Abstract
BackgroundSubtilisin-like serine proteases play an important role in pathogenic fungi during the penetration and colonization of their hosts. In this study, we perform an evolutionary analysis of the subtilisin-like serine protease genes of subphylum Pezizomycotina to find if there are similar pathogenic mechanisms among the pathogenic fungi with different life styles, which utilize subtilisin-like serine proteases as virulence factors. Within Pezizomycotina, nematode-trapping fungi are unique because they capture soil nematodes using specialized trapping devices. Increasing evidence suggests subtilisin-like serine proteases from nematode-trapping fungi are involved in the penetration and digestion of nematode cuticles. Here we also conduct positive selection analysis on the subtilisin-like serine protease genes from nematode-trapping fungi.ResultsPhylogenetic analysis of 189 subtilisin-like serine protease genes from Pezizomycotina suggests five strongly-supported monophyletic clades. The subtilisin-like serine protease genes previously identified or presumed as endocellular proteases were clustered into one clade and diverged the earliest in the phylogeny. In addition, the cuticle-degrading protease genes from entomopathogenic and nematode-parasitic fungi were clustered together, indicating that they might have overlapping pathogenic mechanisms against insects and nematodes. Our experimental bioassays supported this conclusion. Interestingly, although they both function as cuticle-degrading proteases, the subtilisin-like serine protease genes from nematode-trapping fungi and nematode-parasitic fungi were not grouped together in the phylogenetic tree. Our evolutionary analysis revealed evidence for positive selection on the subtilisin-like serine protease genes of the nematode-trapping fungi.ConclusionsOur study provides new insights into the evolution of subtilisin-like serine protease genes in Pezizomycotina. Pezizomycotina subtilisins most likely evolved from endocellular to extracellular proteases. The entomopathogenic and nematode-parasitic fungi likely share similar properties in parasitism. In addition, our data provided better understanding about the duplications and subsequent functional divergence of subtilisin-like serine protease genes in Pezizomycotina. The evidence of positive selection detected in the subtilisin-like serine protease genes of nematode-trapping fungi in the present study suggests that the subtilisin-like serine proteases may have played important roles during the evolution of pathogenicity of nematode-trapping fungi against nematodes.
Highlights
Subtilisin-like serine proteases play an important role in pathogenic fungi during the penetration and colonization of their hosts
In conjunction with the other Pezizomycotina sequences obtained from previous studies and extensive database searching of available genome assembly, we perform the most comprehensive investigation to date of subtilisin-like serine protease genes in Pezizomycotina
The subtilisin-like serine proteases from nematode-trapping fungi, together with those from nematode-parasitic fungi and entomopathogenic fungi, were classified as cuticle-degrading proteases because they were involved in the penetration and digestion of nematode or insect cuticles [11,12,13,14,15,16,17,18,19,20,21,22,23]
Summary
Subtilisin-like serine proteases play an important role in pathogenic fungi during the penetration and colonization of their hosts. Increasing evidence suggests subtilisin-like serine proteases from nematode-trapping fungi are involved in the penetration and digestion of nematode cuticles. Previous studies have suggested that subtilisin-like serine proteases are involved in the penetration and the digestion of nematode cuticles [11,12,13,14,15,16,17,18,19,20,21,22,23]. Only limited studies have been done on the evolutionary pattern of subtilisin-like serine protease genes in nematode-trapping fungi so far [10,11,17]. In conjunction with the other Pezizomycotina sequences obtained from previous studies and extensive database searching of available genome assembly, we perform the most comprehensive investigation to date of subtilisin-like serine protease genes in Pezizomycotina
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