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The chloroplast has recently emerged as pivotal to co-ordinating plant defence responses and as a target of plant pathogens. Beyond its central position in oxygenic photosynthesis and primary metabolism – key targets in the complex virulence strategies of diverse pathogens – the chloroplast integrates, decodes and responds to environmental signals. The capacity of chloroplasts to synthesize phytohormones and a diverse range of secondary metabolites, combined with retrograde and reactive oxygen signalling, provides exquisite flexibility to both perceive and respond to biotic stresses. These processes also represent a plethora of opportunities for pathogens to evolve strategies to directly or indirectly target ‘chloroplast immunity’. This review covers the contribution of the chloroplast to pathogen associated molecular pattern and effector triggered immunity as well as systemic acquired immunity. We address phytohormone modulation of immunity and surmise how chloroplast-derived reactive oxygen species underpin chloroplast immunity through indirect evidence inferred from genetic modification of core chloroplast components and direct pathogen targeting of the chloroplast. We assess the impact of transcriptional reprogramming of nuclear-encoded chloroplast genes during disease and defence and look at future research challenges.

Plant defenses induced by salicylic acid (SA) are vital for resistance against biotrophic pathogens. In basal and receptor-triggered immunity, SA accumulation is promoted by Enhanced Disease Susceptibility1 with its co-regulator Phytoalexin Deficient4 (EDS1/PAD4). Current models position EDS1/PAD4 upstream of SA but their functional relationship remains unclear. In a genetic and transcriptomic analysis of Arabidopsis autoimmunity caused by constitutive or conditional EDS1/PAD4 overexpression, intrinsic EDS1/PAD4 signaling properties and their relation to SA were uncovered. A core EDS1/PAD4 pathway works in parallel with SA in basal and effector-triggered bacterial immunity. It protects against disabled SA-regulated gene expression and pathogen resistance, and is distinct from a known SA-compensatory route involving MAPK signaling. Results help to explain previously identified EDS1/PAD4 regulated SA-dependent and SA-independent gene expression sectors. Plants have evolved an alternative route for preserving SA-regulated defenses against pathogen or genetic perturbations. In a proposed signaling framework, EDS1 with PAD4, besides promoting SA biosynthesis, maintains important SA-related resistance programs, thereby increasing robustness of the innate immune system.

Plant resistance proteins provide race-specific immunity through the recognition of pathogen effectors. The resistance genes I, I-2 and I-3 have been incorporated into cultivated tomato (Solanum lycopersicum) from wild tomato species to confer resistance against Fusarium oxysporum f. sp. lycopersici (Fol) races 1, 2 and 3, respectively. Although the Fol effectors corresponding to these resistance genes have all been identified, only the I-2 resistance gene has been isolated from tomato. To isolate the I-3 resistance gene, we employed a map-based cloning approach and used transgenic complementation to test candidate genes for resistance to Fol race 3. Here, we describe the fine mapping and sequencing of genes at the I-3 locus, which revealed a family of S-receptor-like kinase (SRLK) genes. Transgenic tomato lines were generated with three of these SRLK genes and one was found to confer Avr3-dependent resistance to Fol race 3, confirming it to be I-3. The finding that I-3 encodes an SRLK reveals a new pathway for Fol resistance and a new class of resistance genes, of which Pi-d2 from rice is also a member. The identification of I-3 also allows the investigation of the complex effector–resistance protein interaction involving Avr1-mediated suppression of I-2- and I-3-dependent resistance in tomato.

Pattern recognition receptors (PRRs) and nucleotide-binding domain and leucine-rich repeat (LRR)-containing proteins (NLRs) initiate pattern-triggered immunity (PTI) and effector-triggered immunity (ETI), respectively, each associated with the activation of an overlapping set of defence genes. The regulatory mechanism behind this convergence of PTI- and ETI-mediated defence gene induction remains elusive. We generated transgenic Arabidopsis plants that enable conditional NLR activation without pathogen infection to dissect NLR- and PRR-mediated transcriptional signals. A comparative analysis of over 40 transcriptome datasets linked calmodulin-binding transcription activators (CAMTAs) to the activation of overlapping defence genes in PTI and ETI. We used a dominant camta3 mutant (camta3-D) to assess CAMTA functions in the corresponding transcriptional regulation. Transcriptional regulation by NLRs, although highly similar to PTI responses, can be established independently of pathogen-associated molecular pattern (PAMP) perception, defence phytohormones and host cell death. Conditional expression of the N-terminal coiled-coil domain of the barley MLA (Mildew resistance locus A) NLR is sufficient to trigger similar transcriptional reprogramming as full-length NLRs. CAMTA-binding motifs are overrepresented in the 5′ regulatory regions of the identified primary immune response genes, consistent with their altered expression and disease resistance responses in camta3-D plants. We propose that CAMTA-mediated transcriptional regulation defines an early convergence point in NLR- and PRR-mediated signalling.

This article is a Commentary on Kadota et al., 221: 2160–2175.

As a destructive plant pathogen, Phytophthora infestans secretes diverse host‐entering RxLR effectors to facilitate infection. One critical RxLR effector, PiAvr3b, not only induces effector‐triggered immunity (ETI), which is associated with the potato resistance protein StR3b, but also suppresses pathogen‐associated molecular pattern (PAMP)‐triggered immunity (PTI). To date, the molecular basis underlying such dual activities remains unknown. Based on phylogenetic analysis of global P. infestans isolates, we found two PiAvr3b isoforms that differ by three amino acids. Despite this sequence variation, the two isoforms retain the same properties in activating the StR3b‐mediated hypersensitive response (HR) and inhibiting necrosis induced by three PAMPs (PiNpp, PiINF1, and PsXeg1) and an RxLR effector (Pi10232). Using a combined mutagenesis approach, we found that the dual activities of PiAvr3b were tightly linked and determined by 88 amino acids at the C‐terminus. We further determined that either the W60 or the E134 residue of PiAvr3b was essential for triggering StR3b‐associated HR and inhibiting PiNpp‐ and Pi10232‐associated necrosis, while the S99 residue partially contributed to PTI suppression. Additionally, nuclear localization of PiAvr3b was required to stimulate HR and suppress PTI, but not to inhibit Pi10232‐associated cell death. Our study revealed that PiAvr3b suppresses the plant immune response at different subcellular locations and provides an example in which a single amino acid of an RxLR effector links ETI induction and cell death suppression. Phytophthora infestans RxLR effector Avr3b activates effector‐triggered immunity and suppresses pathogen‐associated molecular pattern‐triggered immunity in the nucleus, while nuclear localization of Avr3b is not required for inhibition of effector‐induced cell death.

Enhanced Disease Susceptibility1 (EDS1) is an important regulator of plant basal and receptor-triggered immunity. Arabidopsis EDS1 interacts with two related proteins, Phytoalexin Deficient4 (PAD4) and Senescence Associated Gene101 (SAG101), whose combined activities are essential for defense signaling. The different sizes and intracellular distributions of EDS1—PAD4 and EDS1—SAG101 complexes in Arabidopsis leaf tissues suggest that they perform nonredundant functions. The nature and biological relevance of EDS1 interactions with PAD4 and SAG101 were explored using yeast three-hybrid assays, in vitro analysis of recombinant proteins purified from Escherichia coli, and characterization of Arabidopsis transgenic plants expressing an eds1 mutant (eds1 L262P ) protein which no longer binds PAD4 but retains interaction with SAG101. EDS1 forms molecularly distinct complexes with PAD4 or SAG101 without additional plant factors. Loss of interaction with EDS1 reduces PAD4 post-transcriptional accumulation, consistent with the EDS1 physical association stabilizing PAD4. The dissociated forms of EDS1 and PAD4 are fully competent in signaling receptor-triggered localized cell death at infection foci. By contrast, an EDS1—PAD4 complex is necessary for basal resistance involving transcriptional up-regulation of PAD4 itself and mobilization of salicylic acid defenses. Different EDS1 and PAD4 molecular configurations have distinct and separable functions in the plant innate immune response.

Summary The intracellular nucleotide‐binding domain leucine‐rich repeat (NLR) class of immune receptors plays an important role in plant viral defence. Plant NLRs recognize viruses through direct or indirect association of viral proteins, triggering a downstream defence response to prevent viral proliferation and movement within the plant. This review focuses on current knowledge of intracellular perception of viral pathogens, activation of NLRs and the downstream signalling components involved in plant viral defence.

Plants are continuously threatened by pathogen attack and, as such, they have evolved mechanisms to evade, escape and defend themselves against pathogens. However, it is not known what types of defense mechanisms a plant would already possess to defend against a potential pathogen that has not co-evolved with the plant. We addressed this important question in a comprehensive manner by studying the responses of 1041 accessions of Arabidopsis thaliana to the foliar pathogen Pseudomonas syringae pv. tomato (Pst) DC3000. We characterized the interaction using a variety of established methods, including different inoculation techniques, bacterial mutant strains, and assays for the hypersensitive response, salicylic acid (SA) accumulation and reactive oxygen species production. Fourteen accessions showed resistance to infection by Pst DC3000. Of these, two accessions had a surface-based mechanism of resistance, six showed a hypersensitive-like response while three had elevated SA levels. Interestingly, A. thaliana was discovered to have a recognition system for the effector AvrPto, and HopAM1 was found to modulate Pst DC3000 resistance in two accessions. Our comprehensive study has significant implications for the understanding of natural disease resistance mechanisms at the species level and for the ecology and evolution of plant–pathogen interactions.

Resistance against oomycete pathogens is mainly governed by intracellular nucleotide-binding leucine-rich repeat (NLR) receptors that recognize matching avirulence (AVR) proteins from the pathogen, RXLR effectors that are delivered inside host cells. Detailed molecular understanding of how and where NLR proteins and RXLR effectors interact is essential to inform the deployment of durable resistance (R) genes. Fluorescent tags, nuclear localization signals (NLSs) and nuclear export signals (NESs) were exploited to determine the subcellular localization of the potato late blight protein R1 and the Phytophthora infestans RXLR effector AVR1, and to target these proteins to the nucleus or cytoplasm. Microscopic imaging revealed that both R1 and AVR1 occurred in the nucleus and cytoplasm, and were in close proximity. Transient expression of NLS- or NES-tagged R1 and AVR1 in Nicotiana benthamiana showed that activation of the R1-mediated hypersensitive response and resistance required localization of the R1/AVR1 pair in the nucleus. However, AVR1-mediated suppression of cell death in the absence of R1 was dependent on localization of AVR1 in the cytoplasm. Balanced nucleocytoplasmic partitioning of AVR1 seems to be a prerequisite. Our results show that R1-mediated immunity is activated inside the nucleus with AVR1 in close proximity and suggest that nucleocytoplasmic transport of R1 and AVR1 is tightly regulated.