Genome offers clue to functions of destructive wheat fungus

June 13, 2011

WEST LAFAYETTE, Ind. - One of the world's most destructive wheat pathogens is genetically built to evade detection before infecting its host, according to a study that mapped the genome of the fungus.

Stephen Goodwin, a Purdue and U.S. Department of Agriculture research plant pathologist, was the principal author on the effort to sequence the genome of the fungus Mycosphaerella graminicola, which causes septoria tritici blotch, a disease that greatly reduces yield and quality in wheat. Surprisingly, Goodwin said, the fungus had fewer genes related to production of enzymes that many other fungi use to penetrate and digest surfaces of plants while infecting them.

"We're guessing that the low number of enzymes is to avoid detection by plant defenses," said Goodwin, whose findings were published in the early online edition of the journal PLoS Genetics.

Enzymes often break down plant cell walls and begin removing nutrients, leading to the plant's death. M. graminicola, however, enters the plant through stomata, small pores in the surface of leaves that allow for exchange of gases and water.

Goodwin said the fungus seems to lay dormant between plant cells, avoiding detection. It later infects the plant, removing necessary nutrients and causing disease.

With the sequenced genome, scientists hope to discover which genes cause toxicity in wheat and determine ways to eliminate that toxicity or improve wheat's defenses against the fungus. Septoria tritici blotch is the No. 1 wheat pathogen in parts of Europe and is probably third in the United States, Goodwin said.

The genome also showed that M. graminicola has eight disposable chromosomes that seem to have no function. Goodwin said that plants with dispensable chromosomes have clear mechanisms for their maintenance, but no such mechanisms were obvious in the fungus.

Goodwin said the extra chromosomes were probably obtained from another species more than 10,000 years ago and have likely been retained for an important function, but it's not clear what that function is.

"That's a long time for these chromosomes to be maintained without an obvious function," he said. "They must be doing something important. Finding out what that is will be a key area for future research."

Goodwin collaborated with 57 scientists from 24 other institutions. The U.S. Department of Energy's Joint Genome Institute and Plant Research International of The Netherlands were equal partners in the research. 

Writer:  Brian Wallheimer, 765-496-2050, bwallhei@purdue.edu 

Source:  Stephen Goodwin, 765-494-4635, sgoodwin@purdue.edu, Steve.Goodwin@ARS.USDA.gov

Ag Communications: (765) 494-2722;
Keith Robinson, robins89@purdue.edu
Agriculture News Page

ABSTRACT

Finished Genome of the Fungal Wheat Pathogen Mycosphaerella graminicola Reveals Dispensome Structure, Chromosome Plasticity,
and Stealth Pathogenosis

Stephen B. Goodwin, Sarrah Ben M'Barek, Braham Dhillon, Alexander H.J. Wittenberg, Charles F. Crane, James K. Hane, Andrew J. Foster, Theo A.J. Van der Lee, Jane Grimwood, Andrea Aerts, John Antoniw, Andy Bailey, Burt Bluhm, Judith Bowler, Jim Bristow, Ate van der Burgt, Blondy Canto-Canché, Alice C.L. Churchill, Laura Conde-Ferráez, Hans J. Cools, Pedro M. Coutinho, Michael Csukai, Paramvir Dehal, Pierre De Wit, Bruno Donzelli, Henri C. van de Geest, Roeland C.H.J. van Ham, Kim E. Hammond-Kosack, Bernard Henrissat, Andrzej Kilian, Adilson K. Kobayashi, Edda Koopmann, Yiannis Kourmpetis, Arnold Kuzniar, Erika Lindquist, Vincent Lombard, Chris Maliepaard, Natalia Martins, Rahim Mehrabi, Jan P.H. Nap, Alisa Ponomarenko, Jason J. Rudd, Asaf Salamov, Jeremy Schmutz, Henk J. Schouten, Harris Shapiro, Ioannis Stergiopoulos, Stefano F.F. Torriani, Hank Tu, Ronald P. de Vries, Cees Waalwijk, Sarah B. Ware, Ad Wiebenga, Lute-Harm Zwiers, Richard P. Oliver, Igor V. Grigoriev, Gert H.J. Kema

The plant-pathogenic fungus Mycosphaerella graminicola (asexual stage: Septoria tritici) causes septoria tritici blotch, a disease that greatly reduces the yield and quality of wheat. This disease is economically important in most wheat-growing areas worldwide and threatens 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 evades host defenses. Although this type of stealth pathogenicity occurs commonly in Mycosphaerella and other Dothideomycetes, the largest class of plant-pathogenic fungi, its genetic basis is not known. To address this problem, the genome of M. graminicola was sequenced completely. The finished genome contains 21 chromosomes, eight of which could be lost with no visible effect on the fungus and thus are dispensable. This eight-chromosome dispensome is dynamic in field and progeny isolates, is different from the core genome in gene and repeat content, and appears to have originated by ancient horizontal transfer from an unknown donor. Synteny plots of the M. graminicola chromosomes versus those of the only other sequenced Dothideomycete, Stagonospora nodorum, revealed conservation of gene content but not order or orientation, suggesting a high rate of intra-chromosomal rearrangement in one or both species. This observed "mesosynteny" is very different from synteny seen between other organisms. A surprising feature of the M. graminicola genome compared to other sequenced plant pathogens was that it contained very few genes for enzymes that break down plant cell walls, which was more similar to endophytes than to 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 endophytic ancestors.