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Review
. 2014 Sep;15(7):737-746.
doi: 10.1111/mpp.12128.

Ubiquitination of pattern recognition receptors in plant innate immunity

Bo Li #  1   2 , Dongping Lu #  3 , Libo Shan  1
Affiliations
Review

Ubiquitination of pattern recognition receptors in plant innate immunity

Bo Li et al. Mol Plant Pathol. 2014 Sep.

Abstract

Lacking an adaptive immune system, plants largely rely on plasma membrane-resident pattern recognition receptors (PRRs) to sense pathogen invasion. The activation of PRRs leads to the profound immune responses that coordinately contribute to the restriction of pathogen multiplication. Protein post-translational modifications dynamically shape the intensity and duration of the signalling pathways. In this review, we discuss the specific regulation of PRR activation and signalling by protein ubiquitination, endocytosis and degradation, with a particular focus on the bacterial flagellin receptor FLS2 (flagellin sensing 2) in Arabidopsis.

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Figures

Figure 1
Figure 1
FLS2 (flagellin sensing 2) signalling pathway in Arabidopsis. The transcription, translation and maturation of FLS2, the Arabidopsis receptor of bacterial flagellin (flg22), require EIN3 (ethylene insensitive 3)/EIL1 (ethylene insensitive 3‐like 1) (Boutrot et al., 2010; Mersmann et al., 2010), GRP7 (glycine‐rich protein 7) (Nicaise et al., 2013), endoplasmic reticulum (ER)‐resident reticulon‐like proteins RTNLB1/RTNLB2 (Lee et al., 2011) and RABA1b (Ras genes from rat brain a1b) (Choi et al., 2013). FLS2 constitutively interacts with BIK1 (Botrytis‐induced kinase 1) and BSK1 (BR‐signalling kinase 1) (Shi et al., 2013), two receptor‐like cytoplasmic kinases (RLCKs) that positively regulate FLS2 signalling, and SCD1 (stomatal cytokinesis‐defective 1) required for certain FLS2 responses (Korasick et al., 2010). BAK1 (brassinosteroid‐insensitive 1‐associated kinase 1) constitutively interacts with BIK1 and the E3 ubiquitin ligases PUB12/13. Binding of flg22 probably causes conformational change of FLS2, which further recruits BAK1 to the complex. The dimerization of FLS2/BAK1 leads to the phosphorylation of the FLS2/BAK1/BIK1 complex, and subsequent release of BIK1. Rapid Ca2+ influx, an oxidative burst mediated by plasma membrane (PM)‐resident NADPH‐oxidase Rboh, and activation of mitogen‐activated protein kinase (MAPK) and calcium‐dependent protein kinase (CDPK) cascades collectively activate and amplify the defence gene reprogramming and other defence responses. PUB12/13 are phosphorylated by BAK1 and interact with FLS2 on flg22 perception, thereby promoting poly‐ubiquitination of FLS2 to tune down the signalling. PUB22/23/24 poly‐ubiquitinate Exo70B, a subunit of the exocyst complex, for 26S proteasome degradation to down‐regulate defence signalling. EE, early endosome; MEKK, MAPK kinase kinase; MKK, MAPK kinase; MPK, MAP kinase (MAPK); TGN, trans‐Golgi network; Ub, ubiquitin.
Figure 2
Figure 2
Endocytic pathways involved in FLS2 (flagellin sensing 2) internalization. The nonactivated FLS2 undergoes a constitutive recycling between plasma membrane (PM) and trans‐Golgi network (TGN)/early endosome (EE) compartments via a brefeldin A (BFA)‐sensitive endosomal pathway. The flg22‐activated FLS2 receptor traffics via a Wortmannin (Wm) and Concanamycin A (ConcA)‐sensitive pathway and is further sorted into the vacuole for degradation. Mono‐ubiquitination mediated by the PEST motif of FLS2 might be involved in FLS2 endocytosis initiation or protein sorting steps. The route of activated FLS2 endocytosis includes the SYP61‐labelled TGN/EE compartment, SYP61‐ and ARA7‐labelled intermediate compartment with properties between TGN/EE and late endosome (LE)/multivesicular body (MVB), ARA6‐labelled LE/MVB compartment and, finally, the vacuole for degradation. MVB containing FLS2 may also traffic into the late prevacuolar compartment (LPVC) before fusion with the vacuole. RABA (Ras genes from rat brain a) family proteins RABA6a and RABA4c play roles in distinct steps of FLS2 endocytosis, and RABA1b is required for normal morphology of TGN/EE and transport of newly synthesized FLS2 to PM. BDM, 2,3‐butanedione monoxime; Ub, ubiquitin.
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