• superoxide;
  • hydrogen peroxide;
  • superoxide dismutase;
  • catalase;
  • polyhydroxyalkanoate;
  • coronatine


  1. Top of page
  2. Abstract
  3. Introduction: the importance of reactive oxygen in plant–pathogen interactions
  4. Tolerating ROS
  5. Extracellular polysaccharides and intracellular polyesters
  6. Reactive oxygen in pathogenicity and virulence
  7. Concluding remarks
  8. References

Reactive oxygen species (ROS) are a key feature of plant (and animal) defences against invading pathogens. As a result, plant pathogens must be able to either prevent their production or tolerate high concentrations of these highly reactive chemicals. In this review, we focus on plant pathogenic bacteria of the genus Pseudomonas and the ways in which they overcome the challenges posed by ROS. We also explore the ways in which pseudomonads may exploit plant ROS generation for their own purposes and even produce ROS directly as part of their infection mechanisms.

Introduction: the importance of reactive oxygen in plant–pathogen interactions

  1. Top of page
  2. Abstract
  3. Introduction: the importance of reactive oxygen in plant–pathogen interactions
  4. Tolerating ROS
  5. Extracellular polysaccharides and intracellular polyesters
  6. Reactive oxygen in pathogenicity and virulence
  7. Concluding remarks
  8. References

The interaction between plant pathogens and their hosts is complex. This complexity arises as a result of a long-standing evolutionary battle in which the pathogen attempts to invade and multiply and the plant attempts to recognize and defend itself from this invasion. The pathogen must then take steps to escape detection or to avoid triggering a response, which will prevent its entry into, or proliferation within, plant tissues. One of the earliest and best-characterized responses of a plant to pathogen invasion is known as the oxidative burst. High concentrations of reactive oxygen species (ROS) are produced at the plasma membrane in the vicinity of the pathogen (Doke, 1983; Lamb & Dixon, 1997; Wojtaszek, 1997). Although ROS are produced as part of normal metabolism during both photosynthesis and respiration (Kim et al., 1999), the concentrations involved are of sufficient magnitude to overwhelm even the plant's own antioxidant defences for a time (Vanacker et al., 1998) and can prove toxic to invading pathogens (Peng & Kuc, 1992; Lamb & Dixon, 1997). Toxicity can occur via the oxidizing power of these ROS, which may attack haeme groups and Fe-S4 clusters (superoxide, inline image) or thiol groups (hydrogen peroxide, H2O2) in proteins (Mehdy, 1994). Further, the superoxide radical can act as a reducing agent towards metal ions in the Fenton reaction, leading to the production of hydroxide radicals (OH˙−, Imlay & Linn, 1988). The hydroxide radical is a strong oxidizing agent and can cause lipid peroxidation and damage to proteins and other cell components (Mehdy, 1994).

In plant defences, ROS not only act as toxins, able to directly kill or slow the growth of the pathogen, but also as part of a signalling cascade which may lead to multifarious defences including the hypersensitive response (Tenhanken et al., 1995; Torres et al., 2005), cell wall modifications (e.g. Bradley et al., 1992) and changes in gene expression (Alvarez et al., 1998). The importance of oxidative signalling in defence is illustrated by a recent study showing that induction of the oxidative signal-inducible1 (OXI1) serine/threonine protein kinase correlates both spatially and temporally with the oxidative burst in Arabidopsis and that OXI1 null mutants and overexpressor lines are more susceptible to Pseudomonas syringae (Petersen et al., 2009).

A large literature is dedicated to the study of the methods used by plant pathogens to avoid detection by the plant immune system and thus escape the oxidative burst. In the case of plant pathogenic bacteria, such as P. syringae, the type three secretion system (T3SS), encoded by hrp genes, is used for this purpose. The T3SS allows the bacteria to deliver effector proteins [type III secreted effector proteins (T3SE)], some of which delay or inhibit the plant's defence responses, including the production of ROS (Grant et al., 2006). Some T3SE localize to the chloroplasts and mitochondria (Bretz & Hutcheson, 2004), locations at which ROS may be generated. Further evidence that the T3SS may be used in manipulating plant ROS-based defences has been provided by Navarro et al. (2004), who found that five genes involved in ROS production in Arabidopsis may be targeted by T3SE secreted by P. syringae pv. tomato and P. syringae pv. maculicola, both of which are able to cause disease on Arabidopsis. However, it is important to note that the production of ROS also occurs in compatible reactions between plant and pathogen, in which T3SE are successfully deployed and disease develops (Kim et al., 1999; Santos et al., 2001), albeit to a lesser extent than during an incompatible, nonhost reaction. Moreover, a recent study by Block et al. (2010) indicates that the effector HopG1a of P. syringae targets mitochondrial function, leading to increased ROS production, rather than suppression of ROS.

An additional and relatively unexplored role for ROS tolerance in plant–pathogen interactions is suggested by studies of bacterial cell death mechanisms in response to bactericidal antibiotics. Kohanski et al. (2007) have shown that bactericidal antibiotics belonging to the quinolone, aminoglycoside and β-lactam family induce production of hydroxyl radicals as the end product of an oxidative cell death pathway in bacteria. This results in damage to DNA, membranes and proteins, and induction of oxidative stress responses. Bacteria impaired in the ability to tolerate oxidative stress show increased sensitivity to these antibiotics. Similarly, Bizzini et al. (2009) have shown that superoxide dismutase (SOD) mutants of Enterococcus faecalis show increased sensitivity to β-lactams and glycopeptides; Gusarov et al. (2009) have shown that SOD mutants of Bacillus subtilis are more sensitive to the Pseudomonas aeruginosa toxin pyocyanin. Gusarov et al. also show that amelioration of oxidative stress in B. subtilis by nitric oxide alleviates antimicrobial activity. ROS tolerance may therefore play a key role not only in pathogen resistance to plant-derived ROS but also in resistance to plant-derived antimicrobial chemicals and other chemical stressors encountered in the plant environment, such as antibiotics produced by plant-associated bacteria and fungi. Thus, the ability to tolerate elevated levels of ROS is likely to be important for all plant pathogenic pseudomonads.

Tolerating ROS

  1. Top of page
  2. Abstract
  3. Introduction: the importance of reactive oxygen in plant–pathogen interactions
  4. Tolerating ROS
  5. Extracellular polysaccharides and intracellular polyesters
  6. Reactive oxygen in pathogenicity and virulence
  7. Concluding remarks
  8. References

As ROS are a common feature of plant defences and bacterial cell death mechanisms, it is likely to be advantageous for any pathogen to be able to resist their effects. Mechanisms for resistance to toxins generally fall into four main categories: exclusion, export, modifications to the target site of the toxin, and enzymic or chemical inactivation of the toxin (Duffy, 2003; Mergeay et al., 2003). In the case of ROS, regulation of the uptake and sequestration of metal ions, particularly Fe(II), can also have a substantial effect on ROS tolerance, as Fe(II) participates in the Fenton reaction that generates the destructive hydroxyl radical (Cornelis et al., 2011). Mutation of specific residues, particularly cysteine residues, can affect the sensitivity or regulatory responses of individual proteins to ROS (e.g. Panmanee et al., 2006; Chen et al., 2006, 2008). However, in general, target site modifications and export mechanisms are likely to provide relatively little protection against high concentrations of ROS, which are not specific to a particular target site, but are able to react with numerous sites in proteins, as well as damaging other cellular components (Mehdy, 1994). Therefore, a common first line of defence is the use of antioxidant enzymes.

Antioxidant enzymes known to be present in Pseudomonas include superoxide dismutase (SOD), an enzyme capable of producing hydrogen peroxide from the superoxide radical. Three types of SOD exist in bacteria, distinguished by their metal cofactors: Mn/Fe, Cu-Zn and Ni (Kim et al., 1999). Protection from hydrogen peroxide is provided by the hydrogen peroxide-degrading enzyme catalase and also peroxidases (Albert et al. 1986; Hasset & Cohen, 1989). Genome sequence analyses indicate that the plant pathogen P. syringae pv. tomato DC3000 possesses three SODs (Mn-SOD, Fe-SOD and Cu-Zn-SOD), three catalases and six peroxidases (Buell et al., 2003). The opportunistic pathogen P. aeruginosa possesses two SODs (Mn-SOD and Fe-SOD), three catalases and four peroxidases (Ochsner et al., 2000). Notably, both P. syringae and P. aeruginosa contain catalases that are known or predicted to have a periplasmic or extracellular location, potentially providing a first line of defence against ROS (Klotz & Hutcheson, 1992; Brown et al., 1995; Klotz et al., 1995). The Cu-Zn SOD present in P. syringae is also predicted to have a periplasmic or extracellular location. The periplasmic and extracellular catalases produced by P. aeruginosa have been reported to show a high level of stability, either alone or in association with other proteins such as the ankyrin AnkB, which may enhance their efficacy during pathogenesis (Howell et al., 2000; Shin et al., 2008).

While ROS-degrading enzymes are common in pathogen genomes and may act as virulence factors (Soto et al., 2006), their importance for bacteria is not entirely understood, and some studies have provided conflicting evidence about their role in ROS tolerance. For instance, induction of SOD expression is correlated with improved survival of oxidant challenge, and bacteria with SOD genes knocked out are more susceptible to such challenge (Touati, 2002). However, work by Scott et al. in 1987 showed that Escherichia coli transformed with multiple copies of the gene for Fe-SOD were more easily killed by the superoxide generator, paraquat (methyl viologen). Further work by the same authors found that E. coli mutants lacking SOD genes were sometimes more resistant to ionizing radiation, whereas those with increased SOD levels were more sensitive (Scott et al., 1989). Nevertheless, SOD mutants of P. aeruginosa have been found to be less viable and to have less resistance to paraquat, as well as less virulence on silkworm (Bombyx mori; Iiyama et al., 2007). The virulence of P. aeruginosa in mice has also been shown to be correlated with SOD activity (Goto et al., 1991).

Although SOD activity has been confirmed to be important for Pseudomonas pathogenesis in animal models, evidence for a role for SOD activity during plant pathogenesis is less clear. The pathogenicity of P. syringae pv. syringae B728a was found to be unaffected in SOD mutants lacking both Fe- and Mn-SOD activity (Kim et al., 1999). However, it is possible that the Cu-Zn SOD produced by this strain is sufficient to protect P. syringae from superoxide toxicity in plant leaves. Interestingly, interrogation of the Pfam database (Finn et al., 2010) shows that Cu-Zn SODs are not only present in plant pathogenic strains of P. syringae but also predicted to be present in a wide range of plant pathogenic and plant symbiotic bacteria, including Agrobacterium spp., Rhizobium spp., Xanthomonas spp., Ralstonia solanacearum, Burkholderia spp. and Pectobacterium atrosepticum, suggesting that these enzymes play a broadly conserved and important role in plant pathogenesis. Nevertheless, other types of SOD have been shown to be important in some plant–pathogen interactions, as the soft-rot pathogen Dickeya dadantii (Erwinia chrysanthemi) 3937 has been shown to require Mn-SOD activity for the successful maceration of Saintpaulia ionantha leaves, although interestingly the Mn-SOD mutant retained the ability to macerate potato tubers (Santos et al., 2001). It seems likely that the relative importance of different antioxidant enzymes varies according to environmental factors such as pH and metal ion availability. Possession of multiple antioxidant enzymes that vary in terms of substrate, cofactor and optimal environmental conditions enables plant pathogenic Pseudomonas to colonize a range of different environments and to adapt to the changing environment present in healthy and diseased plant tissue.

One environment that is less frequently considered in the context of plant pathogenesis is the environment encountered during dispersal. P. syringae and related pathogens are commonly dispersed in aerosols, which carry an inherent risk of dessication and subsequent accumulation of ROS within the cell (Cox, 1989). By demonstrating that exogenous catalase can significantly enhance the ‘resuscitation’ of airborne bacteria cells, including P. syringae cells, Marthi et al. (1991) have shown that antioxidant enzymes are likely to be important not only during pathogenesis but also during the dispersal of pathogenic bacteria.

Extracellular polysaccharides and intracellular polyesters

  1. Top of page
  2. Abstract
  3. Introduction: the importance of reactive oxygen in plant–pathogen interactions
  4. Tolerating ROS
  5. Extracellular polysaccharides and intracellular polyesters
  6. Reactive oxygen in pathogenicity and virulence
  7. Concluding remarks
  8. References

Another important factor in a bacterial pathogen's ability to withstand the oxidative burst is its coating of extracellular polysaccharides (EPS), which act to protect the bacterium against oxidative stress. Examples of EPS found in Pseudomonas species include alginate and levan (Fett & Dunn, 1989; Fett et al., 1989; Chang et al., 2007). EPS can be very complex and can differ greatly between related pathogens, which may be related to their role in bacteria–host interactions, and the pathogen's need to escape detection (de Pinto et al., 2003; Silipo et al., 2010). In P. syringae pv. syringae, EPS has been shown to have a role in leaf colonization and symptom development (Yu et al., 1999); the EPS of P. syringae and P. aeruginosa are known to be upregulated by exposure to ROS (Keith & Bender, 1999). Keith et al. (2003) studied the expression of the algD gene, involved in alginate production, in planta, and found evidence that this gene is upregulated in response to ROS produced by the plant and that this induction of alginate production occurs in both compatible and incompatible plant–pathogen interactions (Keith et al., 2003). In P. syringae pv. syringae B728a, EPS production has been shown to be regulated via quorum sensing (Quiñones et al., 2005). Mutants impaired in quorum sensing lack alginate and have increased sensitivity to ROS, providing further evidence for the importance of EPS in withstanding oxidative stress (Quiñones et al., 2005). The activities of antioxidant enzymes and EPS in bacterial responses to ROS-stress are illustrated in Fig. 1.


Figure 1. Summary of interactions between bacterial ROS tolerance mechanisms and host ROS-based defences. ROS, including H2O2 and inline image, are produced at the plasma membrane of plant cells following detection of a pathogen (1). These ROS have antimicrobial activity, causing damage to bacterial protein, DNA and membranes (2). inline image can also participate in Fenton reactions, leading to the generation of highly reactive OH˙− radicals, causing further damage (3). Bacterial defences include EPS (4) and periplasmic catalase (5), which can neutralize ROS prior to their entering the bacterial cell. Once inside the cell, ROS may be disarmed by cytoplasmic catalase (6) and SOD (7).

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A second set of polymers that have been shown to affect oxidative stress tolerance in Pseudomonas are polyesters, such as poly(3-hydroxyalkanoate) (PHA). PHAs are accumulated as discrete granules and are believed to play a role in carbon storage and stress tolerance (Madison & Huisman, 1999; Castro-Sowinski et al., 2010). Pseudomonads do not generally produce the most widely studied PHA, poly(3-hydroxybutryate) but do produce a variety of medium chain length PHAs (Huisman et al., 1989; Kessler & Palleroni, 2000). PHA synthesis has been shown to enhance the tolerance of pseudomonads to a range of different stresses, including cold and oxidative stress (Ayub et al., 2009; Castro-Sowinski et al., 2010), although the molecular mechanisms underpinning the positive association between PHA accumulation and oxidative stress tolerance are not yet fully understood.

Reactive oxygen in pathogenicity and virulence

  1. Top of page
  2. Abstract
  3. Introduction: the importance of reactive oxygen in plant–pathogen interactions
  4. Tolerating ROS
  5. Extracellular polysaccharides and intracellular polyesters
  6. Reactive oxygen in pathogenicity and virulence
  7. Concluding remarks
  8. References

Thus far, this review has focussed on the concept of bacteria defending themselves against the plant host's ROS production. However, pathogenic pseudomonads are also capable of utilizing ROS for their own ends. For example, several pathovars of P. syringae produce a phytotoxin known as coronatine, which is known to be necessary for full virulence of this pathogen (Bender et al., 1987; Uppalapati et al., 2008). Coronatine has a number of functions in planta, including acting as a mimic of the plant hormone methyl jasmonate to antagonistically suppress salicylate-based defences (Zhao et al., 2003). It is also known to be involved in symptom development, causing a chlorotic halo around the infection site, owing to a loss of chlorophyll a and b contents (Ishiga et al., 2009). Loss of chlorophyll is correlated with a large reduction in the efficiency of photosytem II, owing to a coronatine-induced downregulation of genes involved in chlorophyll synthesis, photosystem proteins, oxygen-evolving complex proteins and the Calvin cycle, as well as the induction of chlorophyllase (Ishiga et al., 2008). It has recently been found that this loss of photosynthetic ability is associated with the light-dependent generation of ROS and downregulation of thylakoid Cu-Zn SOD activity. This ROS generation appears to be necessary for the development of the necrotic lesions that characterize the bacterial speck disease caused by this pathogen (Ishiga et al., 2008). In conjunction with this, coronatine induces many genes involved in tomato ROS homeostasis and suppresses SOD at the thylakoids, increasing the amount of ROS accumulated (Uppalapati et al., 2008). Meanwhile, coronatine upregulates SOD in the cytosol, probably reducing the pathogen's own exposure to ROS (Ishiga et al., 2008). Similarly, both coronatine-producing and nonproducing strains of P. syringae have been shown to induce production of the plant hormone ABA and to increase plant sensitivity to ABA (de Torres-Zabala et al., 2007; Goel et al., 2008; Rico et al., 2010). ABA acts through ROS-dependent signal transduction pathways to regulate stomatal closure and environmental stress responses (Zhang et al., 2009), and high levels of ABA have been shown to alter plant susceptibility to infection (de Torres-Zabala et al., 2007; Goel et al., 2008).

It has been shown in some interactions that the bacterium itself produces ROS that contribute to pathogenicity. For example, Mahajan-Miklos et al. (1999) identified a gene in the opportunistic pathogen, P. aeruginosa PA14, which is essential for fast killing of the nematode, Caenorhabditis elegans, and is also involved in pathogenicity on Arabidopsis. This gene encodes a phenazine toxin, pyocyanin, which leads to the production of superoxide and hydrogen peroxide under aerobic conditions (Mahajan-Miklos et al., 1999). The authors were able to provide evidence that ROS production was important for the pathogenicity effect. More recently, it has been shown that pyocyanin produced by P. aeruginosa directly inactivates catalase in the human lung epithelium via superoxide production (O'Malley et al., 2003) and that the ROS produced by pyocyanin in human cells can inactivate vacuolar ATPase (Ran et al., 2003). Given the overlap between genes involved in pathogenicity of P. aeruginosa on Arabidopsis and other hosts (Mahajan-Miklos et al., 1999), it seems likely that similar mechanisms may also be important in planta.

Concluding remarks

  1. Top of page
  2. Abstract
  3. Introduction: the importance of reactive oxygen in plant–pathogen interactions
  4. Tolerating ROS
  5. Extracellular polysaccharides and intracellular polyesters
  6. Reactive oxygen in pathogenicity and virulence
  7. Concluding remarks
  8. References

It is clear that ROS play a key role in plant–pathogen interactions; they are used by plants as a weapon against pathogens via direct toxicity and are important effectors in bacterial cell death mechanisms. Successful pathogens must therefore be able to tolerate this threat. But plants also use ROS in signalling, which bacteria may be able to manipulate for their own ends or to downregulate to avoid further defence responses. In a final twist, it appears that some Pseudomonas pathogens may even use ROS as a pathogenicity or virulence factor during interactions with plants. A summary of the ways in which various groups of Pseudomonads interact with ROS is given in Table 1. Further work is needed to fully illuminate a number of the areas covered in this review. For instance, the role of PHAs in ROS tolerance remains opaque. Similarly, more insight could be sought into the ways in which plant pathogenic Pseudomonads manipulate plant ROS homeostasis, and the importance of this manipulation for pathogenesis. There is yet to be a full understanding of the consequences of the changes observed in infected plants in this complex and dynamic process. Recent developments such as the demonstration of the connection between HopG1a and ROS production indicate the potential for research in this area to improve our understanding of plant–pathogen interactions.

Table 1. Strategies employed by different groups of Pseudomonas in tolerating and exploiting ROS
StrategyMechanismPlant pathogens (e.g. P. syringae)Rhizosphere Pseudomonas (e.g. P. putida)Opportunistic pathogens (e.g. P. aeruginosa)
  1. a

    Buell et al. (2003);

  2. b

    Katsuwon & Anderson (1989);

  3. c

    Klotz & Hutcheson (1992);

  4. d

    Brown et al. (1995);

  5. e

    Goto et al. (1991);

  6. f

    Keith et al. (2003);

  7. g

    Chang et al. (2007);

  8. h

    Ishiga et al. (2008);

  9. i

    Mahajan-Miklos et al. (1999);

  10. j

    O'Malley et al. (2003).

ROS toleranceCytoplasmic catalaseYesaYesbYesb
Periplasmic catalaseYescYescYesd
ROS production by host or pathogen YeshYesi
Manipulation of host ROS homeostasis Yesh,iYesi,j


  1. Top of page
  2. Abstract
  3. Introduction: the importance of reactive oxygen in plant–pathogen interactions
  4. Tolerating ROS
  5. Extracellular polysaccharides and intracellular polyesters
  6. Reactive oxygen in pathogenicity and virulence
  7. Concluding remarks
  8. References
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