Generalising indirect defence and resistance of plants

Indirect defence, the adaptive top‐down control of herbivores by plant traits that enhance predation, is a central component of plant–herbivore interactions. However, the scope of interactions that comprise indirect defence and associated ecological and evolutionary processes has not been clearly defined. We argue that the range of plant traits that mediate indirect defence is much greater than previously thought, and we further organise major concepts surrounding their ecological functioning. Despite the wide range of plant traits and interacting organisms involved, indirect defences show commonalities when grouped. These categories are based on whether indirect defences boost natural enemy abundance via food or shelter resources, or, alternatively, increase natural enemy foraging efficiency via information or alteration of habitat complexity. The benefits of indirect defences to natural enemies should be further explored to establish the conditions in which indirect defence generates a plant–natural enemy mutualism. By considering the broader scope of plant–herbivore–natural enemy interactions that comprise indirect defence, we can better understand plant‐based food webs, as well as the evolutionary processes that have shaped them.     

Fresh insights into processes of nonhost resistance

Nonhost resistance confers robust protection against pathogenic invaders, and has many similarities to host resistance. Through the different steps of pathogen development, plants make use of diverse defence strategies to present obstacles to the invader. These include preformed barriers, innate immunity in response to general elicitors and, as a last option, resistance mediated by independent and simultaneously acting pairs of pathogen avr and plant R genes. Our understanding of the roles played by these obstacles is relatively poor in nonhost resistance compared to host resistance. There is an obvious need to investigate how these roles may depend on the evolutionary distance between the pathogen host and a certain nonhost plant.     

Plant defence, an evolutionary dilemma: contrasting effects of (specialist and generalist) herbivores and natural enemies

Conclusions Contrasting effects of generalist and specialist herbivores can explain why all plants have not evolved high levels of defence. Maintenance of variation in concentration of defence substances can be explained by a shifting balance between natural selection for defence against herbivory by specialists and generalists. Generalist natural enemies will shift the optimal defence curve to lower concentrations of defences. Physiological costs of production of defence substances and selection by specialist herbivores of plant phenotypes with higher levels of defence compounds for sequestration are no essential elements of this model. They may, however, adjust the predicted optimum defence function and contribute to maintenance of variation of concentrations of defence substances.     

Rapid evolutionary trade-offs between resistance to herbivory and tolerance to abiotic stress in an invasive plant

Release from enemies can lead to rapid evolution in invasive plants, including reduced metabolic investment in defence. Conversely, reassociation with enemies leads to renewed evolution of defence, but the potential costs of this evolution are poorly documented. We report increased resistance of the invader Ambrosia artemisiifolia after reassociation with a coevolved specialist herbivore, and that this increase corresponds with reduced abiotic stress tolerance. Herbivore resistance was higher, but drought tolerance was lower in plants from populations with a longer reassociation history, and this corresponded with changes in phenylpropanoids involved in insect resistance and abiotic stress tolerance. These changes were corroborated by shifts in the expression of underlying biosynthetic genes and plant anti-oxidants. Together, our findings suggest rapid evolution of plant traits after reassociation with coevolved enemies, resulting in genetically based shifts in investment between abiotic and biotic stress responses, providing insights into co-evolution, plant invasion and biological control.     

Systematic distribution and ecological function of the secondary metabolites of the rosidae-asteridae

The systematic distribution of the secondary metabolities of angiosperms has been shaped by the role of these substances as plant defence in the continual chemical werfare between plants and their pests and predators. In the Rosidae-Asteridae, these coevolutionary interactions have caused the gradual replacement of a defence based on tannin and crystals (primitive Rosidae) by defences based on a variety of toxic and repellent substances (advanced Asteridae). Coevolutionary considerations support the concept that within related taxa, biosynthetic sequences of secondary metabolites can correspond directly with chemotaxonomic advancement.     

Bacterial non-host resistance: interactions of Arabidopsis with non-adapted Pseudomonas syringae strains

Although interactions of plants with virulent and avirulent host pathogens are under intensive study, relatively little is known about plant interactions with non-adapted pathogens and the molecular events underlying non-host resistance. Here we show that two Pseudomonas syringae strains for which Arabidopsis is a non-host plant, P. syringae pathovar (pv.) glycinea (Psg) and P. syringae pv. phaseolicola (Psp),induce salicylic acid (SA) accumulation and pathogenesis-related gene expression at inoculation sites, and that induction of these defences is largely dependent on bacterial type III secretion. The defence signalling components activated by non-adapted bacteria resemble those initiated by host pathogens, including SA, non-expressor of PR-1, non-race specific disease resistance 1, phytoalexin-deficient 4 and enhanced disease susceptibility 1. However, some differences in individual defence pathways induced by Psg and Psp exist, suggesting that for each strain, distinct sets of type III effectors are recognized by the plant. Although induction of SA-related defences occurs, it does not directly contribute to bacterial non-host resistance, because Arabidopsis mutants compromised in SA signalling and other classical defence pathways do not permit enhanced survival of Psg or Psp in leaves. The finding that numbers of non-adapted bacteria in leaf extracellular spaces rapidly decline after inoculation suggests that they fail to overcome toxic or structural defence barriers preceding SA-related responses. Consistent with this hypothesis, rapid, type III secretion system-independent upregulation of the lignin biosynthesis genes, PAL1 and BCB, which might contribute to an early induced, cell wall-based defence mechanism, occurs in response to non-adapted bacteria. Moreover, knockout of PAL1 permits increased leaf survival of non-host bacteria. In addition, different survival rates of non-adapted bacteria in leaves from Arabidopsis accessions and mutants with distinct glucosinolate composition or hydrolysis exist. Possible roles for early inducible, cell wall-based defences and the glucosinolate/myrosinase system in bacterial non-host resistance are discussed.     

Plastoquinone: possible involvement in plant disease resistance

The plant Solanum nigrum treated with the pathogen Phytophthora infestans-derived elicitor responded by elevated reactive oxygen species (ROS) production, lipid peroxidation and lipoxygenase (EC 1.13.11.12) activity in comparison with control plants indicating that oxidative stress took place. We demonstrate that these events are accompanied by a significant increase in plastoquinone (PQ) level. It is postulated that PQ may be associated with mechanisms maintaining a tightly controlled balance between the accumulation of ROS and antioxidant activity that determines the full expression of effective defence.     

Advances in understanding the mechanism of resistance to anthracnose and induced defence response in tea plants

The tea plant (Camellia sinensis) is susceptible to anthracnose disease that causes considerable crop loss and affects the yield and quality of tea. Multiple Colletotrichum spp. are the causative agents of this disease, which spreads quickly in warm and humid climates. During plant–pathogen interactions, resistant cultivars defend themselves against the hemibiotrophic pathogen by activating defence signalling pathways, whereas the pathogen suppresses plant defences in susceptible varieties. Various fungicides have been used to control this disease on susceptible plants, but these fungicide residues are dangerous to human health and cause fungicide resistance in pathogens. The problem-solving approaches to date are the development of resistant cultivars and ecofriendly biocontrol strategies to achieve sustainable tea cultivation and production. Understanding the infection stages of Colletotrichum, tea plant resistance mechanisms, and induced plant defence against Colletotrichum is essential to support sustainable disease management practices in the field. This review therefore summarizes the current knowledge of the identified causative agent of tea plant anthracnose, the infection strategies and pathogenicity of C. gloeosporioides, anthracnose disease resistance mechanisms, and the caffeine-induced defence response against Colletotrichum infection. The information reported in this review will advance our understanding of host–pathogen interactions and eventually help us to develop new disease control strategies.     

Cinnamyl alcohol dehydrogenases-C and D, key enzymes in lignin biosynthesis, play an essential role in disease resistance in Arabidopsis

The deposition of lignin during plant–pathogen interactions is thought to play a role in plant defence. However, the function of lignification genes in plant disease resistance is poorly understood. In this article, we provide genetic evidence that the primary genes involved in lignin biosynthesis in Arabidopsis, CAD-C and CAD-D , act as essential components of defence to virulent and avirulent strains of the bacterial pathogen Pseudomonas syringae pv. tomato , possibly through the salicylic acid defence pathway. Thus, in contrast with cellulose synthesis, whose alteration leads to an increase in disease resistance, alteration of the cell wall lignin content leads directly or indirectly to defects in some defence components.     

Context-dependent defence in terrestrial plants: the effects of light and nutrient availability on plant resistance against herbivory

The context‐dependent defence (CDD) hypothesis predicts that defence levels of plant species against herbivory are not fixed but vary with environmental conditions, in a way that is specific for plant species that share evolutionary adaptations to resource conditions exemplified by similar maximum relative growth rates. More specifically, we expected plants from resource‐poor environments to display high defence levels but not when grown under resource‐rich conditions, whereas the reverse – plants from resource‐rich conditions displaying low defence levels but not when grown under resource‐poor conditions – is not necessarily the case. In this study, we used multiple‐choice bioassays in which leaf discs were fed to larvae of Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae) as an efficient and effective way of indicating plant defence levels. This generalist herbivore was capable of detecting both inter‐ and intraspecific differences in defence among plant species. The CDD was tested by exploring the effects of various experimental resource conditions (light, nutrients) upon the herbivore preferences and by comparing these preferences with the maximum relative growth rate of plant species. The experimental results provide general support for the CDD hypothesis with respect to nutrient‐level variation but the effects were not related to the origin of the plant species tested. Variation in light conditions did not result in consistent effects upon herbivore preferences. The CDD therefore can be formulated more precisely as: defence levels of plant species vary under different environmental conditions but in a way that is specific for plant species that share evolutionary adaptations to similar nutrient conditions. This more precise CDD hypothesis is a useful addition to existing optimal‐defence theory because of its focus on the possible plastic effects of resource conditions upon plant defence levels. This is relevant when designing experimental plant–herbivore studies.     

Cytology of induced systemic resistance of tomato to Phytophthora infestans

The infection of tomato leaves by Phytophthora infestans was followed using cytological methods. Fungal ingress and plant reactions in untreated and induced resistant plants were studied. Systemic disease resistance was induced by a local pre-infection with the same fungus. Induction retarded fungal progress at the leaf surface, epidermis and in the mesophyll. The reduced numbers of germinated cysts indicate the presence of fungitoxic substances on the leaf surface of induced plants. Frequency of fungal penetration through the outer epidermal cell wall was reduced, but only in plants exhibiting a high level of induced resistance. Autofluor-escent material, indicating the presence of lignin-like substances, accumulated rapidly beneath some of the appressoria, but this plant response was similar in induced and non-induced plants. Staining with aniline blue indicated that callose deposition was not involved in induced resistance. Thus, none of the cytologically investigated plant reactions correlated with the reduced penetration frequency observed. In the mesophyll, however, the cytological picture corresponding to a hypersensitive reaction occurred more often in induced plants. It is concluded that reduction of disease severity by induction is the result of the combined action of several successive defence reactions.Dedicated to the memory of Professor H. Grisebach     

植物根中质外体屏障结构和生理功能研究进展

综述了近10年来植物根中质外体屏障结构和功能的研究进展。质外体屏障指根中内、外皮层初生壁的凯氏带,或次生壁栓质化和木质化,以及植物体表角质层组成的保护组织,能隔绝水、离子和氧气不能自由进出植物体的屏障结构,具有保护植物体的生理功能。根中凯氏带的分子发育机理研究表明根内皮层类似哺乳动物上皮组织的保护作用。植物根中质外体保证内部各种生理代谢在稳定的内部环境中进行,是植物适应各种逆境的重要屏障结构。根中质外体屏障在植物适应干旱、洪涝灾害、离子胁迫和病虫害的侵袭等方面具有重要作用,在探索适应并修复极端生态环境的植物资源中有广阔的应用前景。     

Intraclonal variation in defence substances and palatability: a study on Carex and lemmings

Clonal sedges consist of integrated ramets at different development stages. Many of these sedges are important food for herbivores, yet differences in herbivore preferences and defence allocation between ramet development stages have not previously been evaluated. In this study we investigated intraclonal ramet variation in level of plant defence and nutrient compounds and intraclonal ramet preferences by lemmings ( Lemmus trimucronatus ) in field samples of a rhizomatous sedge ( Carex stans ). Plant defence was measured as the level of proteinase inhibitor activity (PIA) and the ratio of PIA to soluble plant proteins (SPP), whereas plant nutrients were measured as the level of soluble plant sugars (SPS) and SPP. Flowering ramets generally had a higher content of defence compared to vegetative ramets, which is consistent with the optimal defence theory predicting that defence compounds are allocated to the ramet stage of the highest fitness value. Compared to vegetative ramets, the flowering ramets had a lower content of SPP and a higher content of SPS. The lemmings showed preference differences between the ramet development stages, and to a large extent the ramet content of defence compounds and nutrient compounds covaried with these preferences in the predicted way. This study shows that defence allocation between ramet development stages of the clonal sedge Carex conforms to predictions of the optimal defence theory.     

TOR inhibition primes immunity and pathogen resistance in tomato in a salicylic acid-dependent manner

All organisms need to sense and process information about the availability of nutrients, energy status, and environmental cues to determine the best time for growth and development. The conserved target of rapamycin (TOR) protein kinase has a central role in sensing and perceiving nutritional information. TOR connects environmental information about nutrient availability to developmental and metabolic processes to maintain cellular homeostasis. Under favourable energy conditions, TOR is activated and promotes anabolic processes such as cell division, while suppressing catabolic processes. Conversely, when nutrients are limited or environmental stresses are present, TOR is inactivated, and catabolic processes are promoted. Given the central role of TOR in regulating metabolism, several previous works have examined whether TOR is wired to plant defence. To date, the mechanisms by which TOR influences plant defence are not entirely clear. Here, we addressed this question by testing the effect of inhibiting TOR on immunity and pathogen resistance in tomato. Examining which hormonal defence pathways are influenced by TOR, we show that tomato immune responses and disease resistance to several pathogens increase on TOR inhibition, and that TOR inhibition-mediated resistance probably requires a functional salicylic acid, but not jasmonic acid, pathway. Our results support the notion that TOR is a master regulator of the development–defence switch in plants.     

Experimental warming had little effect on carbon-based secondary compounds, carbon and nitrogen in selected alpine plants and lichens

Global warming is expected to change plant defence through its influence on plant primary resources. Increased temperature (T) will increase photosynthesis, and thus carbon (C) availability, but may also increase soil mineralization and availability of nitrogen (N). More access to C and N is expected to mainly increase plant growth, and, according to hypotheses on resource based defence, this could lower plant concentrations of carbon-based secondary compounds (CBSCs).We used two already established warming experiment with open top chambers (OTCs) and control plots in alpine south-western Norway, one on a ridge (8 years’ treatment) and a one in a leeside (3 years’ treatment), to study the effects of warming on plant and lichen defensive compound concentrations. The study included five vascular plant and six lichen species.One vascular plant species had lower concentration of CBSCs under elevated T, while the others did not respond to the treatment. In lichens there were no effects of warming on CBSCs, but a tendency to reduced total C concentrations. However, there were effects of warming on nitrogen, as the concentration decreased inside OTCs for three species, while it increased for one lichen species. Lichens generally had higher CBSC and total C concentrations on the ridge than in the leeside, but no such pattern were seen for vascular plants.No elevated temperature effect on CBCSs is most probably a result of high constitutive defence under the limiting alpine conditions, suggesting that chemical defence is little subject to change under climate warming, at least on a short-term basis. We suggest that the driving forces of plant defence in the arctic-alpine should be tested individually under controlled conditions, and suggest that competition from other plants may be a greater threat under climate warming than increased herbivory or disease attacks.     

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.     

Tolerance to deer herbivory and resistance to insect herbivores in the common evening primrose (Oenothera biennis)

The evolution of plant defence in response to herbivory will depend on the fitness effects of damage, availability of genetic variation and potential ecological and genetic constraints on defence. Here, we examine the potential for evolution of tolerance to deer herbivory in Oenothera biennis while simultaneously considering resistance to natural insect herbivores. We examined (i) the effects of deer damage on fitness, (ii) the presence of genetic variation in tolerance and resistance, (iii) selection on tolerance, (iv) genetic correlations with resistance that could constrain evolution of tolerance and (v) plant traits that might predict defence. In a field experiment, we simulated deer damage occurring early and late in the season, recorded arthropod abundances, flowering phenology and measured growth rate and lifetime reproduction. Our study showed that deer herbivory has a negative effect on fitness, with effects being more pronounced for late‐season damage. Selection acted to increase tolerance to deer damage, yet there was low and nonsignificant genetic variation in this trait. In contrast, there was substantial genetic variation in resistance to insect herbivores. Resistance was genetically uncorrelated with tolerance, whereas positive genetic correlations in resistance to insect herbivores suggest there exists diffuse selection on resistance traits. In addition, growth rate and flowering time did not predict variation in tolerance, but flowering phenology was genetically correlated with resistance. Our results suggest that deer damage has the potential to exert selection because browsing reduces plant fitness, but limited standing genetic variation in tolerance is expected to constrain adaptive evolution in O. biennis.     

A unified approach to the estimation and interpretation of resistance costs in plants

Plants exhibit a number of adaptive defence traits that endow resistance to past and current abiotic and biotic stresses. It is generally accepted that these adaptations will incur a cost when plants are not challenged by the stress to which they have become adapted--the so-called 'cost of adaptation'. The need to minimise or account for allelic variation at other fitness-related loci (genetic background control) is frequently overlooked when assessing resistance costs associated with plant defence traits. We provide a synthesis of the various experimental protocols that accomplish this essential requirement. We also differentiate those methods that enable the identification of the trait-specific or mechanistic basis of costs (direct methods) from those that provide an estimate of the impact of costs by examining the evolutionary trajectories of resistance allele frequencies at the population level (indirect methods). The advantages and disadvantages for each proposed experimental design are discussed. We conclude that plant resistance systems provide an ideal model to address fundamental questions about the cost of adaptation to stress. We also propose some ways to expand the scope of future studies for further fundamental and applied insight into the significance of adaptation costs.