Papain-like cysteine proteases: key players at molecular battlefields employed by both plants and their invaders

Abstract

Papain-like cysteine proteases (PLCPs) play crucial roles in plant-pathogen/pest interactions. During these parasitic interactions, PLCPs act on non-self substrates, provoking the selection of counteracting inhibitors and other means to evade proteolysis. We review examples of PLCPs acting on molecular battlefields in the extracellular space, plant cytoplasm and herbivore gut. Examples are maize Mir1 (Maize inbred resistance 1), tomato Rcr3 (Required for Cladosporium resistance-3), Pseudomonas AvrRpt2 and AurPphB, insect DvCAL1 (Diabrotica virgifera cathepsin L-like protease-1) and nematode MiCpl1 (Meloidogyne incognita cathepsin L-like protease 1). The data suggest that PLCPs cleave specific proteins and that their translocation, activation and inhibition of PLCPs are tightly regulated.

Figure 1

Characteristics of papain‐like cysteine proteases (PLCPs). (a) Surface representation of the crystal structure of papain, showing its wide substrate‐binding cleft with the catalytic cysteine (yellow). (b) Domain structure of the open reading frame of PLCPs of subfamily C1A. The signal peptide (sp) targets the protein to the endomembrane system; the autoinhibitory prodomain needs to be removed to activate the protease. The protease domain contains three catalytic residues, cysteine (C), histidine (H) and asparagine (N), and often contains two disulphide bridges (SS). (c) Hierarchical subclassification of cysteine proteases according to the MEROPS database (Rawlings et al., 2006). The cysteine protease class (Cys) consists of several clans of proteases. Clan CA contains PLCPs, and is subdivided into different (sub)families, such as C1A, of which papain is the type member. Only families containing the PLCPs discussed here are shown.

Figure 2

Summary of the diverse roles of the papain‐like cysteine proteases (PLCPs) discussed here. PLCPs (heart shapes) are produced by plants (green) and their pests and pathogens (red). Broken lines indicate the predicted localizations based on the presence or absence of a signal peptide. The broken cell wall (bottom) illustrates that putative cytoplasmic phytocystatins act in the herbivore gut on digestive PLCPs.