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Title: Transposable Elements versus the Fungal Genome: Impact on Whole-Genome Architecture and Transcriptional Profiles

Abstract

Transposable elements (TEs) are exceptional contributors to eukaryotic genome diversity. Their ubiquitous presence impacts the genomes of nearly all species and mediates genome evolution by causing mutations and chromosomal rearrangements and by modulating gene expression. We performed an exhaustive analysis of the TE content in 18 fungal genomes, including strains of the same species and species of the same genera. Our results depicted a scenario of exceptional variability, with species having 0.02 to 29.8% of their genome consisting of transposable elements. A detailed analysis performed on two strains of Pleurotus ostreatus uncovered a genome that is populated mainly by Class I elements, especially LTR-retrotransposons amplified in recent bursts from 0 to 2 million years (My) ago. The preferential accumulation of TEs in clusters led to the presence of genomic regions that lacked intra- and inter-specific conservation. In addition, we investigated the effect of TE insertions on the expression of their nearby upstream and downstream genes. Our results showed that an important number of genes under TE influence are significantly repressed, with stronger repression when genes are localized within transposon clusters. Our transcriptional analysis performed in four additional fungal models revealed that this TE-mediated silencing was present only in species withmore » active cytosine methylation machinery. We hypothesize that this phenomenon is related to epigenetic defense mechanisms that are aimed to suppress TE expression and control their proliferation.« less

Authors:
 [1];  [1];  [1];  [2];  [3];  [4];  [4]; ORCiD logo [1];  [1];  [2]; ORCiD logo [5];  [1];  [6]
  1. Public Univ. of Navarre, Navarre (Spain)
  2. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  3. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); St. Petersburg State Univ., St. Petersburg (Russia)
  4. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Hudson Alpha Institute for Biotechnology, Huntsville, AL (United States)
  5. Univ. of California, Riverside, CA (United States)
  6. Univ. of Utah School of Medicine, Salt Lake City, UT (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1378343
Grant/Contract Number:  
AGL2014-55971-R; AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
PLoS Genetics
Additional Journal Information:
Journal Volume: 12; Journal Issue: 6; Journal ID: ISSN 1553-7404
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES

Citation Formats

Castanera, Raul, Lopez-Varas, Leticia, Borgognone, Alessandra, LaButti, Kurt, Lapidus, Alla, Schmutz, Jeremy, Grimwood, Jane, Perez, Gumer, Pisabarro, Antonio G., Grigoriev, Igor V., Stajich, Jason E., Ramirez, Lucia, and Feschotte, Cedric. Transposable Elements versus the Fungal Genome: Impact on Whole-Genome Architecture and Transcriptional Profiles. United States: N. p., 2016. Web. doi:10.1371/journal.pgen.1006108.
Castanera, Raul, Lopez-Varas, Leticia, Borgognone, Alessandra, LaButti, Kurt, Lapidus, Alla, Schmutz, Jeremy, Grimwood, Jane, Perez, Gumer, Pisabarro, Antonio G., Grigoriev, Igor V., Stajich, Jason E., Ramirez, Lucia, & Feschotte, Cedric. Transposable Elements versus the Fungal Genome: Impact on Whole-Genome Architecture and Transcriptional Profiles. United States. https://doi.org/10.1371/journal.pgen.1006108
Castanera, Raul, Lopez-Varas, Leticia, Borgognone, Alessandra, LaButti, Kurt, Lapidus, Alla, Schmutz, Jeremy, Grimwood, Jane, Perez, Gumer, Pisabarro, Antonio G., Grigoriev, Igor V., Stajich, Jason E., Ramirez, Lucia, and Feschotte, Cedric. Mon . "Transposable Elements versus the Fungal Genome: Impact on Whole-Genome Architecture and Transcriptional Profiles". United States. https://doi.org/10.1371/journal.pgen.1006108. https://www.osti.gov/servlets/purl/1378343.
@article{osti_1378343,
title = {Transposable Elements versus the Fungal Genome: Impact on Whole-Genome Architecture and Transcriptional Profiles},
author = {Castanera, Raul and Lopez-Varas, Leticia and Borgognone, Alessandra and LaButti, Kurt and Lapidus, Alla and Schmutz, Jeremy and Grimwood, Jane and Perez, Gumer and Pisabarro, Antonio G. and Grigoriev, Igor V. and Stajich, Jason E. and Ramirez, Lucia and Feschotte, Cedric},
abstractNote = {Transposable elements (TEs) are exceptional contributors to eukaryotic genome diversity. Their ubiquitous presence impacts the genomes of nearly all species and mediates genome evolution by causing mutations and chromosomal rearrangements and by modulating gene expression. We performed an exhaustive analysis of the TE content in 18 fungal genomes, including strains of the same species and species of the same genera. Our results depicted a scenario of exceptional variability, with species having 0.02 to 29.8% of their genome consisting of transposable elements. A detailed analysis performed on two strains of Pleurotus ostreatus uncovered a genome that is populated mainly by Class I elements, especially LTR-retrotransposons amplified in recent bursts from 0 to 2 million years (My) ago. The preferential accumulation of TEs in clusters led to the presence of genomic regions that lacked intra- and inter-specific conservation. In addition, we investigated the effect of TE insertions on the expression of their nearby upstream and downstream genes. Our results showed that an important number of genes under TE influence are significantly repressed, with stronger repression when genes are localized within transposon clusters. Our transcriptional analysis performed in four additional fungal models revealed that this TE-mediated silencing was present only in species with active cytosine methylation machinery. We hypothesize that this phenomenon is related to epigenetic defense mechanisms that are aimed to suppress TE expression and control their proliferation.},
doi = {10.1371/journal.pgen.1006108},
journal = {PLoS Genetics},
number = 6,
volume = 12,
place = {United States},
year = {Mon Jun 13 00:00:00 EDT 2016},
month = {Mon Jun 13 00:00:00 EDT 2016}
}

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trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses
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Search and clustering orders of magnitude faster than BLAST
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Transposable Element Dynamics among Asymbiotic and Ectomycorrhizal Amanita Fungi
journal, June 2014

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Spy: A New Group of Eukaryotic DNA Transposons without Target Site Duplications
journal, June 2014

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MycoCosm portal: gearing up for 1000 fungal genomes
journal, December 2013

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Estimation of Nucleotide Substitution Rates in Eurotiomycete Fungi
journal, December 2002


Selection of Conserved Blocks from Multiple Alignments for Their Use in Phylogenetic Analysis
journal, April 2000


A second-generation assembly of the Drosophila simulans genome provides new insights into patterns of lineage-specific divergence
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Frequent Gene Movement and Pseudogene Evolution Is Common to the Large and Complex Genomes of Wheat, Barley, and Their Relatives
journal, May 2011

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The B73 Maize Genome: Complexity, Diversity, and Dynamics
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  • Science, Vol. 326, Issue 5956, p. 1112-1115
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Genome-Wide Evolutionary Analysis of Eukaryotic DNA Methylation
journal, April 2010


The Paleozoic Origin of Enzymatic Lignin Decomposition Reconstructed from 31 Fungal Genomes
journal, June 2012


Repeat-induced G-C to A-T mutations in Neurospora
journal, June 1989


Eukaryotic Cytosine Methyltransferases
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“One code to find them all”: a perl tool to conveniently parse RepeatMasker output files
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Whole genome comparative analysis of transposable elements provides new insight into mechanisms of their inactivation in fungal genomes
journal, February 2015


Control of Transcription by Cell Size
journal, November 2010


Considering Transposable Element Diversification in De Novo Annotation Approaches
journal, January 2011


LTR Retrotransposons in Fungi
journal, December 2011


Characterization of Transposable Elements in the Ectomycorrhizal Fungus Laccaria bicolor
journal, August 2012


Illumina TruSeq Synthetic Long-Reads Empower De Novo Assembly and Resolve Complex, Highly-Repetitive Transposable Elements
journal, September 2014


Endogenous Small RNA Mediates Meiotic Silencing of a Novel DNA Transposon
journal, June 2015

  • Wang, Yizhou; Smith, Kristina M.; Taylor, John W.
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