Evolutionary origin of type IV classical cadherins in arthropods

Abstract Background 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. Results 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. Conclusions 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

Genome-scale embryonic developmental profile of gene expression in the common house spider Parasteatoda tepidariorum

We performed RNA sequencing (RNA-Seq) at ten successive developmental stages in embryos of the common house spider Parasteatoda tepidariorum. Two independent datasets from two pairs of parents represent the normalized coverage of mapped RNA-Seq reads along scaffolds of the P. tepidariorum genome assembly. Transcript abundance was calculated against existing AUGUSTUS gene models. The datasets have been deposited in the Gene Expression Omnibus (GEO) Database at the National Center for Biotechnology Information (NCBI) under the accession number GSE112712

Distinct Mechanisms Triggering Glial Differentiation in Drosophila Thoracic and Abdominal Neuroblasts 6-4

AbstractNeurons and glia are produced in stereotyped patterns after neuroblast cell division during development of the Drosophila central nervous system. The first cell division of thoracic neuroblast 6-4 (NB6-4T) is asymmetric, giving rise to a glial precursor cell and a neuronal precursor cell. In contrast, abdominal NB6-4 (NB6-4A) divides symmetrically to produce two glial cells. To understand the relationship between cell division and glia–neuron cell fate determination, we examined and compared the effects of known cell division mutations on the NB6-4T and NB6-4A lineages. Based on observation of expression of glial fate determination and early glial differentiation genes, the onset of glial differentiation occurred in NB6-4A but not in NB6-4T when both cell cycle progression and cytokinesis were genetically arrested. On the other hand, glial differentiation started in both lineages when cytokinesis was blocked with intact cell cycle progression. These results showed that NB6-4T, but not NB6-4A, requires cell cycle progression for acquisition of glial fate, suggesting that distinct mechanisms trigger glial differentiation in the different lineages

Cassiar Courier - April 1989

Figure S4. Schematic representation of detected sequences of C. multidentata related to classical cadherins. A. Nine reconstructed genomic sequences of C. multidentata that contain coding sequences closely related to those of Le1-cadherin. The sequences are available under the indicated accession numbers. B. Eight transcriptome contigs connected by raw reads. The sequences of these contigs are available under the indicated accession numbers. Contig33642 was modified by an insertion of 5 nucleotide bases (CCGGA) between the nucleotides 349 and 350 based on assessment of raw reads (asterisk). The assembled transcript and protein sequences are available in Additional file 12. Detected domain elements are shown. (PDF 108 kb

Additional file 7: Figure S6. of Evolutionary origin of type IV classical cadherins in arthropods

Comparison of the exon-intron organizations of type IVa, type IVb and type III cadherin genes. Alignment of the amino acid sequences of the EC1-EC6 region of type IVa cadherins, the EC1-EC8 region of type IVb cadherins, and the EC6-EC13 region of type III cadherins was produced using the ClustalW algorithm without manual adjustment. The classical cadherins shown are DE-, Dp1-, Ea1-, Le1-, Ha1-, Ph1-, Pt1-, Sm2-, Cm-, Le2-, and DN-cadherins. The EC domains for type IVa, type IVb, and type III cadherin are indicated above the DE-, Le1- and, Pt1-cadherin sequence, respectively. Blue lines with breakages indicate exons, and the breaking points indicate intron insertion sites revealed by comparisons with the corresponding genomic sequences. (PDF 1348 kb

Additional file 9: Figure S7. of Evolutionary origin of type IV classical cadherins in arthropods

Amino acid alignment of selected classical cadherins from arthropods and non-arthropod bilaterians. The classical cadherins shown are as follows: DE-cadherin (DE, fruit fly); Tc1-cadherin (Tc1, beetle); Am1-cadherin (Am1, honey bee); Ap1-cadherin (Ap1, aphid); Gb1-cadherin (Gb1, cricket); Fc1-cadherin (Fc1, springtail); Af1-cadherin (Af1, brine shrimp); Dp1-cadherin (Dp1, water flea); Ea1-cadherin (Ea1, copepod); Le1-cadherin (Le1, sea slater); Ha1-cadherin (Ha1, amphipod); Sm1-cadherin (Sm1, centipede); DN-cadherin (DN, fruit fly); Am2-cadherin (Am2, honey bee); Dp2-cadherin (Dp2, water flea); Le2-cadherin (Le2, sea slater); Cm-cadherin (Cm, shrimp); Sm2-cadherin (Sm2, centipede); Mo-cadherin (Mo, mite); Pt1-cadherin (Pt1, spider); Pt2-cadherin (Pt2, spider); Ct-cadherin (Ct, polychaete); Lg-cadherin (Lg, snail); LvG-cadherin (LvG, sea urchin); Bf-cadherin (Bf, amphioxus); Pn-cadherin (Pn, fish); Ta-cadherin (Ta, placozoan); and Mm5-cadherin (Mm5, mouse). The amino acid sequence of Pt1-cadherin is duplicated; one of the duplicates is placed at the top as a reference to show the domain subdivisions. The “-” character indicates introduced gaps. All residues of each cadherin sequence are shown, although some parts of the sequences were aligned poorly or not at all. Excluding the reference sequence, the amino acid sequences derived from different exons are distinguished using arbitrary background colors to indicate the exon-exon junctions in the transcripts. (PDF 385 kb

Additional file 3: Figure S2. of Evolutionary origin of type IV classical cadherins in arthropods

Alignment of the entire amino acid sequences of thirteen type III cadherins in arthropods, and comparison of the exon-intron organizations. The alignment was produced using the ClustalW algorithm without manual adjustment. The classical cadherins shown are Pt1-, Pt2-, Mma1-, Mma2-, Mo-, Sm2-, Cm-, Le2-, Ph2-, Ha2-, Ea2-, Dp2-, and DN-cadherins. The domain organization is indicated above the Pt1-cadherin sequence. Blue lines with breakages indicate exons, and the breaking points indicate intron insertion sites revealed by comparisons with the corresponding genomic sequences. (PDF 5991 kb

Additional file 4: Figure S3. of Evolutionary origin of type IV classical cadherins in arthropods

Characterization of the amino acid sequences of type IVa and type IVb cadherins. A. Alignment of the amino acid sequences of all EC domains (EC1-EC7 or EC1-EC9) of the DE-, Dp1-, Ea1-, Le1-, Ha1-, and Ph1-cadherins (abbreviated as DE, D1, E1, L1, H1, and Ph1, respectively). Conserved hydrophobic residues (blue), Ca2+-binding motifs or residues (red), and XPXF motif sequences (green) are aligned. Thick blue arrows denote the seven β-strands (βA to βG), and each red arrow indicates the inter-EC linker to which the Ca2+-binding motif or residue belongs. No residues are omitted from the alignment, except for three instances where 5–7 residues from the Le1- or Ha1-cadherin sequences are placed outside the alignment (parentheses). The N-terminal sequence (Nt) preceding the EC1 domain is also shown for each cadherin. B. Alignment of the amino acid sequences of the NC and subsequent domains of the DE-, Dp1-, Ea1-, Le1-, Ha1-, and Ph1-cadherins. In both A and B, the conserved cysteine residues are highlighted in pink, and the residues bordering the start and end of the introns are highlighted with yellow and green. (PDF 379 kb

Additional file 8: Figure S6. of Evolutionary origin of type IV classical cadherins in arthropods

Results of blast searches of type IVb cadherin EC domain sequences against the D. melanogaster, T. castaneum and D. pulex RefSeq protein sequences. (XLSX 11 kb

Additional file 6: Figure S5. of Evolutionary origin of type IV classical cadherins in arthropods

Blast-based dot-plot comparisons between the amino acid sequence of Ha1- (A) or Ph1- (B) cadherin and those of DE-, Dp1-, Sm1-, Cm-, Le2-, DN- and Pn-cadherins. Green boxes indicate comparisons between the EC1-EC5 region of Ha1- or Ph1- cadherin and the EC6-EC10 regions of the type III cadherins or the corresponding region of Sm1-cadherin, which exhibited marked collinear similarities. Blue boxes indicate comparisons between the EC6-EC8 region of Ha1- or Ph1-cadherin and the EC11-EC16 regions of the type III cadherins or the corresponding region of Sm1-cadherin, which exhibited ambiguous collinear similarities. (PDF 2623 kb