School of Biological Sciences, The University of Queensland, Brisbane, Queensland, Australia.
Mol Biol Evol. 2012 Jul;29(7):1823-36. doi: 10.1093/molbev/mss060. Epub 2012 Feb 1.
Laminins are a family of multidomain glycoproteins that are important contributors to the structure of metazoan extracellular matrices. To investigate the origin and evolution of the laminin family, we characterized the full complement of laminin-related genes in the genome of the sponge, Amphimedon queenslandica. As a representative of the Demospongiae, a group consistently placed within the earliest diverging branch of animals by molecular phylogenies, Amphimedon is uniquely placed to provide insight into early steps in the evolution of metazoan gene families. Five Amphimedon laminin-related genes possess the conserved molecular features, and most of the domains found in bilaterian laminins, but all display domain architectures distinct from those of the canonical laminin chain types known from model bilaterians. This finding prompted us to perform a comparative genomic analysis of laminins and related genes from a choanoflagellate and diverse metazoans and to conduct phylogenetic analyses using the conserved Laminin N-terminal domain in order to explore the relationships between genes with distinct architectures. Laminin-like genes appear to have originated in the holozoan lineage (choanoflagellates + metazoans + several other unicellular opisthokont taxa), with several laminin domains originating later and appearing only in metazoan (animal) or eumetazoan (placozoans + ctenophores + cnidarians + bilaterians) laminins. Typical bilaterian α, β, and γ laminin chain forms arose in the eumetazoan stem and another chain type that is conserved in Amphimedon, the cnidarian, Nematostella vectensis, and the echinoderm, Strongylocentrotus purpuratus, appears to have been lost independently from the placozoan, Trichoplax adhaerens, and from multiple bilaterians. Phylogenetic analysis did not clearly reconstruct relationships between the distinct laminin chain types (with the exception of the α chains) but did reveal how several members of the netrin family were generated independently from within the laminin family by duplication and domain shuffling and by domain loss. Together, our results suggest that gene duplication and loss and domain shuffling and loss all played a role in the evolution of the laminin family and contributed to the generation of lineage-specific diversity in the laminin gene complements of extant metazoans.
层粘连蛋白是一类具有多种结构域的糖蛋白，是后生动物细胞外基质结构的重要组成部分。为了研究层粘连蛋白家族的起源和进化，我们对海绵动物（属于多孔动物门，分子系统发生学将其置于动物最早分化的分支上）澳大利亚美神虫基因组中的全套层粘连蛋白相关基因进行了鉴定。由于澳大利亚美神虫是多孔动物门的代表，它独特的位置为我们提供了在后生动物基因家族进化早期阶段的深入见解。五种澳大利亚美神虫层粘连蛋白相关基因具有保守的分子特征，并且具有大多数后生动物层粘连蛋白中发现的结构域，但所有基因的结构域架构都与模式后生动物中已知的经典层粘连蛋白链类型不同。这一发现促使我们对纤毛原生物和多种后生动物的层粘连蛋白和相关基因进行了比较基因组分析，并使用保守的层粘连蛋白 N 端结构域进行了系统发育分析，以探索具有不同结构的基因之间的关系。层粘连蛋白样基因似乎起源于原生动物谱系（纤毛原生物+后生动物+其他几个单细胞后口动物分类群），随后出现了几个层粘连蛋白结构域，仅存在于后生动物（动物）或真后生动物（扁盘动物+栉水母+刺胞动物+两侧对称动物）的层粘连蛋白中。典型的两侧对称动物α、β和γ 层粘连蛋白链形式出现在真后生动物的主干中，另一种链类型在澳大利亚美神虫、栉水母 Nematostella vectensis 和棘皮动物 Strongylocentrotus purpuratus 中保守，似乎已经独立于扁盘动物 Trichoplax adhaerens 和多个两侧对称动物丢失。系统发育分析并未清楚地重建不同层粘连蛋白链类型之间的关系（除了α 链），但确实揭示了神经导向因子家族的几个成员如何通过基因复制和结构域改组以及结构域丢失从层粘连蛋白家族中独立产生。总之，我们的研究结果表明，基因复制和丢失、结构域改组和丢失都在层粘连蛋白家族的进化中发挥了作用，并为现存后生动物的层粘连蛋白基因组合的谱系特异性多样性的产生做出了贡献。
