Studies into the mechanisms of volatile emission in plants revealed that herbivory induces them to be released locally at the site of damage and then systemically from undamaged leaves adjacent to those that have been eaten. Soluble compounds transported in the phloem or xylem, gases dispersed by diffusion in the apoplast, as well as electrical and hydraulic signals transmitted by the vascular system have all been suggested as mediating systemic induced resistance against insect attack (Malone 1996; de Bruxelles and Roberts 2001). However, it is still not entirely clear which are the genuine signals responsible for plants systemic responses, nor how they regulate volatile emission (Orians 2005).
The "myriad plant responses to herbivores" have been excellently reviewed by Walling (2000), and several studies have addressed the question of how plant responses to herbivory are controlled at the molecular level (Arimura et al. 2000; Baldwin et al. 2001; Kessler and Baldwin 2002; Fäldt et al. 2003a; Belkhadir et al. 2004). In particular, the salicylic acid-dependent and jas-monic acid/ethylene-dependent signalling pathways have been given much attention (Kunkel and Brooks 2002).
It has been repeatedly demonstrated that the exogenous application of jasmonic acid (JA) to plants causes them to emit volatile blends similar to those released in response to insect feeding, e.g. on conifers (Franceschi et al. 2002; Hudgins et al. 2004), and also for elms (Sect. 10.5). Jasmonic acid is produced via the octadecanoid pathway from linolenic acid, and its role as wound signal has been demonstrated in many plant systems (Karban and Baldwin 1997; Farmer et al. 2003), although it should be noted that jasmonates have many other roles in plants other than just wound signaling (Creelman and Mullet 1997; Cheong and Choi 2003).
In addition, many compounds other than jasmonic acid are involved in mediating plant defense responses (Arimura et al. 2005), including: changes in free calcium and oxidative bursts at the site of injury (Nürnberger and Scheel 2001; Moran et al. 2002); various other forms of jasmonates, including the volatile methyl jasmonate (Cheong and Choi 2003; Farmer et al. 2003); lipid based compounds other than jasmonate (Weber 2002; Farmer et al. 2003); ethylene and salicylic acid (Pieterse and van Loon 1999; Wang et al. 2002); systemin and prosystemin or possibly other oligo-peptides (Ryan et al. 2002; Takayama and Sakagami 2002); and oligosaccharides (Nürnberger and Scheel 2001).
From all this, it should be clear that a plants complete response to insect attack is very complex indeed and that jasmonates are probably not involved in the initial detection and local response to insect attack, but rather are components of the long-distance signals emanating from the region of the attack, stimulating appropriate systemic responses in the rest of the plant (Stratmann 2003). Farmer et al. (2003) made the interesting suggestion that plants probably use different signal compounds or signal ratios rather like musical notes or codes, each specific to particular types of injury. Insect herbivores also attempt to evade or manipulate such signals, presumably to confuse their host plants defense responses (Dodds and Schwechheimer 2002; Arimura et al. 2005), which might explain the finding that the eggs and neonate larvae of many lepidopteran insects contain significant concentrations of jasmonic acid (Tooker and de Moraes 2005).
Although there is now a substantial literature relating to plant wound signaling as briefly summarized above, it needs to be emphasized that it is still far from clear how such signals are physically transmitted around a plant in anything resembling a coherent manner (Malone 1996; Orians 2005), let alone in anything as large as a tree. Furthermore, it should be noted that these studies have been conducted using many different plant species, often with crop plants and their pests, which may be responsible for some of the apparent contradictions in the literature relating to plant defense responses and signaling. This underlines the importance of comparing results within each species, and then contrasting the data to results obtained with wild species such as trees and their natural herbivores, before trying to draw wider conclusions.
The defensive responses of field elms to egg laying by the specialized leaf beetle Xanthogaleruca luteola is an especially instructive example. The localized scratching on leaves by gravid female beetles prior to egg laying does not elicit the emission of a specific volatile blend from the tree, nor does similar scratching with a scalpel blade, but the application of egg masses to these scratches does. Furthermore, since watering cut elm twigs with jasmonic acid stimulated the emission of a similar volatile blend to that which occurs in response to egg laying by X. luteola; this implies that scratching alone does not result in a sufficient release of jasmonate to initiate a defense signal within the plant, but that a specific elicitor is additionally required.
From this, it is reasonable to propose that there must be a network of receptors and molecular regulators initiating and controlling systemic wound signaling within plants (Wasternack and Parthier 1997; Moran et al. 2002; Morris and Walker 2003; Rakwal and Agrawal 2003; Arimura et al. 2005; Lorenzo and Solano 2005). Indeed, the sensitivity of plants to potential insect herbivores was further demonstrated by Bown et al. (2002), who showed that within seconds of herbivorous insect larvae merely walking over tobacco and soybean leaves, changes in cellular Ca2+ levels occurred, along with an oxida-tive burst and an increase in chlorophyll fluorescence, finally resulting in local increases in putative defense signaling compounds.
This is particularly interesting because similar changes in Ca2+ levels along with an electrical depolarization were observed by Maffei et al. (2004), in lima bean leaves that had been partially eaten by the Mediterranean cutworm Spodoptera littoralis. These effects spread through the attacked leaf and preceded the plants' systemic responses.
Such changes in a chewed on leaf's electrical potential could be the first local or systemic signal of insect related damage as suggested by Maffei et al. (2004) but contradicting previous data (Malone 1996), or be occurring as a consequence of an abrupt de-coupling of the photosynthetic mechanisms, which would also explain the apparent increase in leaf fluorescence observed by Bown et al. (2002).
It is not obvious why photosynthesis should be disengaged quite so promptly in response to herbivore contact, unless the maintenance of the redox potentials it generates interferes with wound signaling, if changes in the electrical potentials of wounded leaves really are signals (contrary to Malone 1996). Alternatively, some secondary metabolic compounds are induced when plants are exposed to insects are produced in the plastid, possibly necessitating a diversion of the organelles biosynthetic machinery to such purposes.
Despite these uncertainties, however, it is still viable to hypothesize that networks of surveillance receptors are activated in plants by wounding and exposure to elicitors characteristic of the insects or pathogens (Morris and Walker 2003; Parker 2003; Arimura et al. 2005), presumably in the first instance immediately proximal to the site of any damage. Depending upon the precise permutation of receptors activated, these then initiate a cascade of local tissue responses, including fast defense responses and the release or amplification of a systemic signal code by neighboring tissues, which then activate systemic acquired resistance mechanisms in the rest of the plant (Arimura et al. 2005), as appropriate and as the plant is capable of producing. Presumably there must also be some means of measuring the signals initiated, "cross-talk" between the different signal pathways in the event of complex situations (Maleck and Dietrich 1999; Kunkel and Brooks 2002; Lorenzo and Solano 2005), and some kind of feed-back mechanism to attune the defensive response according to need and damp out old signals (Arimura et al. 2005).
This said, however, Mithofer et al. (2005) observed that patterns of volatile release in lima bean plants occurring in response to repeated small scale mechanical damage that mimicked herbivore feeding patterns were very similar to those released after actual herbivory by S. littoralis or the snail Cepaea hortensis or methyl jasmonate treatment. This may indicate certain generalized defense responses can still be activated even in the absence of specific herbivore related signals, provided they are sufficiently activated and/or if repeated small doses of jasmonates accumulate as can be released by mechanical wounding (Arimura et al. 2005). Herbivores and pathogens also come in many combinations other than just insects alone (Karban and Baldwin 1997; Maleck and Dietrich 1999), and so a plant must be capable of responding in a coordinated manner to all the biotic and abiotic stresses that it is likely to encounter during its lifetime.
Nevertheless, a sophisticated network of receptors is clearly important for activating and controlling plant defense and signaling responses (Kunkel and Brooks 2002; Rathjen and Moffett 2003; Morris and Walker 2003; Lorenzo and Solano 2005). The most studied examples are the 'gene for gene' resist-ance/avirulence responses of Pseudomonas syringae when it attacks arabidopsis or tomato (McDowell and Woffenden 2003; Parker 2003).
The 'avirulence' determinants of P. syringae, often proteases, are probably better termed 'elicitors', which if detected by the host plant through its network of receptors can initiate a defense response, although similar phenomena are being studied in other plant pathogen relationships too, including for viruses and fungi (Parker 2003). If the host lacks the appropriate receptor and/or the pathogens suite of elicitors has changed, then it will not be detected and the attack will probably succeed (McDowell and Woffenden 2003).
Five classes of these putative receptors are recognized, in addition to protein kinases which are thought to be involved in regulating their activity (Rakwal and Agrawal 2003; Morris and Walker 2003). Literally hundreds of these putative 'R' genes and related receptors have been identified in arabidopsis, only a handful of which have been assigned even a putative function (Nürnberger and Scheel 2001; Belkhadir et al. 2004). Long lived organisms such as trees with their ecologically complicated lifestyles, are hardly likely to have less.
Many of these are probably necessary for plants to regulate their own wound and other systemic signals, but others are probably specific for the more common microbial pathogens and insect herbivores (Morris and Walker 2003; Parker 2003). The precise suite activated is presumably responsible for each observed response, including systemic acquired resistance and the release of herbivore specific volatile blends (Arimura et al. 2005). This theory partially explains why in the event of being exposed to a novel insect herbivore or pathogen, trees often respond in an ineffectual manner or even not at all (Sect. 10.10; Dodds and Schwechheimer 2002; McDowell and Woffenden 2003).
For all these reasons, the genes responsible for these receptors and related signaling pathways, are likely to be of great interest to those working on the defense responses of plants and trees for some time to come. However, because they are likely to be constitutively expressed, associating them definitively with a particular foreign organism will be as difficult as for any other constitutively expressed defense trait. Indeed, since receptors are the very modulators of the defense responses and signaling cascades, their interactions are likely to occur at the protein-protein and protein-ligand level, which are much harder to study than changes in gene expression, therefore unraveling the full extent of their role will be problematic for some time to come, even for arabidopsis.
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