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Molecular Evolutionary Analysis of Nematode Zona Pellucida (ZP) Modules Reveals Disulfide-Bond Reshuffling and Standalone ZP-C Domains

Zona pellucida (ZP) modules mediate extracellular protein–protein interactions and contribute to important biological processes including syngamy and cellular morphogenesis. Although some biomedically relevant ZP modules are well studied, little is known about the protein family’s broad-scale divers...

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Autor principal: Weadick, Cameron J
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7456536/
https://www.ncbi.nlm.nih.gov/pubmed/32426804
http://dx.doi.org/10.1093/gbe/evaa095
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author Weadick, Cameron J
author_facet Weadick, Cameron J
author_sort Weadick, Cameron J
collection PubMed
description Zona pellucida (ZP) modules mediate extracellular protein–protein interactions and contribute to important biological processes including syngamy and cellular morphogenesis. Although some biomedically relevant ZP modules are well studied, little is known about the protein family’s broad-scale diversity and evolution. The increasing availability of sequenced genomes from “nonmodel” systems provides a valuable opportunity to address this issue and to use comparative approaches to gain new insights into ZP module biology. Here, through phylogenetic and structural exploration of ZP module diversity across the nematode phylum, I report evidence that speaks to two important aspects of ZP module biology. First, I show that ZP-C domains—which in some modules act as regulators of ZP-N domain-mediated polymerization activity, and which have never before been found in isolation—can indeed be found as standalone domains. These standalone ZP-C domain proteins originated in independent (paralogous) lineages prior to the diversification of extant nematodes, after which they evolved under strong stabilizing selection, suggesting the presence of ZP-N domain-independent functionality. Second, I provide a much-needed phylogenetic perspective on disulfide bond variability, uncovering evidence for both convergent evolution and disulfide-bond reshuffling. This result has implications for our evolutionary understanding and classification of ZP module structural diversity and highlights the usefulness of phylogenetics and diverse sampling for protein structural biology. All told, these findings set the stage for broad-scale (cross-phyla) evolutionary analysis of ZP modules and position Caenorhabditis elegans and other nematodes as important experimental systems for exploring the evolution of ZP modules and their constituent domains.
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spelling pubmed-74565362020-09-03 Molecular Evolutionary Analysis of Nematode Zona Pellucida (ZP) Modules Reveals Disulfide-Bond Reshuffling and Standalone ZP-C Domains Weadick, Cameron J Genome Biol Evol Research Article Zona pellucida (ZP) modules mediate extracellular protein–protein interactions and contribute to important biological processes including syngamy and cellular morphogenesis. Although some biomedically relevant ZP modules are well studied, little is known about the protein family’s broad-scale diversity and evolution. The increasing availability of sequenced genomes from “nonmodel” systems provides a valuable opportunity to address this issue and to use comparative approaches to gain new insights into ZP module biology. Here, through phylogenetic and structural exploration of ZP module diversity across the nematode phylum, I report evidence that speaks to two important aspects of ZP module biology. First, I show that ZP-C domains—which in some modules act as regulators of ZP-N domain-mediated polymerization activity, and which have never before been found in isolation—can indeed be found as standalone domains. These standalone ZP-C domain proteins originated in independent (paralogous) lineages prior to the diversification of extant nematodes, after which they evolved under strong stabilizing selection, suggesting the presence of ZP-N domain-independent functionality. Second, I provide a much-needed phylogenetic perspective on disulfide bond variability, uncovering evidence for both convergent evolution and disulfide-bond reshuffling. This result has implications for our evolutionary understanding and classification of ZP module structural diversity and highlights the usefulness of phylogenetics and diverse sampling for protein structural biology. All told, these findings set the stage for broad-scale (cross-phyla) evolutionary analysis of ZP modules and position Caenorhabditis elegans and other nematodes as important experimental systems for exploring the evolution of ZP modules and their constituent domains. Oxford University Press 2020-05-19 /pmc/articles/PMC7456536/ /pubmed/32426804 http://dx.doi.org/10.1093/gbe/evaa095 Text en © The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Weadick, Cameron J
Molecular Evolutionary Analysis of Nematode Zona Pellucida (ZP) Modules Reveals Disulfide-Bond Reshuffling and Standalone ZP-C Domains
title Molecular Evolutionary Analysis of Nematode Zona Pellucida (ZP) Modules Reveals Disulfide-Bond Reshuffling and Standalone ZP-C Domains
title_full Molecular Evolutionary Analysis of Nematode Zona Pellucida (ZP) Modules Reveals Disulfide-Bond Reshuffling and Standalone ZP-C Domains
title_fullStr Molecular Evolutionary Analysis of Nematode Zona Pellucida (ZP) Modules Reveals Disulfide-Bond Reshuffling and Standalone ZP-C Domains
title_full_unstemmed Molecular Evolutionary Analysis of Nematode Zona Pellucida (ZP) Modules Reveals Disulfide-Bond Reshuffling and Standalone ZP-C Domains
title_short Molecular Evolutionary Analysis of Nematode Zona Pellucida (ZP) Modules Reveals Disulfide-Bond Reshuffling and Standalone ZP-C Domains
title_sort molecular evolutionary analysis of nematode zona pellucida (zp) modules reveals disulfide-bond reshuffling and standalone zp-c domains
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7456536/
https://www.ncbi.nlm.nih.gov/pubmed/32426804
http://dx.doi.org/10.1093/gbe/evaa095
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