Novel Introner-Like Elements in fungi Are Involved in Parallel Gains of Spliceosomal Introns.

Spliceosomal introns are key components of the eukaryotic gene structure. Although they contributed to the emergence of eukaryotes, their origin remains elusive. In fungi, they might originate from the multiplication of invasive introns named Introner-Like Elements (ILEs). However, so far ILEs have...

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Main Authors: Jérôme Collemare, Henriek G Beenen, Pedro W Crous, Pierre J G M de Wit, Ate van der Burgt
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2015-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC4457414?pdf=render
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author Jérôme Collemare
Henriek G Beenen
Pedro W Crous
Pierre J G M de Wit
Ate van der Burgt
author_facet Jérôme Collemare
Henriek G Beenen
Pedro W Crous
Pierre J G M de Wit
Ate van der Burgt
author_sort Jérôme Collemare
collection DOAJ
description Spliceosomal introns are key components of the eukaryotic gene structure. Although they contributed to the emergence of eukaryotes, their origin remains elusive. In fungi, they might originate from the multiplication of invasive introns named Introner-Like Elements (ILEs). However, so far ILEs have been observed in six fungal species only, including Fulvia fulva and Dothistroma septosporum (Dothideomycetes), arguing against ILE insertion as a general mechanism for intron gain. Here, we identified novel ILEs in eight additional fungal species that are phylogenetically related to F. fulva and D. septosporum using PCR amplification with primers derived from previously identified ILEs. The ILE content appeared unique to each species, suggesting independent multiplication events. Interestingly, we identified four genes each containing two gained ILEs. By analysing intron positions in orthologues of these four genes in Ascomycota, we found that three ILEs had inserted within a 15 bp window that contains regular spliceosomal introns in other fungal species. These three positions are not the result of intron sliding because ILEs are newly gained introns. Furthermore, the alternative hypothesis of an inferred ancestral gain followed by independent losses contradicts the observed degeneration of ILEs. These observations clearly indicate three parallel intron gains in four genes that were randomly identified. Our findings suggest that parallel intron gain is a phenomenon that has been highly underestimated in ILE-containing fungi, and likely in the whole fungal kingdom.
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spelling doaj.art-28e6ba94a1324d6b9cba460ab76c21de2022-12-22T02:51:41ZengPublic Library of Science (PLoS)PLoS ONE1932-62032015-01-01106e012930210.1371/journal.pone.0129302Novel Introner-Like Elements in fungi Are Involved in Parallel Gains of Spliceosomal Introns.Jérôme CollemareHenriek G BeenenPedro W CrousPierre J G M de WitAte van der BurgtSpliceosomal introns are key components of the eukaryotic gene structure. Although they contributed to the emergence of eukaryotes, their origin remains elusive. In fungi, they might originate from the multiplication of invasive introns named Introner-Like Elements (ILEs). However, so far ILEs have been observed in six fungal species only, including Fulvia fulva and Dothistroma septosporum (Dothideomycetes), arguing against ILE insertion as a general mechanism for intron gain. Here, we identified novel ILEs in eight additional fungal species that are phylogenetically related to F. fulva and D. septosporum using PCR amplification with primers derived from previously identified ILEs. The ILE content appeared unique to each species, suggesting independent multiplication events. Interestingly, we identified four genes each containing two gained ILEs. By analysing intron positions in orthologues of these four genes in Ascomycota, we found that three ILEs had inserted within a 15 bp window that contains regular spliceosomal introns in other fungal species. These three positions are not the result of intron sliding because ILEs are newly gained introns. Furthermore, the alternative hypothesis of an inferred ancestral gain followed by independent losses contradicts the observed degeneration of ILEs. These observations clearly indicate three parallel intron gains in four genes that were randomly identified. Our findings suggest that parallel intron gain is a phenomenon that has been highly underestimated in ILE-containing fungi, and likely in the whole fungal kingdom.http://europepmc.org/articles/PMC4457414?pdf=render
spellingShingle Jérôme Collemare
Henriek G Beenen
Pedro W Crous
Pierre J G M de Wit
Ate van der Burgt
Novel Introner-Like Elements in fungi Are Involved in Parallel Gains of Spliceosomal Introns.
PLoS ONE
title Novel Introner-Like Elements in fungi Are Involved in Parallel Gains of Spliceosomal Introns.
title_full Novel Introner-Like Elements in fungi Are Involved in Parallel Gains of Spliceosomal Introns.
title_fullStr Novel Introner-Like Elements in fungi Are Involved in Parallel Gains of Spliceosomal Introns.
title_full_unstemmed Novel Introner-Like Elements in fungi Are Involved in Parallel Gains of Spliceosomal Introns.
title_short Novel Introner-Like Elements in fungi Are Involved in Parallel Gains of Spliceosomal Introns.
title_sort novel introner like elements in fungi are involved in parallel gains of spliceosomal introns
url http://europepmc.org/articles/PMC4457414?pdf=render
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AT pedrowcrous novelintronerlikeelementsinfungiareinvolvedinparallelgainsofspliceosomalintrons
AT pierrejgmdewit novelintronerlikeelementsinfungiareinvolvedinparallelgainsofspliceosomalintrons
AT atevanderburgt novelintronerlikeelementsinfungiareinvolvedinparallelgainsofspliceosomalintrons