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Tail Wags the Dog? Functional Gene Classes Driving Genome-Wide GC Content in Plasmodium spp.

Plasmodium parasites are valuable models to understand how nucleotide composition affects mutation, diversification, and adaptation. No other observed eukaryotes have undergone such large changes in genomic Guanine–Cytosine (GC) content as seen in the genus Plasmodium (∼30% within 35–40 Myr). Althou...

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Autores principales: Castillo, Andreina I, Nelson, Andrew D L, Lyons, Eric
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6385630/
https://www.ncbi.nlm.nih.gov/pubmed/30689842
http://dx.doi.org/10.1093/gbe/evz015
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author Castillo, Andreina I
Nelson, Andrew D L
Lyons, Eric
author_facet Castillo, Andreina I
Nelson, Andrew D L
Lyons, Eric
author_sort Castillo, Andreina I
collection PubMed
description Plasmodium parasites are valuable models to understand how nucleotide composition affects mutation, diversification, and adaptation. No other observed eukaryotes have undergone such large changes in genomic Guanine–Cytosine (GC) content as seen in the genus Plasmodium (∼30% within 35–40 Myr). Although mutational biases are known to influence GC content in the human-infective Plasmodium vivax and Plasmodium falciparum; no study has addressed how different gene functional classes contribute to genus-wide compositional changes, or if Plasmodium GC content variation is driven by natural selection. Here, we tested the hypothesis that certain gene processes and functions drive variation in global GC content between Plasmodium species. We performed a large-scale comparative genomic analysis using the genomes and predicted genes of 17 Plasmodium species encompassing a wide genomic GC content range. Genic GC content was sorted and divided into ten equally sized quantiles that were then assessed for functional enrichment classes. In agreement that selection on gene classes may drive genomic GC content, trans-membrane proteins were enriched within extreme GC content quantiles (Q1 and Q10). Specifically, variant surface antigens, which primarily interact with vertebrate immune systems, showed skewed GC content distributions compared with other trans-membrane proteins. Although a definitive causation linking GC content, expression, and positive selection within variant surface antigens from Plasmodium vivax, Plasmodium berghei, and Plasmodium falciparum could not be established, we found that regardless of genomic nucleotide composition, genic GC content and expression were positively correlated during trophozoite stages. Overall, these data suggest that, alongside mutational biases, functional protein classes drive Plasmodium GC content change.
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spelling pubmed-63856302019-02-27 Tail Wags the Dog? Functional Gene Classes Driving Genome-Wide GC Content in Plasmodium spp. Castillo, Andreina I Nelson, Andrew D L Lyons, Eric Genome Biol Evol Research Article Plasmodium parasites are valuable models to understand how nucleotide composition affects mutation, diversification, and adaptation. No other observed eukaryotes have undergone such large changes in genomic Guanine–Cytosine (GC) content as seen in the genus Plasmodium (∼30% within 35–40 Myr). Although mutational biases are known to influence GC content in the human-infective Plasmodium vivax and Plasmodium falciparum; no study has addressed how different gene functional classes contribute to genus-wide compositional changes, or if Plasmodium GC content variation is driven by natural selection. Here, we tested the hypothesis that certain gene processes and functions drive variation in global GC content between Plasmodium species. We performed a large-scale comparative genomic analysis using the genomes and predicted genes of 17 Plasmodium species encompassing a wide genomic GC content range. Genic GC content was sorted and divided into ten equally sized quantiles that were then assessed for functional enrichment classes. In agreement that selection on gene classes may drive genomic GC content, trans-membrane proteins were enriched within extreme GC content quantiles (Q1 and Q10). Specifically, variant surface antigens, which primarily interact with vertebrate immune systems, showed skewed GC content distributions compared with other trans-membrane proteins. Although a definitive causation linking GC content, expression, and positive selection within variant surface antigens from Plasmodium vivax, Plasmodium berghei, and Plasmodium falciparum could not be established, we found that regardless of genomic nucleotide composition, genic GC content and expression were positively correlated during trophozoite stages. Overall, these data suggest that, alongside mutational biases, functional protein classes drive Plasmodium GC content change. Oxford University Press 2019-01-23 /pmc/articles/PMC6385630/ /pubmed/30689842 http://dx.doi.org/10.1093/gbe/evz015 Text en © The Author(s) 2019. 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
Castillo, Andreina I
Nelson, Andrew D L
Lyons, Eric
Tail Wags the Dog? Functional Gene Classes Driving Genome-Wide GC Content in Plasmodium spp.
title Tail Wags the Dog? Functional Gene Classes Driving Genome-Wide GC Content in Plasmodium spp.
title_full Tail Wags the Dog? Functional Gene Classes Driving Genome-Wide GC Content in Plasmodium spp.
title_fullStr Tail Wags the Dog? Functional Gene Classes Driving Genome-Wide GC Content in Plasmodium spp.
title_full_unstemmed Tail Wags the Dog? Functional Gene Classes Driving Genome-Wide GC Content in Plasmodium spp.
title_short Tail Wags the Dog? Functional Gene Classes Driving Genome-Wide GC Content in Plasmodium spp.
title_sort tail wags the dog? functional gene classes driving genome-wide gc content in plasmodium spp.
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6385630/
https://www.ncbi.nlm.nih.gov/pubmed/30689842
http://dx.doi.org/10.1093/gbe/evz015
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