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Title: Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity and stealth pathogenesis

Author
item Goodwin, Stephen - Steve
item M'barek, Sarrah Ben - Plant Research International - Netherlands
item Dhillon, Braham - Purdue University
item Wittenberg, Alexander H. - Plant Research International - Netherlands
item Crane, Charles
item Van Der Lee, Theo A. - Plant Research International - Netherlands
item Grimwood, Jane - Indiana University-Purdue University
item Aerts, Andrea - Joint Genome Institute
item Antoniw, John - Rothamsted Research
item Bailey, Andy - University Of Bristol
item Bluhm, Burt - University Of Arkansas
item Bowler, Judith - Syngenta - United Kingdom
item Bristow, Jim - Joint Genome Institute
item Canto-canche, Blondy - Luiz De Queiroz College Of Agriculture (ESALQ)
item Churchill, Alice - Cornell University - New York
item Conde-ferraez, Laura - Indiana University-Purdue University
item Cools, Hans - Rothamsted Research
item Coutinho, Pedro - National Council For Scientific Research-Cnrs
item Csukai, Michael - Syngenta - United Kingdom
item Dehal, Paramvir - Joint Genome Institute
item De Wit, Pierre - Wageningen Agricultural University
item Donzelli, Bruno
item Foster, Andres - Indiana University-Purdue University
item Hammond-kosack, Kim - Rothamsted Research
item Hane, James - Indiana University-Purdue University
item Henrissat, Bernard - National Council For Scientific Research-Cnrs
item Killian, Andrzej - Diversity Arrays Technology
item Koopmann, Edda - Bayer Crop Sciences, Germany
item Kourmpetis, Yiannis - Wageningen University And Research Center
item Kuzniar, Arnold - Embrapa Genetic Resources
item Lindquist, Erika - Joint Genome Institute
item Lombard, Vincent - National Council For Scientific Research-Cnrs
item Maliepaard, Chris - National Council For Scientific Research-Cnrs
item Martins, Natalia - Embrapa Genetic Resources
item Mahrabi, Rahim - Wageningen Agricultural University
item Oliver, Richard - Indiana University-Purdue University
item Ponomarenko, Alisa - Purdue University
item Rudd, Jason - Rothamsted Research
item Salamov, Asaf - Joint Genome Institute
item Schmutz, Jeremy - Indiana University-Purdue University
item Schouten, Henk - Plant Research International - Netherlands
item Shapiro, Harris - Joint Genome Institute
item Stergiopoulos, Ioannis - Wageningen Agricultural University
item Torriani, Stefano F. - Indiana University-Purdue University
item Tu, Hank - Joint Genome Institute
item De Vries, Ronald - Indiana University-Purdue University
item Wiebenga, Ad - Indiana University-Purdue University
item Zwiers, Lute-harm - Indiana University-Purdue University
item Grigoriev, Igor - Joint Genome Institute
item Kema, Gert H. - Plant Research International - Netherlands

Submitted to: PLoS Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/28/2011
Publication Date: 6/9/2011
Citation: Goodwin, S.B., M'Barek, S., Dhillon, B., Wittenberg, A.J., Crane, C.F., Van Der Lee, T.J., Grimwood, J., Aerts, A., Antoniw, J., Bailey, A., Bluhm, B., Bowler, J., Bristow, J., Canto-Canche, B., Churchill, A., Conde-Ferraez, L., Cools, H., Coutinho, P.M., Csukai, M., Dehal, P., De Wit, P., Donzelli, B., Foster, A.J., Hammond-Kosack, K., Hane, J., Henrissat, B., Killian, A., Koopmann, E., Kourmpetis, Y., Kuzniar, A., Lindquist, E., Lombard, V., Maliepaard, C., Martins, N., Mahrabi, R., Oliver, R., Ponomarenko, A., Rudd, J., Salamov, A., Schmutz, J., Schouten, H.J., Shapiro, H., Stergiopoulos, I., Torriani, S.F., Tu, H., De Vries, R.P., Wiebenga, A., Zwiers, L., Grigoriev, I.V., Kema, G.J. 2011. Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity and stealth pathogenesis. PLoS Genetics. Available at: http://www.plosgenetics.org/article/info%3Adoi%2F10.1371%2Fjournal.pgen.1002070.

Interpretive Summary: The plant-pathogenic fungus Mycosphaerella graminicola (asexual stage: Septoria tritici) causes Septoria tritici blotch of wheat. This disease can cause economically important damage of wheat crops and is a potential threat to global food production. Control of the disease has been hampered by a limited understanding of the genetic and biochemical bases of pathogenicity, including mechanisms of infection and of resistance in the host. Unlike most other plant pathogens, M. graminicola has a long latent period during which it seems able to evade host defenses, but the genetic basis for this trait is not known. To address this problem, the genome of the fungus was sequenced to completion through the Community Sequencing Program of the U.S. Department of Energy’s Joint Genome Institute. The finished genome sequence contains 21 chromosomes, eight of which could be lost with no visible effect on the fungus so are dispensable. The dispensable chromosomes were different from those in the core genome and appear to have originated by ancient horizontal gene transfer from an unknown donor species. A surprising feature of the M. graminicola genome was a low number of genes for enzymes that break down plant cell walls; many of these genes may have been lost during evolution to evade detection by plant defense mechanisms leading to the current stealth pathogenicity. This information will be useful to fungal geneticists and evolutionary biologists to better understand the genetics and evolution of dispensable chromosomes and stealth pathogenicity in M. graminicola. Fungal biologists can use the sequence to knock out gene expression for functional genomics analyses of interacting genetic networks. Plant pathologists may be able to use this information to design better strategies for disease management, particularly once the biochemical bases for the genetic interactions between host and pathogen are better understood.

Technical Abstract: A finished genome was obtained for Mycosphaerella graminicola, the fungal cause of septoria tritici blotch and a global threat to wheat production, containing thirteen core and eight dispensable chromosomes. The latter, called collectively the dispensome, were dynamic in field and progeny isolates. They were distinct in structure, gene and repeat content but contained parts from each core chromosome, suggesting ancient horizontal gene transfer followed by elevated recombination as the major forces driving their evolution. The genome of M. graminicola had far fewer genes for cell wall-degrading enzymes and secondary metabolites compared to other plant pathogens. The stealth pathogenesis of M. graminicola probably involves degradation of proteins rather than carbohydrates to evade host defenses during the biotrophic stage of infection and may have evolved from an endophytic ancestor.