Fibrillarin evolution through the Tree of Life: Comparative genomics and microsynteny network analyses provide new insights into the evolutionary history of Fibrillarin

Fibrillarin (FIB), a methyltransferase essential for life in the vast majority of eukaryotes, is involved in methylation of rRNA required for proper ribosome assembly, as well as methylation of histone H2A of promoter regions of rRNA genes. RNA viral progression that affects both plants and animals...

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Veröffentlicht in:PLoS computational biology 2020-10, Vol.16 (10), p.e1008318-e1008318
Hauptverfasser: Pereira-Santana, Alejandro, Gamboa-Tuz, Samuel David, Zhao, Tao, Schranz, M Eric, Vinuesa, Pablo, Bayona, Andrea, Rodríguez-Zapata, Luis C, Castano, Enrique
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container_issue 10
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container_title PLoS computational biology
container_volume 16
creator Pereira-Santana, Alejandro
Gamboa-Tuz, Samuel David
Zhao, Tao
Schranz, M Eric
Vinuesa, Pablo
Bayona, Andrea
Rodríguez-Zapata, Luis C
Castano, Enrique
description Fibrillarin (FIB), a methyltransferase essential for life in the vast majority of eukaryotes, is involved in methylation of rRNA required for proper ribosome assembly, as well as methylation of histone H2A of promoter regions of rRNA genes. RNA viral progression that affects both plants and animals requires FIB proteins. Despite the importance and high conservation of fibrillarins, there little is known about the evolutionary dynamics of this small gene family. We applied a phylogenomic microsynteny-network approach to elucidate the evolutionary history of FIB proteins across the Tree of Life. We identified 1063 non-redundant FIB sequences across 1049 completely sequenced genomes from Viruses, Bacteria, Archaea, and Eukarya. FIB is a highly conserved single-copy gene through Archaea and Eukarya lineages, except for plants, which have a gene family expansion due to paleopolyploidy and tandem duplications. We found a high conservation of the FIB genomic context during plant evolution. Surprisingly, FIB in mammals duplicated after the Eutheria split (e.g., ruminants, felines, primates) from therian mammals (e.g., marsupials) to form two main groups of sequences, the FIB and FIB-like groups. The FIB-like group transposed to another genomic context and remained syntenic in all the eutherian mammals. This transposition correlates with differences in the expression patterns of FIB-like proteins and with elevated Ks values potentially due to reduced evolutionary constraints of the duplicated copy. Our results point to a unique evolutionary event in mammals, between FIB and FIB-like genes, that led to non-redundant roles of the vital processes in which this protein is involved.
doi_str_mv 10.1371/journal.pcbi.1008318
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RNA viral progression that affects both plants and animals requires FIB proteins. Despite the importance and high conservation of fibrillarins, there little is known about the evolutionary dynamics of this small gene family. We applied a phylogenomic microsynteny-network approach to elucidate the evolutionary history of FIB proteins across the Tree of Life. We identified 1063 non-redundant FIB sequences across 1049 completely sequenced genomes from Viruses, Bacteria, Archaea, and Eukarya. FIB is a highly conserved single-copy gene through Archaea and Eukarya lineages, except for plants, which have a gene family expansion due to paleopolyploidy and tandem duplications. We found a high conservation of the FIB genomic context during plant evolution. Surprisingly, FIB in mammals duplicated after the Eutheria split (e.g., ruminants, felines, primates) from therian mammals (e.g., marsupials) to form two main groups of sequences, the FIB and FIB-like groups. The FIB-like group transposed to another genomic context and remained syntenic in all the eutherian mammals. This transposition correlates with differences in the expression patterns of FIB-like proteins and with elevated Ks values potentially due to reduced evolutionary constraints of the duplicated copy. Our results point to a unique evolutionary event in mammals, between FIB and FIB-like genes, that led to non-redundant roles of the vital processes in which this protein is involved.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>33075080</pmid><doi>10.1371/journal.pcbi.1008318</doi><orcidid>https://orcid.org/0000-0001-6777-6565</orcidid><orcidid>https://orcid.org/0000-0003-2645-9541</orcidid><orcidid>https://orcid.org/0000-0001-7714-9485</orcidid><orcidid>https://orcid.org/0000-0002-6863-7943</orcidid><orcidid>https://orcid.org/0000-0001-6119-2956</orcidid><orcidid>https://orcid.org/0000-0001-7302-6445</orcidid><orcidid>https://orcid.org/0000-0002-4872-8231</orcidid><oa>free_for_read</oa></addata></record>
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identifier ISSN: 1553-7358
ispartof PLoS computational biology, 2020-10, Vol.16 (10), p.e1008318-e1008318
issn 1553-7358
1553-734X
1553-7358
language eng
recordid cdi_plos_journals_2460772732
source PubMed (Medline); MEDLINE; Public Library of Science; DOAJ Directory of Open Access Journals; EZB Electronic Journals Library
subjects Analysis
Animals
Archaea
Bacteria
Bacteria - genetics
Biology and Life Sciences
Cancer
Chromosomal Proteins, Non-Histone - chemistry
Chromosomal Proteins, Non-Histone - classification
Chromosomal Proteins, Non-Histone - genetics
Chromosomal Proteins, Non-Histone - metabolism
Comparative analysis
Computer and Information Sciences
Conservation
Conserved Sequence
Context
DNA methylation
Earth Sciences
Engineering and Technology
Eukarya
Eukaryota - genetics
Eukaryotes
Evolution
Evolutionary biology
Evolutionary genetics
Fibrillarin
Gene expression
Genes
Genetic engineering
Genomes
Genomics
Genomics - methods
Histone H2A
Mammals
Mammals - genetics
Metabolism
Methylation
Methyltransferase
Methyltransferases
Methyltransferases - chemistry
Methyltransferases - classification
Methyltransferases - genetics
Methyltransferases - metabolism
Natural history
Plants - genetics
Primates
Protection and preservation
Proteins
Reproduction (copying)
Ribosomal RNA
rRNA
Synteny
Transposition
Viruses
Viruses - genetics
title Fibrillarin evolution through the Tree of Life: Comparative genomics and microsynteny network analyses provide new insights into the evolutionary history of Fibrillarin
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