Induced disease resistance signaling in plants

To protect themselves from disease, plants have evolved sophisticated inducible defense mechanisms in which the signal molecules salicylic acid, jasmonic acid and ethylene often play crucial roles. Elucidation of signaling pathways controlling induced disease resistance is a major objective in research on plant-pathogen interactions. The capacity of a plant to develop a broad-spectrum, systemic acquired resistance (SAR) after primary infection with a necrotizing pathogen is well known and its signal transduction pathway extensively studied. Plants of which the roots have been colonized by specific strains of non-pathogenic fluorescent Pseudomonas spp. develop a phenotypically similar form of protection that is called rhizobacteria-mediated induced systemic resistance (ISR). In contrast to pathogen-induced SAR, which is regulated by salicylic acid, rhizobacteria-mediated ISR is controlled by a signaling pathway in which the phytohormones jasmonic acid and ethylene play key roles. In the past decade, the model plant species Arabidopsis thaliana has been extensively explored to study the molecular basis of systemically induced resistance. Here we review the current knowledge on induced disease resistance signaling in plants. 1. PLANT DISEASE RESISTANCE Non-host, basal and R-gene mediated resistance Plants are sessile organisms, incapable of fleeing from possibly harmful organisms. In order to defend themselves against pathogen attack, plants possess a range of constitutive and inducible resistance mechanisms. The most effective type is non-host resistance. This non-host resistance is expressed when a plant comes into contact with a pathogen which is incapable of provoking any disease in this plant (Heath 2002). In the absence of non-host resistance, the plant is susceptible. However, even susceptible plants are capable of reacting in a way that may slow down growth of the pathogen. The presence of such basal resistance was evidenced in Arabidopsis by the isolation of enhanced disease susceptibility (eds) mutants. These mutants showed increased susceptibility to moderately virulent pathogens such as Pseudomonas syringae (Glazebrook et al. 1996, Rogers and Ausubel 1997). Basal resistance is often dependent on the action of one or more of the plant hormones jasmonic acid (JA), ethylene (ET) and salicylic acid (SA). Upon attack, the levels of these hormones are usually enhanced. Such enhancement depends on the attacker that is trying to invade the plant, and each of the hormones act in the resistance against a specific set of pathogens. For instance, basal resistance against the oomyceteous pathogen Hyaloperonospora parasitica or the viral pathogen turnip crinkle virus was reduced in Arabidopsis mutants affected in pathogen-induced biosynthesis of SA. In contrast, it was not reduced in mutants impaired in JAor ET-signaling (Delaney et al. 1994, Thomma et al. 1998, Nawrath and Métraux 1999, Kachroo et al. 2000, Ton et al. 2002c). Conversely, JAand ET-signaling mutants showed enhanced susceptibility to the fungal pathogens Alternaria brassicicola and Botrytis cinerea, whereas SA-signaling mutants did not (Thomma et al. 1998, Thomma et al. 1999). Furthermore, ET-insensitive tobacco and Arabidopsis plants have been shown to be more susceptible to a range of necrotizing pathogens, e.g. B. cinerea, Pythium spp. and Fusarium spp. (Geraats et al. 2002). Some pathogens are resisted by a SA-dependent mechanism, as well as JAand ET-dependent mechanisms, e.g. Pseudomonas syringae pv. tomato DC3000 (Pst DC3000) and Xanthomonas campestris pv. armoraciae (Delaney et al. 1994, Pieterse et al. 1998, Ton et al. 1998, Ellis et al. 2002, Ton et al. 2002b). Certain pathogens are resisted by the hormones acting sequentially, e.g. Xanthomonas campestris pv. vesicatoria in tomato (O'Donnell et al. 2003). In this interaction, JA, ET and SA are required in succession. These results clearly demonstrate the intertwining of several signal transduction pathways in basal resistance. Moreover, it shows that the roles of different hormones vary depending on the plant-pathogen interaction. Within plant species, individuals can vary in their level of resistance to a certain pathogen, with some individuals being fully resistant. Such resistance can usually be described by a gene-for-gene relationship. A pathogen carrying a specific avirulence (AVR) gene is recognized only by a plant carrying a corresponding resistance (R) gene. In such an incompatible interaction, the pathogen usually triggers a rapid and local defense response that leads to a hypersensitive reaction. The hypersensitive reaction is often regarded as a form of programmed cell death that Verhagen et al. Induced defense signaling is dependent on e.g. reactive oxygen species. The resulting small necrotic lesion is involved in preventing the pathogen from spreading any further (Dangl et al. 1996). Furthermore, deposition of anti-microbial compounds, strengthening of cell walls and expression of defense-related genes in the vicinity of the lesion all contribute to the restriction of the pathogen (Hammond-Kosack and Jones 1996). Non-host resistance, basal resistance and R-gene mediated resistance play an important role in the plant’s innate immune response. The mechanisms involved in these types of disease resistance have been extensively reviewed (Slusarenko et al. 2000). This review focuses on induction, signaling and expression of systemically induced, broad-spectrum disease resistance. 2. INDUCED DISEASE RESISTANCE 2.1. Biological and chemical induction of disease resistance During evolution plants have developed sophisticated defensive strategies to perceive pathogen attack and to translate this perception into an appropriate adaptive response. When under attack, a plant is capable of enhancing its resistance, and this condition is often referred to as induced, or acquired, resistance. Acquired disease resistance is thought to involve an enhancement of basal resistance (Van Loon 2000, Ton et al. 2002b). A classic example of biologically induced disease resistance is triggered after attack by a necrotizing pathogen (Ross 1961). This attack renders distant, uninfected plant parts more resistant towards a broad spectrum of virulent pathogens (Kuc 1982, Ryals et al. 1996, Sticher et al. 1997). The onset of this enhanced resistance, known as systemic acquired resistance (SAR), is accompanied by a local and systemic increase in SA levels (Malamy et al. 1990, Métraux et al. 1990). Subsequently, a large set of SAR genes, including genes encoding pathogenesis-related (PR) proteins, is up-regulated (Ward et al. 1991, Van Loon 1997, Van Loon and Van Strien 1999). These PR genes are often considered as marker genes for SAR expression. Several PR-proteins possess anti-microbial activity and are thought to contribute to the state of resistance attained. The PR proteins can accumulate to levels from 0.3 up to 1% of the total protein content of the leaf (Lawton et al. 1995). A large variety of chemicals have been shown to activate the SAR response. Benzothiadiazole (BTH), 2,6-dichloroisonicotinic acid (INA), and SA induce the same set of PR genes comparable to biologically-induced SAR (Ward et al. 1991, Uknes et al. 1992, Lawton et al. 1996). Using parsley cells as a model, SAR induction by the commercially available plant activator BION and the biological agent Milsana, as well as a large group of related chemicals, was demonstrated (Siegrist et al. 1998). A second, well-studied biologically-induced disease resistance occurs after root colonization by selected strains of non-pathogenic Pseudomonas spp. (Van Peer et al. 1991, Wei et al. 1991). This type of resistance is generally called rhizobacteria-induced systemic resistance (ISR, Pieterse et al. 1996, Van Loon et al. 1998). ISR has been demonstrated in different plant species against several pathogens under conditions where the rhizobacteria and the pathogen remained spatially separated (Van Loon et al. 1998, Pieterse et al. 2002). The expression of rhizobacteria-mediated ISR was shown to be independent of the presence of SA or enhanced PR-gene expression. Phenotypically, rhizobacteria-mediated ISR resembles pathogen-induced SAR. Although the terms SAR and ISR are synonymous (Hammerschmidt et al. 2001), for convenience we distinguish between pathogenand rhizobacteria-induced resistance by using the term SAR for the pathogen-induced type and ISR for the rhizobacteria-induced type of resistance. The non-protein amino acid β-aminobutyric acid (BABA) appears to have a different mode of action. Like ISR, it induces resistance without the expression of PR-genes (Cohen and Gisi 1994, Zimmerli et al. 2001). However, BABA can induce resistance to H. parasitica in Arabidopsis independent of SA, JA or ET, through a signaling pathway that requires abscisic adid (ABA) and involves priming for callose depositon (Ton and Mauch-Mani 2004, Ton et al. 2005). On the other hand, BABA-induced resistance against the bacterial pathogen Pst DC3000 and the fungal pathogen B. cinerea is SA dependent (Zimmerli et al. 2000, Zimmerli et al. 2001). 2.2. Systemic acquired resistance After local infection by a necrotizing pathogen leading to an HR, the enhanced state of resistance extends systemically into the uninfected plant parts. During the onset of SAR, a locally altered transcriptional response precedes the hypersensitive reaction and a second wave of transcriptional reprogramming, not apparent in a virulent attack, marks the transition from basal to induced resistance (de Torres et al. 2003). The induction of SAR is accompanied by local and systemic accumulation of endogenous levels of the plant hormone SA, followed by PR-gene expression (Malamy et al. 1990, Métraux et al. 1990). The importance of the accumulation of SA for the expression of SAR was demonstrated by using transgenic NahG plants. These plants express the bacterial salicylate hydroxylase nahG gene, making the