Network analysis exposes core functions in major lifestyles of fungal and oomycete plant pathogens

Abstract

Abstract Background Genomic studies demonstrate that components of virulence mechanisms in filamentous eukaryotic pathogens (FEPs, fungi and oomycetes) of plants are often highly conserved, or found in gene families that include secreted hydrolytic enzymes (e.g., cellulases and proteases) and secondary metabolites (e.g., toxins), central to the pathogenicity process. However, very few large-scale genomic comparisons have utilized complete proteomes from dozens of FEPs to reveal lifestyle-associated virulence mechanisms. Providing a powerful means for exploration, and the discovery of trends in large-scale datasets, network analysis has been used to identify core functions of the primordial cyanobacteria, and ancient evolutionary signatures in oxidoreductases. Results We used a sequence-similarity network to study components of virulence mechanisms of major pathogenic lifestyles (necrotroph (ic), N; biotroph (ic), B; hemibiotroph (ic), H) in complete pan-proteomes of 65 FEPs and 17 saprobes. Our comparative analysis highlights approximately 190 core functions found in 70% of the genomes of these pathogenic lifestyles. Core functions were found mainly in: transport (in H, N, B cores); carbohydrate metabolism, secondary metabolite synthesis, and protease (H and N cores); nucleic acid metabolism and signal transduction (B core); and amino acid metabolism (H core). Taken together, the necrotrophic core contains functions such as cell wall-associated degrading enzymes, toxin metabolism, and transport, which are likely to support their lifestyle of killing prior to feeding. The biotrophic stealth growth on living tissues is potentially controlled by a core of regulatory functions, such as: small G-protein family of GTPases, RNA modification, and cryptochrome-based light sensing. Regulatory mechanisms found in the hemibiotrophic core contain light- and CO2-sensing functions that could mediate important roles of this group, such as transition between lifestyles. Conclusions The selected set of enriched core functions identified in our work can facilitate future studies aimed at controlling FEPs. One interesting example would be to facilitate the identification of the pathogenic potential of samples analyzed by metagenomics. Finally, our analysis offers potential evolutionary scenarios, suggesting that an early-branching saprobe (identified in previous studies) has probably evolved a necrotrophic lifestyle as illustrated by the highest number of shared gene families between saprobes and necrotrophs.

Keywords

• Fungus–plant interaction
• Network
• Core function
• Plant pathogen
• Necrotroph
• Biotroph