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

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

doi:10.1371/journal.pgen.1006108

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

Journal Article · Mon Jun 13 00:00:00 EDT 2016 · PLoS Genetics

DOI:https://doi.org/10.1371/journal.pgen.1006108· OSTI ID:1378343

Castanera, Raul ^[1]; Lopez-Varas, Leticia ^[1]; Borgognone, Alessandra ^[1]; LaButti, Kurt ^[2]; Lapidus, Alla ^[3]; Schmutz, Jeremy ^[4]; Grimwood, Jane ^[4];

^[1]; Pisabarro, Antonio G. ^[1]; Grigoriev, Igor V. ^[2];

^[5]; Ramirez, Lucia ^[1]; Feschotte, Cedric ^[6]

Public Univ. of Navarre, Navarre (Spain)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); St. Petersburg State Univ., St. Petersburg (Russia)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Hudson Alpha Institute for Biotechnology, Huntsville, AL (United States)
Univ. of California, Riverside, CA (United States)
Univ. of Utah School of Medicine, Salt Lake City, UT (United States)

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.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AGL2014-55971-R; AC02-05CH11231

OSTI ID:: 1378343

Journal Information:: PLoS Genetics, Vol. 12, Issue 6; ISSN 1553-7404

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 122 works

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Large‐scale Trichoderma diversity was associated with ecosystem, climate and geographic location Hu, Jindong; Zhou, Yi; Chen, Kai Environmental Microbiology, Vol. 22, Issue 3 https://doi.org/10.1111/1462-2920.14798	journal	August 2019
At the nexus of three kingdoms: the genome of the mycorrhizal fungus Gigaspora margarita provides insights into plant, endobacterial and fungal interactions Venice, Francesco; Ghignone, Stefano; Salvioli di Fossalunga, Alessandra Environmental Microbiology, Vol. 22, Issue 1 https://doi.org/10.1111/1462-2920.14827	journal	October 2019
Impact of polymorphic transposable elements on linkage disequilibrium along chromosomes Choudhury, Rimjhim Roy; Rogivue, Aude; Gugerli, Felix Molecular Ecology, Vol. 28, Issue 6 https://doi.org/10.1111/mec.15014	journal	March 2019
Apophysomyces variabilis: draft genome sequence and comparison of predictive virulence determinants with other medically important Mucorales Prakash, Hariprasath; Rudramurthy, Shivaprakash Mandya; Gandham, Prasad S. BMC Genomics, Vol. 18, Issue 1 https://doi.org/10.1186/s12864-017-4136-1	journal	September 2017
A genetic linkage map of Pleurotus tuoliensis integrated with physical mapping of the de novo sequenced genome and the mating type loci Gao, Wei; Qu, Jibin; Zhang, Jinxia BMC Genomics, Vol. 19, Issue 1 https://doi.org/10.1186/s12864-017-4421-z	journal	January 2018
Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan BMC Genomics, Vol. 19, Issue 1 https://doi.org/10.1186/s12864-018-4750-6	journal	May 2018
Comparative genomics applied to Mucor species with different lifestyles Lebreton, Annie; Corre, Erwan; Jany, Jean-Luc BMC Genomics, Vol. 21, Issue 1 https://doi.org/10.1186/s12864-019-6256-2	journal	February 2020
Genome expansion by allopolyploidization in the fungal strain Coniochaeta 2T2.1 and its exceptional lignocellulolytic machinery Mondo, Stephen J.; Jiménez, Diego Javier; Hector, Ronald E. Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1569-6	journal	September 2019
Molecular characterization and overexpression of mnp6 and vp3 from Pleurotus ostreatus revealed their involvement in biodegradation of cotton stalk lignin Wang, Yan; Li, Guoqing; Jiao, Xiaoyu Biology Open, Vol. 8, Issue 2 https://doi.org/10.1242/bio.036483	journal	December 2018
The genome assembly of the fungal pathogen Pyrenochaeta lycopersici from Single-Molecule Real-Time sequencing sheds new light on its biological complexity Dal Molin, Alessandra; Minio, Andrea; Griggio, Francesca PLOS ONE, Vol. 13, Issue 7 https://doi.org/10.1371/journal.pone.0200217	journal	July 2018
Comparative genome analysis indicates high evolutionary potential of pathogenicity genes in Colletotrichum tanaceti Lelwala, Ruvini V.; Korhonen, Pasi K.; Young, Neil D. PLOS ONE, Vol. 14, Issue 5 https://doi.org/10.1371/journal.pone.0212248	journal	May 2019
Unusual genome expansion and transcription suppression in ectomycorrhizal Tricholoma matsutake by insertions of transposable elements Min, Byoungnam; Yoon, Hyeokjun; Park, Julius PLOS ONE, Vol. 15, Issue 1 https://doi.org/10.1371/journal.pone.0227923	journal	January 2020
Using Population and Comparative Genomics to Understand the Genetic Basis of Effector-Driven Fungal Pathogen Evolution Plissonneau, Clémence; Benevenuto, Juliana; Mohd-Assaad, Norfarhan Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00119	journal	February 2017
Transcriptome Changes during Major Developmental Transitions Accompanied with Little Alteration of DNA Methylome in Two Pleurotus Species Wen, Jiawei; Zhang, Zhibin; Gong, Lei Genes, Vol. 10, Issue 6 https://doi.org/10.3390/genes10060465	journal	June 2019
Genome-Wide Characterization and Expression Analyses of Pleurotus ostreatus MYB Transcription Factors during Developmental Stages and under Heat Stress Based on de novo Sequenced Genome Wang, Lining; Gao, Wei; Wu, Xiangli International Journal of Molecular Sciences, Vol. 19, Issue 7 https://doi.org/10.3390/ijms19072052	journal	July 2018
Transposable Elements Adaptive Role in Genome Plasticity, Pathogenicity and Evolution in Fungal Phytopathogens Mat Razali, Nurhani; Cheah, Boon Huat; Nadarajah, Kalaivani International Journal of Molecular Sciences, Vol. 20, Issue 14 https://doi.org/10.3390/ijms20143597	journal	July 2019
Systematic Analysis of the Pleurotus ostreatus Laccase Gene (PoLac) Family and Functional Characterization of PoLac2 Involved in the Degradation of Cotton-Straw Lignin Jiao, Xiaoyu; Li, Guoqing; Wang, Yan Molecules, Vol. 23, Issue 4 https://doi.org/10.3390/molecules23040880	journal	April 2018
A plant pathology perspective of fungal genome sequencing Aylward, Janneke; Steenkamp, Emma T.; Dreyer, Léanne L. IMA Fungus, Vol. 8, Issue 1 https://doi.org/10.5598/imafungus.2017.08.01.01	journal	February 2017
Transposable elements contribute to fungal genes and impact fungal lifestyle Muszewska, Anna; Steczkiewicz, Kamil; Stepniewska-Dziubinska, Marta Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-40965-0	journal	March 2019
Genomic Plasticity Mediated by Transposable Elements in the Plant Pathogenic Fungus Colletotrichum higginsianum Tsushima, Ayako; Gan, Pamela; Kumakura, Naoyoshi Genome Biology and Evolution, Vol. 11, Issue 5 https://doi.org/10.1093/gbe/evz087	journal	April 2019
Comparative genomics of Coniophora olivacea reveals different patterns of genome expansion in Boletales Castanera, Raúl; Pérez, Gúmer; López-Varas, Leticia BMC Genomics, Vol. 18, Issue 1 https://doi.org/10.1186/s12864-017-4243-z	journal	November 2017
Using Population and Comparative Genomics to Understand the Genetic Basis of Effector-Driven Fungal Pathogen Evolution Plissonneau, Clémence; Benevenuto, Juliana; Mohd-Assaad, Norfarhan ETH Zurich https://doi.org/10.3929/ethz-b-000216386	text	January 2017
Asexual reproduction reduces transposable element load in experimental yeast populations Bast, Jens; Jaron, Kamil S.; Schuseil, Donovan eLife, Vol. 8 https://doi.org/10.7554/eLife.48548	journal	September 2019
Filamentous ascomycete genomes provide insights into Copia retrotransposon diversity in fungi Donnart, Tifenn; Piednoël, Mathieu; Higuet, Dominique BMC Genomics, Vol. 18, Issue 1 https://doi.org/10.1186/s12864-017-3795-2	journal	May 2017
Assembly, annotation, and comparison of Macrophomina phaseolina isolates from strawberry and other hosts Burkhardt, Alyssa K.; Childs, Kevin L.; Wang, Jie BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-6168-1	journal	November 2019
Protesta en Patzicía. Los pueblos de indios y la vacatio regis en el reino de Guatemala Pollack, Aaron Revista de Indias, Vol. 78, Issue 272 https://doi.org/10.3989/revindias.2018.005	journal	April 2018
Comparative study of genome-wide plant biomass-degrading CAZymes in white rot, brown rot and soft rot fungi Kameshwar, Ayyappa Kumar Sista; Qin, Wensheng Taylor & Francis https://doi.org/10.6084/m9.figshare.6741647	text	January 2018
Impact of polymorphic transposable elements on linkage disequilibrium along chromosomes Choudhury, Rimjhim Roy; Rogivue, Aude; Gugerli, Felix Wiley-Blackwell https://doi.org/10.7892/boris.123718	text	January 2019
Somatic transposition and meiotically driven elimination of an active helitron family inPleurotus ostreatus Borgognone, Alessandra; Castanera, Raúl; Muguerza, Elaia DNA Research https://doi.org/10.1093/dnares/dsw060	journal	January 2017
Genome Anatomy of Pyrenochaeta unguis-hominis UM 256, a Multidrug Resistant Strain Isolated from Skin Scraping Toh, Yue Fen; Yew, Su Mei; Chan, Chai Ling PLOS ONE, Vol. 11, Issue 9 https://doi.org/10.1371/journal.pone.0162095	journal	September 2016
New lipases by mining of Pleurotus ostreatus genome Piscitelli, Alessandra; Tarallo, Vincenzo; Guarino, Lucia PLOS ONE, Vol. 12, Issue 9 https://doi.org/10.1371/journal.pone.0185377	journal	September 2017
Comparative Genomics of Smut Pathogens: Insights From Orphans and Positively Selected Genes Into Host Specialization Benevenuto, Juliana; Teixeira-Silva, Natalia S.; Kuramae, Eiko E. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00660	journal	April 2018
Horizontal Gene Transfer From Bacteria and Plants to the Arbuscular Mycorrhizal Fungus Rhizophagus irregularis Li, Meng; Zhao, Jinjie; Tang, Nianwu Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00701	journal	May 2018
An Overview of Genomics, Phylogenomics and Proteomics Approaches in Ascomycota Muggia, Lucia; Ametrano, Claudio G.; Sterflinger, Katja Life, Vol. 10, Issue 12 https://doi.org/10.3390/life10120356	journal	December 2020

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