Obligate biotrophy features unraveled by the genomic analysis of rust fungi

Sébastien Duplessis (1) , Christina A C. A. Cuomo (2) , Yao-Cheng Y.-C. Lin (3) , Andrea Aerts (4) , Emilie Tisserant (1) , Claire Veneault-Fourrey (1) , David L. Joly , Stéphane S. Hacquard (1) , Joelle Amselem (5) , Brandi B. Cantarel (6) , Readman R. Chin (7) , Pedro M Coutinho (6) , Nicolas N. Feau , Matthew M. Field (7) , Pascal Frey (1) , Éric Gelhaye (1) , Jonathan J. Goldberg (2) , Manfred G M. G. Grabherr (2) , Chimappa D C. D. Kodira (2) , Annegret Kohler (1) , Ursula U. Kues (8) , Erika A E. A. Lindquist (4) , Susan S. Lucas (4) , Rohit R. Mago (9) , Evan E. Mauceli (2) , Emmanuelle Morin (1) , Claude C. Murat (1) , Jasmyn J. J. J. Pangilinan (4) , Robert R. Park (10) , Matthew M. Pearson (2) , Hadi H. Quesneville (11) , Nicolas Rouhier (1) , Sharadha Sakthikumar (2) , Asaf A A. A. Salamov (4) , Jeremy J. Schmutz (4) , Benjamin B. Selles (1) , Harris Shapiro (4) , Philippe P. Tanguay , Gerald A G. A. Tuskan (4) , Bernard Henrissat (6) , Yves Y. van de Peer (3) , Pierre P. Rouze (3) , Jeffrey G. J. G. Ellis (9) , Peter N P. N. Dodds (9) , Jacqueline E. J. E. Schein (7) , Shaobin S. Zhong (12) , Richard C R. C. Hamelin , Igor V I. V. Grigoriev (4) , Les J L. J. Szabo (12, 13) , Francis Martin (1)

1 IAM - Interactions Arbres-Microorganismes
2 Institute of Massachuetts Institute of technology and harward university
3 Department of plant systems biology
4 Joint Genome institute
5 BIOGER - BIOlogie et GEstion des Risques en agriculture
6 AFMB - Architecture et fonction des macromolécules biologiques
7 Genome sciences
8 Division of molecular wood biotechnology and technical mycology - Büsgen-Institute, Bûsgenweg
9 Plant Industry
10 Plant breeding institute Cobbitty
11 URGI - Unité de Recherche Génomique Info
12 Department of plant pathology
13 Cereal diseases laboratory US D epartment of agriculture

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 larici-populina, the causal agent of poplar leaf rust, and the 89-Mb 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 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.

Mots clés: COMPARATIVE GENOMICS; PLANT PATHOGEN; BASIDIOMYCETE; EVOLUTION; RUST EVOLUTION

Domaines: Sciences agricoles

Sébastien Duplessis, Christina A C. A. Cuomo, Yao-Cheng Y.-C. Lin, Andrea Aerts, Emilie Tisserant, et al.. Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108 (22), pp.9166-9171. ⟨10.1073/pnas.1019315108⟩. ⟨hal-01000169⟩