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Title: Genome expansion and gene loss in powdery mildew fungi reveal functional tradeoffs in extreme parasitism

Author
item SPANU, PIETRO - Imperial College
item Cadle-Davidson, Lance
item MILGROOM, MICHAEL - Cornell University
item AMSELEM, JOELLE - Institut National De La Recherche Agronomique (INRA)
item BURGIS, TIMOTHY - Imperial College
item ABBOTT, JAMES - Imperial College
item BUTCHER, SARAH - Imperial College
item PANSTRUGA, RALPH - Max Planck Society
item BROWN, JAMES - John Innes Center
item KELLER, BEAT - University Of Zurich

Submitted to: Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/2/2010
Publication Date: 12/10/2010
Citation: Spanu, P.D., Cadle Davidson, L.E., Milgroom, M., Amselem, J., Burgis, T.A., Abbott, J.A., Butcher, S.A., Panstruga, R., Brown, J.K., Keller, B. 2010. Genome expansion and gene loss in powdery mildew fungi reveal functional tradeoffs in extreme parasitism. Science. 330: 1543-1546.

Interpretive Summary: Organisms with nuclei (eukaryotes) have huge variation in DNA genome size, ranging from microsporidia (~2.9 million base pairs (Mb)) to the lung-fish (~1.2 trillion base pairs). This extraordinary variation is largely a result of the proliferation of mobile DNA elements also called “jumping genes.” These jumping genes are essentially DNA parasites that use the organism for their own survival and proliferation. As a result, eukaryotes have defense mechanisms to constrain their proliferation. In this study we report that genomes of powdery mildew fungi are ~120Mb, four times the size of the genomes of similar fungi, due to a massive proliferation of jumping genes. We found that one of the main defenses against jumping genes is missing from powdery mildews, which could explain this proliferation. The fact that powdery mildews require living hosts and feed inside plant cells suggests that genome miniaturisation is not a necessary accompaniment of parasitism. Indeed other plant pathogenic fungi such as the potato late blight pathogen, rusts, and truffles show similar genome expansion, suggesting that the phenomenon of jumping gene proliferation is connected to their common lifestyle.

Technical Abstract: Eukaryotic genomes vary in size over five orders of magnitude ranging from microsporidia (~2.9Mb) to the lung-fish (~1.2Tb). This extraordinary variation is largely a result of the proliferation of mobile DNA elements also referred to as “genomic parasites.” The constraints on genome size may be imposed by fitness cost or from stochastic mechanisms that favour the production of small genomes. Specific molecular mechanisms such RNA interference, nucleic acid editing and repeat- induced point mutation (RIP) have evolved to limit the multiplication of mobile genomic parasites. In this study we report that four genomes of the powdery mildew fungi Erysiphales are ~120Mb, and that this is due to a massive and extraordinary amplification of retro-transposons which result in > 70% repetitive DNA. We have found that all the three genes encoding enzymes known to be necessary for Repeat Induced Point mutation (RIP) are absent from all powdery mildews analysed. A comparative genome-wide analysis of repetitive DNA in Blumeria graminis f.sp. hordei and other Ascomycetes reveals an absence of RIP-ing in the repetitive DNA. The fact that B. graminis, like all powdery mildews, is an obligate biotrophic pathogen whose significant trophic stage is intracellular suggests that genome miniaturisation is not a necessary accompaniment of parasitism observed elsewhere. Indeed other plant pathogenic fungi such as the rusts (Basidiomycetes), Phytophthora infestans (Oomycetes) and mycorrhizal fungi such as truffles and the Glomales show similar genome expansion, suggesting that the phenomenon is connected to their common life style.