In silico Identification and Expression of Protocadherin Gene Family in Octopus vulgaris

Abstract

Connecting millions of neurons to create a functional neural circuit is a daunting challenge. Vertebrates developed a molecular system at the cell membrane to allow neurons to recognize each other by distinguishing self from non-self through homophilic protocadherin interactions. In mammals, the protocadherin gene family counts about 50 different genes. By hetero-multimerization, protocadherins are capable of generating an impressive number of molecular interfaces. Surprisingly, in the California two-spot octopus, Octopus bimaculoides, an invertebrate belonging to the Phylum Mollusca, over 160 protocadherins (PCDHs) have been identified. Here we briefly discuss the role of PCDHs in neural wiring and conduct a comparative study of the protocadherin gene family in two closely related octopus species, Octopus vulgaris and O. bimaculoides. A first glance at the expression patterns of protocadherins in O. vulgaris is also provided. Finally, we comment on PCDH evolution in the light of invertebrate nervous system plasticity.

Keywords: DSCAM; cephalopod; neural wiring; octopus; plasticity; protocadherins.

FIGURE 1

Distribution and evolution of the protocadherin gene family in metazoans. (A) Abundance of protocadherins in the genomes of different chordate and non-chordate species. Data are derived from: Wu and Maniatis (1999), Noonan et al. (2004a,b), Wu (2005), Whittaker et al. (2006), Yu et al. (2007), Noda and Satoh (2008), Yu et al. (2008), Jiang et al. (2009), Hulpiau and van Roy (2011), Albertin et al. (2015), and Ravi et al. (2015). The attribution to clustered vs. non-clustered PCDHs in the graph (Lottia gigantea and Octopus bimaculoides) is derived from Authors’ estimation (Albertin et al., 2015). (B) Bayesian phylogenetic reconstruction of the evolutionary relationships between protocadherins in different species. Chordate PCDHs are visualized in blue and non-chordate PCDHs are shown in red. Molluscan PCDHs are highlighted in red. The included cephalopod species are Octopus vulgaris and O. bimaculoides, which are highlighted in yellow. Octopus protocadherins interdigitate on the tree (see Supplementary Figure S2).

FIGURE 2

Protocadherin and Dscam expression in O. vulgaris. (A) A schematic overview of the octopus and the main components of its nervous system. The octopus brain (SEM: supra-esophageal mass; SUB: sub-esophageal mass; OL: optic lobe), arm nerve cord, stellate and gastric ganglia are visualized. (B) Relative expression levels (coded according to Row Z-score) of selected Ov-PCDHs (see Supplementary Information and Supplementary Figure S1) and Ov-DSCAM are shown in the brain (supra-esophageal mass; sub-esophageal mass; optic lobe), arm (muscle tissue and axial nerve cord) and arm tip.