Mechanisms of plant response to pathogens

Plant disease resistance is dependent on the genetic background of both host and pathogen and relies on a series of complex mechanisms of molecular recognition and signal transduction (Crute 1985). In general, plant resistance occurs in the following circumstances:

1. The pathogen fails to infect the plant because it belongs to a taxonomic group outside the host range of the pathogen (nonhost resistance). This is the most common form of resistance exhibited by plants.
2. The plant contains preformed physical and chemical barriers, which prevent pathogen penetration.
3. The plant recognises the presence of the pathogen and rapidly triggers an array of defence mechanisms, which involve differential gene expression (host resistance).

It is now clear that, in the latter type of resistance, disease susceptibility frequently results from poor pathogen perception, rather than a lack of host resistance machinery. Therefore, early recognition of the pathogen at the level of single cells is essential to mount an efficient defence response. Successful pathogen recognition triggers the activation of several and diverse defence responses. Sometimes, resistance is manifested at the macroscopic level by the appearance of necrotic lesions at the site of infection. This is the result of rapid localised cell death termed hypersensitive response (HR) which is thought to limit pathogen growth and spread. Early and local responses associated with the HR include the transient opening of ion channels, production of reactive oxygen species, cell wall fortification, production of antimicrobial pytoalexins, host cell death and synthesis of pathogenesis-related proteins (PRP), which are thought collectively to confer the observed resistance to bacterial, fungal and viral pathogens (Hammond-Kosack and Jones 1996).

In addition to localised responses, plants often induce defence mechanisms in uninfected areas. Defence responses at such secondary sites are collectively referred to as systemic acquired resistance (SAR). SAR can be distinguished from other inducible resistances based upon the spectrum of pathogen protection and the associated changes in gene expression. SAR is induced following infection by necrotising pathogens (e.g. Colletotrichum lagenarium, tobacco mosaic virus, etc.) or experimentally by treatments with salicylic acid (SA) (Stichter et al. 1997). SAR leads to induction of pathogenesis related (PR)s genes, such as glucanases and chitinases (Stichter et al. 1997) and confers a long lasting, broad-spectrum disease resistance that is dependent upon SA accumulation (Stichter et al. 1997). SA has been shown to have multiple roles and appears to be a common signalling molecule in both the HR and SAR responses (Malek and Lawton 1998).

A series of Arabidopsis mutants exhibiting a constitutive SAR have been identified (Bowling et al. 1997). They display high levels of PR gene expression, and broad-spectrum pathogen resistance (Bowling et al. 1997). Nevertheless, these mutants also displayed phenotypic alterations such as reduced size or altered morphology, which suggests that genetic manipulation for constitutive SAR in crop plants may result in yield losses. However, transfer of two bacterial genes coding for enzymes that convert chorismate into SA in tobacco plants resulted in overproduction of salicylic acid and enhanced resistance to viral and fungal infection (Verberne et al. 2000). The plants did not present any phenotypic alteration but genes encoding acidic pathogenesis-related (PR) proteins, were constitutively expressed.

In addition to the SA-dependent pathway, an SA-independent pathway has been identified and termed induced systemic resistance (ISR) (Pieterse et al. 1998). ISR is not associated with SAR gene expression and confers quantitative resistance (40–60% protection) to fungal and bacterial pathogens. Moreover, ISR is dependent on jasmonic acid (JA) and ethylene signalling (Knoester et al. 1999). The necrotrophic bacteria Erwinia carotovora, has been shown to induce expression of certain PR genes via an SA-independent, and potentially even SAantagonistic, pathway during an early phase of infection (Vidal et al. 1997). Similarly, infection of Arabidopsis with necrotrophs such as Alternaria brassicola leads to induction of thionin and defensin-like genes such as PDF1.2 (whose expression is SA-independent) but does not result in PR-1 induction (Penninckx et al. 1996). It is likely that the plant response to pathogen invasion involves a combination of the different mechanisms described (Somssich and Hahlbrock 1998). That may explain why different pathogens may induce the same defence mechanism (i.e. synthesis of PRP).