Abstract
Ustilago maydis is a biotrophic fungus causing corn smut disease in maize. The secreted effector protein Pit2 is an inhibitor of papain-like cysteine proteases (PLCPs) essential for virulence. Pit2 inhibitory function relies on a conserved 14 amino acids motif (PID14). Here we show that synthetic PID14 peptides act more efficiently as PLCP inhibitors than the full-length Pit2 effector. Mass spectrometry shows processing of Pit2 by maize PLCPs, which releases an inhibitory core motif from the PID14 sequence. Mutational analysis demonstrates that two conserved residues are essential for Pit2 function. We propose that the Pit2 effector functions as a substrate mimicking molecule: Pit2 is a suitable substrate for apoplastic PLCPs and its processing releases the embedded inhibitor peptide, which in turn blocks PLCPs to modulate host immunity. Remarkably, the PID14 core motif is present in several plant associated fungi and bacteria, indicating the existence of a conserved microbial inhibitor of proteases (cMIP).
Highlights
Ustilago maydis is a biotrophic fungus causing corn smut disease in maize
This study shows the mechanism of action of the U. maydis effector protein Pit[2], a molecular mimicry substrate and an inhibitor of plant papain-like cysteine proteases (PLCPs) which has been described to be conserved in different smuts
Functional diversification between U. maydis and S. reilianum was demonstrated for the effector Tin[233]
Summary
Ustilago maydis is a biotrophic fungus causing corn smut disease in maize. The secreted effector protein Pit[2] is an inhibitor of papain-like cysteine proteases (PLCPs) essential for virulence. Few eukaryotic plant pathogen model systems can be used to elucidate the function of fungal effectors One of those examples is the biotrophic fungus Ustilago maydis responsible for corn smut disease in maize. Cmu[1], for example, is a cytosolic localized chorismate mutase effector which functions by manipulating host signaling cascades and has been postulated to decrease salicylic acid levels in the cell, priming plant cells for an upcoming infection[4,5]. Another translocated effector manipulating signaling cascades is. Unrelated plant pathogens such as bacteria, fungi, oomycetes, nematodes and viruses produce inhibitors of PLCPs in order to interfere with their activity and subcellular localization[13]
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