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Increased taxon sampling reveals thousands of hidden orthologs in flatworms

Gains and losses shape the gene complement of animal lineages and are a fundamental aspect of genomic evolution. Acquiring a comprehensive view of the evolution of gene repertoires is limited by the intrinsic limitations of common sequence similarity searches and available databases. Thus, a subset...

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Autores principales: Martín-Durán, José M., Ryan, Joseph F., Vellutini, Bruno C., Pang, Kevin, Hejnol, Andreas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5495077/
https://www.ncbi.nlm.nih.gov/pubmed/28400424
http://dx.doi.org/10.1101/gr.216226.116
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author Martín-Durán, José M.
Ryan, Joseph F.
Vellutini, Bruno C.
Pang, Kevin
Hejnol, Andreas
author_facet Martín-Durán, José M.
Ryan, Joseph F.
Vellutini, Bruno C.
Pang, Kevin
Hejnol, Andreas
author_sort Martín-Durán, José M.
collection PubMed
description Gains and losses shape the gene complement of animal lineages and are a fundamental aspect of genomic evolution. Acquiring a comprehensive view of the evolution of gene repertoires is limited by the intrinsic limitations of common sequence similarity searches and available databases. Thus, a subset of the gene complement of an organism consists of hidden orthologs, i.e., those with no apparent homology to sequenced animal lineages—mistakenly considered new genes—but actually representing rapidly evolving orthologs or undetected paralogs. Here, we describe Leapfrog, a simple automated BLAST pipeline that leverages increased taxon sampling to overcome long evolutionary distances and identify putative hidden orthologs in large transcriptomic databases by transitive homology. As a case study, we used 35 transcriptomes of 29 flatworm lineages to recover 3427 putative hidden orthologs, some unidentified by OrthoFinder and HaMStR, two common orthogroup inference algorithms. Unexpectedly, we do not observe a correlation between the number of putative hidden orthologs in a lineage and its “average” evolutionary rate. Hidden orthologs do not show unusual sequence composition biases that might account for systematic errors in sequence similarity searches. Instead, gene duplication with divergence of one paralog and weak positive selection appear to underlie hidden orthology in Platyhelminthes. By using Leapfrog, we identify key centrosome-related genes and homeodomain classes previously reported as absent in free-living flatworms, e.g., planarians. Altogether, our findings demonstrate that hidden orthologs comprise a significant proportion of the gene repertoire in flatworms, qualifying the impact of gene losses and gains in gene complement evolution.
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spelling pubmed-54950772017-07-18 Increased taxon sampling reveals thousands of hidden orthologs in flatworms Martín-Durán, José M. Ryan, Joseph F. Vellutini, Bruno C. Pang, Kevin Hejnol, Andreas Genome Res Method Gains and losses shape the gene complement of animal lineages and are a fundamental aspect of genomic evolution. Acquiring a comprehensive view of the evolution of gene repertoires is limited by the intrinsic limitations of common sequence similarity searches and available databases. Thus, a subset of the gene complement of an organism consists of hidden orthologs, i.e., those with no apparent homology to sequenced animal lineages—mistakenly considered new genes—but actually representing rapidly evolving orthologs or undetected paralogs. Here, we describe Leapfrog, a simple automated BLAST pipeline that leverages increased taxon sampling to overcome long evolutionary distances and identify putative hidden orthologs in large transcriptomic databases by transitive homology. As a case study, we used 35 transcriptomes of 29 flatworm lineages to recover 3427 putative hidden orthologs, some unidentified by OrthoFinder and HaMStR, two common orthogroup inference algorithms. Unexpectedly, we do not observe a correlation between the number of putative hidden orthologs in a lineage and its “average” evolutionary rate. Hidden orthologs do not show unusual sequence composition biases that might account for systematic errors in sequence similarity searches. Instead, gene duplication with divergence of one paralog and weak positive selection appear to underlie hidden orthology in Platyhelminthes. By using Leapfrog, we identify key centrosome-related genes and homeodomain classes previously reported as absent in free-living flatworms, e.g., planarians. Altogether, our findings demonstrate that hidden orthologs comprise a significant proportion of the gene repertoire in flatworms, qualifying the impact of gene losses and gains in gene complement evolution. Cold Spring Harbor Laboratory Press 2017-07 /pmc/articles/PMC5495077/ /pubmed/28400424 http://dx.doi.org/10.1101/gr.216226.116 Text en © 2017 Martín-Durán et al.; Published by Cold Spring Harbor Laboratory Press http://creativecommons.org/licenses/by-nc/4.0/ This article, published in Genome Research, is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
spellingShingle Method
Martín-Durán, José M.
Ryan, Joseph F.
Vellutini, Bruno C.
Pang, Kevin
Hejnol, Andreas
Increased taxon sampling reveals thousands of hidden orthologs in flatworms
title Increased taxon sampling reveals thousands of hidden orthologs in flatworms
title_full Increased taxon sampling reveals thousands of hidden orthologs in flatworms
title_fullStr Increased taxon sampling reveals thousands of hidden orthologs in flatworms
title_full_unstemmed Increased taxon sampling reveals thousands of hidden orthologs in flatworms
title_short Increased taxon sampling reveals thousands of hidden orthologs in flatworms
title_sort increased taxon sampling reveals thousands of hidden orthologs in flatworms
topic Method
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5495077/
https://www.ncbi.nlm.nih.gov/pubmed/28400424
http://dx.doi.org/10.1101/gr.216226.116
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