Variable genome evolution in fungi after transposon-mediated amplification of a housekeeping gene

Dhillon, Braham; Kema, Gert H.  J.; Hamelin, Richard C.; Bluhm, Burt H.; Goodwin, Stephen B.

doi:10.1186/s13100-019-0177-0

Title: Variable genome evolution in fungi after transposon-mediated amplification of a housekeeping gene

Abstract

Transposable elements (TEs) can be key drivers of evolution, but the mechanisms and scope of how they impact gene and genome function are largely unknown. Previous analyses revealed that TE-mediated gene amplifications can have variable effects on fungal genomes, from inactivation of function to production of multiple active copies. For example, a DNA methyltransferase gene in the wheat pathogen Zymoseptoria tritici (synonym Mycosphaerella graminicola) was amplified to tens of copies, all of which were inactivated by Repeat-Induced Point mutation (RIP) including the original, resulting in loss of cytosine methylation. In another wheat pathogen, Pyrenophora tritici-repentis, a histone H3 gene was amplified to tens of copies with little evidence of RIP, leading to many potentially active copies. To further test the effects of transposon-aided gene amplifications on genome evolution and architecture, the repetitive fraction of the significantly expanded genome of the banana pathogen, Pseudocercospora fijiensis, was analyzed in greater detail. These analyses identified a housekeeping gene, histone H3, which was captured and amplified to hundreds of copies by a hAT DNA transposon, all of which were inactivated by RIP, except for the original. In P. fijiensis the original H3 gene probably was not protected from RIP, but most likely was maintainedmore »« less

Authors:

Dhillon, Braham ^[1]; Kema, Gert H. J. ^[2]; Hamelin, Richard C. ^[3]; Bluhm, Burt H. ^[1];

^[4]

University of Arkansas, Fayetteville, AR (United States)
Wageningen University (Netherlands); Wageningen University and Research Centre (Netherlands)
University of British Columbia, Vancouver, BC (Canada)
US Dept. of Agriculture (USDA), West Lafayette, IN (United States); Purdue University, West Lafayette, IN (United States)

Publication Date:: Tue Aug 27 00:00:00 EDT 2019

Research Org.:: USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Org.:: USDOE Office of Science (SC); United States Department of Agriculture (USDA); Agricultural Research Service (ARS)

OSTI Identifier:: 1627014

Grant/Contract Number:: AC02-05CH11231; W-7405-ENG-48

Resource Type:: Accepted Manuscript

Journal Name:: Mobile DNA

Additional Journal Information:: Journal Volume: 10; Journal Issue: 1; Journal ID: ISSN 1759-8753

Publisher:: BioMed Central

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; genetics and heredity; fungal evolution; genome evolution; purifying selection; transduplication

Citation Formats


                    Dhillon, Braham, Kema, Gert H.  J., Hamelin, Richard C., Bluhm, Burt H., and Goodwin, Stephen B. Variable genome evolution in fungi after transposon-mediated amplification of a housekeeping gene.  United States: N. p., 2019. 
Web.  doi:10.1186/s13100-019-0177-0.

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                    Dhillon, Braham, Kema, Gert H.  J., Hamelin, Richard C., Bluhm, Burt H., & Goodwin, Stephen B. Variable genome evolution in fungi after transposon-mediated amplification of a housekeeping gene.  United States.  https://doi.org/10.1186/s13100-019-0177-0

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                    Dhillon, Braham, Kema, Gert H.  J., Hamelin, Richard C., Bluhm, Burt H., and Goodwin, Stephen B. Tue .  
"Variable genome evolution in fungi after transposon-mediated amplification of a housekeeping gene".  United States.  https://doi.org/10.1186/s13100-019-0177-0.  https://www.osti.gov/servlets/purl/1627014.

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@article{osti_1627014,

  title        = {Variable genome evolution in fungi after transposon-mediated amplification of a housekeeping gene},

  author       = {Dhillon, Braham and Kema, Gert H.  J. and Hamelin, Richard C. and Bluhm, Burt H. and Goodwin, Stephen B.},

  abstractNote = {Transposable elements (TEs) can be key drivers of evolution, but the mechanisms and scope of how they impact gene and genome function are largely unknown. Previous analyses revealed that TE-mediated gene amplifications can have variable effects on fungal genomes, from inactivation of function to production of multiple active copies. For example, a DNA methyltransferase gene in the wheat pathogen Zymoseptoria tritici (synonym Mycosphaerella graminicola) was amplified to tens of copies, all of which were inactivated by Repeat-Induced Point mutation (RIP) including the original, resulting in loss of cytosine methylation. In another wheat pathogen, Pyrenophora tritici-repentis, a histone H3 gene was amplified to tens of copies with little evidence of RIP, leading to many potentially active copies. To further test the effects of transposon-aided gene amplifications on genome evolution and architecture, the repetitive fraction of the significantly expanded genome of the banana pathogen, Pseudocercospora fijiensis, was analyzed in greater detail. These analyses identified a housekeeping gene, histone H3, which was captured and amplified to hundreds of copies by a hAT DNA transposon, all of which were inactivated by RIP, except for the original. In P. fijiensis the original H3 gene probably was not protected from RIP, but most likely was maintained intact due to strong purifying selection. Comparative analyses revealed that a similar event occurred in five additional genomes representing the fungal genera Cercospora, Pseudocercospora and Sphaerulina. These results indicate that the interplay of TEs and RIP can result in different and unpredictable fates of amplified genes, with variable effects on gene and genome evolution.},

  doi          = {10.1186/s13100-019-0177-0},

  journal      = {Mobile DNA},

  number       = 1,

  volume       = 10,

  place        = {United States},

  year         = {Tue Aug 27 00:00:00 EDT 2019},

  month        = {Tue Aug 27 00:00:00 EDT 2019}

}

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Journal Article Krishnan, Parvathy ; Ma, Xin ; McDonald, Bruce A. ; ... - BMC Evolutionary Biology (Online)

Background: Fungal plant pathogens secrete a large arsenal of hydrolytic enzymes during the course of infection, including peptidases. Secreted peptidases have been extensively studied for their role as effectors. In this study, we combined transcriptomics, comparative genomics and evolutionary analyses to investigate all 39 secreted peptidases in the fungal wheat pathogen Zymoseptoria tritici and its close relatives Z. pseudotritici and Z. ardabiliae. Results: RNA-seq data revealed that a majority of the secreted peptidases displayed differential transcription during the course of Z. tritici infection, indicative of specialization for different stages in the life cycle. Evolutionary analyses detected widespread evidence of adaptivemore »« less
https://doi.org/10.1186/s12862-018-1123-3

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Combating a Global Threat to a Clonal Crop: Banana Black Sigatoka Pathogen Pseudocercospora fijiensis (Synonym Mycosphaerella fijiensis) Genomes Reveal Clues for Disease Control

Journal Article Arango Isaza, Rafael E. ; Diaz-Trujillo, Caucasella ; Dhillon, Braham ; ... - PLoS Genetics

Black Sigatoka or black leaf streak disease, caused by the Dothideomycete fungus Pseudocercospora fijiensis (previously: Mycosphaerella fijiensis), is the most significant foliar disease of banana worldwide. Due to the lack of effective host resistance, management of this disease requires frequent fungicide applications, which greatly increase the economic and environmental costs to produce banana. Weekly applications in most banana plantations lead to rapid evolution of fungicide-resistant strains within populations causing disease-control failures throughout the world. Given its extremely high economic importance, two strains of P. fijiensis were sequenced and assembled with the aid of a new genetic linkage map. The 74-Mbmore »« less
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https://doi.org/10.1371/journal.pgen.1005876

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Additional file 1: of Variable genome evolution in fungi after transposon-mediated amplification of a housekeeping gene
dataset, January 2019

Dhillon, Braham; Kema, Gert; Hamelin, Richard
figshare
DOI: 10.6084/m9.figshare.9739991
This dataset is a supplement to the current record