Obligate biotrophy features unraveled by the genomic analysis of the rust fungi, Melampsora larici-populina and Puccinia graminis f. sp. tritici

Authors: DUPLESSIS, SEBASTIEN - Institut National De La Recherche Agronomique (INRA); CUOMO, CHRISTINA - Broad Institute Of Mit/harvard; LIN, YAO-CHENG - Ghent University; AERTS, ANDREA - Joint Genome Institute; TISSERANT, EMILIE - Institut National De La Recherche Agronomique (INRA); VENEAULT-FOURREY, CLAIRE - Institut National De La Recherche Agronomique (INRA); JOLY, DAVID - Canadian Forest Service; HACQUARD, STEPHANE - Institut National De La Recherche Agronomique (INRA); AMSELEM, JOELLE - Institut National De La Recherche Agronomique (INRA); CANTAREL, BRANDI - National Council For Scientific Research-Cnrs; CHIU, READMAN - Genome Science Centre-Canada; COUTHINHO, PEDRO - National Council For Scientific Research-Cnrs; FEAU, NICOLAS - Canadian Forest Service; FIELD, MATHEW - Genome Science Centre-Canada; FREY, PASCAL - Institut National De La Recherche Agronomique (INRA); GELHAYE, ERIC - Institut National De La Recherche Agronomique (INRA); GOLDBERG, JONATHAN - Broad Institute Of Mit/harvard; GRABHERR, MANFRED - Broad Institute Of Mit/harvard; KODIRA, CHINNAPPA - Broad Institute Of Mit/harvard; KOHLER, ANNEGRET - Institut National De La Recherche Agronomique (INRA); KUES, URSULA - Georg August University; LINDQUIST, ERIKA - Joint Genome Institute; LUCAS, SUSAN - Joint Genome Institute; MAUCELI, EVAN - Broad Institute Of Mit/harvard; MORIN, EMMANUELLE - Institut National De La Recherche Agronomique (INRA); MURAT, CLAUDE - Institut National De La Recherche Agronomique (INRA); PEARSON, MATTHEW - Broad Institute Of Mit/harvard; QUESNEVILLE, HADI - Institut National De La Recherche Agronomique (INRA); ROUHIER, NICOLAS - Institut National De La Recherche Agronomique (INRA); SAKTHIKUMAR, SHARADHA - Broad Institute Of Mit/harvard; SCHMUTZ, JEREMY - Joint Genome Institute; SELLES, BENJAMIN - Institut National De La Recherche Agronomique (INRA); SHAPIRO, HARRIS - Joint Genome Institute; TANGAY, PHILIPPE - Canadian Forest Service; TUSKAN, GERALD - Oak Ridge National Laboratory; VAN DE PEER, YVES - Ghent University; HENRISSAT, BERNARD - National Council For Scientific Research-Cnrs; ROUZE, PIERRE - Ghent University; SCHEIN, JACQUIE - Genome Science Centre-Canada; DODDS, PETER - Commonwealth Scientific And Industrial Research Organisation (CSIRO); ZHONG, SHAOBIN - University Of Minnesota; HAMELIN, RICHARD - Canadian Forest Service; BIRREN, BRUCE - Broad Institute Of Mit/harvard; GRIGORIEV, IGOR - Joint Genome Institute; Szabo, Les; MARTIN, FRANCIS - Institut National De La Recherche Agronomique (INRA)

Submitted to: Phytopathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/31/2011
Publication Date: 5/31/2011
Citation: Duplessis, S., Cuomo, C.A., Lin, Y., Aerts, A., Tisserant, E., Veneault-Fourrey, C., Joly, D., Hacquard, S., Amselem, J., Cantarel, B., Chiu, R., Couthinho, P., Feau, N., Field, M., Frey, P., Gelhaye, E., Goldberg, J., Grabherr, M., Kodira, C., Kohler, A., Kues, U., Lindquist, E., Lucas, S., Mauceli, E., Morin, E., Murat, C., Pearson, M., Quesneville, H., Rouhier, N., Sakthikumar, S., Schmutz, J., Selles, B., Shapiro, H., Tangay, P., Tuskan, G.A., Van De Peer, Y., Henrissat, B., Rouze, P., Schein, J., Dodds, P.N., Zhong, S., Hamelin, R.C., Birren, B.W., Grigoriev, I.V., Szabo, L.J., Martin, F. 2011. Obligate biotrophy features unraveled by the genomic analysis of the rust fungi, Melampsora larici-populina and Puccinia graminis f. sp. tritici. Phytopathology. 108:9166-9171.

Interpretive Summary: Rust fungi (Pucciniales, Basidiomycota), is a diverse group of plant pathogens composed of more than 120 genera and 6,000 species and are one of the most economically important groups of pathogens of native and cultivated plants. They are obligate biotrophic parasites that have evolved specialized feeding structures structures, formed within host tissue, to efficiently acquire nutrients and suppress host defense responses. The genomes of two evolutionarly divergent rust fungi, Puccinia graminis (wheat stem rust pathogen) and Melampsora larici-populina (leaf rust pathogen of poplar) were sequenced. Genomic features specific to the obligate biotrophic life-style were identified. This represents the first genome wide characterization of any rust fungi and provides critical information that will facilitate a better understanding of the complex interactions between these pathogens and their hosts. This knowledge will enable scientist to develop new approaches to control these economically important plant pathogens.

Technical Abstract: 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 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 ~16,850 predicted proteins of M. larici-populina to the 18,240 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 planta suggests that they play a role in the 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.