REACTIVE OXYGEN SPECIES AND PLANT DEFENSE RESPONSE

Resistance trait is defense and tolerance. On recognition of pathogen, plant cell activate and deploy defense responses to inhibit pathogen growth. Defense responses are conditioned by nutritional and signaling status of the plant. Living organisms perform oxidation-reduction (redox) reaction such as anabolic, a reductive processes to store energy and catabolic, an oxidative processes to release it. Atomic oxygen is abundant in earth crust and the molecular oxygen present in atmosphere and water is required by living organisms. The oxygen (O2) reservoir is the result of photosynthesis a process that liberates dioxygen from water and is kept approximately constant by respiration in which O2 is used as electron acceptor.  The toxic effect of O2 is due to its reactive derivatives. The power of its radical (superoxide, hydroxyl radical) and non-radical (hydrogen peroxide) derivatives can be used to convey redox information or are released, when antioxidant defence is withdrawn, to trigger cell death (Foyer and Noctor 2003).

Reactive oxygen species (ROS) such as hydrogen peroxide (H2O2), hydroxyl radical (OH), superoxide anion radical (O2) and singlet oxygen (1O2) are toxic intermediate resulting from reduction of molecular oxygen. ROS are partially reduced or activated form of atomospheric oxygen (O2) (Choudhury et al., 2017). They are unavoidable byproducts of aerobic metabolism. H2O2 is a stable ROS, not very reactive, is electrically neutral and can pass through cell membranes and reach the cell location from the site of its formation and is used as a substrate by various peroxidases (generation of phenoxyl radical which are building blocks for lignin synthesis) (Wojtaszek 1997). During hypersensitive response (HR) H2O2 triggers localized cell death and it seems nitric oxide too plays a role in disease resistance (Delledonne et al., 1998).  Release of reactive oxygen species known as the oxidative burst function in rapid amplification of signal. The oxidative burst drives the crosslinking of the cell wall, induces plant gene involved in cellular protection and defense. Brisson et al. (1994) propose that rapid oxidative cross-linking enhances the effectiveness of the plant cell wall as a barrier to slow pathogen ingress and spread prior to the deployment of the transcription-dependent defences such as, phytoalexins, lytic enzymes and other antimicrobial proteins. Moreover rapid oxidative cross-linking of the cell wall also serves trap pathogens in cells to undergo hypersensitive cell death restricting pathogen.

The relationship between the oxidative burst and other plant defense responses are (Baker and Orlandi 1995; Wojtaszek 1997):

  • An oxygen consumption
  • Immobilization of  plant cell wall proteins
  • Changes in membrane permeability and ion fluxes
  • The production of phytoalexins
  • Systemic Acquired Resistance
  • Lignin production
  • Lipid peroxidation
  • A role in hypersensitive cell death

Sugars may act as signal molecule interacting with the hormonal signaling inducing plant immunity. It enhances oxidative burst on infection, increasing lignification of cell walls, stimulate synthesis of flavonoids and induce pathogenesis related (PR) proteins (Morkunas and Ratajczak 2014). In plants photosynthesis and key step in the synthesis of defense-related hormone occur in chloroplasts (Lu and Yao 2018). Chloroplast are the generator of ROS and nitric oxide and also a site for calcium signaling. These signaling molecule are essential for plant defense responses (Lu and Yao 2018). The reaction centres photosystem I and photosystem II in chloroplast thylakoids are the major generation site of ROS (Asada 2006). Increased level of ROS in chloroplasts have signaling roles in the onset of immune reactions upon infection (Kangasjarvi et al., 2009). Production of ROS in extracellular space, the apoplast can influence their generation in the chloroplast and both can regulate nuclear gene expression (Shapiguzov et al., 2012). The chloroplast further amplifies the signal and transmits it to the nucleus via various cytosolic signaling networks. Apoplastic ROS signaling can also reach the nucleus through cytosolic pathway directly. Intracellular transmission of apoplastic and chloroplastic ROS-induced signals connect neighbouring cells (local signaling) or participate in long distance (systemic) signaling throughout the plant (Lu and Yao 2018).

Formation of superoxide radical in chloroplasts is a part of Mehler reaction and that H2O2 is formed only from superoxide anion (O2) (Asada et al., 1974).The initial reaction during the pathogen induced oxidative burst is one-electron reduction of molecular oxygen to form superoxide anion (O2). Superoxide the first reduction product of ground state-oxygen is capable of both oxidation and reduction. It may react to produce several other reactive species. The hydroxyl radical initiates radical chain reaction including lipid peroxidation, enzyme inactivation and degradation of nucleic acid (Mehdy 1994).  O2generation and nicotinamide adenine dinucleotide phosphate (NADPH) oxidation occurs on the plasma membrane upon incompatible recognition of the host cells leading to hypersensitive cell death (Doke 1983).  Other signaling components involve salicylic acid (SA) and cytosolic Ca+2.   H2O2 has a regulatory influence on Ca+2 concentration in different cellular compartment (Foyer and Noctor 2003). Cytosolic Ca+2 is a second messenger during signal transduction from the cell surface to internal compartments of the plant cell (Bach et al., 1993).

Elicitor receptor associate to, active oxygen synthesis via G proteins, increased intracellular Ca+2 due to Ca+2 channel opening and activation of a protein kinase that activates a membrane-bound NAD(P)H oxidase by phosphorylation (Mehdy 1994). Plants have plasma membrane enzyme similar to the neutrophil NADPH oxidase with a regulatory mechanisms for Ca+2 and G protein stimulation of O2and H2O2 production at the cell surface (Keller et al., 1998).  O2 simultaneously dismutates to H2O2, which is membrane permeable. O2and H2O2 kills pathogen. H2O2 also participates in oxidative cross-linking of cell wall proteins and regulation of host gene expression (Mehdy 1994). SA inhibits catalase activity in and induce an increase in H2O2. SA inducing defense associated genes during SAR is mediated by increased amount of H2O2 (Chen et al., 1993).

Signaling route starts from a ROS burst in the apoplast. Elevated level of ROS can oxidize membrane lipids, activate Ca2+ channel, activate receptor like kinases (RLK) and diffuse through aquaporins and induce abscisic acid signaling. All these activity occur in cytosol inducing transcription factor (Podgorska  et al., 2017). Plants use the toxic properties of ROS to control invading pathogen. 

References:

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Asada, K., Kiso, K. and Yoshikawa, K. 1974 Univalent Reduction of Molecular Oxygen by Spinach Chloroplasts on Illumination.  J. Biol. Chem. 249(7): 2175 – 2181

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Bach, M., Schnitzler, J-P. and Seitz, H. U.  1993 Elicitor-Induced Changes in  Ca+2 Influx, K+ Efflux and 4-Hydroxybenzoic Acid Synthesis in Protoplasts of Daucus carota L.1. Plant Physiol.103: 407 – 412

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Choudhury, F. K., Rivero, R. M., Blumwald, E. and Mittler, R.  2017 Reactive Oxygen Species, Abiotic Stress and Stress Combination. Plant Journ. 90(5): 856 – 867

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Delledonne, M., Xia, Y., Dixon, R. A. and Lamb, C. 1998 Nitric Oxide Functions as a Signal in Plant Disease Resistance. Nature 394 (6693): 585 – 588

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Doke, N. 1983 Generation of Superoxide Anion by Potato Tuber Protoplasts during the Hypersensitive response to Hyphal Wall Components of Phytophthora infestans and Specific Inhibition of the Reaction by Suppressors of Hypersensitivity. Physiol. Plant Pathol. 23(3): 359 – 367

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Kangasjarvi, S., Nurmi, M., Tikkanen, M. and Aro, E. M.  2009 Cell-specific Mechanisms and Systemic Signaling as Emerging Themes in Light Acclimation of C3 Plants. Plant Cell Environ. 32(9): 1230 – 1240

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Keller, T., Damude, H. G., Werner, D., Doerner, P. and Dixon, R. A. 1998 A Plant Homolog of the Neutrophil NADPH Oxidase gp91phox  Subunit Gene Encodes a Plasma Membrane Protein with  Ca+2  Binding Motifs. The Plant Cell 10: 255 – 266

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Shapiguzov, A., Vainonen, J. P., Wrzaczek, M. and Kangasjarvi, J. 2012 ROS-Talk-How the Apoplast, the Chloroplast and the Nucleus get the Message Through. Front. Plant Sci. 3: 292

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