Evolutionary history of the vertebrate Piwi gene family

PIWIs are regulatory proteins that belong to the Argonaute family. Piwis are primarily expressed in gonads and protect the germline against the mobilization and propagation of transposable elements (TEs) through transcriptional gene silencing. Vertebrate genomes encode up to four Piwi genes: Piwil1,...

Full description

Bibliographic Details
Main Authors: Javier Gutierrez, Roy Platt, Juan C. Opazo, David A. Ray, Federico Hoffmann, Michael Vandewege
Format: Article
Language:English
Published: PeerJ Inc. 2021-11-01
Series:PeerJ
Subjects:
Online Access:https://peerj.com/articles/12451.pdf
_version_ 1797418435242622976
author Javier Gutierrez
Roy Platt
Juan C. Opazo
David A. Ray
Federico Hoffmann
Michael Vandewege
author_facet Javier Gutierrez
Roy Platt
Juan C. Opazo
David A. Ray
Federico Hoffmann
Michael Vandewege
author_sort Javier Gutierrez
collection DOAJ
description PIWIs are regulatory proteins that belong to the Argonaute family. Piwis are primarily expressed in gonads and protect the germline against the mobilization and propagation of transposable elements (TEs) through transcriptional gene silencing. Vertebrate genomes encode up to four Piwi genes: Piwil1, Piwil2, Piwil3 and Piwil4, but their duplication history is unresolved. We leveraged phylogenetics, synteny and expression analyses to address this void. Our phylogenetic analysis suggests Piwil1 and Piwil2 were retained in all vertebrate members. Piwil4 was the result of Piwil1 duplication in the ancestor of gnathostomes, but was independently lost in ray-finned fishes and birds. Further, Piwil3 was derived from a tandem Piwil1 duplication in the common ancestor of marsupial and placental mammals, but was secondarily lost in Atlantogenata (Xenarthra and Afrotheria) and some rodents. The evolutionary rate of Piwil3 is considerably faster than any Piwi among all lineages, but an explanation is lacking. Our expression analyses suggest Piwi expression has mostly been constrained to gonads throughout vertebrate evolution. Vertebrate evolution is marked by two early rounds of whole genome duplication and many multigene families are linked to these events. However, our analyses suggest Piwi expansion was independent of whole genome duplications.
first_indexed 2024-03-09T06:32:37Z
format Article
id doaj.art-0640f4ae23d04533a3292fd0625d20cf
institution Directory Open Access Journal
issn 2167-8359
language English
last_indexed 2024-03-09T06:32:37Z
publishDate 2021-11-01
publisher PeerJ Inc.
record_format Article
series PeerJ
spelling doaj.art-0640f4ae23d04533a3292fd0625d20cf2023-12-03T11:02:07ZengPeerJ Inc.PeerJ2167-83592021-11-019e1245110.7717/peerj.12451Evolutionary history of the vertebrate Piwi gene familyJavier Gutierrez0Roy Platt1Juan C. Opazo2David A. Ray3Federico Hoffmann4Michael Vandewege5Department of Biology, Eastern New Mexico University, Portales, NM, United States of AmericaHost Pathogen Interaction Program, Texas Biomedical Research Institute, San Antonio, TX, United States of AmericaInstituto de Ciencias Ambientales y Evolutivas, Universidad Austral de Chile, Valdivia, ChileDepartment of Biological Sciences, Texas Tech University, Lubbock, TX, United States of AmericaDepartment of Biochemistry, Molecular Biology, Entomology, and Plant Pathology, Mississippi State University, Starkville, MS, United States of AmericaDepartment of Biology, Eastern New Mexico University, Portales, NM, United States of AmericaPIWIs are regulatory proteins that belong to the Argonaute family. Piwis are primarily expressed in gonads and protect the germline against the mobilization and propagation of transposable elements (TEs) through transcriptional gene silencing. Vertebrate genomes encode up to four Piwi genes: Piwil1, Piwil2, Piwil3 and Piwil4, but their duplication history is unresolved. We leveraged phylogenetics, synteny and expression analyses to address this void. Our phylogenetic analysis suggests Piwil1 and Piwil2 were retained in all vertebrate members. Piwil4 was the result of Piwil1 duplication in the ancestor of gnathostomes, but was independently lost in ray-finned fishes and birds. Further, Piwil3 was derived from a tandem Piwil1 duplication in the common ancestor of marsupial and placental mammals, but was secondarily lost in Atlantogenata (Xenarthra and Afrotheria) and some rodents. The evolutionary rate of Piwil3 is considerably faster than any Piwi among all lineages, but an explanation is lacking. Our expression analyses suggest Piwi expression has mostly been constrained to gonads throughout vertebrate evolution. Vertebrate evolution is marked by two early rounds of whole genome duplication and many multigene families are linked to these events. However, our analyses suggest Piwi expansion was independent of whole genome duplications.https://peerj.com/articles/12451.pdfRNAiGene duplicationArgonaute gene familySelectionTranscriptomicsPhylogenetics
spellingShingle Javier Gutierrez
Roy Platt
Juan C. Opazo
David A. Ray
Federico Hoffmann
Michael Vandewege
Evolutionary history of the vertebrate Piwi gene family
PeerJ
RNAi
Gene duplication
Argonaute gene family
Selection
Transcriptomics
Phylogenetics
title Evolutionary history of the vertebrate Piwi gene family
title_full Evolutionary history of the vertebrate Piwi gene family
title_fullStr Evolutionary history of the vertebrate Piwi gene family
title_full_unstemmed Evolutionary history of the vertebrate Piwi gene family
title_short Evolutionary history of the vertebrate Piwi gene family
title_sort evolutionary history of the vertebrate piwi gene family
topic RNAi
Gene duplication
Argonaute gene family
Selection
Transcriptomics
Phylogenetics
url https://peerj.com/articles/12451.pdf
work_keys_str_mv AT javiergutierrez evolutionaryhistoryofthevertebratepiwigenefamily
AT royplatt evolutionaryhistoryofthevertebratepiwigenefamily
AT juancopazo evolutionaryhistoryofthevertebratepiwigenefamily
AT davidaray evolutionaryhistoryofthevertebratepiwigenefamily
AT federicohoffmann evolutionaryhistoryofthevertebratepiwigenefamily
AT michaelvandewege evolutionaryhistoryofthevertebratepiwigenefamily