ATM and ATR, two central players of the DNA damage response, are involved in the induction of systemic acquired resistance by extracellular DNA, but not the plant wound response.

Background: The plant immune response to DNA is highly self/nonself-specific. Self-DNA triggered stronger responses by early immune signals such as H2O2 formation than nonself-DNA from closely related plant species. Plants lack known DNA receptors. Therefore, we aimed to investigate whether a differential sensing of self-versus nonself DNA fragments as damage- versus pathogen-associated molecular patterns (DAMPs/PAMPs) or an activation of the DNA-damage response (DDR) represents the more promising framework to understand this phenomenon. Results: We treated Arabidopsis thaliana Col-0 plants with sonicated self-DNA from other individuals of the same ecotype, nonself-DNA from another A. thaliana ecotype, or nonself-DNA from broccoli. We observed a highly self/nonself-DNA-specific induction of H2O2 formation and of jasmonic acid (JA, the hormone controlling the wound response to chewing herbivores) and salicylic acid (SA, the hormone controlling systemic acquired resistance, SAR, to biotrophic pathogens). Mutant lines lacking Ataxia Telangiectasia Mutated (ATM) or ATM AND RAD3-RELATED (ATR) - the two DDR master kinases - retained the differential induction of JA in response to DNA treatments but completely failed to induce H2O2 or SA. Moreover, we observed H2O2 formation in response to in situ-damaged self-DNA from plants that had been treated with bleomycin or SA or infected with virulent bacteria Pseudomonas syringae pv. tomato DC3000 or pv. glycinea carrying effector avrRpt2, but not to DNA from H2O2-treated plants or challenged with non-virulent P. syringae pv. glycinea lacking avrRpt2. Conclusion: We conclude that both ATM and ATR are required for the complete activation of the plant immune response to extracellular DNA whereas an as-yet unknown mechanism allows for the self/nonself-differential activation of the JA-dependent wound response.

Arabidopsis thaliana Response to Extracellular DNA: Self Versus Nonself Exposure.

The inhibitory effect of extracellular DNA (exDNA) on the growth of conspecific individuals was demonstrated in different kingdoms. In plants, the inhibition has been observed on root growth and seed germination, demonstrating its role in plant-soil negative feedback. Several hypotheses have been proposed to explain the early response to exDNA and the inhibitory effect of conspecific exDNA. We here contribute with a whole-plant transcriptome profiling in the model species Arabidopsis thaliana exposed to extracellular self- (conspecific) and nonself- (heterologous) DNA. The results highlight that cells distinguish self- from nonself-DNA. Moreover, confocal microscopy analyses reveal that nonself-DNA enters root tissues and cells, while self-DNA remains outside. Specifically, exposure to self-DNA limits cell permeability, affecting chloroplast functioning and reactive oxygen species (ROS) production, eventually causing cell cycle arrest, consistently with macroscopic observations of root apex necrosis, increased root hair density and leaf chlorosis. In contrast, nonself-DNA enters the cells triggering the activation of a hypersensitive response and evolving into systemic acquired resistance. Complex and different cascades of events emerge from exposure to extracellular self- or nonself-DNA and are discussed in the context of Damage- and Pathogen-Associated Molecular Patterns (DAMP and PAMP, respectively) responses.

Breaking Bad News: Dynamic Molecular Mechanisms of Wound Response in Plants.

Recognition and repair of damaged tissue are an integral part of life. The failure of cells and tissues to appropriately respond to damage can lead to severe dysfunction and disease. Therefore, it is essential that we understand the molecular pathways of wound recognition and response. In this review, we aim to provide a broad overview of the molecular mechanisms underlying the fate of damaged cells and damage recognition in plants. Damaged cells release the so-called damage associated molecular patterns to warn the surrounding tissue. Local signaling through calcium (Ca2+), reactive oxygen species (ROS), and hormones, such as jasmonic acid, activates defense gene expression and local reinforcement of cell walls to seal off the wound and prevent evaporation and pathogen colonization. Depending on the severity of damage, Ca2+, ROS, and electrical signals can also spread throughout the plant to elicit a systemic defense response. Special emphasis is placed on the spatiotemporal dimension in order to obtain a mechanistic understanding of wound signaling in plants.

Nucleic Acid Sensing in Mammals and Plants: Facts and Caveats.

The accumulation of nucleic acids in aberrant compartments is a signal of danger: fragments of cytosolic or extracellular self-DNA indicate cellular dysfunctions or disruption, whereas cytosolic fragments of nonself-DNA or RNA indicate infections. Therefore, nucleic acids trigger immunity in mammals and plants. In mammals, endosomal Toll-like receptors (TLRs) sense single-stranded (ss) or double-stranded (ds) RNA or CpG-rich DNA, whereas various cytosolic receptors sense dsDNA. Although a self/nonself discrimination could favor targeted immune responses, no sequence-specific sensing of nucleic acids has been reported for mammals. Specific immune responses to extracellular self-DNA versus DNA from related species were recently reported for plants, but the underlying mechanism remains unknown. The subcellular localization of mammalian receptors can favor self/nonself discrimination based on the localization of DNA fragments. However, autoantibodies and diverse damage-associated molecular patterns (DAMPs) shuttle DNA through membranes, and most of the mammalian receptors share downstream signaling elements such as stimulator of interferon genes (STING) and the master transcription regulators, nuclear factor (NF)-κB, and interferon regulatory factor 3 (IRF3). The resulting type I interferon (IFN) response stimulates innate immunity against multiple threats-from infection to physical injury or endogenous DNA damage-all of which lead to the accumulation of eDNA or cytoplasmatic dsDNA. Therefore, no or only low selective pressures might have favored a strict self/nonself discrimination in nucleic acid sensing. We conclude that the discrimination between self- and nonself-DNA is likely to be less strict-and less important-than assumed originally.