• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of plntphysLink to Publisher's site
Plant Physiol. Jun 2006; 141(2): 373–378.
PMCID: PMC1475467
Special Issue on Reactive Oxygen Species

Reactive Oxygen Species Signaling in Response to Pathogens1

The production of reactive oxygen species (ROS), via consumption of oxygen in a so-called oxidative burst, is one of the earliest cellular responses following successful pathogen recognition. Apoplastic generation of superoxide (O2), or its dismutation product hydrogen peroxide (H2O2), has been documented following recognition of a variety of pathogens (Doke, 1983; Auh and Murphy, 1995; Grant et al., 2000b). Avirulent pathogens, successfully recognized via the action of disease resistance (R) gene products in plant immune system, elicit a biphasic ROS accumulation with a low-amplitude, transient first phase, followed by a sustained phase of much higher magnitude that correlates with disease resistance (Lamb and Dixon, 1997). However, virulent pathogens that avoid host recognition induce only the transient, low-amplitude first phase of this response, suggesting a role for ROS in the establishment of the defenses. In line with this conclusion, elicitors of defense responses, often referred to as microbe-associated molecular patterns (MAMPs), also trigger an oxidative burst. Initial characterization of the oxidative burst left unclear whether ROS acted as executioners of pathogen, host cells (in the form of the familiar hypersensitive response [HR]), or both, or, alternatively, as signaling molecules that were not directly involved in the mechanisms that actually stopped pathogen growth.

In the plant cell, ROS can directly cause strengthening of host cell walls via cross-linking of glycoproteins (Bradley et al., 1992; Lamb and Dixon, 1997), or lipid peroxidation and membrane damage (Lamb and Dixon, 1997; Montillet et al., 2005). However, it is also evident that ROS are important signals mediating defense gene activation (Levine et al., 1994). Additional regulatory functions for ROS in defense occur in conjunction with other plant signaling molecules, particularly with salicylic acid (SA) and nitric oxide (NO; see Fig. 1). However, ROS also regulate additional plant responses in relation to other signals. Here, we discuss these roles of ROS with a focus on the response to pathogen infection.

Figure 1.
ROS production and functions in response to pathogens.

MECHANISMS OF ROS PRODUCTION IN RESPONSE TO PATHOGENS

Several enzymes have been implicated in apoplastic ROS production following successful pathogen recognition. The use of inhibitors pointed to plasma membrane NADPH oxidases (inhibited by diphenylene iodonium [DPI] but not by cyanide or azide; Grant et al., 2000a) and cell wall peroxidases (inhibited by cyanide or azide but not by DPI; Grant et al., 2000a; Bolwell et al., 2002) as the two most likely biochemical sources. The NADPH oxidase, also known as the respiratory burst oxidase (RBO), was initially described in mammalian neutrophils as a multicomponent complex mediating microbial killing (Lambeth, 2004). gp91phox is the enzymatic subunit of this oxidase and transfers electrons to molecular oxygen to generate superoxide. Arabidopsis (Arabidopsis thaliana) has 10 Atrboh (Arabidopsis RBO homolog) genes homologous to gp91phox (Torres and Dangl, 2005). Several recent reports demonstrate that members of the Rboh family mediate the production of apoplastic ROS during the defense responses, as well as in response to abiotic environmental and developmental cues (Torres and Dangl, 2005). However, we know very little about either the precise subunit structure of the plant NADPH oxidase or its activation. Both are likely different than in mammalian neutrophils (Torres and Dangl, 2005).

Peroxidases form a complex family of proteins that catalyze the oxidoreduction of various substrates using H2O2. In particular, pH-dependent peroxidases in the cell wall can also be a source of apoplastic H2O2 in the presence of a reductant released from responding cells (Wojtaszek, 1997; Bolwell et al., 1998). The expression of these enzymes is induced following recognition of bacterial and fungal pathogens (Chittoor et al., 1997; Sasaki et al., 2004). A French bean (Phaseolus vulgaris) cationic peroxidase and H2O2 (detected by cerium chloride staining) were colocalized in the vicinity of invading bacteria together with other components of the papillae (Brown et al., 1998). These results suggested that H2O2 generation by this enzyme could lead to the generation of subcellular, polarized physical barriers at infection sites.

Although the primary oxidative burst following pathogen recognition occurs in the apoplast, ROS produced in other cellular compartments may also have functions in defense. High levels of ROS can be produced inside the plant cell as by-products of metabolic processes, in particular, light-driven production of ROS as a by-product of photosynthesis (Karpinski et al., 2003; Apel and Hirt, 2004). Uncoupling, or inhibition, of the photosystem machinery in the chloroplast and photorespiration associated with chloroplast and peroxisome function can lead to the formation of high levels of ROS that can dramatically affect cellular homeostasis. It is important to recall the nearly ubiquitous requirement for light in the HR (Goodman and Novacky, 1994), as illustrated by the requirement of high-intensity light for cell death mediated by resistance gene proteins (Tang et al., 1998). Under high-light conditions, photorespiratory ROS mediate different mechanisms of lipid peroxidation leading to cell death than in the dark, underscoring the importance of light during the HR (Montillet et al., 2005).

Various ROS-scavenging systems, including ascorbate peroxidases, glutathione, superoxide dismutases, and catalases, maintain ROS homeostasis in different compartments of the plant cell (Mittler et al., 2004). These enzymes could restrict the ROS-dependent damage or finely tune ROS-dependent signal transduction. High-intensity light stress in plants with down-regulated scavenging systems leads to an ectopic oxidative burst and cell death that is phenotypically similar to HR (Chamnongpol et al., 1998; Dat et al., 2003). Differential regulation of these enzymes, in part mediated by SA, may contribute to increases in ROS and activation of defenses following infection (Dorey et al., 1998; Mittler et al., 1999; Klessig et al., 2000). In tobacco, the reduction of catalase and ascorbate peroxidase activities resulted in plants hyper-responsive to pathogens (Mittler et al., 1999), whereas the overexpression of catalase leads to more disease-sensitive plants (Polidoros et al., 2001). Collectively, these results suggest that the ROS-scavenging systems can have an important role in managing ROS generated in response to pathogens. Further, compartmentalization of both ROS production and activation of ROS-scavenging systems could contribute to fine-tuning of ROS levels and their signaling properties.

FUNCTIONS OF ROS FOLLOWING INFECTION

Pharmacological approaches also suggest that different parts of the overall ROS production in response to infection appear to be mediated by different mechanisms. Though the involvement of an NADPH oxidase has been predominant in most cases (Bolwell et al., 1998; Grant et al., 2000b; Torres and Dangl, 2005), both NADPH oxidases and cell wall peroxidases might mediate ROS production in response to the same pathogen (Grant et al., 2000a). A more detailed temporal resolution of the activity of each system may reveal that the pools of ROS produced by each mechanism do not functionally overlap. For example, differential effects of DPI on ROS accumulation during the HR- and MAMP-mediated basal defense responses were reported, with the latter being considerably less attenuated by DPI (Soylu et al., 2005). These results suggest that alternative mechanisms might be activated to produce ROS during some basal defense responses, while NADPH oxidases might have later effects following R-mediated pathogen recognition. However, the use of inhibitors in this work, as in other research, needs to be validated with genetic approaches.

ROS were proposed to orchestrate the establishment of plant defense response and HR following successful pathogen recognition (Apostol et al., 1989; Levine et al., 1994). Genetic proof for NADPH oxidase-Rboh function in the pathogen-induced oxidative burst came from the analysis of rboh mutants and antisense lines (Simon-Plas et al., 2002; Torres et al., 2002; Yoshioka et al., 2003). Down-regulation or elimination of Rboh leads to elimination of extracellular peroxide formation. Yet, this lack of ROS has variable effects on pathogen growth and HR. For example, a double mutant of the Arabidopsis atrbohD and atrbohF genes displays reduced HR in response to avirulent bacteria (Torres et al., 2002). Similarly, Nbrboh-silenced Nicotiana benthamiana plants are more susceptible to avirulent oomycete Phytophthora infestans, and HR is suppressed (Yoshioka et al., 2003). By contrast, the Arabidopsis atrbohF mutant is more resistant to a weakly virulent strain of the oomycete Hyaloperonospora parasitica and actually displays enhanced HR (Torres et al., 2002). There is also evidence of functional overlap between different Rboh proteins. For example, in Arabidopsis, various phenotypes of the individual atrbohD and atrbohF mutants are accentuated in the double mutant atrbohD atrbohF (Torres et al., 2002; Kwak et al., 2003). Thus, while the Rboh proteins are required for ROS production following successful pathogen recognition, these ROS may serve diverse signaling functions in disease resistance and HR.

Plant Rac2 homologs (called Rop for Rho-like proteins) also regulate the production of ROS by the NADPH oxidase, as they do in animals (Kawasaki et al., 1999; Moeder et al., 2005). Interestingly, different plant Rac proteins appear to act as either positive or negative regulators of ROS production. For example, Osrac1 is a positive regulator of ROS production and cell death (Ono et al., 2001), whereas Ntrac5 acts as a negative regulator of ROS production via NtrbohD (Morel et al., 2004). These analyses suggest that combinations of Rac isoforms with specific Rboh isoforms may mediate differential regulatory outcomes and could explain the differential functions of NADPH oxidases in regulation of defense and cell death.

ROS production has been associated with the formation of defensive barriers against powdery mildew in barley (Hordeum vulgare; Huckelhoven and Kogel, 2003). ROS produced in the barley/powdery mildew interaction were observed in vesicles inside the cell, suggesting that the polarized delivery of ROS, among other factors, might contribute to inhibition of pathogen growth (Collins et al., 2003). Interestingly, specific granules in mammalian neutrophils are a site for assembly and activation of the oxidase enzyme system (Segal, 2005). Further verification will be needed to assess if a plant NADPH oxidase is responsible for this ROS in vesicles and its specific function in the interaction with powdery mildew.

ROS, in association with SA, were proposed to mediate the establishment of systemic defenses (systemic acquired resistance [SAR]; Durrant and Dong, 2004). The rapidity of ROS production and the potential for H2O2 to freely diffuse across membranes suggested that ROS could function as an intercellular or intracellular second messenger (Levine et al., 1994; Lamb and Dixon, 1997). ROS metabolism could also affect the function of NPR1, a crucial mediator of these systemic responses, by controlling NPR1 redox state (Mou et al., 2003). However, although H2O2 may mediate the accumulation of defense markers beyond the initial infection site, inhibitor studies indicate that it is unlikely that it is itself the translocated signal that mediates SAR (Bi et al., 1995; Dorey et al., 1999; Costet et al., 2002), and genetic proof will be needed to clearly establish the role, if any, of ROS in SAR. Interestingly, there is also evidence that NADPH oxidase mediates the systemic production of ROS in response to successful viral infection in Arabidopsis, although the functional relevance of this remains unclear (Love et al., 2005).

Although ROS usually correlates with successful disease resistance responses, some pathogens may induce production of ROS to their own advantage. For example, necrotrophs appear to stimulate ROS production in the infected tissue to induce cell death that facilitates subsequent infection (Govrin and Levine, 2000). The fungal necrotroph Botrytis triggers significant changes in the peroxisomal antioxidant system, leading to a collapse of the protective mechanism at advanced stages of infection. This process is partly related to senescence (Kuzniak and Sklodowska, 2005). Interference with the chlorophyll degradation pathway also results in overaccumulation of ROS and an increase in susceptibility to some necrotrophic pathogens (Kariola et al., 2005). In addition, there are also reports of ROS being produced, together with increased levels of ROS detoxification enzymes, during compatible interactions involving virus (Allan et al., 2001; Clarke et al., 2002). Some proteins of the Rac family also appear to function in pathogen susceptibility (Schultheiss et al., 2003). Thus, ROS is produced as part of a complex network of signals that respond to pathogen attack and mediate multiple responses, sometimes with opposite effects, in different contexts or in response to different pathogens.

INTERACTION OF ROS WITH OTHER SIGNALS

Interaction with other plant defense regulators may account for these divergent outcomes in ROS signaling. SA is a plant signaling molecule involved in defense responses, local and systemic, to pathogen attack (Durrant and Dong, 2004). SA levels increase dramatically in cells surrounding infection sites (Enyedi et al., 1992). ROS was proposed to act synergistically in a signal amplification loop with SA to drive the HR and the establishment of systemic defenses (Draper, 1997). This model was based, in large part, on experiments using submaximal doses of both exogenous H2O2 and pathogen to drive SA accumulation; subsequent increases in SA enhanced ROS production (Leon et al., 1995; Shirasu et al., 1997). SA accumulation can also down-regulate those ROS-scavenging systems that, in turn, can contribute to increased overall ROS levels following pathogen recognition (Klessig et al., 2000). However, ROS and SA antagonize each other's action in the regulation of cell death expansion at the margins of pathogen-triggered HR lesions in the lesion mimic mutant lsd1 (Torres et al., 2005). lsd1 fails to contain the initial HR following pathogen recognition (Dietrich et al., 1997). Unexpectedly, ROS produced by AtrbohD and AtrbohF are negative regulators of the unrestricted cell death expanding from the margins of an initial HR site in lsd1, whereas SA produced through isochorismate synthase is a positive regulator of this cell death (Torres et al., 2005). These surprising results underscore how ROS can mediate different functions in different cellular and spatial contexts, and in relation to other regulatory signals. Similarly, SA and the hormone jasmonic acid seem also to either synergize or antagonize in their signaling functions at different concentrations. Synergy, in this case, drives ROS production and cell death (Mur et al., 2006).

ROS signaling has also been linked to NO, another reactive oxygen derivative produced following pathogen recognition (Delledonne et al., 1998; Durner et al., 1998). NO seems to work in conjunction with ROS in the potentiation of the pathogen-induced cell death (Delledonne et al., 2001). Cytological studies show that ROS and NO are associated with cell death adjacent to infected cells and that both signals modulate each other's accumulation (Tada et al., 2004; Zeier et al., 2004). Interestingly, both ROS and NO collaborate to mediate abscisic acid (ABA)-induced stomata closure (Desikan et al., 2004). NO synthesis and stomata closure in response to ABA are severely reduced in the NADPH oxidase double mutant atrbohD atrbohF, suggesting that endogenous H2O2 production elicited by ABA is required for NO synthesis (Bright et al., 2006). Collectively, these data suggest that the interplay between these molecules mediates a variety of physiological responses.

Calcium metabolism is intimately related to ROS signaling. Increases in cytosolic Ca2+ is also one of the fastest responses upon pathogen infection, and the use of specific inhibitors show that Ca2+ influx is required for ROS production after elicitation (Blume et al., 2000; Grant et al., 2000b). Ca2+ can activate an Rboh protein in vitro (Sagi and Fluhr, 2001), and all plant Rboh proteins contain two EF-hands in their N-terminal region that may account for this Ca2+ regulation (Torres and Dangl, 2005). On the other hand, ROS appears to be required to prime Ca2+ influx after elicitation (Levine et al., 1996). Therefore, Ca2+ fluxes appear to function both upstream and downstream of ROS production, indicating a complex spatiotemporal Ca2+ regulation of these signaling networks. Phosphorylation events have also been proposed to occur both upstream and downstream of ROS production in response to pathogens (Nurnberger and Scheel, 2001; Apel and Hirt, 2004).

ROS generated via the NADPH oxidase and subsequent Ca2+ channel activation may represent a common signaling link in many plant responses. For example, ROS functions as an intermediate in ABA signaling during stomata closure through the activation of Ca2+ channels in guard cells (Pei et al., 2000). Thus, activation of Ca2+ channels represents a common signaling cassette in response to at least ABA and pathogen response. ROS may be the crucial signal in each system, since fungal elicitors induce both elevation of free cytosolic Ca2+ and stomata closure in guard cells (Klusener et al., 2002). The same Atrboh genes have been implicated in each system (Torres et al., 2002; Kwak et al., 2003), suggesting that the same NADPH oxidases regulate different ROS-dependent functions in different cellular contexts.

Responses associated with ROS may also interact with ethylene signaling. Ethylene can induce programmed cell death and senescence (de Jong et al., 2002). Both ROS and ethylene have been implicated in signaling in response to viral infection (Love et al., 2005). Interestingly, the ethylene receptor ETR1 can function as an ROS sensor, mediating stomatal closure in response to H2O2 (Desikan et al., 2005). Thus, this protein may constitute a node mediating cross talk between ethylene and H2O2. Thus, ROS signaling interacts with many other regulatory events in a complex network of signals that govern the response to pathogens and other factors of the environment as well as developmental cues. This cross talk may account for the multiplicity of responses mediated by ROS and explain why ROS produced by the same mechanism exert variable effects in different contexts.

CONCLUDING REMARKS

The rapid production of ROS in the apoplast in response to pathogens has been proposed to orchestrate the establishment of different defensive barriers against the pathogens. Based on genetic analysis, the NADPH oxidase appears to be the predominant enzymatic mechanism responsible for this oxidative burst. However, other mechanisms of ROS production in other compartments, as well as various ROS-scavenging systems, may modify and regulate these responses. ROS produced by the NADPH oxidase alone can mediate diverse and sometimes opposite functions in different cellular contexts, underscoring the complexity of ROS signaling. More efforts should be put toward understanding the interplay between the different pools of ROS, and the flux of information between different compartments to further understand the regulatory capabilities of ROS. We are only beginning to understand the spatiotemporal relationships of ROS generation and removal and the interaction of ROS with other signaling molecules. This promises to be an important, and technically challenging, avenue for future work.

Notes

1This work was supported by the National Science Foundation (grant no. IBN–0077887 to J.L.D.), by the National Institutes of Health (grant no. R01–GM057171 to J.L.D.), and by the Gatsby Charitable Trust (to the Sainsbury Laboratory).

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Jeffery L. Dangl (ude.cnu.liame@lgnad).

www.plantphysiol.org/cgi/doi/10.1104/pp.106.079467.

References

  • Allan AC, Lapidot M, Culver JN, Fluhr R (2001) An early tobacco mosaic virus-induced oxidative burst in tobacco indicates extracellular perception of the virus coat protein. Plant Physiol 126: 97–108 [PMC free article] [PubMed]
  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55: 373–399 [PubMed]
  • Apostol I, Heinstein PF, Low PS (1989) Rapid stimulation of an oxidative burst during elicitation of cultured plant cells. Plant Physiol 99: 109–116 [PMC free article] [PubMed]
  • Auh C-K, Murphy TM (1995) Plasma membrane redox enzyme is involved in the synthesis of O2− and H2O2 by Phytophthora elicitor-stimulated rose cells. Plant Physiol 107: 1241–1247 [PMC free article] [PubMed]
  • Bi Y-M, Kenton P, Mur L, Darby R, Draper J (1995) Hydrogen peroxide does not function downstream of salicylic acid in the induction of PR protein expression. Plant J 8: 235–246 [PubMed]
  • Blume B, Nürnberger T, Nass N, Scheel D (2000) Receptor-mediated increase in cytoplasmic free calcium required for activation of pathogen defense in parsley. Plant Cell 12: 1425–1440 [PMC free article] [PubMed]
  • Bolwell GP, Bindschedler LV, Blee KA, Butt VS, Davies DR, Gardner SL, Gerrish C, Minibayeva F (2002) The apoplastic oxidative burst in response to biotic stress in plants: a tree component system. J Exp Bot 53: 1367–1376 [PubMed]
  • Bolwell GP, Davies DR, Gerrish C, Auh CK, Murphy TM (1998) Comparative biochemistry of the oxidative burst produced by rose and French bean cells reveals two distinct mechanisms. Plant Physiol 116: 1379–1385 [PMC free article] [PubMed]
  • Bradley D, Kjellbom P, Lamb C (1992) Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell 70: 21–30 [PubMed]
  • Bright J, Desikan R, Hancock JT, Weir IS, Neill SJ (2006) ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J 45: 113–122 [PubMed]
  • Brown I, Trethowan J, Kerry M, Mansfield JW, Bolwell GP (1998) Location of components of the oxidative cross-linking of glycoproteins and callose synthesis in papillae formed during the interaction between non-pathogenic strains of Xanthomonas campestris and French bean mesophyll cells. Plant J 15: 333–343
  • Chamnongpol S, Willekens H, Moeder W, Langebartels C, Sanderman HJ, Van Montagu M, Inze D, Van Camp W (1998) Defense activation and enhanced pathogen tolerance induced by H2O2 in transgenic tobacco. Proc Natl Acad Sci USA 95: 5818–5823 [PMC free article] [PubMed]
  • Chittoor JM, Leach JE, White FF (1997) Differential induction of a peroxidase gene family during infection of rice by Xanthomonas oryzae pv. oryzae. Mol Plant Microbe Interact 10: 861–871 [PubMed]
  • Clarke SF, Guy PL, Burritt DJ, Jameson PE (2002) Changes in the activities of antioxidant enzymes in response to virus infection and hormone treatment. Physiol Plant 114: 157–164 [PubMed]
  • Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, Qiu JL, Huckelhoven R, Stein M, Freialdenhoven A, Somerville SC, et al (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425: 973–977 [PubMed]
  • Costet L, Dorey S, Fritig B, Kauffmann S (2002) A pharmacological approach to test the diffusible signal activity of reactive oxygen intermediates in elicitor-treated tobacco leaves. Plant Cell Physiol 43: 91–98 [PubMed]
  • Dat JF, Pellinen R, Beeckman T, Van De Cotte B, Langebartels C, Kangasjarvi J, Inze D, Van Breusegem F (2003) Changes in hydrogen peroxide homeostasis trigger an active cell death process in tobacco. Plant J 33: 621–632 [PubMed]
  • de Jong AJ, Yakimova ET, Kapchina VM, Woltering EJ (2002) A critical role for ethylene in hydrogen peroxide release during programmed cell death in tomato suspension cells. Planta 214: 537–545 [PubMed]
  • Delledonne M, Xia Y, Dixon RA, Lamb CJ (1998) Nitric oxide functions as a signal in plant disease resistance. Nature 394: 585–588 [PubMed]
  • Delledonne M, Zeier J, Marocco A, Lamb CJ (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc Natl Acad Sci USA 98: 13454–13459 [PMC free article] [PubMed]
  • Desikan R, Cheung MK, Bright J, Henson D, Hancock JT, Neill SJ (2004) ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells. J Exp Bot 55: 205–212 [PubMed]
  • Desikan R, Hancock JT, Bright J, Harrison J, Weir I, Hooley R, Neill SJ (2005) A role for ETR1 in hydrogen peroxide signaling in stomatal guard cells. Plant Physiol 137: 831–834 [PMC free article] [PubMed]
  • Dietrich RA, Richberg MH, Schmidt R, Dean C, Dangl JL (1997) A novel zinc-finger protein is encoded by the Arabidopsis lsd1 gene and functions as a negative regulator of plant cell death. Cell 88: 685–694 [PubMed]
  • Doke N (1983) Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiol Plant Pathol 23: 345–357
  • Dorey S, Baillieul F, Saindrenan P, Fritig B, Kauffmann S (1998) Tobacco class I and II catalases are differentially expressed during elicitor-induced hypersensitive cell death and localized acquired resistance. Mol Plant Microbe Interact 11: 1102–1109
  • Dorey S, Kopp M, Geoffroy P, Fritig B, Kauffmann S (1999) Hydrogen peroxide from the oxidative burst is neither necessary nor sufficient for hypersensitive cell death induction, phenylalanine ammonia lyase stimulation, salicylic acid accumulation or scopoletin consumption in cultured tobacco cells treated with elicitor. Plant Physiol 121: 163–173 [PMC free article] [PubMed]
  • Draper J (1997) Salicylate, superoxide synthesis and cell suicide in plant defense. Trends Plant Sci 2: 162–165
  • Durner J, Wendehenne D, Klessig DF (1998) Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc Natl Acad Sci USA 95: 10328–10333 [PMC free article] [PubMed]
  • Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42: 185–209 [PubMed]
  • Enyedi AJ, Yalpani N, Silverman P, Raskin I (1992) Localization, conjugation and function of salicylic acid in tobacco during the hypersensitive reaction to tobacco mosaic virus. Proc Natl Acad Sci USA 89: 2480–2484 [PMC free article] [PubMed]
  • Goodman RN, Novacky AJ (1994) The hypersensitive response in plants to pathogens. APS Press, St. Paul
  • Govrin E, Levine A (2000) The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr Biol 10: 751–757 [PubMed]
  • Grant JJ, Yun B-W, Loake GJ (2000. a) Oxidative burst and cognate redox signalling reported by luciferase imaging: identification of a signal network that functions independently of ethylene, SA and Me-JA but is dependent on MAPKK activity. Plant J 24: 569–582 [PubMed]
  • Grant M, Brown I, Adams S, Knight M, Ainslie A, Mansfield J (2000. b) The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death. Plant J 23: 441–450 [PubMed]
  • Huckelhoven R, Kogel K-H (2003) Reactive oxygen intermediates in plant-microbe interactions: Who is who in powdery mildew resistance? Planta 216: 891–902 [PubMed]
  • Kariola T, Brader G, Li J, Palva ET (2005) Chlorophyllase 1, a damage control enzyme, affects the balance between defense pathways in plants. Plant Cell 17: 282–294 [PMC free article] [PubMed]
  • Karpinski S, Gabrys H, Mateo A, Karpinska B, Mullineaux PM (2003) Light perception in plant disease defence signalling. Curr Opin Plant Biol 6: 390–396 [PubMed]
  • Kawasaki T, Henmi K, Ono E, Hataleuama S, Iwano M, Satoh H, Shimamoto K (1999) The small GTP-binding protein Rac is a regulator of cell death in plants. Proc Natl Acad Sci USA 96: 10922–10926 [PMC free article] [PubMed]
  • Klessig DF, Durner J, Noad R, Navarre DA, Wendehenne D, Kumar D, Zhou JM, Shah J, Zhang S, Kachroo P, et al (2000) Nitric oxide and salicylic acid signaling in plant defense. Proc Natl Acad Sci USA 97: 8849–8855 [PMC free article] [PubMed]
  • Klusener B, Young JJ, Murata Y, Allen GJ, Mori IC, Hugovieux V, Schroeder JI (2002) Convergence of calcium signaling pathways of pathogenic elicitors and abscisic acid in Arabidopsis guard cells. Plant Physiol 130: 2152–2163 [PMC free article] [PubMed]
  • Kuzniak E, Sklodowska M (2005) Fungal pathogen-induced changes in the antioxidant systems of leaf peroxisomes from infected tomato plants. Planta 222: 192–200 [PubMed]
  • Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JD, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22: 2623–2633 [PMC free article] [PubMed]
  • Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48: 251–275 [PubMed]
  • Lambeth JD (2004) NOX enzymes and the biology of reactive oxygen. Nature Rev Immunol 4: 181–189 [PubMed]
  • Leon J, Lawton MA, Raskin I (1995) Hydrogen peroxide stimulates salicylic acid biosynthesis in tobacco. Plant Physiol 108: 1673–1678 [PMC free article] [PubMed]
  • Levine A, Pennell R, Palmer R, Lamb CJ (1996) Calcium-mediated apoptosis in a plant hypersensitive response. Curr Biol 6: 427–437 [PubMed]
  • Levine A, Tenhaken R, Dixon R, Lamb CJ (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79: 583–593 [PubMed]
  • Love AJ, Yun B-W, Laval V, Loake GJ, Milner JL (2005) Cauliflower mosaic virus, a compatible pathogen of Arabidopsis, engages three distinct defense-signaling pathways and activates rapid systemic generation of reactive oxygen species. Plant Physiol 139: 935–948 [PMC free article] [PubMed]
  • Mittler R, Herr EH, Orvar BL, van Camp W, Wilikens H, Inzé D, Ellis BE (1999) Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyperresponsive to pathogen infection. Proc Natl Acad Sci USA 96: 14165–14170 [PMC free article] [PubMed]
  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9: 490–498 [PubMed]
  • Moeder W, Yoshioka K, Klessig DF (2005) Involvement of the small GTPase Rac in the defense responses of tobacco to pathogens. Mol Plant Microbe Interact 18: 116–124 [PubMed]
  • Montillet J-L, Chamnongpol S, Rusterucci C, Dat J, van de Cotte B, Agnel J-P, Battesti C, Inze D, Van Breusegem F, Triantaphylides C (2005) Fatty acid hydroperoxides and H2O2 in the execution of hypersensitive cell death in tobacco leaves. Plant Physiol 138: 1516–1526 [PMC free article] [PubMed]
  • Morel J, Fromentin J, Blein JP, Simon-Plas F, Elmayan T (2004) Rac regulation of NtrbohD, the oxidase responsible for the oxidative burst in elicited tobacco cell. Plant J 37: 282–293 [PubMed]
  • Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113: 935–944 [PubMed]
  • Mur LA, Kenton P, Atzorn R, Miersch O, Wasternack C (2006) The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol 140: 249–262 [PMC free article] [PubMed]
  • Nurnberger T, Scheel D (2001) Signal transmission in the plant immune response. Trends Plant Sci 6: 372–379 [PubMed]
  • Ono E, Wong HL, Kawasaki T, Hasegawa M, Kodama O, Shimamoto K (2001) Essential role of the small GTPase Rac in disease resistance of rice. Proc Natl Acad Sci USA 98: 759–764 [PMC free article] [PubMed]
  • Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406: 731–734 [PubMed]
  • Polidoros AN, Mylona PV, Scandalios JP (2001) Transgenic tobacco plants expressing the maize Cat2 gene have altered catalase levels that affect plant-pathogen interactions and resistance to oxidative stress. Transgenic Res 10: 555–569 [PubMed]
  • Sagi M, Fluhr R (2001) Superoxide production by plant homologues of the gp91(phox) NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol 126: 1281–1290 [PMC free article] [PubMed]
  • Sasaki K, Iwai T, Hiraga S, Kuroda K, Seo S, Mitsuhara I, Miyasaka A, Iwano M, Ito H, Matsui H, et al (2004) Ten rice peroxidases redundantly respond to multiple stresses including infection with rice blast fungus. Plant Cell Physiol 45: 1442–1452 [PubMed]
  • Schultheiss H, Dechert C, Kogel K-H, Huckelhoven R (2003) Functional analysis of barley RAC/ROP G-protein family members in susceptibility to the powdery mildew fungus. Plant J 36: 589–601 [PubMed]
  • Segal AW (2005) How neutrophils kill microbes. Annu Rev Immunol 23: 197–223 [PMC free article] [PubMed]
  • Shirasu K, Nakajima H, Rajasekhar VK, Dixon RA, Lamb CJ (1997) Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell 9: 261–270 [PMC free article] [PubMed]
  • Simon-Plas F, Elmayan T, Blein J-P (2002) The plasma membrane oxidase NtrbohD is responsible for AOS production in elicited tobacco cells. Plant J 31: 137–148 [PubMed]
  • Soylu S, Brown I, Mansfield JW (2005) Cellular reactions in Arabidopsis following challenge by strains of Pseudomonas syringae: from basal resistance to compatibility. Physiol Molec Plant Pathol 66: 232–243
  • Tada Y, Mori T, Shinogi T, Yao N, Takahashi S, Betsuyaku S, Sakamoto M, Park P, Nakayashiki H, Tosa Y, et al (2004) Nitric oxide and reactive oxygen species do not elicit hypersensitive cell death but induce apoptosis in the adjacent cells during the defense response of oat. Mol Plant Microbe Interact 17: 245–253 [PubMed]
  • Tang X, Xie M, Kim YJ, Zhou J, Klessig DF, Martin GB (1998) Overexpression of Pto activates defense responses and confers broad resistance. Plant Cell 11: 15–29 [PMC free article] [PubMed]
  • Torres MA, Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opin Plant Biol 8: 397–403 [PubMed]
  • Torres MA, Dangl JL, Jones JD (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci USA 99: 517–522 [PMC free article] [PubMed]
  • Torres MA, Jones JD, Dangl JL (2005) Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat Genet 37: 1130–1134 [PubMed]
  • Wojtaszek P (1997) Oxidative burst: an early plant response to pathogen. Biochem J 322: 681–692 [PMC free article] [PubMed]
  • Yoshioka H, Numata N, Nakajima K, Katou S, Kawakita K, Rowland O, Jones JD, Doke N (2003) Nicotiana benthamiana gp91phox homologs NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophthora infestans. Plant Cell 15: 706–718 [PMC free article] [PubMed]
  • Zeier J, Delledonne M, Mishina T, Severi E, Sonoda M, Lamb CJ (2004) Genetic elucidation of nitric oxide signaling in incompatible plant-pathogen interactions. Plant Physiol 136: 2875–2886 [PMC free article] [PubMed]

Articles from Plant Physiology are provided here courtesy of American Society of Plant Biologists
PubReader format: click here to try

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...