Metabolomic assessment of induced and activated chemical defence in the invasive red alga Gracilaria vermiculophylla

In comparison with terrestrial plants the mechanistic knowledge of chemical defences is poor for marine macroalgae. This restricts our understanding in the chemically mediated interactions that take place between algae and other organisms. Technical advances such as metabolomics, however, enable new approaches towards the characterisation of the chemically mediated interactions of organisms with their environment. We address defence responses in the red alga Gracilaria vermiculophylla using mass spectrometry based metabolomics in combination with bioassays. Being invasive in the north Atlantic this alga is likely to possess chemical defences according to the prediction that well-defended exotics are most likely to become successful invaders in systems dominated by generalist grazers, such as marine macroalgal communities. We investigated the effect of intense herbivore feeding and simulated herbivory by mechanical wounding of the algae. Both processes led to similar changes in the metabolic profile. Feeding experiments with the generalist isopod grazer Idotea baltica showed that mechanical wounding caused a significant increase in grazer resistance. Structure elucidation of the metabolites of which some were up-regulated more than 100 times in the wounded tissue, revealed known and novel eicosanoids as major components. Among these were prostaglandins, hydroxylated fatty acids and arachidonic acid derived conjugated lactones. Bioassays with pure metabolites showed that these eicosanoids are part of the innate defence system of macroalgae, similarly to animal systems. In accordance with an induced defence mechanism application of extracts from wounded tissue caused a significant increase in grazer resistance and the up-regulation of other pathways than in the activated defence. Thus, this study suggests that G. vermiculophylla chemically deters herbivory by two lines of defence, a rapid wound-activated process followed by a slower inducible defence. By unravelling involved pathways using metabolomics this work contributes significantly to the understanding of activated and inducible defences for marine macroalgae.     

The green macroalga Dictyosphaeria ocellata influences the structure of the bacterioplankton community through differential effects on individual bacterial phylotypes

Marine macroalgae are subjected to large numbers of bacteria in their environment. These bacteria have the potential to affect the health and ecology of algae in a variety of ways and can be both beneficial and harmful to the algae. Therefore, algae have likely evolved mechanisms to differentially regulate the growth of bacterial species. In this study, we examined the effects of the green alga Dictyosphaeria ocellata on the bacterioplankton community in field enclosure experiments and on individual, naturally co-occurring bacterial strains in laboratory co-culture experiments. In field experiments, we compared the bacterioplankton communities of enclosures with and without D. ocellata using denaturing gradient gel electrophoresis and found that the alga significantly changed the bacterial community composition. Seven bacterial phylotypes were eliminated in the presence of the alga and five were found exclusively with the alga. We also examined the effects of algal-treated water on the development of the bacterial community within enclosures and found no change in the community composition. Laboratory co-culture experiments revealed that D. ocellata and D. ocellata extracts affect the growth of individual bacterial strains in a species-specific manner and that the mechanisms responsible for these effects also differed by bacterial species.     

The price of safety: food deprivation in early life influences the efficacy of chemical defence in an aposematic moth

Aposematism is the combination of a primary signal with a secondary defence that predators must learn to associate with one another. However, variation in the level of defence, both within and between species, is very common. As secondary defences influence individual fitness, this variation in quality and quantity requires an evolutionary explanation, particularly as it may or may not correlate with variation in primary signals. The costs of defence production are expected to play a considerable role in generating this variation, yet studies of the cost of chemical defence have focused on species that sequester their defences, while studies in species that produce them de novo are scarce. Here we examine effects of resource availability on the production of chemical defences in female wood tiger moths Arctia plantaginis. This species produces defensive fluids when attacked, and advertises this protection with bright colours on its hindwings. Furthermore, the chemicals in these fluids are produced de novo. In order to establish if the production of this chemical protection is costly, and thus resource‐limited, we manipulated resource availability (i.e. food) during larval development and measured its subsequent effects on adult chemical defence. We presented defensive fluids from female moths to wild blue tits, in the absence of any visual cues, to determine their effectiveness against avian predators. Our results demonstrate that the defensive fluids produced by female moths repel birds, and that these defences require resource investment to produce. We found that moths that were resource‐limited during development had less effective chemical defences, despite producing the same volume of defensive fluids as the control moths. As a reduction in available resources negatively influences the effectiveness of the chemical defence, resource availability may explain the variation seen among individuals.     

Seasonal variation in the relationship between growth rate and phlorotannin production in the kelp Ecklonia radiata

Most theories for the evolution of plant chemical defences assume that defences are costly. In order to investigate the potential cost of phlorotannin production in the brown alga (kelp) Ecklonia radiata, I measured the correlation between changes in phlorotannin levels and growth rates for E. radiata in two seasons, spring and autumn. In spring, when both phlorotannin levels and growth rates in E. radiata were highest, there was a significant negative relationship between changes in phlorotannin levels and growth, consistent with a cost of phlorotannin production. No relationship was evident in autumn, indicating that moderate levels of phlorotannins and growth could be maintained simultaneously. These and related results suggest that the cost of defence will vary as a function of (1) endogenous patterns of growth or metabolite production and (2) variation in available resources. Evidence for a cost of phlorotannins in E. radiata adds to the paradox of the maintenance of high levels of phlorotannins in Australasian brown algae.     

Inducible chemical defences in animals

Phenotypic plasticity is extremely widespread in the behaviour, morphology and life‐history of animals. However, inducible changes in the production of defensive chemicals are described mostly in plants and surprisingly little is known about similar plasticity in chemical defences of animals. Inducible chemical defences may be common in animals because many are known to produce toxins, the synthesis of toxins is likely to be costly, and there are a few known cases of animals adjusting their toxin production to changes in environmental conditions. We outline what is known about the occurrence of inducible chemical defences in animals and argue that there is immense potential for progress in this field. Possible directions include surveying diverse taxa to explore how general its occurrence may be and testing for selection acting on inducible chemical defences. Data on inducible chemical defences would provide insight into life‐history tradeoffs by enabling novel tests of how time‐costs and resource‐costs affect life‐history. If the synthesis of toxic compounds by animals proves accessible to manipulation, as it is in plants and fungi, this will open the way to refined estimates of the fitness costs of defence, ultimately providing a clearer picture of how plasticity evolves and is maintained in nature. Synthesis Inducible changes in the behaviour, morphology, and life‐history of animals are extremely widespread, but surprisingly little is known about similar changes in the production of defensive chemicals. We outline what is known about the occurrence of inducible chemical defences in animals and argue that there is immense potential for progress in this field. Possible directions include surveying diverse taxa to explore how general its occurrence may be and testing for selection acting on inducible chemical defences. Data on inducible chemical defences would provide insight into life‐history tradeoffs by enabling novel tests of how time‐costs and resource‐costs affect life‐history. If the synthesis of toxic compounds by animals proves accessible to manipulation, we will be able to estimate the fitness costs of defence more precisely, and ultimately provide a clearer picture of how plasticity evolves and is maintained in nature.     

Ecological trade-offs between jasmonic acid-dependent direct and indirect plant defences in tritrophic interactions

Recent studies on plants genetically modified in jasmonic acid (JA) signalling support the hypothesis that the jasmonate family of oxylipins plays an important role in mediating direct and indirect plant defences. However, the interaction of two modes of defence in tritrophic systems is largely unknown. In this study, we examined the preference and performance of a herbivorous leafminer (Liriomyza huidobrensis) and its parasitic wasp (Opius dissitus) on three tomato genotypes: a wild-type (WT) plant, a JA biosynthesis (spr2) mutant, and a JA-overexpression 35S::prosys plant. Their proteinase inhibitor production and volatile emission were used as direct and indirect defence factors to evaluate the responses of leafminers and parasitoids. Here, we show that although spr2 mutant plants are compromised in direct defence against the larval leafminers and in attracting parasitoids, they are less attractive to adult flies compared with WT plants. Moreover, in comparison to other genotypes, the 35S::prosys plant displays greater direct and constitutive indirect defences, but reduced success of parasitism by parasitoids. Taken together, these results suggest that there are distinguished ecological trade-offs between JA-dependent direct and indirect defences in genetically modified plants whose fitness should be assessed in tritrophic systems and under natural conditions.     

Temperature induced bacterial virulence and bleaching disease in a chemically defended marine macroalga

Host-pathogen interactions have been widely studied in humans and terrestrial plants, but are much less well explored in marine systems. Here we show that a marine macroalga, Delisea pulchra, utilizes a chemical defence - furanones - to inhibit colonization and infection by a novel bacterial pathogen, Ruegeria sp. R11, and that infection by R11 is temperature dependent. Ruegeria sp. R11 formed biofilms, invaded and bleached furanone-free, but not furanone-producing D. pulchra thalli, at high (24°C) but not low (19°C) temperatures. Bleaching is commonly observed in natural populations of D. pulchra near Sydney, Australia, during the austral summer when ocean temperatures are at their peak and the chemical defences of the alga are reduced. Furanones, produced by D. pulchra as a chemical defence, inhibit quorum sensing (QS) in bacteria, and this may play a role in furanone inhibition of R11 infection of furanone-free thalli as R11 produces QS signals. This interplay between temperature, an algal chemical defence mechanism and bacterial virulence demonstrates the complex impact environmental change can have on an ecosystem.     

Experimental evolution of external immune defences in the red flour beetle

The red flour beetle, Tribolium castaneum, secretes quinones that control the microbial flora in the surrounding environment. These secretions act as an external immune defence that provides protection against pathogens. At high concentrations, however, these secretions are harmful to the host itself, and selection may thus have optimized the level of expression under natural conditions. Here, we show that the expression of external immunity responded to selection during experimental evolution within a few generations. At the same time, one component of internal immune defence (phenoloxidase activity) was compromised in beetles selected for either high or low external defences. Intriguingly, offspring protection against a natural pathogen was reduced in flour obtained from beetle lines selected for low amounts of secretions. Altogether, this suggests that external and internal immune defences work together efficiently under natural conditions, whereas every manipulation on the side of external immune defence comes with costs to the internal immune defence.     

Benefits,costs and reactivity of inducible defences: an experimental test with rotifers

1. A key aspect of the ecology and evolution of adaptive prey responses to predator risk is the timing by which the former develop a defensive trait in response to inducing signals released by the latter. This property, called reactivity, has been shown to affect population stability and persistence. 2. Theoretically, the minimal predator density required by prey to exhibit induced defences is expected to increase with the effectiveness of the defence and decrease with its cost. Likewise, the time required for the prey population to exhibit an induced defence is expected to increase together with cost. 3. The freshwater rotifers Brachionus calyciflorus and B. havanaensis and their predator Asplanchna brightwelli were used to test the hypothesis that prey species exhibiting defences that offer a larger fitness benefit and lower fitness cost are more reactive to predator signals, in terms of requiring shorter exposure time and lower signal concentration to trigger a morphological defence reaction. 4. Our results showed that both prey species exhibited costly and effective defences after induction by predator infochemicals. Faster reactions were observed at higher levels of predator cues. Nevertheless, the observed relationship between reactivity and benefit/cost of defences did not agree with our expectations. 5. To our knowledge, this is the first study in which the timing of induction of morphological defences is experimentally assessed over a gradient of risk signals. We propose new research directions to disentangle the mechanisms and project the consequences of prey decisions at the morphological level.     

Spatial associations among palatable and unpalatable macroalgae: A test of associational resistance with a herbivorous amphipod

Associational resistance is the process by which plants may gain protection from spatial associations with neighbouring plants. We tested whether association with an unpalatable alga, Dictyopteris acrostichoides, affects the abundance and colonisation behaviour of the herbivorous amphipod Peramphithoe parmerong on its preferred host alga Sargassum linearifolium. Despite predictions, natural densities on S. linearifolium when surrounded by D. acrostichoides were higher than on isolated individuals of S. linearifolium. Colonisation experiments in the laboratory and the field tested the hypotheses that the observed variation in field abundance with algal neighbourhood was due to variation in the size of habitat patches, physical obstruction of host finding by D. acrostichoides and variation in the relative abundance of S. linearifolium and D. acrostichoides. None of these possible mechanisms was found to significantly alter rates of amphipod colonisation on the scales of individuals selecting among algal pieces in the laboratory or among habitat patches in the field. The failure of colonisation processes to explain observed variation in natural amphipod densities suggests that post-colonisation processes such as survival or emigration may vary with the spatial associations among algae.     

Cost of chemical defence in the red alga Delisea pulchra

The concept of a cost of defence is fundamental to theories for the evolution of defences against consumers. However, the evidence for a cost of plant chemical defences is mixed, and often indirect. This is particularly true for marine macroalgae (seaweeds), for which inferences of cost to date rely almost exclusively on phenotypic correlations between one class of secondary metabolites (brown algal phlorotannins) and growth (or, in one instance, fecundity). No studies of the cost of seaweed chemical defense have experimentally manipulated the presence of secondary metabolites in a controlled fashion and only one previous study has considered genetic background as a factor. Here we measured the cost of halogenated furanones to the red seaweed Delisea pulchra in three ways: a) phenotypic correlations between concentrations of furanones and fecundity in field collected thalli; b) genetic correlations between concentrations of furanones and growth for clones of thalli grown from tetraspores, and c) by comparing growth rates of thalli for which furanone production was experimentally inhibited (furanone -) vs thalli which produced furanones (furanone +). Two of our three tests-correlations between furanones and fecundity, and the growth of furanone (+) vs furanone (−) thalli-indicated a cost of furanones to D. pulchra but genetic correlations between furanones and growth did not. We suggest that these apparently conflicting results are consistent with the consequences of apical growth in this alga, and may further result from a cost of furanones only being manifested at critical developmental stages or times of tissue differentiation.     

Effect of Detachment on the Palatability of two Kelp Species

Many species of macroalgae survive after becoming dislodged from their primary substratum, but little is known about their capacity to express anti-herbivore defences after detachment. We examined the effect of detachment on the relative palatability of the two kelp species Lessonia nigrescens and Macrocystis integrifolia to mesograzers. Laboratory and field experiments were conducted on the northern-central coast of Chile to investigate whether (i) time after detachment and (ii) grazing on detached and attached algae could trigger internal defence mechanisms in the algae, which may have acted as deterrents to grazing. In order to examine palatability, feeding assays were run after each experiment using fresh algal pieces and artificial food. Time after detachment had a significant influence on palatability of L. nigrescens but not of M. integrifolia. During the first 12 days of detachment, detached L. nigrescens held in grazer-free laboratory tanks were not significantly more palatable than attached conspecifics from the field but thereafter detached individuals became more palatable. Floating individuals of M. integrifolia showed no effect of detachment, indicating that this alga maintains its defence after detachment. An experiment conducted in the field confirmed these results for M. integrifolia. An additional laboratory experiment confirmed that attachment status plays an important role on algal defence reaction for L. nigrescens when exposed to grazers. Detached and previously grazed individuals of this species were less palatable than grazer-free control algae, but grazing had no effect on palatability of attached algae. Our results indicate that kelps have varying capacities for development of anti-grazing responses once they become detached, possibly depending on their capacity to float and survive after detachment.     

Optimal defence, kin conflict and the distribution of furanocoumarins among offspring of wild parsnip

The factors influencing the allocation of chemical defences to plant offspring have largely been unexplored, conceptually and experimentally. Because evolutionary interactions between maternal plants and their progeny can affect resource allocation patterns among sibling offspring, we suggest that kin conflict as well as herbivore–plant interaction theories need to be considered to predict chemical defence allocation patterns. Optimal defence theory predicts that maternal plants should defend more heavily those offspring in which resources have been disproportionately invested. In contrast, kin conflict theory predicts that natural selection will favour genotypes that can compete successfully for maternal defences irrespective of their quality, even at the expense of the fitness of siblings and the maternal plant. Evidence for these defence patterns were evaluated by examining the allocation of furanocoumarins to seeds of the wild parsnip (Pastinaca sativa, Apiaceae). Furanocoumarins are toxins that are localized within the oil tubes of the maternal tissues of seeds. We evaluated the role of offspring investment (endosperm mass) and seed genotype on furanocoumarin allocation by mating an array of pollen donors with pollen recipients. Furanocoumarins were found to be positively correlated with endosperm mass on one side of the seed, a result consistent with optimal defence theory; however, on the other side of the seed, furanocoumarin content was influenced by seed genotype and was unrelated to endosperm mass. These effects varied with maternal plant. Further experiments demonstrated that nearly 80% of furanocoumarin production occurs after pollination, when fertilization products are active. Although the amount of furanocoumarin influenced by the seed genotype is small relative to the total quantity in the seed, these furanocoumarins are the first line of defence against important predators, such as the parsnip webworm, Depressaria pastinacella (Lepidoptera: Oecophoridae). We found that parsnip webworm larvae were able to discriminate among genotypes within an inflorescence. In line with previous studies, these results suggest that a genotype's ability to influence furanocoumarin defence may affect its probability of survival. We conclude that the distribution of defences among plant offspring in wild parsnip is probably influenced by competition among seed genotypes that conflicts with maternal optimal defence. This revised version was published online in July 2006 with corrections to the Cover Date.     

Eutrophication-induced changes in benthic algae affect the behaviour and fitness of the marine amphipod Gammarus locusta

This study, conducted in mesocosms, natural field sites, and in laboratory aquaria, showed that eutrophication altered the nutrient status and dominance patterns among marine macroalgae, which in turn, stimulated gammaridean density. Gammaridean abundance correlated positively with both nutrient addition and the amount of green algae (also stimulated by nutrient enrichment). Path analysis indicated that the direct effect of nutrients on gammaridean density was of less importance than the indirect effect through increased production of green algae. In cage colonisation experiments, either in the field or in a control mesocosm kept under ambient nutrient conditions, more gammarids colonised nutrient enriched algae (E-algae) than algae with ambient nutrient levels (A-algae). Gammarus locusta generally grew faster on nutrient enriched algal specimens and when reared on green rather than on brown algae (fucoids). The nutrient status of periphytic algae did not affect gammaridean growth significantly, but the number of egg-carrying females (and thus egg production) was significantly higher among gammarids reared on E-periphyton. The gammaridean habitat preference order (red > green > brown > periphyton) was almost the reverse of their growth rate in feeding assays (periphyton > green > brown). This implies that macroalgae may be more important as a habitat than as a food source for these animals, which then have to become mobile in search of optimal food items. In this process, algal nutrient content was important as the gammarids in our study actively chose high quality nutrient-rich food, which, in addition, increased their fitness. Stimulated growth rates and egg production may ultimately lead to population increase, which, combined with the preference for high nutrient food items may dampen the initial effect of nutrient enrichment (i.e. blooms of green macroalgae) in shallow coastal waters.     

The ecology and evolution of induced responses to herbivory and how plants perceive risk

1. Plants perceive herbivore damage or increased risk and respond. These changes may increase plant fitness, although effects on fitness have often been assumed without supporting evidence. 2. Three models have been proposed to explain induced rather than constitutive defence. The optimal defence model posits that induction allow plants to reduce allocation costs; it predicts demonstrably lower costs when defences are not needed. The moving target model posits that induction increases spatial and temporal variability; it predicts that variability will be difficult for herbivores and will provide defence. The information transfer model posits that induced responses provide cues to other tissues on that individual plant and to other organisms in the community; it predicts that induced cues will provide systemic resistance, deter herbivores, and/or attract enemies of herbivores, thereby benefiting the induced plant. 3. All three models predict that cues must be reliable to be useful. In some cases, cues provide specific information about the damaged plant tissue and the herbivore and this specific information may allow plants to fine-tune responses. Recent theory posits that selection should favour plants that minimise recognition errors and reduce fitness costs associated with errors. 4. Future research should focus on exploring different modalities used by plants to perceive herbivore risk, the benefits and costs of perceiving cues and inducing resistance, and the basic natural history of these phenomena. Induced responses have great unrealised potential in agriculture, and research should focus on host plant resistance rather than attempting to involve other trophic levels.     

Consequences of the overproduction of methyl jasmonate on seed production, tolerance to defoliation and competitive effect and response of Arabidopsis thaliana

* Accumulation of methyl jasmonate (MeJA) after herbivore attack in plants is associated with the induction of defenses that can benefit fitness, but are costly to express; effects often explored using exogenous application of jasmonates. * Here I explored the consequences of the overexpression of MeJA on seed production, tolerance to defoliation and competitive effect and response, using a genotype of Arabidopsis thaliana that overexpresses jasmonic acid carboxyl methyltransferase (JMT) and contains threefold higher levels of MeJA than wild-type plants. * Without competition, JMT plants produced 37-40% less total seed mass than vector controls or wild-type plants, and had reduced seed germination. Defoliation reduced height more strongly in wild-type than in JMT plants, but reduced total seed production equally. In a competition experiment, the presence of a neighbor reduced fitness more strongly in wild-type than in JMT plants, but JMT plants exhibited dampened opportunity costs and benefits of induction with jasmonic acid of itself or its neighbor. This may have related to the higher constitutive expression but reduced inducibility of jasmonate-mediated defenses, including trypsin inhibitors, exhibited by JMT plants. * In natural plant populations, overexpression of MeJA-mediated responses should be beneficial to resistance to herbivores, pathogens and competitors, but is directly costly to fitness and probably constrains plasticity in response to changing environmental conditions.     

Extrafloral nectary phenotypic plasticity is damage- and resource-dependent in Vicia faba

Phenotypic plasticity enables many damaged plants to increase nectar secretion rates from extrafloral nectaries (EFNs), or in the case of broad bean, Vicia faba L. to produce additional EFNs, to attract natural enemies of herbivores. While plants benefit greatly from these defensive mutualisms, the costs of producing EFNs are largely unknown. We hypothesized that if EFN production is costly, then damaged plants with high resource levels would be able to produce more EFNs than plants that are resource-limited. Here, we show that this indirect inducible defence does follow this general pattern. Vicia faba enriched with 6 or 12 g of 14:14:14 NPK fertilizer increased EFN numbers after leaf damage by 46 and 60%, respectively, compared with nutrient-poor plants. Thus, EFN production is both damage- and resource-dependent. Analogous to direct defences, production of EFNs may limit the overall loss of leaf tissue when risk of herbivory increases.     

Testing the optimal defence hypothesis for two indirect defences: extrafloral nectar and volatile organic compounds

Many plants respond to herbivory with an increased production of extrafloral nectar (EFN) and/or volatile organic compounds (VOCs) to attract predatory arthropods as an indirect defensive strategy. In this study, we tested whether these two indirect defences fit the optimal defence hypothesis (ODH), which predicts the within-plant allocation of anti-herbivore defences according to trade-offs between growth and defence. Using jasmonic acid-induced plants of Phaseolus lunatus and Ricinus communis, we tested whether the within-plant distribution pattern of these two indirect defences reflects the fitness value of the respective plant parts. Furthermore, we quantified photosynthetic rates and followed the within-plant transport of assimilates with (13)C labelling experiments. EFN secretion and VOC emission were highest in younger leaves. Moreover, the photosynthetic rate increased with leaf age, and pulse-labelling experiments suggested transport of carbon to younger leaves. Our results demonstrate that the ODH can explain the within-plant allocation pattern of both indirect defences studied.     

Strategies of chemical anti-predator defences in leaf beetles: is sequestration of plant toxins less costly than de novo synthesis?

The evolution of defensive traits is driven both by benefits gained from protection against enemies and by costs of defence production. We tested the hypothesis that specialisation of herbivores on toxic host plants, accompanied by the ability to acquire plant defensive compounds for herbivore defence, is favoured by the lower costs of sequestration compared to de novo synthesis of defensive compounds. We measured physiological costs of chemical defence as a reduction in larval performance in response to repeated removal of secretions (simulating predator attack) and compared these costs between five species synthesising defences de novo and three species sequestering salicylic glucosides (SGs) from their host plants. Experiments simulating low predator pressure revealed no physiological costs in terms of survival, weight and duration of development in any of study species. However, simulation of high predation caused reduction in relative growth rate in Chrysomela lapponica larvae producing autogenous defences more frequently, than in larvae sequestering SGs. Still meta-analysis of combined data showed no overall difference in costs of autogenous and sequestered defences. However, larvae synthesising their defences de novo demonstrated secretion-conserving behaviour, produced smaller amounts of secretions, replenished them at considerably lower rates and employed other types of defences (regurgitation, evasion) more frequently when compared to sequestering larvae. These latter results provide indirect evidence for biosynthetic constraints for amounts of defensive secretions produced de novo, resulting in low defence effectiveness. Lifting these constraints by sequestration may have driven some leaf beetle lineages toward sequestration of plant allelochemicals as the main defensive strategy.     

Natural variation in priming of basal resistance: from evolutionary origin to agricultural exploitation

Biotic stress has a major impact on the process of natural selection in plants. As plants have evolved under variable environmental conditions, they have acquired a diverse spectrum of defensive strategies against pathogens and herbivores. Genetic variation in the expression of plant defence offers valuable insights into the evolution of these strategies. The 'zigzag' model, which describes an ongoing arms race between inducible plant defences and their suppression by pathogens, is now a commonly accepted model of plant defence evolution. This review explores additional strategies by which plants have evolved to cope with biotic stress under different selective circumstances. Apart from interactions with plant-beneficial micro-organisms that can antagonize pathogens directly, plants have the ability to prime their immune system in response to selected environmental signals. This defence priming offers disease protection that is effective against a broad spectrum of virulent pathogens, as long as the augmented defence reaction is expressed before the invading pathogen has the opportunity to suppress host defences. Furthermore, priming has been shown to be a cost-efficient defence strategy under relatively hostile environmental conditions. Accordingly, it is possible that selected plant varieties have evolved a constitutively primed immune system to adapt to levels of disease pressure. Here, we examine this hypothesis further by evaluating the evidence for natural variation in the responsiveness of basal defence mechanisms, and discuss how this genetic variation can be exploited in breeding programmes to provide sustainable crop protection against pests and diseases.