Obligate Biotrophy Features Unraveled by the Genomic Analysis of Rust Fungi

Rust fungi are some of the most devastating pathogens of crop plants. They are obligate biotrophs, which extract nutrients only from living plant tissues and cannot grow apart from their hosts. Their lifestyle has slowed the dissection of molecular mechanisms underlying host invasion and avoidance or suppression of plant innate immunity. We sequenced the 101–mega–base pair genome of Melampsora larici-populina, the causal agent of poplar leaf rust, and the 89–mega–base pair genome of Puccinia graminis f. sp. tritici, the causal agent of wheat and barley stem rust. We then compared the 16,399 predicted proteins of M. larici-populina to the 17,773 predicted proteins of P. graminis f. sp tritici. Genomic features related to their obligate biotrophic life-style include expanded lineage-specific gene families, a large repertoire of effector-like small secreted proteins (SSPs), impaired nitrogen and sulfur assimilation pathways, and expanded families of amino-acid, oligopeptide and hexose membrane transporters. The dramatic upregulation of transcripts coding for SSPs, secreted hydrolytic enzymes, and transporters in plants suggests that they play a role in host infection and nutrient acquisition. Some of these genomic hallmarks are mirrored in the genomes of other microbial eukaryotes that have independently evolved to infect plants, indicating convergent adaptation to a biotrophic existence inside plant cells.

Duplessis, S., A. Cuomo, C., Lin, Y.-C., Aerts, A., Tisserant, E., Veneault-Fourrey, C., L. Joly, D., Hacquard, S., Amselem, J., L. Cantarel, B., Chiu, C.-H., Couthinho, P., Feau, N., Field, M., Frey, P., Gelhaye, E., Goldberg, J., Grabherr, M., D. Kodira, C., Kohler, A., Kües, U., A. Lindquist, E., Lucas, S., Mago, R., Mauceli, E., Morin, E., Murat, C., L. Pangilinan, J., Park, R., Pearson, M., Quesneville, H., Rouhier, N., Sakthikumar, S., A. Salamov, A., Schmutz, J., Selles, B., Shapiro, H.J., Tangay, P., Henrissat, B., Van de Peer, Y., Rouzé, P., G. Ellis, J., N. Dodds, P., E. Schein, J., Zhong, S., C. Hamelin, R., V. Grigoriev, I., J. Szabon, L., Martina, F. (2011) Obligate Biotrophy Features Unraveled by the Genomic Analysis of Rust Fungi. Proc. Natl. Acad. Sci. USA 108(22):9166-71.

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