Cargando…
Genomes as documents of evolutionary history: a probabilistic macrosynteny model for the reconstruction of ancestral genomes
MOTIVATION: It has been argued that whole-genome duplication (WGD) exerted a profound influence on the course of evolution. For the purpose of fully understanding the impact of WGD, several formal algorithms have been developed for reconstructing pre-WGD gene order in yeast and plant. However, to th...
Autores principales: | , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Oxford University Press
2017
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5870716/ https://www.ncbi.nlm.nih.gov/pubmed/28881993 http://dx.doi.org/10.1093/bioinformatics/btx259 |
_version_ | 1783309539358015488 |
---|---|
author | Nakatani, Yoichiro McLysaght, Aoife |
author_facet | Nakatani, Yoichiro McLysaght, Aoife |
author_sort | Nakatani, Yoichiro |
collection | PubMed |
description | MOTIVATION: It has been argued that whole-genome duplication (WGD) exerted a profound influence on the course of evolution. For the purpose of fully understanding the impact of WGD, several formal algorithms have been developed for reconstructing pre-WGD gene order in yeast and plant. However, to the best of our knowledge, those algorithms have never been successfully applied to WGD events in teleost and vertebrate, impeded by extensive gene shuffling and gene losses. RESULTS: Here, we present a probabilistic model of macrosynteny (i.e. conserved linkage or chromosome-scale distribution of orthologs), develop a variational Bayes algorithm for inferring the structure of pre-WGD genomes, and study estimation accuracy by simulation. Then, by applying the method to the teleost WGD, we demonstrate effectiveness of the algorithm in a situation where gene-order reconstruction algorithms perform relatively poorly due to a high rate of rearrangement and extensive gene losses. Our high-resolution reconstruction reveals previously overlooked small-scale rearrangements, necessitating a revision to previous views on genome structure evolution in teleost and vertebrate. CONCLUSIONS: We have reconstructed the structure of a pre-WGD genome by employing a variational Bayes approach that was originally developed for inferring topics from millions of text documents. Interestingly, comparison of the macrosynteny and topic model algorithms suggests that macrosynteny can be regarded as documents on ancestral genome structure. From this perspective, the present study would seem to provide a textbook example of the prevalent metaphor that genomes are documents of evolutionary history. AVAILABILITY AND IMPLEMENTATION: The analysis data are available for download at http://www.gen.tcd.ie/molevol/supp_data/MacrosyntenyTGD.zip, and the software written in Java is available upon request. SUPPLEMENTARY INFORMATION: Supplementary data are available at Bioinformatics online. |
format | Online Article Text |
id | pubmed-5870716 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2017 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-58707162018-04-05 Genomes as documents of evolutionary history: a probabilistic macrosynteny model for the reconstruction of ancestral genomes Nakatani, Yoichiro McLysaght, Aoife Bioinformatics Ismb/Eccb 2017: The 25th Annual Conference Intelligent Systems for Molecular Biology Held Jointly with the 16th Annual European Conference on Computational Biology, Prague, Czech Republic, July 21–25, 2017 MOTIVATION: It has been argued that whole-genome duplication (WGD) exerted a profound influence on the course of evolution. For the purpose of fully understanding the impact of WGD, several formal algorithms have been developed for reconstructing pre-WGD gene order in yeast and plant. However, to the best of our knowledge, those algorithms have never been successfully applied to WGD events in teleost and vertebrate, impeded by extensive gene shuffling and gene losses. RESULTS: Here, we present a probabilistic model of macrosynteny (i.e. conserved linkage or chromosome-scale distribution of orthologs), develop a variational Bayes algorithm for inferring the structure of pre-WGD genomes, and study estimation accuracy by simulation. Then, by applying the method to the teleost WGD, we demonstrate effectiveness of the algorithm in a situation where gene-order reconstruction algorithms perform relatively poorly due to a high rate of rearrangement and extensive gene losses. Our high-resolution reconstruction reveals previously overlooked small-scale rearrangements, necessitating a revision to previous views on genome structure evolution in teleost and vertebrate. CONCLUSIONS: We have reconstructed the structure of a pre-WGD genome by employing a variational Bayes approach that was originally developed for inferring topics from millions of text documents. Interestingly, comparison of the macrosynteny and topic model algorithms suggests that macrosynteny can be regarded as documents on ancestral genome structure. From this perspective, the present study would seem to provide a textbook example of the prevalent metaphor that genomes are documents of evolutionary history. AVAILABILITY AND IMPLEMENTATION: The analysis data are available for download at http://www.gen.tcd.ie/molevol/supp_data/MacrosyntenyTGD.zip, and the software written in Java is available upon request. SUPPLEMENTARY INFORMATION: Supplementary data are available at Bioinformatics online. Oxford University Press 2017-07-15 2017-07-12 /pmc/articles/PMC5870716/ /pubmed/28881993 http://dx.doi.org/10.1093/bioinformatics/btx259 Text en © The Author 2017. Published by Oxford University Press. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com |
spellingShingle | Ismb/Eccb 2017: The 25th Annual Conference Intelligent Systems for Molecular Biology Held Jointly with the 16th Annual European Conference on Computational Biology, Prague, Czech Republic, July 21–25, 2017 Nakatani, Yoichiro McLysaght, Aoife Genomes as documents of evolutionary history: a probabilistic macrosynteny model for the reconstruction of ancestral genomes |
title | Genomes as documents of evolutionary history: a probabilistic macrosynteny model for the reconstruction of ancestral genomes |
title_full | Genomes as documents of evolutionary history: a probabilistic macrosynteny model for the reconstruction of ancestral genomes |
title_fullStr | Genomes as documents of evolutionary history: a probabilistic macrosynteny model for the reconstruction of ancestral genomes |
title_full_unstemmed | Genomes as documents of evolutionary history: a probabilistic macrosynteny model for the reconstruction of ancestral genomes |
title_short | Genomes as documents of evolutionary history: a probabilistic macrosynteny model for the reconstruction of ancestral genomes |
title_sort | genomes as documents of evolutionary history: a probabilistic macrosynteny model for the reconstruction of ancestral genomes |
topic | Ismb/Eccb 2017: The 25th Annual Conference Intelligent Systems for Molecular Biology Held Jointly with the 16th Annual European Conference on Computational Biology, Prague, Czech Republic, July 21–25, 2017 |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5870716/ https://www.ncbi.nlm.nih.gov/pubmed/28881993 http://dx.doi.org/10.1093/bioinformatics/btx259 |
work_keys_str_mv | AT nakataniyoichiro genomesasdocumentsofevolutionaryhistoryaprobabilisticmacrosyntenymodelforthereconstructionofancestralgenomes AT mclysaghtaoife genomesasdocumentsofevolutionaryhistoryaprobabilisticmacrosyntenymodelforthereconstructionofancestralgenomes |