R
ecent research has highlighted how plants respond to the diversity of organ-isms that attack them in the field1–4. Much of this current interest derives from cel-lular studies of plant defence pathways. These studies take a reductionist approach and attempt to identify individual signalling pathways that link wounding or attack by a pathogen or her-bivore to specific gene expression events. For example, in Arabidopsis this approach has been successful in identifying key signalling mol-ecules and their relative position in particular pathways. It has also identified possible points of cross-talk between pathways and synergistic or antagonistic events. Recently, there has been increasing interest in the possible interactions between plant signalling pathways, including those involved in responses to disease and herbivory4.Induced defence is also an important area of ecological study5. In contrast with molecular studies, the ecological view of induced defence is broad, and is seen within the context of the overall ‘defence strategy’ of the host plant. This wider strategy includes constitutive defences, the ‘quality’ of host tissues as a resource for consumers, and tolerance (i.e. the capacity of the plant to adjust its physiology to buffer the effects of herbivory or disease). With few exceptions6, ecologists have paid little attention to plant responses to multiple enemies, and studies of non-crop hosts have concentrated largely on defence against herbivores.
Here we consider induced resistances from the contrasting perspectives of molecular biol-ogy and ecolbiol-ogy, and whether integration of these different standpoints offers any novel insights into plant defence against multiple
enemies. We will concentrate on three broad issues: cross-talk between pathways, speci-ficity of induced resistances and the evolution of induced resistances in the context of attack by multiple enemies.
Cellular perspective on systemic induced resistance
Of the several pathways of systemic induced defence in plants the best characterized are sys-temic acquired resistance (SAR), which pro-vides enhanced resistance to pathogen infection, and the wound response pathway, which provides resistance to insect feeding. Both pathways have been shown to induce the expression of distinct sets of genes. SAR has been shown to be induced by salicylic acid and, in at least some systems, salicylic acid appears to be both necessary and sufficient for induc-ing SAR. By contrast, the wound response pathway appears to be induced by jasmonic acid and ethylene without salicylic acid. Although it has been widely accepted that the pathways responsive to pathogen or herbivore attack are distinct, some recent evidence sug-gests that jasmonic acid also mediates induced resistance to some pathogens7,8. Thus, the strict division of induced responses might be incor-rect. In addition, the salicylic acid and jas-monic acid signalling pathways can interact1. Although the nature of the cross-talk is not yet fully defined, recent data suggest that induc-tion of the salicylic acid pathway often inhibits the systemic induction of the jasmonic acid pathway by later herbivory. Conversely, the induction of the jasmonic acid pathway can reduce induction of the salicylic acid pathway following subsequent pathogen attack9–12.
Ecological perspective on systemic induced resistance
The molecular biology of induced resistances has been investigated mostly in herbaceous species. More than 100 species are known to express induced resistance following her-bivory, but two-thirds of these are trees or shrubs5. The vast majority of ecological research into induced resistance deals with her-bivores, ranging from mites to large mammals, and it is clear that induced systemic resistances are widespread and of sufficient magnitude to significantly reduce herbivore populations5,13. In long-lived plants, induced changes can persist to reduce herbivore populations in the years following induction14, and in several for-est systems the decay of induced resistance can be over several herbivore generations14.
Where the mechanisms underlying these ecologically significant induced defences have been defined, it is clear that different plant species use a great diversity of responses. As well as induced chemical and morphological changes, responses include elements that are more closely linked to
Coping with multiple enemies:
an integration of molecular
and ecological perspectives
Nigel D. Paul, Paul E. Hatcher and Jane E. Taylor
How plants respond to attack by the range of herbivores and pathogens that confront them in the field is the subject of considerable research by both molecular biologists and ecologists. However, in spite of the shared focus of these two bodies of research, there has been little integration between them. We consider the scope for such integration, and how greater dialogue between molecular biologists and ecologists could advance understanding of plant responses to multiple enemies.
Box 1. Rumex –Gastrophysa–Uromyces: an ecological model for host–herbivore–pathogen interactions
The beetle Gastrophysa viridula and the biotrophic rust fungus Uromyces rumicis (Fig. 1) both attack the leaves of Rumex species (docks). The physiology and ecology of this system have been intensively studied. Rust infection of dock reduces the growth, survivorship and fecun-dity of G. viridula (Fig. 2), which is associated with changes in the nutritional status of host tissues following infection26
. Conversely, G. viridula feeding induces resistances to the rust fungus, both locally and systemically (Fig. 2)27
. These effects are not confined to controlled environments: rust infection is significantly and substantially reduced in the field by both bee-tle grazing28
and artificial wounding27
. Thus, the combined effect of the beetle and the rust fun-gus on the host might be expected to be inhibited (i.e. the effect less than that of one of the agents alone). However, the effect is usually either equivalent (in Rumex obtusifolius, damage is equivalent to that of the agents; Fig. 2) or additive (in R. crispus, damage is equivalent to the sum of the effects of each agent alone; Fig. 2)29,30
, illustrating the difficulty in extrapolating from the effects of the agents on each other to their effect on the host. This effect is robust even when plants are grown with differing levels of nitrogen fertilization29
. Tripartite interactions in dock are not confined to Gastrophysa and Uromyces, because herbivory also significantly reduced field infection by two other fungal pathogens of dock, the necrotroph Ramularia
rubella, and the hemibiotroph Venturia rumicis28
tolerance (for example, altered protein or nitrogen content in regrowth leaves) than resistance per se5. Ecologists have also con-sidered the broader issue of the selective advantages of induced resistance, in particu-lar the relationship between the benefits and costs of induction15. This in turn leads to ques-tions concerning the population genetics and evolution of induced defence. Current theories are based on the concept that current herbivory or disease is correlated with the risk of future attack16. In this sense, current or past attack can be seen as having the potential to provide information about the future environment. On this basis, induced resistances will be selected for only if (i) current attack is a reliable pre-dictor of future attack, and (ii) if attack reduces plant fitness.
This body of ecological information on induced defence against herbivores is in stark contrast with the limited knowledge of com-parable responses to pathogens. Given the limited understanding of plant pathogens in natural systems it is not surprising that responses to multiple enemies are also poorly understood. One of the few examples of mul-tiple defence to have been studied in a non-crop system – Rumex spp. attacked by the beetle Gastrophysa viridula and the rust fun-gus Uromyces rumicis – highlights the poten-tial complexity of such interactions (Box 1; Figs 1 and 2). Several whole plant studies using crops also highlight the diversity of her-bivore–pathogen interactions: with examples of attack by one organism inducing resistance to attack by another, but there are also many examples of exceptions6.
Defence against multiple enemies
Cross-talk
Molecular biologists have considered ‘defence on multiple fronts’ in terms of inter-actions between different pathways of induced resistance1,3,17. For example, whether induc-tion of the salicylic acid pathway influences subsequent induction of the jasmonic acid pathway and vice versa. In this respect there is evidence that resistance induced via one pathway can suppress induced responses
mediated via another pathway9–11. However, this is only part of the story, and there are examples of induction by one agent resulting in increased resistance to another12. It is also increasingly clear that the concept of specific pathogen and wounding (herbivore)-induced pathways mediated by salicylic acid and jasmonic acid, respectively, is simplistic1. Jasmonic acid also mediates resistances to cer-tain pathogens, and both the salicylic acid and jasmonic acid pathways induce a spectrum of
Fig. 1. (a) Rumex obtusifolius foliage attacked by the rust fungus Uromyces rumicis. (b) Rumex obtusifolius foliage attacked by the chrysomelid beetle Gastrophysa viridula, which attacks Rumex spp. throughout its larval stages (illustrated), and as an adult.
Fig. 2. (a) Fecundity of Gastrophysa viridula reared on Rumex obtusifolius (white) and R. crispus (grey), infected by Uromyces rumicis (rust). Adults had been fed on the no-choice treatments since hatching in Petri dishes, given excess food, and reared at constant temperature. Data for control and infected plants are means of 9–15 plants 61 SE. Modified from Ref. 26. (b) Infection of Rumex obtusifolius (white) and R. crispus
(grey) by Uromyces rumicis (rust) seven days after feeding by the beetle Gastrophysa viridula. Data for control plants, and grazed and ungrazed leaves of grazed plants are means of 14–15 plants 61 SE. Modified from Ref. 27. (c) The effects of grazing by the beetle Gastrophysa viridula
and infection by Uromyces rumicis, alone and in combination, on the growth of Rumex obtusifolius (white) and R. crispus (grey). Key: control 5plants with neither beetle nor rust; beetle 5plants with beetles only; rust 5plants with rust only; RB 5plants infected by U.
rumi-cis that were then grazed by G. viridula. Data are means of 15 plants 61 SE. Modified from Ref. 30.
1000 900 800 700 600 500 400 300 200 100 0
(a) (b) (c)
0 5 10 15 20 25 30 35
0 20 40 60 80 100 120
Control Beetle Rust RB
Plant dr
y w
eight (g)
Trends in Plant Science
Number of eggs laid b
y
G.
vir
idula
Control plants
Control plants Rusted
leaves
Ungrazed leaf
Grazed leaf
Infected plant
U
. r
umicis
pustules (cm
–2
gene products that although distinct to the pathway show considerable overlap between the two (Fig. 3). The relationship between spe-cific gene products and resistance is an area of research that could benefit from closer liaison between molecular biologists and ecologists. We echo the recent suggestion that the value of plant defence investigations would be increased if they were to concentrate on how a putative defence actually contributes to resistance18.
Likewise, the literature dealing with herbi-vores and pathogens, rather than altered levels
of gene products, frequently indicates that the effects of induced resistances are often not spe-cific to any particular attacker. Thus, although induced resistances might show some degree of ‘fine-tuning’ (Fig. 3), it might be expected that resistance induced by one attacker would be effective against a range of other potential attackers. Molecular studies focusing on bio-chemical mechanisms of ‘cross-talk’ between pathways would benefit from complementary studies considering, for example, the extent to which induced changes are specific in terms of their effects on a range of attackers.
Specificity
As we have discussed, many of the biochem-ical responses induced by resistance pathways are effective against a wide range of organ-isms. This specificity of effect, or lack of, must be distinguished from the plant’s specificity of response (Fig. 3). The plant’s specificity of response is the ability of the plant to distin-guish between different types of biotic chal-lenge and to produce different sets of chemicals in response to each challenge. Research suggests that plants do possess specificity of response10,19.
Reviews of the molecular biology of induced resistance suggest that plants might ‘fine-tune’ induced resistances to specific attackers3,17. These arguments seem consistent with current evolutionary theory. Induced resistance is selected for when past or current attack is correlated with the risk of future attack. Such correlation is likely to be great-est when considering current and future attack by the same organism, favouring selection of a ‘fine-tuned’ induced response. However, selection reflects the interplay of benefits and costs of induced resistances, which should be considered when determining the selective advantage of ‘fine-tuned’ resistances. There are many questions here, such as:
• Is the cost of a fine-tuned resistance less than that of a broad-spectrum resistance? • Is induced resistance finely tuned to a
par-ticular attacker likely to confer more or less benefit than a broad-spectrum induced resistance?
Although these questions remain unanswered it is notable that the suggestion of fine-tuning appears to be at odds with much of the litera-ture that shows that resistance induced by one organism is often effective against a range of potential attackers. This might be explained partly by a wider range of induced changes than are often considered as resistance mecha-nisms. Systemic changes in the nutritional quality of host tissues (e.g. nitrogen chem-istry) following pathogen infection might have rather non-specific effects on herbivores, and potentially modify responses to induced allelochemicals. There is less evidence that herbivore-induced changes in ‘non-defence’ chemistry have systemic effects on pathogens. However, these broader changes in host chem-istry should not be overlooked when consid-ering the biology of plant responses to multiple enemies.
Evolution of induced resistances in the context of attack by multiple enemies
There has been considerable debate over whether a characteristic of the host affecting a particular attacker has necessarily resulted from selection pressure imposed by that attacker5. Of course, this also applies to char-acteristics acting against multiple enemies.
Fig. 3. Specificity and overlap in induced resistances: a question of perspective? There is no question that the host plant has the capacity to recognize attack by different organisms with a high degree of specificity. At the level of recognition, it is likely that there is no ‘overlap’ or ‘cross-talk’ between responses to different attackers. The signal transduction pathways involved in induction following attack by herbivores or pathogens also appear to be largely specific, but recent evidence suggests that there are elements of cross-talk, both positive and negative. It is clear that different attackers can affect the expression of distinct sets of genes, and result in different sets of gene products, but such ‘fine-tuning’ might also include indi-vidual elements that are less specific17
. For example, a herbivore might induce the expres-sion of genes abcde and a pathogen might induce genes defgh. This could be taken as evidence of specificity or overlap. A more concrete example is that both herbivores and pathogens might induce specific sets of genes related to the synthesis of phenolics, but induction of PAL, and/or the resultant general up-regulation of phenolic metabolism is com-mon to a wide range of attackers. The effects of these gene products on attackers can be even less specific: the major classes of secondary chemicals that are inducible by arthropods have been shown to have anti-microbial properties and vice versa6
. In addition, ‘non-defence’ changes, such as alterations in tissue nitrogen might have wider-ranging effects. Finally, pathogen and herbivore-induced changes viewed from the perspective of their effects on the overall functioning and fitness of the host plant, including both defence and ‘civilian’ responses are likely to show considerable overlap.
Trends in Plant Science Recognition
Signalling pathways
Gene products (+ or —)
Effects on attackers
Effects on host plant
Overlap between responses a b c d e
f g h d e
Further, because the products of induced resistance(s) might be active against a wide range of organisms, it is possible that broad-spectrum induced resistance is the result entirely of selection by a single attacker, rather than integrated selection by diverse enemies. However, given that attack by multiple and diverse enemies is commonplace in the field, can current models for the selection of induced resistances be applied to this situation? Such models are based on ‘information’, defined as the ability of current attack to predict future attack. Selection for induced resistance is pre-dicted when past or current attack provides ‘information’ concerning (i.e. is well corre-lated with) the risk of future attack. Such cor-relation has been shown experimentally in a few systems20and might be expected for many others. However, is it likely that attack by a herbivore contains any information about
future attack by pathogens, or vice versa? Arguably, herbivory, by creating wounds that might be vulnerable to invasion by microor-ganisms2,5predicts an increased risk of future pathogen attack. However, this is a localized response, consistent with the induction of resistance in the vicinity of wounds. Is it likely that herbivory predicts the risk of pathogen attack in ungrazed tissues? Equally, on a whole-plant basis, is past or current pathogen attack likely to be closely correlated to future herbivory? If such correlations between cur-rent and future attack are unlikely across mul-tiple enemies, this suggests that selection of broad-spectrum induced resistance is unlikely. Selection based on ‘information’ is also diffi-cult to relate to negative interactions between induced responses, such that the response to one attacker might constrain the plant’s abil-ity to respond to another. Indeed, recent
argu-ments suggest that such interactions reflect the manipulation of pathways by attackers21, although this appears to be based on the con-cept of specific herbivore (jasmonic acid) and pathogen (salicylic acid) pathways, which is at odds with some recent evidence.
An alternative view of selection arises if we develop the suggestion5 that induced resist-ance should be considered in the context of the overall response of a plant to attack. This includes what have been called ‘civilian’ responses in host physiology5. For example, following foliar attack, civilian responses include remobilization of reserves from stor-age tissues, increased partitioning of assimi-late to leaves rather than roots and up-regulation of photosynthesis in undamaged leaves. Mechanisms of tolerance appear com-mon to attack by both leaf-feeding herbivores and foliar pathogens. These physiological
Fig. 4. ‘Defence’ and ‘civilian’ elements of induced responses and the possible interactions between them. The range of responses in host metabolism and physiology that result from attack by herbivores and attack by pathogens can be divided into ‘defence’ and ‘civilian’ reactions. Induced defence includes responses mediated via the salicylic acid and jasmonic acid pathways, which are well defined. Civilian responses reflect the interplay of damage and tolerance – physiological and metabolic adjustments made in response to damage. The nature of damage varies markedly with the attacking organism, but adjustment at the whole-plant level shares a degree of commonality between, for example, the range of organisms that attack the foliage. The regulation of the balance between damage and tolerance remains poorly defined. Even less defined are the interactions between the civilian and defence responses. Possible interactions include the effects of salicylic acid and jasmonic acid on civilian responses independent of defence, and the effects of metabolic shifts necessary for induced resistance on civilian responses. Equally, the shifts in metabolism and physiology inherent in civilian responses might influence the expression of induced resistances (at the level of the production of resistance compounds and/or the responses of attackers to those compounds). Host growth, development and, ulti-mately, fitness cannot be seen as a function of defence or civilian responses, but as the outcome of the interaction between both sets of responses.
Trends in Plant Science
SA-dependent JA-dependent
Systemin
Salicylic acid Jasmonic acid
or ethylene
Proteinase inhibitors
Basic PR proteins
Acidic PR proteins, defensins,
thionins
Wound-induced SAR
SA-independent SAR
SA-induced SAR
Defence
?
Civilian
Host growth and development
Host fitness
Pathogen Herbivore attack
? Damage
responses to attack buffer the host from the effects of an initial attack but can increase vulnerability to the effects of future attack. Taking up this theme, a more phytocentric viewpoint of selection for induced resistance might be that current attack (regardless of the organisms doing the attacking) conveys information about the vulnerability of the plant to the physiological effects of any future attack. We hypothesize that attack by any (foliar) attacker is a reliable predictor of the physiological effect of future attack by any (other) foliar attacker(s). This is also consistent with the suggestion that induced resistances allow maximum expression of the plant’s potential to tolerate herbivory or disease5, because the spatial distribution of attack over the plant is altered, maintaining undamaged tissues capable of compensatory physiological changes5.
Viewing current attack as providing infor-mation about the physiological effects of future attacks requires integration between induced resistance and changes in the primary physiology of the plant following attack. Physiological responses to salicylic acid and jasmonic acid are known to extend far beyond induced resistance, but their effects on ‘civilian’ responses are poorly understood22–24. However, it is notable that exogenous applications of both salicylic acid and jasmonic acid have been shown to inhibit photosynthesis, reducing levels of Rubisco and chlorophylls24. Exogenous applications of salicylic acid or jasmonic acid lack the temporal and spatial organization of responses to attack by consumer organisms. However, these effects of exogenous jas-monic acid and salicylic acid are in marked contrast with the increase in photosynthesis in undamaged leaves that is a common response to herbivory and disease. This para-dox highlights the need for a greater under-standing of post-induction changes in ‘civilian’ genes that have no direct relation-ship to resistance.
Salicylic acid and jasmonic acid also inter-act with other plant growth regulators, includ-ing abscisic acid and ethylene, which are central to the coordination of responses to the abiotic environment4. The relationships between plant responses to biotic and abiotic stress have recently been discussed in terms of how abiotic stress might influence induced resistances deployed in agriculture1or whether the abiotic environment provides ‘information’ about the risk of future herbivory or disease16. We argue that responses to biotic and abiotic stress are linked because optimizing induced responses to minimize the physiological effects of attack is highly dependent on the abiotic environment. This includes civilian responses such as altered partitioning between shoot and root, as well as chemical resistance6.
Conclusions
We have approached the issue of defence against multiple enemies from the contrasting backgrounds of molecular biology and plant ecology. Once the initial hurdle of the lack of a common terminology was overcome, it became clear that the major limitation to integrating these viewpoints was the gap between the level of organization we normally dealt with. A key
constraint on the integration of the details of signalling pathways and specific gene products in the few model systems with field data was the relative scarcity of whole plant investiga-tions of induced responses to herbivory and/or disease. There is a risk that quantifying the effects of induced responses on the herbivores or on the pathogens rather than on the host plant has falsely emphasized mechanisms that induce resistance, but fail to benefit plants, while underestimating the significance of tolerance and other induced ‘civilian’ responses21.
Consideration of this ‘middle ground’ has highlighted the need to integrate the available information from this ‘phytocentric’ view-point. We echo the view5 that defence and civilian aspects of induced responses to attack should be considered together (Fig. 4). By analogy with the term used in the context of abiotic stress, induced resistance and tolerance can be treated as elements of acclimation to attack by herbivores and/or pathogens. Although tolerance and (constitutive) resis-tance might be alternative adaptive strategies25, tolerance and induced resistances can be con-sidered as complementary elements of pheno-typic plasticity. Thus, we would argue that it would be fruitful for molecular biologists, ecologists and plant physiologists to consider the functional links between tolerance and induced resistance.
Clearly, progress in this area will benefit from the use of appropriate model systems. We agree with the recent suggestion that resolving uncertainties about signalling conflicts and synergies in induced resistance will benefit from the use of systems that are convenient for genetic, molecular, biochemical and physio-logical studies1. However, the use of standard laboratory models can provide little infor-mation about the ecology of plant responses to multiple enemies. We would argue that mol-ecular biologists should not shy away from applying well-established techniques to native plants whose responses to multiple attackers have been defined in the field.
Acknowledgements
We thank NERC for financial support, and Peter Ayres and John Whittaker for many valuable discussions.
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U
ntil recently, research in programmed cell death (PCD) in animals focused more on the role of the proteolytic cas-cade of caspases than on the morphotype of death. Caspases play a pivotal role in animal cell death, serving both as the amplifiers of extracellular death signals and the means by which specific cellular components are disas-sembled by apoptosis. However, PCD can also occur independently of caspases; this findingled to a re-examination of the role played by these proteases in relation to cell death. In studies where the activity of caspases was blocked with general caspase inhibitors, apop-totic death was either prevented1,2 or only partially executed3. Genetic knockouts of apoptotic factors of the caspase cascade [including Apaf-1 (Ref. 4) , caspase 3 (Ref. 5) and caspase 8 (Ref. 6)] did not prevent death even though some or all the apoptotic features
were blocked. In spite of this apoptosis inhibi-tion, the cells died – they exhibited a type of death termed oncosis7, which is generally con-sidered to be unprogrammed. The observation that cells can inducibly die, even when another programmed cell death is blocked, provokes the question, what is the basis of this oncotic-like death and can it be described at the mol-ecular level? What is emerging from more critical analyses of cell death is that caspase-driven death might not be the central execution pathway8, but instead operates on top of an underlying oncotic-like pathway. When cas-pase-driven death is blocked, the underlying death pathway is revealed as being oncotic.
PCD occurs in other organisms, including plants, but without the apoptotic morphotype where corpse morphology is the result of cas-pase action9. Thus, it is not altogether surpris-ing that there is neither sequence similarity to caspase genes in yeast and plant sequence data-bases nor unequivocal evidence for caspase activity in these organisms. Is there a primor-dial death mechanism that is universal in all eukaryotes, but upon which the caspase pro-teolytic cascade operates in animal cells? Do caspases represent an evolved sophistication of cell death control and corpse management in animals? Analyses of death control and corpse management in organisms such as plants and yeast should answer these questions.
What features are shared among different cells?
Programmed cell death, which occurs indepen-dently of a central role for caspases, has returned
Does the plant mitochondrion
integrate cellular stress and
regulate programmed cell
death?
Alan Jones
Research on programmed cell death in plants is providing insight into the primordial mechanism of programmed cell death in all eukaryotes. Much of the attention in studies on animal programmed cell death has focused on determining the importance of signal proteases termed caspases. However, it has recently been shown that cell death can still occur even when the caspase cascade is blocked, revealing that there is an underlying oncotic default pathway. Many programmed plant cell deaths also appear to be oncotic. Shared features of plant and animal programmed cell death can be used to deduce the primordial components of eukaryotic programmed cell death. From this perspective, we must ask whether the mitochondrion is a common factor that can serve in plant and animal cell death as a stress sensor and as a dispatcher of programmed cell death.
Nigel D. Paul*and Jane E. Taylor are at the Dept of Biological Sciences, Institute of Environmental and Natural Sciences, University of Lancaster, Lancaster, UK LA1 4YQ; Paul E. Hatcher is at the Dept of Agricultural Botany, School of Plant Sciences, University of Reading, 2 Earley Gate, Whiteknights, Reading, UK RG6 6AU (tel 144 118 931 6369; fax 144 118 935 1804; e-mail [email protected]).
