Genomes of obligate plant pathogens reveal adaptations for obligate parasitism.

M any destructive crop diseases are caused by filamentous microbes from the kingdoms Fungi (e.g., ascomycetes and basidomycetes) and Stramenopila (oomycetes). Many of these pathogens exploit plants by extracting nutrients from living plant cells (biotrophy) (1). In some cases, biotrophic pathogens have evolved to a state of absolute dependency on their hosts. These obligate biotrophs have lost the capacity for saprotrophic growth, display narrow host specificity, and are difficult or impossible to culture on synthetic media (2). When viewed from an interfacial perspective, these lineages provide fascinating case studies of how microbes can evolve to occupy highly specialized niches inside hostile plant hosts. How is it that these parasites can penetrate and grow within host organs, modify host cell structure, reprogram host metabolism, and reproduce prolifically, all while successfully evading the plant immune system (3)? There is much to be learned about these adaptations from comparative genomics. One such example is provided by a paper in PNAS that describes the genomes of two obligate rust pathogens (basidiomycota) and draws informative comparisons to genomes from related species with different lifestyles (4). Below, I discuss insights from this study in the context of similar analyses of obligate parasites from ascomycetes and oomycetes (5, 6). These comparisons reveal striking commonalities, suggestive of convergent pathways that have been followed as these three lineages independently evolved to an obligate lifestyle. Duplessis et al. (4) describe the genome and transcriptome of Puccinia graminis f. sp. tritici (stem rust of wheat and barley) and Melampsora larici-populina (leaf rust of poplar), which represent over 6,000 rust pathogen species (Pucciniales). Rust diseases affect many plant species and include major threats, such as the UG99 strain, that can overcome resistance genes that wheat growers have relied on for decades (7). The basidiomycete phylum contains saprotrophs and facultative parasites with biotrophic or necrotrophic (host-killing) lifestyles. Obligate parasitism in the rust lineage is the derived state, and genome sequences are available for representatives of each lifestyle. Thus, rust pathogens are well-positioned, from a phylogenetic standpoint, for genomelevel comparisons from which inferences about adaptations to an obligate lifestyle can be drawn.