Genetic Requirements for Signaling from an Autoactive Plant NB-LRR Intracellular Innate Immune Receptor

Roberts, Melinda; Tang, Saijun; Stallmann, Anna; Dangl, Jeffery L.; Bonardi, Vera

doi:10.1371/journal.pgen.1003465

Cited by 102 publications

(138 citation statements)

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“…5a,b). Similar to a previous report (Roberts et al, 2013), we observed that individual adr1, adr1-L1 and adr1-L2 knock-out mutants affect lsd1-2 phenotypes Among the three ADR genes, ADR1-L1 and ADR1-L2 are expressed at higher levels, whereas ADR1 is expressed at a lower level ( Fig. S6; Roberts et al, 2013).…”

Section: Discussionsupporting

confidence: 90%

TNL‐mediated immunity in Arabidopsis requires complex regulation of the redundant ADR1 gene family

et al. 2016

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SummaryNucleotide-binding leucine-rich repeat proteins (NLRs) serve as intracellular immune receptors in animals and plants. Sensor NLRs perceive pathogen-derived effector molecules and trigger robust host defense. Recent studies revealed the role of three coiled-coil-type NLRs (CNLs) of the ADR1 family -ADR1, ADR1-L1 and ADR1-L2 -as redundant helper NLRs, whose function is required for defense mediated by multiple sensor NLRs.From a mutant snc1-enhancing (MUSE) forward genetic screen in Arabidopsis targeted to identify negative regulators of snc1 that encodes a TIR-type NLR (TNL), we isolated two alleles of muse15, both carrying mutations in ADR1-L1. Interestingly, loss of ADR1-L1 also enhances immunity-related phenotypes in other autoimmune mutants including cpr1, bal and lsd1. This immunity-enhancing effect is not mediated by increased SNC1 protein stability, nor is it fully dependent on the accumulation of the defense hormone salicylic acid (SA).Transcriptional analysis revealed an upregulation of ADR1 and ADR1-L2 in the adr1-L1 background, which may overcompensate the loss of ADR1-L1, resulting in enhanced immunity. Interestingly, autoimmunity of snc1 and chs2, which encode typical TNLs, is fully suppressed by the adr1 triple mutant, suggesting that the ADRs are required for TNL downstream signaling.This study extends our knowledge on the interplay among ADRs and reveals their complexity in defense regulation.

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Section: Discussionsupporting

confidence: 90%

TNL‐mediated immunity in Arabidopsis requires complex regulation of the redundant ADR1 gene family

et al. 2016

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“…53,54 Signaling gradients that establish cell death control borders at sites of pathogen recognition have been demonstrated in plants. 48,[55][56][57][58] Importantly, the studies that reported a pro-survival role of autophagy during pathogentriggered HR cell death used relatively old plants. 8,51,52 With age, autophagy mutants become prematurely senescent and accumulate high levels of ROS that can drive accumulation of SA, potentially increasing their vulnerability to ER stress.…”

Section: Discussionmentioning

confidence: 99%

The plant metacaspase AtMC1 in pathogen-triggered programmed cell death and aging: functional linkage with autophagy

et al. 2014

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Autophagy is a major nutrient recycling mechanism in plants. However, its functional connection with programmed cell death (PCD) is a topic of active debate and remains not well understood. Our previous studies established the plant metacaspase AtMC1 as a positive regulator of pathogen-triggered PCD. Here, we explored the linkage between plant autophagy and AtMC1 function in the context of pathogen-triggered PCD and aging. We observed that autophagy acts as a positive regulator of pathogen-triggered PCD in a parallel pathway to AtMC1. In addition, we unveiled an additional, pro-survival homeostatic function of AtMC1 in aging plants that acts in parallel to a similar pro-survival function of autophagy. This novel pro-survival role of AtMC1 may be functionally related to its prodomain-mediated aggregate localization and potential clearance, in agreement with recent findings using the single budding yeast metacaspase YCA1. We propose a unifying model whereby autophagy and AtMC1 are part of parallel pathways, both positively regulating HR cell death in young plants, when these functions are not masked by the cumulative stresses of aging, and negatively regulating senescence in older plants. An emerging theme in cell death research is that cellular processes thought to be regulated by linear signaling pathways are, in fact, complex. Autophagy, initially considered merely a nutrient recycling mechanism necessary for cellular homeostasis, was recently shown to regulate cell death, mechanistically interacting with components that control apoptosis. Deficient autophagy can result in apoptosis [1][2][3] and autophagy hyper-activation can also lead to programmed cell death (PCD). 4 In addition, the pro-survival function of autophagy is mediated by apoptosis inhibition and apoptosis mediates autophagy, although this cross-regulation is not fully understood. 5In plants, autophagy can also have both pro-survival and pro-death functions. Autophagy-deficient plants exhibit accelerated senescence, 6-8 starvation-induced chlorosis, 6,7,9 hypersensitivity to oxidative stress 10 and endoplasmic reticulum stress.11 Further, autophagy-deficient plants cannot limit the spread of cell death after infection with tissue-destructive microbial infections.12,13 The plant phytohormone salicylic acid (SA) mediates most of these phenotypes.8 Autophagy has an essential, pro-survival role in situations where there is an increasing load of damaged proteins and organelles that need to be eliminated, that is, during aging or stress. Autophagy has an opposing, pro-death role during developmentally regulated cell death 14,15 or during the pathogentriggered hypersensitive response PCD (hereafter, HR) that occurs locally at the site of attempted pathogen attack. 16,17The dual pro-death/pro-survival functions of plant autophagy remain a topic of active debate.Also under scrutiny are possible novel functions of caspases and caspase-like proteins as central regulators of pro-survival processes. Caspases were originally defined as executioners of PCD in an...

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“…These functions include promoting SA-mediated basal resistance, a low-level postinfection response that impedes the growth of virulent pathogens, and SAR (Falk et al, 1999;Wiermer et al, 2005;Truman et al, 2007;Vlot et al, 2009;Rietz et al, 2011). Additionally, EDS1 regulates SA-independent defense signaling in one or more pathways acting redundantly with SA (Bartsch et al, 2006;Venugopal et al, 2009;Roberts et al, 2013). FMO1, for example, acts upstream of SA in systemic uninfected tissues (Mishina and Zeier, 2006;Shah and Zeier, 2013) and is associated with EDS1-dependent local responses that are genetically separable from SA (Bartsch et al, 2006).…”

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confidence: 99%

Contrasting Roles of the Apoplastic Aspartyl Protease APOPLASTIC, ENHANCED DISEASE SUSCEPTIBILITY1-DEPENDENT1 and LEGUME LECTIN-LIKE PROTEIN1 in Arabidopsis Systemic Acquired Resistance ,

Breitenbach¹,

Wenig²,

Wittek³

et al. 2014

Plant Physiology

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Systemic acquired resistance (SAR) is an inducible immune response that depends on ENHANCED DISEASE SUSCEPTIBILITY1 (EDS1).Here, we show that Arabidopsis (Arabidopsis thaliana) EDS1 is required for both SAR signal generation in primary infected leaves and SAR signal perception in systemic uninfected tissues. In contrast to SAR signal generation, local resistance remains intact in eds1 mutant plants in response to Pseudomonas syringae delivering the effector protein AvrRpm1. We utilized the SAR-specific phenotype of the eds1 mutant to identify new SAR regulatory proteins in plants conditionally expressing AvrRpm1. Comparative proteomic analysis of apoplastenriched extracts from AvrRpm1-expressing wild-type and eds1 mutant plants led to the identification of 12 APOPLASTIC, EDS1-DEPENDENT (AED) proteins. The genes encoding AED1, a predicted aspartyl protease, and another AED, LEGUME LECTIN-LIKE PROTEIN1 (LLP1), were induced locally and systemically during SAR signaling and locally by salicylic acid (SA) or its functional analog, benzo 1,2,3-thiadiazole-7-carbothioic acid S-methyl ester. Because conditional overaccumulation of AED1-hemagglutinin inhibited SAinduced resistance and SAR but not local resistance, the data suggest that AED1 is part of a homeostatic feedback mechanism regulating systemic immunity. In llp1 mutant plants, SAR was compromised, whereas the local resistance that is normally associated with EDS1 and SA as well as responses to exogenous SA appeared largely unaffected. Together, these data indicate that LLP1 promotes systemic rather than local immunity, possibly in parallel with SA. Our analysis reveals new positive and negative components of SAR and reinforces the notion that SAR represents a distinct phase of plant immunity beyond local resistance.

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Genetic Requirements for Signaling from an Autoactive Plant NB-LRR Intracellular Innate Immune Receptor

Cited by 102 publications

References 59 publications

TNL‐mediated immunity in Arabidopsis requires complex regulation of the redundant ADR1 gene family

TNL‐mediated immunity in Arabidopsis requires complex regulation of the redundant ADR1 gene family

The plant metacaspase AtMC1 in pathogen-triggered programmed cell death and aging: functional linkage with autophagy

Contrasting Roles of the Apoplastic Aspartyl Protease APOPLASTIC, ENHANCED DISEASE SUSCEPTIBILITY1-DEPENDENT1 and LEGUME LECTIN-LIKE PROTEIN1 in Arabidopsis Systemic Acquired Resistance ,

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