Summary
Hypersensitive response (HR)‐conferred resistance is associated with induction of programmed cell death and pathogen spread restriction in its proximity. The exact role of chloroplastic ...reactive oxygen species and its link with salicylic acid (SA) signaling in HR remain unexplained.
To unravel this, we performed a detailed spatiotemporal analysis of chloroplast redox response in palisade mesophyll and upper epidermis to potato virus Y (PVY) infection in a resistant potato genotype and its transgenic counterpart with impaired SA accumulation and compromised resistance.
Besides the cells close to the cell death zone, we detected individual cells with oxidized chloroplasts further from the cell death zone. These are rare in SA‐deficient plants, suggesting their role in signaling for resistance. We confirmed that chloroplast redox changes play important roles in signaling for resistance, as blocking chloroplast redox changes affected spatial responses at the transcriptional level.
Through spatiotemporal study of stromule induction after PVY infection, we show that stromules are induced by cell death and also as a response to PVY multiplication at the front of infection. Overall induction of stromules is attenuated in SA‐deficient plants.
One of the earliest hallmarks of plant immune response is production of reactive oxygen species (ROS) in different subcellular compartments, which regulate plant immunity. A suitable equilibrium, ...which is crucial to prevent ROS overaccumulation leading to oxidative stress, is maintained by salicylic acid (SA), a chief regulator of ROS. However, ROS not only act downstream of SA signaling, but are also proposed to be a central component of a self-amplifying loop that regulates SA signaling as well as the interaction balance between different phytohormones. The exact role of this crosstalk, the position where SA interferes with ROS signaling and ROS interferes with SA signaling and the outcome of this regulation, depend on the origin of ROS but also on the pathosystem. The precise spatiotemporal regulation of organelle-specific ROS and SA levels determine the effectiveness of pathogen arrest and is therefore crucial for a successful immune response. However, the regulatory interplay behind still remains poorly understood, as up until now, the role of organelle-specific ROS and SA in hypersensitive response (HR)-conferred resistance has mostly been studied by altering the level of a single component. In order to address these aspects, a sophisticated combination of research methods for monitoring the spatiotemporal dynamics of key players and transcriptional activity in plants is needed and will most probably consist of biosensors and precision transcriptomics.
Summary
The hypersensitive defence response is found in all higher plants and is characterized by a rapid cell death at the point of pathogen ingress. It is usually associated with pathogen ...resistance, though, in specific situations, it may have other consequences such as pathogen susceptibility, growth retardation and, over evolutionary timescales, speciation. Due to the potentially severe costs of inappropriate activation, plants employ multiple mechanisms to suppress inappropriate activation of HR and to constrain it after activation. The ubiquity of this response among higher plants despite its costs suggests that it is an extremely effective component of the plant immune system.
Summary
Activation of nucleotide‐binding leucine‐rich repeat receptors (NLRs) results in immunity and a localized cell death. NLR cell death activity requires oligomerization and in some cases plasma ...membrane (PM) localization. The exact mechanisms underlying PM localization of NLRs lacking predicted transmembrane domains or recognizable lipidation motifs remain elusive.
We used confocal microscopy, genetically encoded molecular tools and protein‐lipid overlay assays to determine whether PM localization of members of the Arabidopsis HeLo‐/RPW8‐like domain ‘helper’ NLR (RNL) family is mediated by the interaction with negatively charged phospholipids of the PM.
Our results show that PM localization and stability of some RNLs and one CC‐type NLR (CNL) depend on the direct interaction with PM phospholipids. Depletion of phosphatidylinositol‐4‐phosphate from the PM led to a mis‐localization of the analysed NLRs and consequently inhibited their cell death activity. We further demonstrate homo‐ and hetero‐association of members of the RNL family. Our results provide new insights into the molecular mechanism of NLR localization and defines an important role of phospholipids for CNL and RNL PM localization and consequently, for their function.
We propose that RNLs interact with anionic PM phospholipids and that RNL‐mediated cell death and immune responses happen at the PM.
The plant immune system involves cell-surface receptors that detect intercellular pathogen-derived molecules, and intracellular receptors that activate immunity upon detection of pathogen-secreted ...effector proteins that act inside the plant cell. Immunity mediated by surface receptors has been extensively studied
, but that mediated by intracellular receptors has rarely been investigated in the absence of surface-receptor-mediated immunity. Furthermore, interactions between these two immune pathways are poorly understood. Here, by activating intracellular receptors without inducing surface-receptor-mediated immunity, we analyse interactions between these two distinct immune systems in Arabidopsis. Pathogen recognition by surface receptors activates multiple protein kinases and NADPH oxidases, and we find that intracellular receptors primarily potentiate the activation of these proteins by increasing their abundance through several mechanisms. Likewise, the hypersensitive response that depends on intracellular receptors is strongly enhanced by the activation of surface receptors. Activation of either immune system alone is insufficient to provide effective resistance against the bacterial pathogen Pseudomonas syringae. Thus, immune pathways activated by cell-surface and intracellular receptors in plants mutually potentiate to activate strong defences against pathogens. These findings reshape our understanding of plant immunity and have broad implications for crop improvement.
The hypersensitive response (HR) is a localized programmed cell death phenomenon that occurs in response to pathogen recognition at the site of attempted invasion. Despite more than a century of ...research on HR, little is known about how it is so tightly regulated and how it can be contained spatially to a few cells.
AtMC1 is an Arabidopsis thaliana plant metacaspase that positively regulates the HR. Here, we used an unbiased approach to identify new AtMC1 regulators. Immunoaffinity purificationof AtMC1-containing complexes led us to the identification of the protease inhibitor AtSerpin1.
Our data clearly showed that coimmunoprecipitation between AtMC1 and AtSerpin1 and formation of a complex between them was lost upon mutation of the AtMC1 catalytic site, and that the AtMC1 prodomain was not required for the interaction. AtSerpin1 blocked AtMC1 self-processing and inhibited AtMC1-mediated cell death. Our results constitute an in vivo example of a Serpin acting as a suicide inhibitor in plants, reminiscent of the activity of animal or viral serpins on immune/cell death regulators, including caspase-1.
These results indicate a conserved function of a protease inhibitor on cell death regulators from different kingdoms with unrelated modes of action (i.e. caspasesvsmetacaspases).
Plants are constantly exposed to microorganisms in the environment and, as a result, have evolved intricate mechanisms to recognize and defend themselves against potential pathogens. One of these ...responses is the downregulation of photosynthesis and other processes associated with primary metabolism that are essential for plant growth. It has been suggested that the energy saved by downregulation of primary metabolism is diverted and used for defense responses. However, several studies have shown that upregulation of primary metabolism also occurs during plant-pathogen interactions. We propose that upregulation of primary metabolism modulates signal transduction cascades that lead to plant defense responses. In support of this thought, we here compile evidence from the literature to show that upon exposure to pathogens or elicitors, plants induce several genes associated with primary metabolic pathways, such as those involved in the synthesis or degradation of carbohydrates, amino acids and lipids. In addition, genetic studies have confirmed the involvement of these metabolic pathways in plant defense responses. This review provides a new perspective highlighting the relevance of primary metabolism in regulating plant defense against pathogens with the hope to stimulate further research in this area.
In plants, the reactive oxygen species (ROS) formed during normal conditions are essential in regulating several processes, like stomatal physiology, pathogen immunity and developmental signaling. ...However, biotic and abiotic stresses can cause ROS over-accumulation leading to oxidative stress. Therefore, a suitable equilibrium is vital for redox homeostasis in plants, and there have been major advances in this research arena. Salicylic acid (SA) is known as a chief regulator of ROS; however, the underlying mechanisms remain largely unexplored. SA plays an important role in establishing the hypersensitive response (HR) and systemic acquired resistance (SAR). This is underpinned by a robust and complex network of SA with Non-Expressor of Pathogenesis Related protein-1 (NPR1), ROS, calcium ions (Ca2+), nitric oxide (NO) and mitogen-activated protein kinase (MAPK) cascades. In this review, we summarize the recent advances in the regulation of ROS and antioxidant defense system signalling by SA at the physiological and molecular levels. Understanding the molecular mechanisms of how SA controls redox homeostasis would provide a fundamental framework to develop approaches that will improve plant growth and fitness, in order to meet the increasing global demand for food and bioenergy.
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•Reactive oxygen species display duality in plants, as they act as signalling molecules under normal conditions, whereas they act as oxidant molecules under adverse conditions thereby leading to altered redox status.•Salicylic acid plays a key role in plant immunity by regulating the redox signalling and the antioxidant defence system.•SA induces the hypersensitive response and systemic acquired resistance (SAR).•It involves multifaceted network of the SA receptor Non-Expressor of Pathogenesis Related protein-1, reactive oxygen species, calcium ions, nitric oxide and mitogen-activated protein kinase cascades.
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