Dual function of a secreted fungalysin metalloprotease in Ustilago maydis

Abstract

Fungalysins from several phytopathogenic fungi have been shown to be involved in cleavage of plant chitinases. While fungal chitinases are responsible for cell wall remodeling during growth and morphogenesis, plant chitinases are important components of immunity. This study describes a dual function of the Ustilago maydis fungalysin UmFly1 in modulation of both plant and fungal chitinases. Genetic, biochemical and microscopic experiments were performed to elucidate the in vitro and in planta functions of U. maydis UmFly1. U. maydis ∆umfly1 mutants show significantly reduced virulence, which coincides with reduced cleavage of the maize chitinase ZmChiA within its chitin-binding domain. Moreover, deletion of umfly1 affected the cell separation of haploid U. maydis sporidia. This phenotype is associated with posttranslational activation of the endogenous chitinase UmCts1. Genetic complementation of the ∆umfly1 mutant with a homologous gene from closely related, but nonpathogenic, yeast fully rescued the cell separation defect in vitro, but it could not recover the ∆umfly1 defect in virulence and cleavage of the maize chitinase. We report on the dual function of the secreted fungalysin UmFly1. We hypothesize that co-evolution of U. maydis with its host plant extended the endogenous function of UmFly1 towards the modulation of plant chitinase activity to promote infection.

Hevein-Like Antimicrobial Peptides Wamps: Structure–Function Relationship in Antifungal Activity and Sensitization of Plant Pathogenic Fungi to Tebuconazole by WAMP-2-Derived Peptides

“…WAMP homologues with Ala and Lys at this position effectively inhibit fungalysin, while those with Glu and Asn, do not; however, they still retain the ability to suppress spore germination of the plant pathogenic fungi in vitro. Recent studies of the secreted fungalysin metalloprotease of Ustilago maydis showed that the enzyme has a dual function in the fungal morphogenesis and plant pathogenesis by modulating activity of both fungal and plant chitinases [64]. Thus, we believe that the inhibition of fungalysin by WAMPs can play a plant protective role in two ways: (i) by rescuing plant defense chitinases from proteolysis by fungalysin and thus restoring their ability to degrade fungal cell walls, (ii) by protecting fungal chitinases involved in fungal cell wall remodeling during the morphogenesis.…”

A secreted LysM effector protects fungal hyphae through chitin-dependent homodimer polymerization

“…In plants, chitin is recognized in the extracellular space through membrane-exposed Lysin motif (LysM)-containing receptor molecules [1,11,12,13]. In turn, many successful fungal pathogens have evolved effector molecules that either protect their cell walls against plant chitinases or prevent or perturb the elicitation of chitin-triggered host immunity [3,10,14,15,16].…”

A M35 family metalloprotease is required for fungal virulence against insects by inactivating host prophenoloxidases and beyond

“…In fish pathogenic bacterium Aeromonas salmonicida, a M35 MP AsaP1 is also found indispensable for bacterial virulence against fishes [9]. A M36 enzyme UmFly1 is required for the virulence of the smut fungus Ustilago maydis by dual cleavage of the maize and fungal chitinases [10]. The M36 family Mpr1 identified from the mammalian pathogen Cryptococcus neoformans was found to play a role in invading the central nervous system by targeting brain endothelium [11].…”