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Title: Altered patterns of gene duplication and differential gene gain and loss in fungal pathogens

Abstract

Background: Duplication, followed by fixation or random loss of novel genes, contributes to genome evolution. Particular outcomes of duplication events are possibly associated with pathogenic life histories in fungi. To date, differential gene gain and loss have not been studied at genomic scales in fungal pathogens, despite this phenomenon's known importance in virulence in bacteria and viruses. Results: To determine if patterns of gene duplication differed between pathogens and nonpathogens, we identified gene families across nine euascomycete and two basidiomycete species. Gene family size distributions were fit to power laws to compare gene duplication trends in pathogens versus non-pathogens. Fungal phytopathogens showed globally altered patterns of gene duplication, as indicated by differences in gene family size distribution. We also identified sixteen examples of gene family expansion and five instances of gene family contraction in pathogenic lineages. Expanded gene families included those predicted to be important in melanin biosynthesis, host cell wall degradation and transport functions. Contracted families included those encoding genes involved in toxin production, genes with oxidoreductase activity, as well as subunits of the vacuolar ATPase complex. Surveys of the functional distribution of gene duplicates indicated that pathogens show enrichment for gene duplicates associated with receptor and hydrolase activities,more » while euascomycete pathogens appeared to have not only these differences, but also significantly more duplicates associated with regulatory and carbohydrate binding functions. Conclusion: Differences in the overall levels of gene duplication in phytopathogenic species versus non-pathogenic relatives implicate gene inventory flux as an important virulence-associated process in fungi. We hypothesize that the observed patterns of gene duplicate enrichment, gene family expansion and contraction reflect adaptation within pathogenic life histories. These adaptations were likely shaped by ancient, as well as contemporary, intimate associations with monocot hosts.« less

Authors:
 [1];  [2];  [3];  [3];  [3]
  1. Sandia National Lab. (SNL-NM), Albuquerque, NM (United States). Dept. of Computational Systems Biology
  2. Univ. of Dublin (Ireland). Trinity College. Smurfit Inst. of Genetics
  3. North Carolina State Univ., Raleigh, NC (United States). Center for Integrated Fungal Research. Dept. of Plant Pathology
Publication Date:
Research Org.:
Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
OSTI Identifier:
1626461
Grant/Contract Number:  
NA0003525
Resource Type:
Accepted Manuscript
Journal Name:
BMC Genomics
Additional Journal Information:
Journal Volume: 9; Journal Issue: 1; Journal ID: ISSN 1471-2164
Publisher:
Springer
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Biotechnology & Applied Microbiology; Genetics & Heredity

Citation Formats

Powell, Amy J., Conant, Gavin C., Brown, Douglas E., Carbone, Ignazio, and Dean, Ralph A. Altered patterns of gene duplication and differential gene gain and loss in fungal pathogens. United States: N. p., 2008. Web. doi:10.1186/1471-2164-9-147.
Powell, Amy J., Conant, Gavin C., Brown, Douglas E., Carbone, Ignazio, & Dean, Ralph A. Altered patterns of gene duplication and differential gene gain and loss in fungal pathogens. United States. https://doi.org/10.1186/1471-2164-9-147
Powell, Amy J., Conant, Gavin C., Brown, Douglas E., Carbone, Ignazio, and Dean, Ralph A. Fri . "Altered patterns of gene duplication and differential gene gain and loss in fungal pathogens". United States. https://doi.org/10.1186/1471-2164-9-147. https://www.osti.gov/servlets/purl/1626461.
@article{osti_1626461,
title = {Altered patterns of gene duplication and differential gene gain and loss in fungal pathogens},
author = {Powell, Amy J. and Conant, Gavin C. and Brown, Douglas E. and Carbone, Ignazio and Dean, Ralph A.},
abstractNote = {Background: Duplication, followed by fixation or random loss of novel genes, contributes to genome evolution. Particular outcomes of duplication events are possibly associated with pathogenic life histories in fungi. To date, differential gene gain and loss have not been studied at genomic scales in fungal pathogens, despite this phenomenon's known importance in virulence in bacteria and viruses. Results: To determine if patterns of gene duplication differed between pathogens and nonpathogens, we identified gene families across nine euascomycete and two basidiomycete species. Gene family size distributions were fit to power laws to compare gene duplication trends in pathogens versus non-pathogens. Fungal phytopathogens showed globally altered patterns of gene duplication, as indicated by differences in gene family size distribution. We also identified sixteen examples of gene family expansion and five instances of gene family contraction in pathogenic lineages. Expanded gene families included those predicted to be important in melanin biosynthesis, host cell wall degradation and transport functions. Contracted families included those encoding genes involved in toxin production, genes with oxidoreductase activity, as well as subunits of the vacuolar ATPase complex. Surveys of the functional distribution of gene duplicates indicated that pathogens show enrichment for gene duplicates associated with receptor and hydrolase activities, while euascomycete pathogens appeared to have not only these differences, but also significantly more duplicates associated with regulatory and carbohydrate binding functions. Conclusion: Differences in the overall levels of gene duplication in phytopathogenic species versus non-pathogenic relatives implicate gene inventory flux as an important virulence-associated process in fungi. We hypothesize that the observed patterns of gene duplicate enrichment, gene family expansion and contraction reflect adaptation within pathogenic life histories. These adaptations were likely shaped by ancient, as well as contemporary, intimate associations with monocot hosts.},
doi = {10.1186/1471-2164-9-147},
journal = {BMC Genomics},
number = 1,
volume = 9,
place = {United States},
year = {Fri Mar 28 00:00:00 EDT 2008},
month = {Fri Mar 28 00:00:00 EDT 2008}
}

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The Role of Lineage-Specific Gene Family Expansion in the Evolution of Eukaryotes
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Genomics of the fungal kingdom: Insights into eukaryotic biology
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Purification and Characterization of an Endophytic Fungal Proteinase That Is Abundantly Expressed in the Infected Host Grass
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The Genome of the Diatom Thalassiosira Pseudonana: Ecology, Evolution, and Metabolism
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The Genome of the Basidiomycetous Yeast and Human Pathogen Cryptococcus neoformans
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Phytophthora Genome Sequences Uncover Evolutionary Origins and Mechanisms of Pathogenesis
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Widespread Lateral Gene Transfer from Intracellular Bacteria to Multicellular Eukaryotes
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The red Queen Hypothesis and Plant/Pathogen Interactions
journal, September 1996


The Dawn of Fungal Pathogen Genomics
journal, September 2006


The evolutionary history of Cytochrome P450 genes in four filamentous Ascomycetes
journal, February 2007

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A Human-Curated Annotation of the Candida albicans Genome
journal, June 2005


Repeat-Induced Point Mutation and the Population Structure of Transposable Elements in Microbotryum violaceum
journal, July 2005


Works referencing / citing this record:

Safety of the fungal workhorses of industrial biotechnology: update on the mycotoxin and secondary metabolite potential of Aspergillus niger, Aspergillus oryzae, and Trichoderma reesei
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Recombination and lineage-specific gene loss in the aflatoxin gene cluster of Aspergillus flavus
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Extensive Intra-Kingdom Horizontal Gene Transfer Converging on a Fungal Fructose Transporter Gene
journal, June 2013


Induction of antibacterial proteins and peptides in the coprophilous mushroom Coprinopsis cinerea in response to bacteria
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Induction of antibacterial proteins and peptides in the coprophilous mushroom Coprinopsis cinerea in response to bacteria
journal, October 2018


Proteome of the Nematode-Trapping Cells of the Fungus Monacrosporium haptotylum
journal, August 2013

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The Evolution of Fungal Metabolic Pathways
journal, December 2014


Diet shifts provoke complex and variable changes in the metabolic networks of the ruminal microbiome
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Fungal evolutionary genomics provides insight into the mechanisms of adaptive divergence in eukaryotes
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Induction of antibacterial proteins and peptides in the coprophilous mushroom Coprinopsis cinerea in response to bacteria
journal, October 2018


Diet Alters Both the Structure and Taxonomy of the Ovine Gut Microbial Ecosystem
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Comparative genomic analyses reveal the features for adaptation to nematodes in fungi
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Selection for Higher Gene Copy Number after Different Types of Plant Gene Duplications
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