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Cited by 11Axon Guidance and Neuronal SignalingDevelopmental Biology and Gene RegulationMarine Invertebrate Physiology and Ecology

Evolution and Diversity of Semaphorins and Plexins in Choanoflagellates

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Junqueira Alves, Chrystian, Silva Ladeira, Júlia, Hannah, Theodore, Pedroso Dias, Roberto J, Zabala Capriles, Priscila V, Yotoko, Karla, Zou, Hongyan, Friedel, Roland H·2021·Genome Biology and Evolution
DOI 10.1093/gbe/evab035PMC PMC8011033
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Abstract

Semaphorins and plexins are cell surface ligand/receptor proteins that affect cytoskeletal dynamics in metazoan cells. Interestingly, they are also present in Choanoflagellata, a class of unicellular heterotrophic flagellates that forms the phylogenetic sister group to Metazoa. Several members of choanoflagellates are capable of forming transient colonies, whereas others reside solitary inside exoskeletons; their molecular diversity is only beginning to emerge. Here, we surveyed genomics data from 22 choanoflagellate species and detected semaphorin/plexin pairs in 16 species. Choanoflagellate semaphorins (Sema-FN1) contain several domain features distinct from metazoan semaphorins, including an N-terminal Reeler domain that may facilitate dimer stabilization, an array of fibronectin type III domains, a variable serine/threonine-rich domain that is a potential site for O-linked glycosylation, and a SEA domain that can undergo autoproteolysis. In contrast, choanoflagellate plexins (Plexin-1) harbor a domain arrangement that is largely identical to metazoan plexins. Both Sema-FN1 and Plexin-1 also contain a short homologous motif near the C-terminus, likely associated with a shared function. Three-dimensional molecular models revealed a highly conserved structural architecture of choanoflagellate Plexin-1 as compared to metazoan plexins, including similar predicted conformational changes in a segment that is involved in the activation of the intracellular Ras-GAP domain. The absence of semaphorins and plexins in several choanoflagellate species did not appear to correlate with unicellular versus colonial lifestyle or ecological factors such as fresh versus salt water environment. Together, our findings support a conserved mechanism of semaphorin/plexin proteins in regulating cytoskeletal dynamics in unicellular and multicellular organisms.

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Authors
Junqueira Alves, C., Silva Ladeira, J., Hannah, T., Pedroso Dias, R. J., Zabala Capriles, P. V., Yotoko, K., Zou, H., & Friedel, R. H.
Affiliations
  • Friedman Brain Institute, Nash Family Department of Neuroscience and Department of Neurosurgery, Icahn School of Medicine at Mount Sinai, New York, New York
  • Programa de Pós-graduação em Modelagem Computacional, Universidade Federal de Juiz de Fora, Minas Gerais, Brazil
  • Icahn School of Medicine at Mount Sinai (US)
  • Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora, Minas Gerais, Brazil
  • Universidade Federal de Viçosa (BR)
Corresponding author
Friedel, Roland H
ORCID
Venue
Genome Biology and Evolution
Publisher
Oxford University Press (OUP)
Published
2021-02-24
Volume
13
Issue
3
ISSN
1759-6653 (ISSN-L)
DOI
10.1093/gbe/evab035
PMC
PMC8011033
OpenAlex
W3131870834
Cited by
11
References
2
Citations by year
2025: 5 · 2024: 1 · 2023: 2 · 2022: 2 · 2021: 1
FWCI
0.69
Type
journal article
Language
en
Open access
Licence
Locations
  • Genome Biology and Evolution (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
Funders
  • University of Texas Southwestern Medical Center
  • National Institutes of Health
  • National Institute of Neurological Disorders and Stroke (R01NS092735)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
Keywords
semaphorins, plexins, choanoflagellates, fibronectin type III domain, SEA domain, autoproteolysis, cytoskeletal dynamics, protein domain evolution
MeSH terms
Axon Guidance, Protein Domains, Animals, Biological Evolution, Ligands, Models, Molecular, Nerve Tissue Proteins, Phylogeny, Protein Conformation, Receptors, Cell Surface, Cell Adhesion Molecules, Semaphorins, Biodiversity, Choanoflagellata

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