Identification of RAG-like transposons in protostomes suggests their ancient bilaterian origin

Abstract Background V(D) J recombination is essential for adaptive immunity in jawed vertebrates and is initiated by the RAG1-RAG2 endonuclease. The RAG1 and RAG2 genes are thought to have evolved from a RAGL (RAG-like) transposon containing convergently-oriented RAG1-like (RAG1L) and RAG2-like (RAG...

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Main Authors: Eliza C. Martin, Célia Vicari, Louis Tsakou-Ngouafo, Pierre Pontarotti, Andrei J. Petrescu, David G. Schatz
Format: Article
Language:English
Published: BMC 2020-05-01
Series:Mobile DNA
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13100-020-00214-y
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author Eliza C. Martin
Célia Vicari
Louis Tsakou-Ngouafo
Pierre Pontarotti
Andrei J. Petrescu
David G. Schatz
author_facet Eliza C. Martin
Célia Vicari
Louis Tsakou-Ngouafo
Pierre Pontarotti
Andrei J. Petrescu
David G. Schatz
author_sort Eliza C. Martin
collection DOAJ
description Abstract Background V(D) J recombination is essential for adaptive immunity in jawed vertebrates and is initiated by the RAG1-RAG2 endonuclease. The RAG1 and RAG2 genes are thought to have evolved from a RAGL (RAG-like) transposon containing convergently-oriented RAG1-like (RAG1L) and RAG2-like (RAG2L) genes. Elements resembling this presumptive evolutionary precursor have thus far only been detected convincingly in deuterostomes, leading to the model that the RAGL transposon first appeared in an early deuterostome. Results We have identified numerous RAGL transposons in the genomes of protostomes, including oysters and mussels (phylum Mollusca) and a ribbon worm (phylum Nemertea), and in the genomes of several cnidarians. Phylogenetic analyses are consistent with vertical evolution of RAGL transposons within the Bilateria clade and with its presence in the bilaterian ancestor. Many of the RAGL transposons identified in protostomes are intact elements containing convergently oriented RAG1L and RAG2L genes flanked by terminal inverted repeats (TIRs) and target site duplications with striking similarities with the corresponding elements in deuterostomes. In addition, protostome genomes contain numerous intact RAG1L-RAG2L adjacent gene pairs that lack detectable flanking TIRs. Domains and critical active site and structural amino acids needed for endonuclease and transposase activity are present and conserved in many of the predicted RAG1L and RAG2L proteins encoded in protostome genomes. Conclusions Active RAGL transposons were present in multiple protostome lineages and many were likely transmitted vertically during protostome evolution. It appears that RAGL transposons were broadly active during bilaterian evolution, undergoing multiple duplication and loss/fossilization events, with the RAGL genes that persist in present day protostomes perhaps constituting both active RAGL transposons and domesticated RAGL genes. Our findings raise the possibility that the RAGL transposon arose earlier in evolution than previously thought, either in an early bilaterian or prior to the divergence of bilaterians and non-bilaterians, and alter our understanding of the evolutionary history of this important group of transposons.
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spelling doaj.art-8757fa8ae4e04c768150c42d80df827e2022-12-21T19:22:20ZengBMCMobile DNA1759-87532020-05-0111112010.1186/s13100-020-00214-yIdentification of RAG-like transposons in protostomes suggests their ancient bilaterian originEliza C. Martin0Célia Vicari1Louis Tsakou-Ngouafo2Pierre Pontarotti3Andrei J. Petrescu4David G. Schatz5Department of Bioinformatics and Structural Biochemistry, Institute of Biochemistry of the Romanian AcademyEvolutionary biology team, Aix Marseille Université IRD, APHM, MEPHI, IHU Méditerranée InfectionEvolutionary biology team, Aix Marseille Université IRD, APHM, MEPHI, IHU Méditerranée InfectionEvolutionary biology team, Aix Marseille Université IRD, APHM, MEPHI, IHU Méditerranée InfectionDepartment of Bioinformatics and Structural Biochemistry, Institute of Biochemistry of the Romanian AcademyDepartment of Immunobiology, Yale School of MedicineAbstract Background V(D) J recombination is essential for adaptive immunity in jawed vertebrates and is initiated by the RAG1-RAG2 endonuclease. The RAG1 and RAG2 genes are thought to have evolved from a RAGL (RAG-like) transposon containing convergently-oriented RAG1-like (RAG1L) and RAG2-like (RAG2L) genes. Elements resembling this presumptive evolutionary precursor have thus far only been detected convincingly in deuterostomes, leading to the model that the RAGL transposon first appeared in an early deuterostome. Results We have identified numerous RAGL transposons in the genomes of protostomes, including oysters and mussels (phylum Mollusca) and a ribbon worm (phylum Nemertea), and in the genomes of several cnidarians. Phylogenetic analyses are consistent with vertical evolution of RAGL transposons within the Bilateria clade and with its presence in the bilaterian ancestor. Many of the RAGL transposons identified in protostomes are intact elements containing convergently oriented RAG1L and RAG2L genes flanked by terminal inverted repeats (TIRs) and target site duplications with striking similarities with the corresponding elements in deuterostomes. In addition, protostome genomes contain numerous intact RAG1L-RAG2L adjacent gene pairs that lack detectable flanking TIRs. Domains and critical active site and structural amino acids needed for endonuclease and transposase activity are present and conserved in many of the predicted RAG1L and RAG2L proteins encoded in protostome genomes. Conclusions Active RAGL transposons were present in multiple protostome lineages and many were likely transmitted vertically during protostome evolution. It appears that RAGL transposons were broadly active during bilaterian evolution, undergoing multiple duplication and loss/fossilization events, with the RAGL genes that persist in present day protostomes perhaps constituting both active RAGL transposons and domesticated RAGL genes. Our findings raise the possibility that the RAGL transposon arose earlier in evolution than previously thought, either in an early bilaterian or prior to the divergence of bilaterians and non-bilaterians, and alter our understanding of the evolutionary history of this important group of transposons.http://link.springer.com/article/10.1186/s13100-020-00214-yRecombination activating genesRAGEvolutionTransposonAdaptive immunityTransposon molecular domestication
spellingShingle Eliza C. Martin
Célia Vicari
Louis Tsakou-Ngouafo
Pierre Pontarotti
Andrei J. Petrescu
David G. Schatz
Identification of RAG-like transposons in protostomes suggests their ancient bilaterian origin
Mobile DNA
Recombination activating genes
RAG
Evolution
Transposon
Adaptive immunity
Transposon molecular domestication
title Identification of RAG-like transposons in protostomes suggests their ancient bilaterian origin
title_full Identification of RAG-like transposons in protostomes suggests their ancient bilaterian origin
title_fullStr Identification of RAG-like transposons in protostomes suggests their ancient bilaterian origin
title_full_unstemmed Identification of RAG-like transposons in protostomes suggests their ancient bilaterian origin
title_short Identification of RAG-like transposons in protostomes suggests their ancient bilaterian origin
title_sort identification of rag like transposons in protostomes suggests their ancient bilaterian origin
topic Recombination activating genes
RAG
Evolution
Transposon
Adaptive immunity
Transposon molecular domestication
url http://link.springer.com/article/10.1186/s13100-020-00214-y
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