Dynamics and innovations within oomycete genomes: insights into biology, pathology, and evolution

Abstract

The eukaryotic microbes known as oomycetes are common inhabitants of terrestrial and aquatic environments and include saprophytes and pathogens. Lifestyles of the pathogens extend from biotrophy to necrotrophy, obligate to facultative pathogenesis, and narrow to broad host ranges on plants or animals. Sequencing of several pathogens has revealed striking variation in genome size and content, a plastic set of genes related to pathogenesis, and adaptations associated with obligate biotrophy. Features of genome evolution include repeat-driven expansions, deletions, gene fusions, and horizontal gene transfer in a landscape organized into gene-dense and gene-sparse sectors and influenced by transposable elements. Gene expression profiles are also highly dynamic throughout oomycete life cycles, with transcriptional polymorphisms as well as differences in protein sequence contributing to variation. The genome projects have set the foundation for functional studies and should spur the sequencing of additional species, including more diverse pathogens and nonpathogens.

Fig 1

Evolutionary history of oomycetes, lifestyles, and genome sequencing overview. The main part of the figure portrays phylogenetic relationships between the major orders based on 28S rRNA sequences. Orders comprising the peronosporalean group (∼1,000 species), saprolegnians (∼500 species), and basal clades are noted (8). While Phytophthora was traditionally considered part of the Pythiales, it is now recognized to belong to the Peronosporales along with the downy mildews (70). Species with publicly released genome data are listed along with their predicted gene number, genome size, and repetitive DNA content if known; values are based on the most recent publication or data on websites. n.d., the percentage of repeats was not determined. The phylogram in the lower right shows the position of oomycetes compared to other eukaryotes.

Fig 2

Structural and transcriptional landscape of the P. infestans genome. (A) Expression patterns of genes in a portion of a chromosome. Genes with >2-fold-higher mRNAs in one life stage than on average are colored based on when expression is highest according to the key in the upper right (HY, hyphae; SP, sporangia; CLSP, sporangia cleaving into zoospores; ZO, swimming zoospores; GC, zoospore cysts germinating and making infection structures, e.g., appressoria). Genes not changing are in dark gray at half height. Note that the scaffold is split into two portions and that the horizontal axis represents gene order and not distance. (B) Representative gene-dense and gene-sparse regions. Shown are gene orientations, expression patterns as in panel A, and flanking DNA transposon (T) or retroelement-like (R) sequences. The two regions are separated by 450 kb, which is also gene sparse. (C) Example of closely spaced opposing promoters from genes with strong EST support from panel B. The 301-nt intergenic region includes a combined 142 nt of 5′ untranslated regions (UTRs) and has five predicted transcription factor binding sites (TFBS). The genes have a similar configuration in P. sojae.