skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

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

Journal Article · · Mobile DNA
 [1];  [2];  [3];  [1]; ORCiD logo [4]
  1. University of Arkansas, Fayetteville, AR (United States)
  2. Wageningen University (Netherlands); Wageningen University and Research Centre (Netherlands)
  3. University of British Columbia, Vancouver, BC (Canada)
  4. US Dept. of Agriculture (USDA), West Lafayette, IN (United States); Purdue University, West Lafayette, IN (United States)

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.

Research Organization:
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC); United States Department of Agriculture (USDA); Agricultural Research Service (ARS)
Grant/Contract Number:
AC02-05CH11231; W-7405-ENG-48
OSTI ID:
1627014
Journal Information:
Mobile DNA, Vol. 10, Issue 1; ISSN 1759-8753
Publisher:
BioMed CentralCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 1 work
Citation information provided by
Web of Science

References (52)

Combating a Global Threat to a Clonal Crop: Banana Black Sigatoka Pathogen Pseudocercospora fijiensis (Synonym Mycosphaerella fijiensis) Genomes Reveal Clues for Disease Control journal August 2016
Evolution of the EKA family of powdery mildew avirulence-effector genes from the ORF 1 of a LINE retrotransposon text January 2015
Evolutionary impact of transposable elements on genomic diversity and lineage-specific innovation in vertebrates journal September 2015
Identification of a functional transposon insertion in the maize domestication gene tb1 journal September 2011
Host specialization of the blast fungus Magnaporthe oryzae is associated with dynamic gain and loss of genes linked to transposable elements journal May 2016
Clustal W and Clustal X version 2.0 journal September 2007
Selection of Conserved Blocks from Multiple Alignments for Their Use in Phylogenetic Analysis journal April 2000
RIP: the evolutionary cost of genome defense journal September 2004
Genome Expansion and Gene Loss in Powdery Mildew Fungi Reveal Tradeoffs in Extreme Parasitism journal December 2010
In silico reversal of repeat-induced point mutation (RIP) identifies the origins of repeat families and uncovers obscured duplicated genes journal January 2010
In silico Phylogenetic Analysis of hAT Transposable Elements in Plants journal June 2018
Rearrangement of duplicated DNA in specialized cells of Neurospora journal December 1987
RIPCAL: a tool for alignment-based analysis of repeat-induced point mutations in fungal genomic sequences journal November 2008
A Retrotransposon-Mediated Gene Duplication Underlies Morphological Variation of Tomato Fruit journal March 2008
Recurrence of repeat-induced point mutation (RIP) in Neurospora crassa. journal April 1991
A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi journal January 2011
Hidden Markov model speed heuristic and iterative HMM search procedure journal August 2010
Repeat-Induced Point Mutation (RIP) as an Alternative Mechanism of Evolution Toward Virulence in Leptosphaeria maculans journal August 2009
PIWI proteins and their interactors in piRNA biogenesis, germline development and gene expression journal June 2014
Origin and Domestication of the Fungal Wheat Pathogen Mycosphaerella graminicola via Sympatric Speciation journal November 2006
Structure and Evolution of the hAT Transposon Superfamily journal July 2001
A resurrected mammalian hAT transposable element and a closely related insect element are highly active in human cell culture journal October 2012
Mobile Elements: Drivers of Genome Evolution journal March 2004
Evolutionary Dynamics of hAT DNA Transposon Families in Saccharomycetaceae journal December 2014
DNA Transposons: Nature and Applications in Genomics journal April 2010
ProtTest: selection of best-fit models of protein evolution journal January 2005
Evolution of the EKA family of powdery mildew avirulence-effector genes from the ORF 1 of a LINE retrotransposon journal November 2015
Comparative Genomics of a Plant-Pathogenic Fungus, Pyrenophora tritici-repentis , Reveals Transduplication and the Impact of Repeat Elements on Pathogenicity and Population Divergence journal January 2013
OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes journal September 2003
Coevolution between a Family of Parasite Virulence Effectors and a Class of LINE-1 Retrotransposons journal October 2009
Pseudogene-mediated posttranscriptional silencing of HMGA1 can result in insulin resistance and type 2 diabetes journal July 2010
Accidental Amplification and Inactivation of a Methyltransferase Gene Eliminates Cytosine Methylation in Mycosphaerella graminicola journal July 2010
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies journal January 2014
Alu elements: know the SINEs journal January 2011
A Telomeric Avirulence Gene Determines Efficacy for the Rice Blast Resistance Gene Pi-ta journal November 2000
A Telomeric Avirulence Gene Determines Efficacy for the Rice Blast Resistance Gene Pi-ta journal November 2000
Transposable element-assisted evolution and adaptation to host plant within the Leptosphaeria maculans-Leptosphaeria biglobosa species complex of fungal pathogens journal January 2014
Frequent emergence and functional resurrection of processed pseudogenes in the human and mouse genomes journal March 2007
How important are transposons for plant evolution? journal December 2012
Basic local alignment search tool journal October 1990
The Functional Role of Pack-MULEs in Rice Inferred from Purifying Selection and Expression Profile journal January 2009
teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. journal September 1995
Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism text January 2010
Complete Genome Sequence of Clostridium botulinum CJ0611A1, a Type A(B) Isolate Associated with an International Outbreak of Botulism from Commercial Carrot Juice journal January 2021
Effector diversification within compartments of the Leptosphaeria maculans genome affected by Repeat-Induced Point mutations journal February 2011
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies text January 2014
Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium journal March 2010
MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0 journal October 2013
Massive horizontal transfer of transposable elements in insects journal April 2017
RevTrans: multiple alignment of coding DNA from aligned amino acid sequences journal July 2003
Mating pair stabilization mediates bacterial conjugation species specificity journal June 2022
PAML: a program package for phylogenetic analysis by maximum likelihood journal January 1997