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

Authors: DHILLON, BRAHAM - UNIVERSITY OF ARKANSAS; KEMA, GERT - PLANT RESEARCH INTERNATIONAL - NETHERLANDS; HAMELIN, RICHARD - UNIVERSITY OF BRITISH COLUMBIA; BLUHM, BURT - UNIVERSITY OF ARKANSAS; Goodwin, Stephen - Steve

Submitted to: MOBILE DNA
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/1/2019
Publication Date: 8/30/2019
Citation: Dhillon, B., Kema, G.H., Hamelin, R., Bluhm, B., Goodwin, S.B. 2019. Variable genome evolution in fungi after transposon-mediated amplification of a housekeeping gene. Molecular Biology and Evolution. 10:37. https://doi.org/10.1186/s13100-019-0177-0.
DOI: https://doi.org/10.1186/s13100-019-0177-0

Interpretive Summary: Transposable elements (TEs) are mobile pieces of DNA that can have large effects on gene and genome evolution, but the extent to which they cause changes in fungi is largely unknown. To test the effects of TE-aided gene amplifications on the evolution of fungal genomes, transposable elements in the genomes of several related fungi were analyzed in detail. These analyses identified an essential gene, histone H3, which was captured and amplified to hundreds of copies by a specific type of transposable element. All of the copies were inactivated by a fungal mechanism that mutates and inactivates transposons, except for the original, which contrasts with analyses in other fungi in which all copies including the original, or no copies, had been inactivated. Together these results indicate that effects of multiple gene copies on gene and genome evolution can be different and unpredictable. This information will be of interest to geneticists and evolutionary biologists studying gene and genome evolution and to plant pathologists trying to understand the evolution of pathogenicity.

Technical Abstract: Transposable elements (TEs) can be key drivers of evolution, but the exact mechanisms of how they impact gene and genome function are largely unknown. Previous analyses have shown that TE-mediated gene amplification can have variable effects on fungal genomes, from inactivation of function to production of multiple active copies. To further test the effects of transposon-aided gene amplifications on genome architecture, the repetitive fraction of the significantly expanded Pseudocercospora fijiensis genome 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. Comparative genome analyses in related fungi revealed that a similar event occurred in five additional sequenced fungal genomes from three genera (Cercospora, Pseudocercospora and Sphaerulina). Histone H3 amplification was described previously in the related wheat pathogen Pyrenophora tritici-repentis. Our analyses showed key differences in the results of amplification events for fungi in the class Dothideomycetes. Previously, 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 P. tritici-repentis, a histone H3 gene was amplified to tens of copies, but there was little evidence of RIP, leading to many potentially active copies. In contrast, for banana-infecting P. fijiensis and its relatives, a histone H3 gene was amplified to hundreds of copies, all of which were inactivated by RIP except for the original. The original H3 gene was not protected from RIP, but probably was maintained due to strong negative selection. Together these results indicate that the interplay of TEs and RIP can result in different and unpredictable fates of amplified genes on gene and genome evolution.