Comparative Genomics of Smut Pathogens: Orphan and Positively Selected Genes as Potential Drivers of Host Specialization

Host specialization is a key evolutionary process for the diversification and emergence of new pathogens. However, the molecular determinants of host range are largely unknown. Smut fungi are suitable pathogens to investigate host specialization because most of smut species infect only a single or a small number of susceptible hosts. To identify the genetic basis of host specialization in smut fungi, we compared the genomes of nine species isolated from eight distinct hosts: maize, barley, sugarcane, wheat, oats, Zizania latifolia (a wild-rice relative), Echinocloa colona (a wild grass) and Persicaria sp.(a wild dicot plant). The smut genomes were of small size, ranging from 18.38 to 24.64 Mb, and had low repetitive element content (2.34 – 25.12%) compared to other filamentous plant pathogens. The smut species shared 65.46% of all orthologous groups as identified by OrthoMCL analyses. Most of the species-specific (orphan) genes were uncharacterized proteins, including genes encoding candidate effectors. All one-to-one orthologous genes were screened for positive selection. Using site-specific models, we found significant evidence of positive selection at individual sites in 31 genes. Using branch-site models, we found evidence for episodic selection in 41 to 286 genes, depending on the analyzed lineage. The genetic basis of host specialization in smut fungi is complex and seems to involve a range of evolutionary process, including gene gain/loss and episodic selection events. Species-specific effectors and positively selected genes will be good candidates for further characterization in regards to their role in host adaptation.