Abstract
The lysin motif (LysM) containing proteins can bind chitin and are ubiquitous in various organisms including fungi. In plant pathogenic fungi, a few LysM proteins have been characterized as effectors to suppress chitin-induced immunity in plant hosts and therefore contribute to fungal virulence. The effector mechanism is still questioned in fungus-animal interactions. In this study, we found that LysM proteins are also present in animal pathogenic fungi and have evolved divergently. The genome of the insect pathogen Beauveria bassiana encodes 12 LysM proteins, and the genes were differentially transcribed by the fungus when grown in different conditions. Deletion of six genes that were expressed by the fungus growing in insects revealed that two, Blys2 and Blys5, were required for full fungal virulence. Both proteins could bind chitin and Blys5 (containing two LysM domains) could additionally bind chitosan and cellulose. Truncation analysis of Blys2 (containing five LysM domains) indicated that the combination of LysM domains could determine protein-binding affinity and specificity for different carbohydrates. Relative to the wild-type strain, loss of Blys2 or Blys5 could impair fungal propagation in insect hemocoels and lead to the upregulation of antifungal gene in insects. Interestingly, the virulence defects of ΔBlys2 and ΔBlys5 could be fully restored by complementation with the Slp1 effector from the rice blast fungus Magnaporthe oryzae. In contrast to Slp1 and Blys2, Blys5 could potentially protect fungal hyphae against chitinase hydrolysis. The results of this study not only advance the understanding of LysM protein evolution but also establish the effector mechanism of fungus-animal interactions.
Highlights
Insect pathogenic fungi such as the ascomycete species Beauveria bassiana and Metarhizium robertsii have been developed as promising biocontrol agents [1, 2]
It has been reported that small molecules such as the cyclopeptide destruxins produced by Metarhizium species and the red pigment oosporein produced by B. bassiana can facilitate fungal infection of insect hosts by inhibiting host immunities [8, 9]
lysin motif (LysM) proteins are present in the genome of B. bassiana whereas in Metarhizium robertsii, eight are present in M. oryzae and 18 in C. higginsianum
Summary
Insect pathogenic fungi are of importance for both applied and basic research. Relative to the advances in understanding fungus-plant interactions, the mechanisms of the molecular pathogenesis of entomopathogenic fungi are rather limitedly understood. By using the insect pathogen Beauveria bassiana as a model, we revealed that two of 12 encoded LysM protein genes Blys and Blys that were transcribed by the fungus growing in insects are required for full fungal virulence against insect hosts. The virulence defects of ΔBys and ΔBys could be fully restored by complementation with the divergent Slp effector from the plant pathogen Magnaporthe oryzae. Both Blys and Blys can deregulate insect immune responses, and the latter can protect fungal cells from chitinase hydrolysis. The findings of this study establish the contribution of LysM effectors to fungal virulence against insect hosts
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