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Alcaligenes denitrifi cans (Basnayake & Birch, 1995), detoxifi cation of fusaric acid from
Fusarium species by proteins from Ralstonia solonacearum (Toyoda et al ., 1988) and
production of the antifungal metabolite, cladosporol, by Cladosporium tenuissima that
inhibits
-1,3-glucan biosynthesis, thereby preventing growth of Cronartium fl accidum
and Peridermum pini (Moricca et al. , 2001).
β
3.2.4
Induced resistance
Induced resistance, defi ned as 'the process of active resistance dependent on the host
plant's physical or chemical barriers, activated by biotic or abiotic agents (inducing
agents)' (Kloepper et al ., 1992), has been a major area of recent research (see Chapter 4).
Biological control involves microorganisms as the inducers and a combination of
experiments involving spatial or temporal separation between inducer microorganisms and
the pathogen has enabled this mode of action to be identifi ed, even though inducers may
exhibit other modes of actions in the same pathosystem. Use of mutants lacking expres-
sion of other modes of action has also helped to identify a role for induced resistance.
Bacteria, fi lamentous fungi and yeasts have all been shown to exhibit induced resistance
in the phyllosphere, rhizosphere, spermosphere and post-harvest environments, with
individual isolates or species showing activity against a number of viral, bacterial and
fungal plant pathogens, either locally or systemically (Wilson et al ., 1994; Whipps, 2001;
Kloepper et al ., 2004; Compant et al ., 2005a; Jacobsen, 2006; Woo et al ., 2006; Bakker
et al ., 2007). Some well-established examples of microorganisms exhibiting induced
resistance include bacteria such as Bacillus spp. (Bargabus et al ., 2002, 2003; Collins &
Jacobsen, 2003; Kloepper et al ., 2004), Pseudomonas spp. (van Peer et al ., 1991; Bakker
et al ., 2007; Weller, 2007) and Lysobacter enzymogenes (Kilic-Ekici & Yuen, 2003) and
fungi such as Trichoderma spp. (Yedidia et al ., 2003; Shoresh et al ., 2005; Woo et al .,
2006), Fusarium spp. (Fravel et al ., 2003), mycorrhizal fungi (Whipps, 2004), binucle-
ate Rhizoctonia isolates (Jabaji-Hare & Neate, 2005) and the fungus-like Straminopile
Pythium oligandrum (Benhamou et al ., 1997).
The mechanisms involved in resistance induced by biocontrol microorganisms, largely
determined from studies on bacteria, appear to differ subtly to those involved with abiotic
inducers and necrotising pathogens. The former (termed induced systemic resistance
(ISR)) generally involves ethylene and jasmonate signalling along with expression of the
regulatory gene NPR1 and the latter (termed systemic acquired resistance (SAR)) involves
salicylate (SA) signalling with activation of pathogenesis-related (PR) proteins (Bakker
et al ., 2003). However, these separations are not absolute. For example, there is cross-talk
between the signalling pathways (van Loon & Glick, 2004), and some Pseudomonas spp.
apparently can induce SA-dependent signalling by producing small amounts of SA in the
rhizosphere (de Meyer et al. , 1999) although this behaviour has been challenged (Ran et al .,
2005b). In addition, some Bacillus spp. exhibit ISR dependent on SA, but independent of
jasmonate and expression of NPR1 (Ryu et al. , 2003; Kloepper et al ., 2004). Interestingly,
induced resistance involving Trichoderma spp. seems to involve the jasmonate/ethylene
signalling pathway (Shoresh et al ., 2005) similar to ISR in most bacteria. Consequently, to
ease description the general term induced resistance is used here.
Numerous physiological changes have been associated with microbially induced
resistance. These include (a) strengthening of epidermal and cortical walls and deposition
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