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Review
. 2014;5(7):710-21.
doi: 10.4161/viru.29755.

Go in for the kill: How plants deploy effector-triggered immunity to combat pathogens. [Corrected]

Liang Wu  1 , Huan Chen, Chad Curtis, Zheng Qing Fu
Affiliations
Review

Go in for the kill: How plants deploy effector-triggered immunity to combat pathogens. [Corrected]

Liang Wu et al. Virulence. 2014.

Erratum in

  • Corrigendum.
    [No authors listed] [No authors listed] Virulence. 2016;7(2):209. doi: 10.1080/21505594.2016.1152150. Virulence. 2016. PMID: 27006993 Free PMC article.

Abstract

Plant resistance (R) proteins perceive specific pathogen effectors from diverse plant pathogens to initiate defense responses, designated effector-triggered immunity (ETI). Plant R proteins are mostly nucleotide binding-leucine rich repeat (NB-LRR) proteins, which recognize pathogen effectors directly or indirectly through sophisticated mechanisms. Upon activation by effector proteins, R proteins elicit robust defense responses, including a rapid burst of reactive oxygen species (ROS), induced biosynthesis and accumulation of salicylic acid (SA), a rapid programmed cell death (PCD) called hypersensitive response (HR) at the infection sites, and increased expression of pathogenesis-related (PR) genes. Initiation of ETI is correlated with a complex network of defense signaling pathways, resulting in defensive cellular responses and large-scale transcriptional reprogramming events. In this review, we highlight important recent advances on the recognition of effectors, regulation and activation of plant R proteins, dynamic intracellular trafficking of R proteins, induction of cell death, and transcriptional reprogramming associated with ETI. Current knowledge gaps and future research directions are also discussed in this review.

Keywords: MAMP; MAMP-triggered immunity; avirulence protein; effector-triggered immunity; effectors; hypersensitive response; resistance protein; transcriptional reprogramming.

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Figures

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Figure 1. Recognition of pathogen effectors by plant resistance (R) proteins. (A) Structures of R proteins. The majority of R proteins are NB (nucleotide binding)-LRR (leucine-rich repeat) proteins, which are grouped into CC (coiled-coil)-NB-LRRs and TIR (toll/interleukin 1 receptor like)-NB-LRRs based on their distinct N-terminal domains. Some R proteins have a C-terminal extension required for their biological function, such as RRS1-R, which has a WRKY domain. (B–D) Simplified model showing examples of recognition between plant R proteins and pathogen effectors. (B) RRS1-R recognizes effector PopP2 through direct interaction, and relocated into nucleus to promote defense-related gene expression through its C-terminal WRKY transcription activator domain. (C) RIN4 is targeted by type III effectors AvrRpm1 and AvrRpt2, and surveilled by resistance proteins RPM1 and RPS2, respectively. RPM1 recognizes AvrRpm1-meidtaed phosphorylation of RIN4, while RPS2 detects the degradation of RIN4 by cysteine protease activity of AvrRpt2. (D) TAL (Transcription activator-like) effector AvrBs3 from xanthomonads (Xanthomonas spp.) induces the expression of R protein Bs3 after its nuclear localization to activate ETI (effector-triggered immunity). Recognition of effectors by plant R proteins triggers robust cellular defense responses, and transcriptional reprogramming of defense genes. TFs, transcription factors.
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Figure 2. Plant defense responses associated with ETI. Reactive oxygen species (ROS) production plays important roles in plant defense response during ETI (left). Plasma membrane-localized NADPH oxidases contribute to the production of ROS in plant apoplast, which triggers programmed cell death (PCD). In plants, these NADPH oxidase are called respiratory burst oxidase homologs (RBOHs). Catalase is an anti-oxidative enzyme that prevents accumulation of peroxisomal ROS. CAT2 (Catalase 2) and NCA1 (no catalase activity 1), which are required for catalase activities in plants, should in theory prevent PCD. However, both CAT2 and NCA1 contribute to autophagy-dependent PCD. In addition to the primary pro-death function of autophagy, autophagy downregulates ROS signaling in older plants or under long day condition. Autophagy limits PCD by a negative feedback pathway. Integrated model depicts selected transcriptional regulators associated with diverse R proteins to control the expression of defense genes (right). Association of R protein RRS1-R (WRKY52) with its cognate effector causes activation of defense genes, perhaps through derepression of transcriptional activity of WRKY domain or activation of other regulators. Upon avr pathogen infection, diverse activated R proteins MLA10, Pb1, SNC1, RPS4, and N are able to activate HvMYB6, OsWRKY45, TPR1, AtSPL6, and NbSPL6, respectively through protein-protein interactions, thus resulting in induction of defense genes. After perception of specific effector, MLA10 associates with HvWRKY1/2 repressors and thereby de-repress immune response. In addition, activated MLA10 enables to release HvMYB6 from HvWRKY1 repressor, which antagonistically associates with DNA binding domain of HvMYB6. The corepressor TRP1 represses transcription of two negative regulators of plant defense (DND1 and DND2), leading to induction of defense responses. Transcription of two tomato SIWRKY72 genes (SIWRKY72a and SIWRKY72b) are upregulated in defense response triggered by Mi-1 and these genes are required in Mi-1-mediated resistance. Both MED14 and MED16 are involved in induction of a large number of defense genes and resistance to RPT2. Blue lines indicate that diverse R proteins activate (arrows) or repress (truncated lines) activities of corresponding transcriptional regulators after perception of avr effectors. Dark red lines indicate that representative transcriptional (co)factors positively (arrows) or negatively (truncated lines) regulate transcription of downstream defense genes. Simple model for ELP2, SDG8 and MORC1 (CRT1)-mediated epigenetic control of transcriptome reprogramming in ETI is shown below. The histone acetyltransferase (HAT) activity of ELP2 for histone acetylation positively regulates defense genes including NPR1, PR1, PR2, PR5, EDS1, and PAD4. In addition, as a DNA demethylase, it reduces DNA methylation levels in NPR1 promoter and PAD4 coding regions after infection of Pst DC3000 avrRpt2, resulting in induction of NPR1 and PAD4. The histone lysine methytransferase SDG8, which trimethylated histone 3 lysine 36 (H3K36), is required for induction of LAZ5 (RPS4-like) and RPM1 R genes. Loss of SDG8 increases monomethylated H3K36 levels that probably is a general mark for transcription represson of a subset of R genes including RPM1. MORC1 (CRT1) causes heterochromatin condensation and is required for RPM1-mediated defense signaling. Avr Effectors, avirulence proteins; R, resistance proteins; PM, plasma membrane; RBOH, respiratory burst oxidase homolog; CAT2, catalase 2; NCA1, no catalase activity 1; ROS, reactive oxygen species; PCD, programmed cell death; RPM1, a CC-NB-LRR protein conferring resistance to Pseudomonas syringae pv Maculicola 1 (RPM1); RRS1-R, recessive resistance to Ralstonia solanacearum 1; MLA10, mildew A10 R protein; Pb1, Panicle blast 1; Mi-1, tomato cultivar Motelle; SNC1, a TIR-NB-LRR protein identified from suppressor of npr-1, constitutive 1 (SNC1); RPS4, resistance to P. syringae 4; N, Nicotiana TIR-NB-LRR receptor N; RPT2, resistance to P. syringae pv tomato 2; HvWRKY1/2, OsWRKY45 and SlWRKY72a/b, WRKY DNA-binding domain transcription factors in Hordeum vulgare (Hv), Oryza sativa (Os) and tomato Solanum lycopersicum (Sl); HvMYB6, R2R3 type MYB6-like transcription factor; MED14/16, mediator 14/16; NbSPL6 and AtSPL6, Squamosa promoter binding protein-like 6 (SPL6) transcription factors in Nicotiana benthamiana (Nb) and Arabidopsis thaliana (At); TPR1 (MOS10), Topless-related 1 (modifier of snc1, 10); DND1/2, Defense no Death1/2; ELP2, Elongator subunit 2; SDG8, SET (Su[var]3–9, E[z] and Trithorax conserved) DOMAIN GROUP 8; MORC1 (CRT1), Microrchidia 1 [MORC1] ATPase (compromised recognition of TCV-1 [CRT1]); Me, methylation; Ac, acetylation.
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