JXB Advance Access originally published online on December 12, 2003
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Journal of Experimental Botany, Vol. 55, No. 395, pp. 159-168, January 1, 2004
© 2004 Oxford University Press
Crosstalk: An Ecological Perspective |
Crosstalk between plant responses to pathogens and herbivores: a view from the outside in
Received 23 September 2003; Accepted 31 October 2003
1 Department of Biological Sciences, Lancaster Environment Centre, IENS, Lancaster University, Lancaster LA1 4YQ, UK
2 School of Plant Sciences, The University of Reading, Reading RG6 6AU, UK
* To whom correspondence should be addressed. Fax: +44 (0)1524 843854. E-mail: J.E.Taylor{at}Lancaster.ac.uk
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Abstract |
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Plants encounter numerous pests and pathogens in the natural environment. An appropriate response to attack by such organisms can lead to tolerance or resistance mechanisms that enable the plant to survive. Many studies concentrate on the signalling pathways that enable plants to recognize and respond to attack, and measure the downstream effect in either biochemical or molecular terms. At the whole plant level, ecologists examine the fitness costs of attack not only for the plant but also over a range of trophic levels. The links between these differing levels of study are beginning to be addressed by the adoption of molecular approaches in more ecologically relevant settings. This review will describe the different approaches used by ecologists and cell biologists in this field and will try to address the question of how we can explore the response to, and consequences, of attack by multiple enemies.
Key words: Crosstalk, herbivore, pathogen, peroxidase, Rumex obtusifolius, Uromyces rumicis.
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Introduction |
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‘Crosstalk’ may be defined as occurring when a common cellular component is used in more than one signal transduction chain and leads to an exchange of information between different signalling pathways. It is used in many cases to explain how two or more signalling pathways might interact and lead to different cellular outcomes. In ecological or agronomic terms the expression ‘crosstalk’ could be used to define quite a different process that exists at a very different level of organization. For example, if it is possible to consider ‘crosstalk’ between pathogen-induced and herbivore-induced signalling pathways, could not the same term be used when considering how the attack of a plant by one organism influences the whole plant response to simultaneous or subsequent attack by a different organism? However, the use of ‘crosstalk’ in this way may obscure two very different perspectives on the basic question of why ‘crosstalk’ merits investigation. In cellular terms, ‘crosstalk’ is studied to increase understanding of the control of signalling pathways and networks, and how they are regulated. Ecologically or agriculturally, ‘crosstalk’ is studied to address a whole series of issues about how a plant interacts with its environment. These issues include the question of whether plant responses to different environmental factors are independent of one another and, if they are not, do these interactions between responses have fitness consequences, either positive or negative? If the answer to this last question is yes, the next obvious question is, are these interactions subject to specific selection? In these ecological and agricultural terms interaction is the key term. Interactions may be based partly on ‘crosstalk’ as defined in cellular terms, but many other mechanisms are possible.
These very different questions are reflected in the different ways in which the specific disciplines of cell biology and ecology approach ‘crosstalk’. Cell biology concentrates on the detail of the signalling interactions, that are currently developing into ideas of signalling networks (Hetherington and Woodward, 2003). This can be seen as a ‘from the bottom-up’ approach. This is a fundamental contrast to the ‘from the top-down’ ecological approach that concentrates on the interactions between plant responses to different environmental factors, biotic and/or abiotic, and then uses the outcomes of such interactions to try to explore the underlying mechanisms.
In this review we will consider these different approaches, what information they can provide and the extent to which it is possible to bring them together to provide an integrated understanding of ‘crosstalk’ across a range of scales of organization. In doing so we will focus on one specific case of ‘crosstalk’, that is the interactions between herbivores and pathogens and a shared host plant, partly by references to our own studies of such ‘tripartite’ interactions (reviewed by Hatcher et al., 2003).
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‘Crosstalk’ at different scales of organization |
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We considered before (Paul et al., 2000) the different scales of organization at which tripartite interactions might be approached (Fig. 1). While this may be a simplified description, it provides a useful shorthand to examine the very different approaches of different disciplines.
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Cellular and molecular biologists typically consider the first three levels of organization: recognition, signalling pathways, and changes in gene expression. Whilst there seems little doubt that initial processes by which the host recognizes attack by a herbivore or pathogen are generally highly specific, there is increasing evidence for a lack of specificity in signalling and, especially, gene expression (see below). Ecologists and physiologists, at least in the context of plant–pathogen–herbivore interactions, deal with the last three scales: metabolic and physiological changes, effects on attackers, and overall effects on host fitness. These responses are generally interpreted in the context of changes in whole plant functions (e.g. loss of photosynthetic capacity or changes in bulk tissue chemistry such as C:N ratio), an approach that is consistent with the typical viewpoint of ecologists, who have only recently begun to consider the extent to which such events can be viewed in terms of signalling processes (see below). This is clearly a fundamental contrast with cell biologists who would view interactions between herbivores and pathogens from the perspective of specific signalling pathways, and how these affect downstream gene expression profiles. Both approaches are valid but they leave a ‘mechanism gap’ in that neither of these approaches directly addresses how the changes in gene expression lead to the phenotypic response of the plant. A few workers have attempted to bridge the gap by correlating altered gene expression with changes in pathogen or herbivore performance. However, even this correlative approach does not necessarily demonstrate the underlying mechanism, especially given the diversity of changes in gene expression, and the likely multi-component nature of resistance. In addition, neither the cell biology nor ecological approaches address the cumulative effect on the overall homeostasis of the plant, and the balancing act that the plant must adopt, in response to multiple stimuli in a natural environment.
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‘Crosstalk’ at the level of signalling pathways |
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There is evidence in the literature to indicate that when attacked by a pathogen or herbivore a plant might deploy, amongst other signals, salicylic acid (SA), jasmonic acid (JA) and other oxylipins, abscisic acid (ABA), and ethylene (Bostock, 1999; de Bruxelles and Roberts, 2001; Kessler and Baldwin, 2002) to induce a resistance response. Furthermore, none of these pathways is wholly specific to herbivory and/or disease. For example, the ABA signalling pathway is involved in the response of plants to pathogens (Audenaert et al., 2002; Mohr and Cahill, 2003), cold (Viswanathan and Zhu, 2002; Kim et al., 2002), drought (Uno et al., 2000), salt (Shi and Zhu, 2002; Zhu, 2002), high light (Fryer et al., 2003), heavy metals (Hsu and Kao, 2003), and, perhaps, herbivory (Schmelz et al., 1999). The involvement of multiple signals in response to multiple environmental stimuli has led to increasing acceptance of the concept that plants utilize signal networks not independent linear pathways, and the increasing evidence for complex signalling topology (Genoud and Metraux, 1999; Hetherington and Woodward, 2003) suggests that interactions between pathways may be the norm not the exception, even at the signalling level. The issue for plant cell biologists is how to investigate and analyse such complex signalling networks, while whole plant biologists are faced with, perhaps, the greater challenge of how increased understanding of such complex signalling networks can be related to whole plant phenotypic changes.
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‘Crosstalk’ at the level of gene expression profiles |
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Whether or not there is ‘crosstalk’ sensuo stricto between signalling systems there is increasing evidence for commonality in the gene expression profiles induced by different defence signalling pathways. A number of recent papers have tried to examine changes in the transcriptome in response to attack by pathogens and/or herbivores. Van Wees et al. (2003) have recently used expression profiling to examine the response of both wild-type Arabidopsis, and a range of mutants, to infection by the fungal pathogen Alternaria brassicicola. Plants demonstrated a dramatic response to infection within 12 h, at which time no lesions were visible and this response persisted for up to 36 h. Some 645 genes were induced and 265 of these required a functional JA signalling pathway. When compared with a previous report of expression profiling from the same laboratory in response to infection with Pseudomonas syringae (Glazebrook et al., 2003), it was clear that, despite the fact that resistance to both pathogens required different signalling processes, there were many genes that were induced by both pathogens. It was also evident that although these two pathogens could be considered as different stimuli, the genes that require a functional JA pathway do so irrespective of the nature of the attacking pathogen. The authors suggested, therefore, that the regulatory mechanisms controlling defence responses act similarly in response to different pathogens, and that the signalling network topology might be similar, irrespective of the type of pathogen studied. Further work by Schenk et al. (2003) again using A. brassicicola has used microarrays and RT-qPCR to examine not only the local response but also the systemic response. They were able to show that there was a substantial change in the expression of genes associated with signal transduction, cell wall synthesis and cellular housekeeping in distal tissues. In addition, particularly for defence-related transcripts, the time-course of induction was very similar for both local and systemic tissues, but the magnitude of induction in systemic tissues was limited compared to that at the site of inoculation. Hence it seems that a plant initiates a distant defence response, priming the plant for future attack, without investing excessive resource. Scheideler et al. (2002) using custom-made EST-based arrays examined the changes in gene expression in Arabidopsis tissue infected with Pseudomonas syringae pv. tomato over a relatively short time-course. A significant change in expression pattern was seen by 7 h post-infection that indicated a major shift in the expression of genes from those that have a housekeeping role to those underpinning defence metabolism. The overall picture from such studies suggests that expression patterns change very quickly in response to pathogen attack, i.e. within 6–12 h; these patterns encompass defence-related genes and housekeeping genes; and that systemic acquired resistance is a reflection of the local response, but the systemic response is ‘measured’.
Ian Baldwin’s laboratory have carried out a number of expression studies using the native tobacco, Nicotiana attenuata, and two of the herbivores that attack it Manduca sexta (Hui et al., 2003) and Tupiocoris notatus (Voelckel and Baldwin, 2003). Using mRNA differential display RT-PCR and subtractive hybridization to isolate cDNAs encoding differentially expressed transcripts these authors were able to construct a microarray for use in verifying differential expression. Results from this work suggest that a range of signalling pathways are used in response to attack including the SA-, ethylene-, cytokinin-, and oxylipin pathways, and that pathogen and cell-wall associated transcripts are altered as part of this defence process. In both cases of attack there seemed to be changes in transcripts associated with photosynthesis. Just as in the case for pathogens, there is clearly a complex reorganization of gene expression in response to herbivore attack that not only involves genes associated directly with defence, but also those that regulate key primary metabolic pathways.
The substantial overlap in the defence genes induced by very different attackers (or signalling pathways) is consistent with the ecological understanding of resistance (Hatcher et al., 2003). We have argued that ‘fine tuning’ of resistances to particular attackers lies with the balance of a relatively small subset of pathogen- or herbivore-regulated genes, the magnitude of their induction, and the spatial and temporal patterns of induction, what we termed the kaleidoscope of defence (Hatcher et al., 2003). There may be parallels here with concepts in cellular biology, where the regulation of signalling may depend on specific spatial and temporal patterns in the use of shared signals. Understanding the whole-plant implications of transcriptome changes that show great overlap between different attackers will also require careful attention to spatial and temporal patterns of induction. This highlights the need for caution in interpreting data showing that different attackers induce the same defence gene(s) as evidence that the attacking organisms interact. This applies equally to any consideration of interactions between herbivory or disease, and abiotic factors. Another caveat in interpreting transcriptome data, at least in the context of plant interactions with herbivores or pathogens, is the self-evident statement that attackers do not respond to the transcriptome, but to products down-stream of transcription. Thus, while transcriptome analysis is revealing exciting new information on the dynamics of resistances, the assessment of such dynamics ultimately requires measurement of resistance mechanisms per se, not just the transcriptome.
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‘Crosstalk’ at the level of ecological/agricultural studies |
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Taking an ecological/agronomic perspective on tripartite interactions, even measuring the component mechanisms of resistance may be rather remote from the ultimate goal of considering how interactions influence individuals, or populations of the organisms involved. This question has been addressed both in terms of the ecology of tripartite interactions and with a view to the commercial deployment of plant defence against multiple attack.
The role of tripartite insect–fungus–plant interactions in agricultural crops can be illustrated by the largely unexplored interactions between insects and fungi on oilseed rape. For example, infection by stem canker, Leptosphaeria maculans, is enhanced by feeding of the weevils Ceutorhynchus pallidactylus and C. napi (Broschewitz and Daebeler, 1987; Alford et al., 2003); infection of pods with grey mould, Botryotinia fuckeliana, is associated with Dasineura brassicae and C. assimilis feeding (Lane and Gladders, 2000), and pollen beetle (Meligethes spp) feeding on unopened buds predisposes pods to fungal infection (Gratwick, 1992). Furthermore, the brassica pod midge, D. brassicae, uses fungal lesions of pods as oviposition sites (Gratwick, 1992).
The potential use of elicitors of plant resistance in agriculture, especially in the context of attack by multiple enemies has been the focus of extensive research by Thaler and co-workers. Although having a clear practical application, Thaler’s research is founded on an underlying hypothesis that addresses a fundamental aspect of ‘crosstalk’; that is that different resistance responses should be matched to guilds or groups of attackers, but that attack by a particular group may have consequences for how a plant deals with subsequent attack. They have used tomato plants grown in the field to try to unpick these interactions between signalling systems for pests and pathogens. Using a range of herbivores from different feeding guilds it has been shown that induced resistance is rather general and will suppress many members of a herbivore community (Thaler et al., 2001). The effect is not restricted to one trophic level; parasitoids were shown to be more effective at killing herbivores feeding on control rather than JA-induced plants, a response attributed to the ‘quality’ of the herbivore (Thaler, 2002). Hence the plant response to attack will not only affect herbivore numbers, it will also affect the quality of the herbivore for other natural enemies.
The work of Thaler and co-workers also provides a whole-organism perspective on the several lines of evidence suggesting that there is ‘crosstalk’ between the SA and JA response pathways (Bostock et al., 2001; Traw et al., 2003). Such ‘crosstalk’ may be synergistic, but the SA signalling pathway can, in some cases, down-regulate the induction of the JA pathway (Doares et al., 1995). Dual induction of these pathways in cultivated tomatoes has shown that the biological consequence of this interaction is dependent upon the attacking species (Thaler et al., 2002a), and the timing and the strength of elicitation (Thaler et al., 2002b). Using both biochemical and biological indicators Thaler et al. (2002b) demonstrated that, although it was not always possible to show a detectable biochemical effect of the negative interaction between SA and JA, there was a biological effect as seen in a reduction in resistance to the herbivore. These results highlight the care required in choosing a sufficient range of biochemical indicators if we are to gain an accurate and robust prediction of the biological outcome. More importantly, it further underlines the need to demonstrate, and not just infer, the link between a change in gene expression in response to attack and the biological outcome (i.e. resistance).
Studies in our laboratory have been concerned with tripartite interactions between the herbivore Gastrophysa viridula DeGeer and the pathogen Uromyces rumicis (Schum) Wint. that both attack Rumex obtusifolius L. Interactions in terms of the growth and fitness of all three organisms have been examined (Hatcher et al., 1994a, b, 1997a). These changes were interpreted in terms of mutual effects on plant characteristics such as carbohydrate and/or nitrogen concentration, the accumulation of defensive compounds such as oxalate (Hatcher et al., 1997b) or changes in leaf physical properties (Moore et al., 2003a). Such changes are a subset of the multiple physiological outcomes of attack by herbivores or pathogens, which not only show substantial overlap with each other but also with changes induced by a range of environmental variables (Table 1). The overlap in these physiological, metabolic and morphological characteristics are the phenotypic product of interactions, including ‘crosstalk’, in signalling pathways and the changes in the transcriptome. The links between the dynamics of gene expression and variability in ‘resistance’ as perceived by herbivore or pathogen remain relatively poorly understood but are likely to have significant consequences for the host as well as for attacking organisms. For example, while the effects of some induced resistance mechanisms are transient others are permanent.
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One example of the latter is the systemic induction of cell wall peroxidases that we observe in Rumex following localized G. viridula attack (Moore et al., 2003a). The induction of peroxidase activity is transient, lasting for 1–2 d, but the resultant leaf stiffening results in irreversible reductions in leaf growth. Thus, limited G. viridula grazing that caused no significant change in whole-plant photosynthesis led to long-term growth reductions as a consequence of an irreversible induced response. The systemic resistance induced by G. viridula is expressed in a significant subsequent effect on the gregariousness of G. viridula larvae grazing on treated plants compared with ungrazed controls. In addition, localized grazing by the pest induced systemic resistance to the rust pathogen (Hatcher et al., 1994a), and more broad-spectrum pathogen resistance in the field (Hatcher and Paul, 2000a). Hence the response induced by G. viridula is effective against subsequent attack by both the beetle and a range of fungal pathogens. The balance between the benefit of this more broad-spectrum resistance and the cost of irreversible limits on leaf growth poses intriguing ecological questions. It is certainly in marked contrast to the cost-benefit analysis associated with the temporary diversion of resources away from growth to support the transient synthesis of defensive metabolites, especially if these are specific in their action.
More recently, the localized application of exogenous JA to R. obtusifolius has been found to mimic the effects of herbivory on the systemic induction of cell-wall peroxidase, and, in turn, on cell expansion, leaf growth and G. viridula behaviour (Moore et al., 2003b). By contrast, localized U. rumicis infection of Rumex, causes only a transient reduction in leaf growth rates without any induction of cell wall associated peroxidase (Fig. 2). In addition, localized application of exogenous SA led to no reduction in growth (Fig. 3). Thus, two attackers, both leading to the same observable end-point, reduced leaf growth, appeared to be acting through very different mechanisms. Of course, this lack of ‘crosstalk’ or other interactions ‘up-stream’ of leaf growth does not mean that the effects of rust and beetle grazing do not interact ‘down-stream’ in terms of whole-plant growth or fitness (Fig. 1). Indeed, the apparent independence of their effects leads to the prediction that their effects might be at least additive. Additive interactions between U. rumicis and G. viridula have been observed in our field experiment (Hatcher et al., 1994c), but were attributed to a series of ecological mechanisms reflected in the altered behaviour of G. viridula (Hatcher and Paul, 2000b). However, one key response was that the decline in nutritional quality in rusted leaves caused beetles to disperse to developing leaves, which normally suffer rather little beetle damage. Such responses will reflect physiological mechanisms investigated in the laboratory, but also depend on aspects of the biology of all three organisms that could only have been fully considered in the field. These include not only the order of attack, but also the relative timing of attack with respect to the development of the other participants.
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‘Crosstalk’ in the natural environment: the role of ‘context’ |
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In our work with Rumex, the order in which beetle and rust is applied also has an effect on the outcome at the whole plant level (Hatcher et al., 1994c). However, beyond that, the order of attack also has consequences for any other organism that tries to attack, because the host phenotype, as perceived by the attacker, is dependent on the previous history of the individual plant (reviewed by Paul et al., 2000; Hatcher et al., 2003). Similar conclusions can be drawn from studies of ‘crosstalk’ in plant–consumer interactions at other scales of organization. Whole plant responses to exogenous elicitors in tomato show that signal interaction is more consistent when elicitors are applied at the same time or in high doses (Thaler et al., 2002b). Ian Baldwin has also explored the transcriptional response when N. attenuata is attacked sequentially by different pest species and has shown that the transcriptional imprint following attack is determined by the order of the attack (I Baldwin, personal communication). This has been described as ‘context-specific’ gene induction, which reflects the order of elicitation, rather than simply species-specific gene induction. The idea of context-specific responses in defence is consistent with broader concepts of phenotypic plasticity and, as such, context encompasses far more than ‘crosstalk’ in the narrow sense: it includes the whole spectrum of interactions from the cellular to the whole-organism. Context also extends far beyond plant–herbivore–pathogen interactions to encompass the many interactions that can occur in a plant confronted with the multiple environmental factors acting in the field. Interactions between light and herbivory or disease offer an intriguing example. Effects of light on herbivory or disease are likely to be considered by ecologists in terms of changes in tissue carbohydrate concentration, C:N ratio, or cuticular development that may directly influence the attacker (Bentz, 2003; Cipollini, 2002; Burns et al., 2002). Such mechanisms would be secondary to a cell biologist who will look at the effects of light from the viewpoint of the shared signals or signalling pathways (Mullineaux et al., 2000).
The example of light also exemplifies basic differences in experimental approaches between the two different types of investigator (cellular and ecological) that hinder the acquisition of data that might bridge the mechanism gap between cellular and ecological studies. We assessed the light conditions cited in a random selection of 100 papers on the more cellular and molecular aspects of induced defence published over the past five years (Fig. 4). Surprisingly, around 45% of these papers gave no specific information on photosynthetically active radiation (PAR 400–700 nm), making it impossible to relate their data to responses that might be observed under field conditions. Another 35% cited PAR irradiances of less than 200 µmol quanta m–2 s–1, which is less than 10% of peak irradiances in the field. Of the remaining papers the majority used irradiances in the range 300–700 µmol quanta m–2 s–1, with just one small subset using irradiances exceeding 1000 µmol quanta m–2 s–1. The use of low PAR might be expected to influence defence in many ways. Low light is known to influence constitutive defences, for example, constitutive levels of furanocoumarins in parsnip were reduced by plant shading (Berenbaum and Zangerl, 1998). In addition, there is increasing evidence that variation in irradiance within the environmental range can induce local and systemic changes in the expression of genes usually associated with defence, and that such induction can interact with responses to disease or wounding (Mullineaux et al., 2000). There is also recent evidence that SA signalling in response to pathogen attack is linked to phytochrome signalling (Genoud et al., 2002). In addition, solar ultraviolet radiation (UVR), which is much reduced in glasshouse and controlled environment studies, is known to regulate the expression of many defence-related genes (A-H Mackerness, 2000).
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On this basis the light environment used in most studies of cellular and molecular aspects of defence provide a context very different from the field. Controlled environment systems capable of delivering light environments close to the field are now quite widely available, and a recent paper demonstrates that Arabidopsis can be used effectively in field studies where PAR irradiances exceeding 1500 µmol quanta m–2 s–1 were commonplace (Kulheim et al., 2002). Studying the interactions of Arabidopsis with herbivores and pathogens under light conditions closer to those in the field not only provide a valuable insight into light as a context for defence, it would also allow much greater confidence in extrapolating cellular and molecular data to field conditions.
The investigations of Kulheim et al. (2002) also provide a model for the use of mutants that are well-defined in molecular terms to address physiological/ecological questions in the field. The work of Baldwin and co-workers offers another approach for bringing molecular tools to bear on major ecological questions (Roda and Baldwin, 2003). Such mechanistic studies would be valuable steps in linking molecular and ecological studies of interactions, not least those involving responses to multiple enemies, and so put ‘crosstalk’ in the narrow sense, in the far wider context of interactions acting under field conditions.
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Acknowledgements |
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The authors gratefully acknowledge the NERC for funding for their work and the contribution made by Dr Jason Moore who received an NERC studentship.
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