温血拟壁钱（Parasteatoda tepidariorum）基因组中发现的两个III型钙黏蛋白基因在节肢动物中呈现出复杂但祖传的外显子 - 内含子组织。来自鳃足动物、桡足动物、等足动物、端足动物和十足目甲壳动物的基因组和转录组数据使我们重新定义了IV型钙黏蛋白类别，我们将其分为IVa型和IVb型，它们显示出相似的结构域组织，除了IVb型钙黏蛋白比IVa型钙黏蛋白具有更多的细胞外钙黏蛋白（EC）结构域（分别为九个和七个）。我们还表明，IVa型钙黏蛋白基因存在于六足动物、鳃足动物和桡足动物的基因组中，而软甲纲动物中仅存在IVb型钙黏蛋白基因。此外，对IVb型钙黏蛋白的比较特征分析表明，其N端区域存在两个额外的EC结构域代表了原始特征。此外，我们在昆虫的IVa型钙黏蛋白中鉴定出两个高度保守的半胱氨酸残基的进化丢失。
我们从基因组角度提供了两侧对称动物中经典钙黏蛋白进化的观点，重点关注节肢动物，并表明在早期节肢动物分化之后，昆虫IV型钙黏蛋白的前体通过从祖先III型状态的逐步简化变化而进化。此外，与IVa/IVb型钙黏蛋白相关的极化基因组特征的互补分布可能对我们解释泛甲壳动物系统发育有影响。
