Obligate biotrophy features unraveled by the genomic analysis of rust fungi

Sébastien Duplessis, Christina A. Cuomo, Yao Cheng Lin, Andrea Aerts, Emilie Tisserant, Claire Veneault-Fourrey, David L. Joly, Stéphane Hacquard, Joëlle Amselem, Brandi L. Cantarel, Readman Chiu, Pedro M. Coutinho, Nicolas Feaue, Matthew Field, Pascal Frey, Eric Gelhaye, Jonathan Goldberg, Manfred G. Grabherr, Chinnappa D. Kodira, Annegret KohlerUrsula Kües, Erika A. Lindquist, Susan M. Lucas, Rohit Mago, Evan Mauceli, Emmanuelle Morin, Claude Murat, Jasmyn L. Pangilinan, Robert Park, Matthew Pearson, Hadi Quesneville, Nicolas Rouhier, Sharadha Sakthikumar, Asaf A. Salamov, Jeremy Schmutz, Benjamin Selles, Harris Shapiro, Philippe Tanguay, Gerald A. Tuskan, Bernard Henrissat, Yves Van De Peer, Pierre Rouzé, Jeffrey G. Ellis, Peter N. Dodds, Jacqueline E. Schein, Shaobin Zhong, Richard C. Hamelin, Igor V. Grigoriev, Les J. Szabo, Francis Martin

Research output: Contribution to journalArticle

381 Scopus citations

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 or suppression of plant innate immunity. We sequenced the 101-Mb genome of Melampsora laricipopulina, the causal agent of poplar leaf rust, and the 89-Mb genome of Puccinia graminis f. sp. tritici, the causal agent ofwheat and barley stem rust. We then compared the 16,399 predicted proteins of M. larici-populina with the 17,773 predicted proteins of P. graminis f. sp tritici. Genomic features related to their obligate biotrophic lifestyle include expanded lineage-specific gene families, a large repertoire of effector-like small secreted proteins, impaired nitrogen and sulfur assimilation pathways, and expanded families of amino acid and oligopeptide membrane transporters. The dramatic up-regulation of transcripts coding for small secreted proteins, secreted hydrolytic enzymes, and transporters in planta 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.

Original languageEnglish (US)
Pages (from-to)9166-9171
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume108
Issue number22
DOIs
StatePublished - May 31 2011

Keywords

  • Basidiomycete
  • Comparative genomics
  • Evolution
  • Plant pathogen
  • Rust disease

ASJC Scopus subject areas

  • General

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    Duplessis, S., Cuomo, C. A., Lin, Y. C., Aerts, A., Tisserant, E., Veneault-Fourrey, C., Joly, D. L., Hacquard, S., Amselem, J., Cantarel, B. L., Chiu, R., Coutinho, P. M., Feaue, N., Field, M., Frey, P., Gelhaye, E., Goldberg, J., Grabherr, M. G., Kodira, C. D., ... Martin, F. (2011). Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proceedings of the National Academy of Sciences of the United States of America, 108(22), 9166-9171. https://doi.org/10.1073/pnas.1019315108