Abstract
ABSTRACT Subtilisin-like Pr1 proteases of insect-pathogenic fungi are a large family of extracellular cuticle-degrading enzymes that presumably determine a capability of hyphal invasion into insect hemocoel through normal cuticle infection, but remain poorly understood although often considered as virulence factors for genetic improvement of fungal potential against pests. Here, we report that not all of 11 Pr1 family members necessarily function in Beauveria bassiana, an ancient wide-spectrum pathogen evolved insect pathogenicity ~200 million years ago. These Pr1 proteases are phylogenetically similar to or distinct from 11 homologues (Pr1A–K) early named in Metarhizium anisopliae complex, a young entomopathogen lineage undergoing molecular evolution toward Pr1 diversification, and hence renamed Pr1A1/A2, Pr1B1–B3, Pr1 C, Pr1F1–F4,4 and Pr1 G, respectively. Multiple analyses of all single gene-deleted and rescued mutants led to the recognition of five conserved members (Pr1C, Pr1G, Pr1A2, Pr1B1, and Pr1B2) contributing significantly to the fungal pathogenicity to insect. The conserved Pr1 proteases were proven to function only in cuticle degradation, individually contribute 19–29% to virulence, but play no role in post-infection cellular events critical for fungal killing action. Six other Pr1 proteases were not functional at all in either cuticle degradation during host infection or virulence-related cellular events post-infection. Therefore, only the five conserved proteases are collectively required for, and hence mark evolution of, insect pathogenicity in B. bassiana. These findings provide the first referable base for insight into the evolution of Pr1 family members in different lineages of fungal insect pathogens.
Highlights
Beauveria bassiana and Metarhizium anisopliae complex are two representative lineages of filamentous fungal insect pathogens that serve as biological control agents of arthropod pests and main sources of fungal insecticides and acaricides
All B. bassiana Pr1 proteases fall into the clades of Metarhizium classes I (Pr1 C) and II (SF1 and subfamily 2 (SF2)), but some subfamily 1 (SF1)/2 members are distinct, at or below subclade levels, from those homologues early named in M. anisopliae (15,23) or annotated in M. robertsii [24], as illustrated in Supplementary Fig. S1
In B. bassiana, SF1 consists of six members (Pr1 G, two Pr1A, and three Pr1B paralogues) but contains no homologue of Pr1I or Pr1 K while SF2 consists of four Pr1 F paralogues but lacks Pr1D, Pr1E, and Pr1 J homologues that coexist with unique Pr1 F in the two Metarhizium species
Summary
Beauveria bassiana and Metarhizium anisopliae complex are two representative lineages of filamentous fungal insect pathogens that serve as biological control agents of arthropod pests and main sources of fungal insecticides and acaricides (reviewed in [1,2]). These insect pathogens infect a host through the normal route of cuticular penetration by the hyphae from germ tubes of conidia attached to insect surface. Extracellular Pr1 activity (EPA) required for host cuticle degradation is often used as a biochemical marker of fungal virulence against target pest species [21,22]
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