Obligate biotrophy features unraveled by the genomic analysis of rust fungi

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 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.

Fig. 1.

Predicted pattern of gene families gain and loss in representative fungal genomes. The figure represents the total number of protein families in each species or node estimated by Dollo parsimony principle. The numbers on the branches of the phylogenetic tree correspond to expanded (Left, black), contracted (Right, red), or inferred ancestral (oval) protein families along each lineage by comparison with the putative pan-proteome. For each species, the number of gene families, orphan genes, and the total gene number are indicated on the right.

Fig. 2.

Expression profiling of candidate rust effector genes. Global gene expression in infected poplar or wheat leaves (in planta) versus resting urediniospores (USp) in M. larici-populina (Mlp, Top) and P. graminis f. sp. tritici (Pgt, Bottom). Log₂-fold change ratio of significantly induced genes in planta compared with resting urediniospores plotted versus the P value. Gray circles, significantly in planta-induced genes; red circles, SSP encoding genes.