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

Abstract

Background: 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. Results: 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 likelymore » 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. Conclusions: 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.« less

Authors:
 [1];  [2];  [3];  [1]; ORCiD logo [4]
  1. Univ. of Arkansas, Fayetteville, AR (United States). Division of Agriculture, Dept. of Plant Pathology
  2. Wageningen Univ. (Netherlands). Lab. of Phytopathology; Wageningen Univ. and Research Centre (Netherlands). Plant Research International B.V.
  3. Univ. of British Columbia, Vancouver, BC (Canada). Faculty of Forest and Conservation Sciences
  4. US Dept. of Agriculture (USDA), West Lafayette, IN (United States). Agricultural Research Service (ARS), Crop Production and Pest Control Research Unit; Purdue Univ., West Lafayette, IN (United States)
Publication Date:
Research Org.:
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); 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
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Genetics & 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. https://doi.org/10.1186/s13100-019-0177-0.
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
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.
@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 = {Background: 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. Results: 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. Conclusions: 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 = {2019},
month = {8}
}

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