Rumble in the nuclear jungle: compartmentalization, trafficking, and nuclear action of plant immune receptors

Abstract

Plants and animals have evolved structurally related innate immune sensors inside cells to detect the presence of microbial molecules. An evolutionary ancient folding machinery becomes engaged for the synthesis of autorepressed receptor forms in both kingdoms. The receptors act as regulatory signal transduction switches and are activated upon direct or indirect perception of non-self structures. Recent findings indicate that nucleo-cytoplasmic partitioning and nuclear activity is critical for the function of several plant immune sensors, thereby linking receptor function to transcriptional reprogramming of host cells for pathogen defense. This implies short signalling pathways and reveals parallels with regulatory control mechanisms of animal steroid receptors.

Figure 1

Intracellular immune sensors of microbial structures in plants and animals. Graphic representation of the tripartite modular structure of human NLRs, the apoptotic regulators human Apaf-1 and C. elegans CED-4, and R proteins. NB and ATPase activity is mediated by the central NB-ARC domain. The C-terminal LRRs are believed to sense, directly or indirectly, microbe-derived ligands. Structurally diverse N-terminal effector domains include the CARD, PYR, BIR, TIR, CC, and BEAF and BED. A WRKY DNA-binding domain is located at the C-terminus of RRS1. AD, activation domain.

Figure 2

Intracellular immune sensors act as a regulatory signal transduction switch and are translocated into the nucleus. (A) In the absence of cognate microbial structures, the immune sensor is in an autorepressed, ADP-bound resting state. Direct or indirect perception of a microbial effector is thought to induce first a conformational change in the NB-ARC domain allowing exchange of ADP by ATP. This is believed to trigger a second conformational change in the N-terminal effector domain, thereby activating the receptor. The ATPase activity of the NB-ARC domain switches the conformation of the protein back to its resting state. (B) Translocation of immune receptors into the nucleus could either involve continuous cycling or is unidirectional. In the latter scenario, a presumed nuclear degradation pathway might explain disproportionately low levels of nuclear receptor pools.

Figure 3

Nuclear action of MLA links effector-specific and MAMP-triggered immune responses. (A) One or several MAMP receptors initiate PAMP signalling via intracellular MAPK cascades, which in turn stimulate the induction of unknown WRKY transcriptional activators (pink color) and WRKY1/2 repressors (blue color). The WRKY repressors are thought to prevent chronic defense gene activation. Autorepressed MLA receptors are folded by RAR1, SGT1, and cytosolic HSP90 and might continuously cycle between nucleus and cytoplasm. (B) Integrated PAMP- and MLA-triggered immune response upon coactivation of one or several MAMP receptors and MLA by cognate powdery mildew effectors (designated AVR_A). Activated MLA stimulates nuclear association with WRKY1/2 repressors, thereby derepressing MAMP-triggered immunity. Derepression of basal defense responses is thought to amplify expression of defense-related genes (bold arrow) and might drive attacked host cells into cellular suicide. Whether AVRA is directly or indirectly recognized by the cytoplasmic and/or nuclear MLA pool remains unknown.