The ubiquitin/26S proteasome system in plant-pathogen interactions: a never-ending hide-and-seek game

Abstract

The ubiquitin/26S proteasome system (UPS) plays a central role in plant protein degradation. Over the past few years, the importance of this pathway in plant-pathogen interactions has been increasingly highlighted. UPS is involved in almost every step of the defence mechanisms in plants, regardless of the type of pathogen. In addition to its proteolytic activities, UPS, through its 20S RNase activity, may be part of a still unknown antiviral defence pathway. Strikingly, UPS is not only a weapon used by plants to defend themselves, but also a target for some pathogens that have evolved mechanisms to inhibit and/or use this system for their own purposes. This article attempts to summarize the current knowledge on UPS involvement in plant-microbe interactions, a complex scheme that illustrates the never-ending arms race between hosts and microbes.

Figure 1

An overview of the ubiquitin/26S proteasome system (UPS). (A) The UPS pathway begins with the ATP‐dependent activation of ubiquitin by an E1 enzyme. Ubiquitin is then transferred to an E2 enzyme, and finally attached to the target protein via an E3 enzyme. Multiple cycles of ubiquitin conjugation lead to a polyubiquitinated substrate that is degraded by the 26S proteasome complex, releasing short peptides. (B) Types of E3 ubiquitin ligase enzymes. See text for details. (C) Structure of the 26S proteasome. The 20S core protease is composed of four heptameric rings, forming three cavities. The outer rings contain α subunits and the inner rings β subunits. Three of the β subunits (namely β1, β2 and β5) harbour a protease activity. One or two 19S regulatory particles can be attached to the outer rings. The 19S regulatory particle is composed of two complexes, the lid and the base. The base contains six proteasomal ATPases attached to the α rings of the 20S proteasome. The Rpn10 subunit can interact either with the lid or the base and stabilizes the complex. Adapted from Delauréet al., 2008.

Figure 2

SGT1 (suppressor of G2 allele of skp1) involvement in plant defence mechanisms. (A) RPM1 (resistance to Pseudomonas syringae pv. maculicola 1) degradation during the onset of the hypersensitive response (HR). To date, the E3 ligase mediating RPM1 degradation still remains unknown. As SGT1 interacts with RAR1 (required for Mla12 resistance 1), a protein that regulates RPM1 stability, SGT1 may be required in this degradation mechanism. (B) Examples of the crucial role played by SGT1 in plant defence mechanisms (R gene products are indicated by green shading). PVX, Potato virus X; TMV, Tobacco mosaic virus; (1), Azevedo et al., 2006; (2), Liu et al., 2002; (3), Azevedo et al., 2002; (4), Fu et al., 2009; (5), Bhaskar et al., 2008; (6), Tör et al., 2002.

Figure 3

Evolution of the Pseudomonas syringae virulence factor AvrPtoB and the host R proteins Fen (fenthion sensitivity) and Pto. (A) AvrPtoB_1–387 overcomes plant basal defences, causing disease. (B) Fen recognizes AvrPtoB_1–387 and triggers programmed cell death (PCD)‐based plant resistance. (C) AvrPtoB acquires an E3 ligase domain, causing ubiquitin/26S proteasome system (UPS)‐dependent Fen degradation, thus enhancing disease. (D) Pto, impervious to E3 ligase activity (via its kinase activity and phosphorylation of AvrPtoB), evolves to recognize AvrPtoB, restoring plant immunity. Adapted from Rosebrock et al., 2007.

Figure 4

The ubiquitin/26S proteasome system (UPS), a central element in plant defence and pathogen virulence mechanisms. A summary figure. BSCTV, Beet severe curly top virus; BWYV, Beet western yellows virus; CABYV, Cucurbit aphid‐borne yellows virus; FBNYV, Faba bean necrotic yellows virus; LMV, Lettuce mosaic virus; TMV, Tobacco mosaic virus; ToMV, Tomato mosaic virus.