Avoidance and suppression of plant defenses by herbivores and pathogens

Plants are nutritious and hence herbivores and phytopathogens have specialized to attack and consume them. In turn, plants have evolved adaptations to detect and withstand these attacks. Such adaptations we call ‘defenses’ and they can operate either directly between the plant and the plant consumer or indirectly i.e. when taking effect via other organisms such as predators and parasitoids of herbivores. Plant defenses put selection pressure on plant-consumers and, as a result, herbivores and pathogens have evolved counter-adaptations to avoid, resist, or manipulate plant defenses. Here we review how plant consumers have adapted to cope with plant defenses and we will put special emphasis on the phenomenon of suppression of plant defenses.     

Plant responses induced by herbivores

Physiological and chemical traits of many plant species change in response to real or simulated herbivory. These changes often have significant impacts on behavior, growth, survivorship, feeding and oviposition of insects. However, evidence that plants gain direct or indirect protection from insect enemies thereby is equivocal at present. Evidence is lacking for an impact of induced defenses on insect population dynamics, but few studies have sought it. More detailed studies of plant physiology, biochemistry, genetics and net benefit to individual plants are needed to identify the adaptive significance of induced defenses.     

Parasitism by Cuscuta pentagona attenuates host plant defenses against insect herbivores

Considerable research has examined plant responses to concurrent attack by herbivores and pathogens, but the effects of attack by parasitic plants, another important class of plant-feeding organisms, on plant defenses against other enemies has not been explored. We investigated how attack by the parasitic plant Cuscuta pentagona impacted tomato (Solanum lycopersicum) defenses against the chewing insect beet armyworm (Spodoptera exigua; BAW). In response to insect feeding, C. pentagona-infested (parasitized) tomato plants produced only one-third of the antiherbivore phytohormone jasmonic acid (JA) produced by unparasitized plants. Similarly, parasitized tomato, in contrast to unparasitized plants, failed to emit herbivore-induced volatiles after 3 d of BAW feeding. Although parasitism impaired antiherbivore defenses, BAW growth was slower on parasitized tomato leaves. Vines of C. pentagona did not translocate JA from BAW-infested plants: amounts of JA in parasite vines grown on caterpillar-fed and control plants were similar. Parasitized plants generally contained more salicylic acid (SA), which can inhibit JA in some systems. Parasitized mutant (NahG) tomato plants deficient in SA produced more JA in response to insect feeding than parasitized wild-type plants, further suggesting cross talk between the SA and JA defense signaling pathways. However, JA induction by BAW was still reduced in parasitized compared to unparasitized NahG, implying that other factors must be involved. We found that parasitized plants were capable of producing induced volatiles when experimentally treated with JA, indicating that resource depletion by the parasite does not fully explain the observed attenuation of volatile response to herbivore feeding. Collectively, these findings show that parasitic plants can have important consequences for host plant defense against herbivores.     

Like herbivores,parasitic plants are limited by host nitrogen content

Herbivores generally benefit from increased plant nitrogen content, because the nitrogen content of animals is much higher than that of plants. Consequently, high plant nitrogen alleviates the profound stoichiometric imbalance that herbivores face in their diets. Parasitic plants provide the opportunity to test this generalization for consumers across kingdoms. We fertilized two microhabitats in a California salt marsh that were dominated by Salicornia virginica or a mixture of S. virginica and Jaumea carnosa. The nitrogen content of both host plants and of the holoparasite Cuscuta salina (dodder) increased in fertilized plots in both microhabitats. Cuscuta preferred to attack Jaumea, although Jaumea had lower nitrogen content than Salicornia. When host nitrogen content was altered by fertilizing plots, however, the percent cover of the parasite doubled. Although parasitic plants and their hosts have similar tissue nitrogen contents, suggesting no stoichiometric imbalance between host and consumer, parasitic plants do not feed on host tissue, but on host xylem and phloem, which are very low in nitrogen. Consequently, parasitic plants face the same dietary stoichiometric constraints as do herbivores, and both herbivores and holoparasitic plants may respond positively to increases in host nitrogen status.     

Plant breeding: importance of plant secondary metabolites for protection against pathogens and herbivores

Summary Chemical protection plays a decisive role in the resistance of plants against pathogens and herbivores. The so-called secondary metabolites, which are a characteristic feature of plants, are especially important and can protect plants against a wide variety of microorganisms (viruses, bacteria, fungi) and herbivores (arthropods, vertebrates). As is the situation with all defense systems of plants and animals, a few specialized pathogens have evolved in plants and have overcome the chemical defense barrier. Furthermore, they are often attracted by a given plant toxin. During domestication of our crop and food plants secondary metabolites have sometimes been eliminated. Taking lupins as an example, it is illustrated that quinolizidine alkaloids are important as chemical defense compounds and that the alkaloid-free varieties (sweet lupins), which have been selected by plant breeders, are highly susceptible to a wide range of herbivores to which the alkaloid-rich wild types were resistant. The potential of secondary metabolites for plant breeding and agriculture is discussed.     

Proteinase inhibitor gene families: Strategies for transformation to improve plant defenses against herbivores

Recent evidence indicates that the presence of serine proteinase inhibitors in plant leaves can reduce predation by insects. Plants can now be transformed with proteinase inhibitor genes with strong promoters to express the inhibitor proteins in relatively high levels at specific times. Inhibitors having variable specificities against digestive proteinases of insects and pathogens can now be assessed for their possible role(s) in natural plant defense and for their potential usefulness in protecting crop plants against herbivores.     

Disentangling effects of induced plant defenses and food quantity on herbivores by fitting nonlinear models

Abstract Plants can respond to herbivore damage through both broad-scale (systemic) and localized induced responses. While many studies have quantified the impact of systemic responses on herbivores, measuring the impact of localized changes is difficult because plant tissues that have suffered direct damage may represent both a lower quality and a lower quantity of food. This article uses nonlinear models to disentangle the confounding effects of prior herbivory on food quantity and quality. The first (null) model assumes that herbivore performance is determined only by the quantity of food available to an average herbivore. Modified models allow two distinct effects of damage-induced defenses: an increase in the amount of food each herbivore is required to consume in order to achieve maximum performance and a reduction in the maximum performance even when herbivores are fed ad lib. Maximum likelihood methods were used to fit the models to data from field experiments in which Colorado potato beetle (Leptinotarsa decemlineata) larvae were reared on three varieties of potatoes that had been damaged to varying degrees by adult beetles. Prior damage reduced the mean mass of beetles at pupation, and this effect was due to both a decrease in food quantity and induced changes in food quality. In contrast, beetle survival was affected in some cases by reduced food quantity but showed no responses that could be attributed to induced defenses. I discuss this result in the context of previous studies of induced (mostly systemic) responses in the potato-potato beetle system, and I suggest that detailed studies of particular chemical responses and the proposed method of combining bioassays with quantitative models should be used as complementary approaches in future studies of herbivore-induced defenses in plants.     

Strategies used by bacterial pathogens to suppress plant defenses

Plant immune systems effectively prevent infections caused by the majority of microbial pathogens that are encountered by plants. However, successful pathogens have evolved specialized strategies to suppress plant defense responses and induce disease susceptibility in otherwise resistant hosts. Recent advances reveal that phytopathogenic bacteria use type III effector proteins, toxins, and other factors to inhibit host defenses. Host processes that are targeted by bacteria include programmed cell death, cell wall-based defense, hormone signaling, the expression of defense genes, and other basal defenses. The discovery of plant defenses that are vulnerable to pathogen attack has provided new insights into mechanisms that are essential for both bacterial pathogenesis and plant disease resistance.     

Not poles apart: Antarctic soil fungal communities show similarities to those of the distant Arctic

Antarctica's extreme environment and geographical isolation offers a useful platform for testing the relative roles of environmental selection and dispersal barriers influencing fungal communities. The former process should lead to convergence in community composition with other cold environments, such as those in the Arctic. Alternatively, dispersal limitations should minimise similarity between Antarctica and distant northern landmasses. Using high‐throughput sequencing, we show that Antarctica shares significantly more fungi with the Arctic, and more fungi display a bipolar distribution, than would be expected in the absence of environmental filtering. In contrast to temperate and tropical regions, there is relatively little endemism, and a strongly bimodal distribution of range sizes. Increasing southerly latitude is associated with lower endemism and communities increasingly dominated by fungi with widespread ranges. These results suggest that micro‐organisms with well‐developed dispersal capabilities can inhabit opposite poles of the Earth, and dominate extreme environments over specialised local species.     

Jasmonate-deficient plants have reduced direct and indirect defences against herbivores

Plants employ a variety of defence mechanisms, some of which act directly by having a negative effect on herbivores and others that act indirectly by attracting natural enemies of herbivores. In this study we asked if a common jasmonate‐signalling pathway links the regulation of direct and indirect defences in plants. We examined the performance of herbivores (direct defence) and the attraction of natural enemies of herbivores (indirect defence) to wild‐type tomato plants and mutant plants that are deficient in the production of the signalling hormone jasmonic acid. Wild‐type plants supported lower survivorship of caterpillars compared with jasmonic acid‐deficient plants. Damaged wild‐type plants were more attractive to predaceous mites compared with undamaged wild‐type plants, whereas damaged jasmonate‐deficient plants were not more attractive to predators. Damaged wild‐type plants induced a greater production of volatile compounds (primarily the sesquiterpene β‐caryophyllene and the monoterpenes α‐pinene, β‐pinene, 2‐carene and β‐phellandrene) compared with damaged jasmonate‐deficient plants. Treating jasmonate‐deficient plants with exogenous jasmonic acid restored both the direct and indirect defence capabilities, demonstrating that jasmonic acid is an essential regulatory component for the expression of direct and indirect plant defence.     

Constitutive plant toxins and their role in defense against herbivores and pathogens

Most recent investigations have focused on induced, rather than constitutive, plant defenses. Yet significant research has helped to illuminate some of the principal characteristics of constitutive defenses, including mechanisms of action and synergistic effects, as well as strategies used by herbivores and pathogens to circumvent them.     

Transgenic tobacco and peanut plants expressing a mustard defensin show resistance to fungal pathogens

Defensins are small positively charged, antimicrobial peptides (~5 kDa in size) and some of them exhibit potent antifungal activity. We have cloned the complete cDNA containing an ORF of 243 bp of a defensin of mustard. The deduced amino acid sequence of the peptide showed more than 90% identity to the amino acid sequence of the well-characterized defensins, RsAFP-1 and RsAFP-2 of Raphanus sativus. We have generated and characterized transgenic tobacco and peanut plants constitutively expressing the mustard defensin. Transgenic tobacco plants were resistant to the fungal pathogens, Fusarium moniliforme and Phytophthora parasitica pv. nicotianae. Transgenic peanut plants showed enhanced resistance against the pathogens, Pheaoisariopsis personata and Cercospora arachidicola, which jointly cause serious late leaf spot disease. These observations indicate that the mustard defensin gene can be deployed for deriving fungal disease resistance in transgenic crops.     

Plant resistance to parasitic plants: molecular approaches to an old foe

Parasitic weeds pose severe constraint on major agricultural crops. Varying levels of resistance have been identified and exploited in the breeding programmes of several crops. However, the level of protection achieved to date is either incomplete or ephemeral. Resistance is mainly determined by the coexistence of several mechanisms controlled by multigenic and quantitative systems. Efficient control of the parasite requires a better understanding of the interaction and their associated resistance mechanisms at the histological, genetic and molecular levels. Application of postgenomic technologies and the use of model plants should improve the understanding of the plant-parasitic plant interaction and drive not only breeding programmes through either marker-assisted selection (MAS) or transgenesis but also the development of alternative methods to control the parasite. This review presents the current approaches targeting the characterization of resistance mechanisms and explores their potentiality to control parasitic plants.     

Plant quality and predation risk mediated by plant ontogeny: consequences for herbivores and plants

Bottom‐up and top‐down impacts on herbivores can be influenced by plant productivity, structural complexity, vigor and size. Although these traits are likely to vary with plant development, the influence of plant ontogeny on the relative importance of plant quality (i.e. bottom‐up forces) and predation risk (i.e. top‐down forces) has been the focus of little previous investigation. We evaluated the role of plant ontogeny for the relative importance of bottom‐up and top‐down forces on insect herbivore abundance, species richness, and species diversity attacking the tropical tree Casearia nitida. We also quantified the cascading effects on herbivory, growth and reproduction of this plant species. Plant quality traits (nitrogen and phenolic compounds) were assessed in saplings and reproductive trees. Bottom‐up forces were manipulated by fertilizing plants from both ontogenetic stages. Top‐down forces were manipulated by excluding insectivorous birds from saplings and reproductive trees. Plant ontogeny influenced foliage quality in terms of total phenolics, which were in greater concentration in reproductive trees than in saplings; however, it did not influence bottom‐up forces as modified by fertilization. Bird exclusion increased herbivore density with the same magnitude on both stages. Ontogeny influenced species diversity, which was greater in reproductive trees than in saplings, and also influenced treatment impacts on species richness and diversity. Although top‐down forces increased herbivory equally on plants of each ontogenetic stage, the two stages showed different overcompensation responses to increased damage: caged saplings produced greater leaf biomass than non‐caged saplings, whereas caged trees increased in height proportionally more than non‐caged trees. In sum, plant ontogeny influenced the impact of bird predation on herbivore density, species richness, and species diversity, and the growth variables affected by increased damage in caged plants. We suggest that plant ontogeny can contribute to some extent to the influence of plant quality and the third trophic level on herbivores in this system.     

Assessing the biosecurity risk from pathogens and herbivores to indigenous plants: lessons from weed biological control

Some potentially invasive herbivores/pathogens in their home range may attack plants originating from another geographic area. Methods are required to assess the risk these herbivores/pathogens pose to these plants in their indigenous ecosystems. The processes and criteria used by weed biological control researchers to assess the impact of potential biological control agents on a plant species in its non-native range provide a possible framework for assessing risks to indigenous plants. While there are similarities between these criteria such as the need for clear objectives, studies in the native range of the herbivore/pathogen, good knowledge of the ecology of the target plant and taxonomy of the plant and herbivore/pathogen, and modelling of the interaction between the two organisms, there are some important differences in approach. These include the need to consider the threat classification of the plant, the likely greater risk from polyphagous herbivores/pathogens than oligophagous or monophagous species, and the need to consider the impact of an additional natural enemy in conjunction with a suite of existing natural enemies. The costs of conducting a risk assessment of a herbivore/pathogen in another country that damages plants indigenous to another geographic area means that criteria will be needed for deciding which foreign herbivore/pathogen species should be assessed. These criteria could include the threat classification of the plant, the amount of damage to the particular plant organs affected, and the importance in key ecosystems.     

Chemical defenses and the susceptibility of tropical marine brown algae to herbivores

Summary I assayed phenolic and tannin concentrations in a number of species of temperate and tropical brown algae of the genera Sargassum and Turbinaria. Tropical species in both genera contained consistently low levels of phenolics and tannins (species means ranged between 0 and 1.6% [measured as % dry weight of the thallus]). Levels of phenolics in temperate species of Sargassum were variable and consistently much higher than in tropical species (species means ranged between 3 and 12% by dry weight). This pattern of latitudinal variation in phenolic levels in Sargassum conflicts with previous predictions for latitudinal variation in the chemical defenses of marine organisms. The low levels of phenolics present in the tropical species that I analyzed may also explain recent results (Hay 1984; Lewis 1985) demonstrating that tropical Sargassum and Turbinaria are often preferentially consumed by herbivorous fishes and echinoids.     

Elm defence against herbivores and pathogens: morphological,chemical and molecular regulation aspects

Elms (Ulmus spp.) have long been appreciated for their environmental tolerance, landscape and ornamental value, and the quality of their wood. Although elm trees are extremely hardy against abiotic stresses such as wind and pollution, they are susceptible to attacks of biotic stressors. Over 100 phytopathogens and invertebrate pests are associated with elms: fungi, bacteria and insects like beetles and moths, and to a lesser extent aphids, mites, viruses and nematodes. While the biology of the pathogen and insect vector of the Dutch elm disease has been intensively studied, less attention has been paid so far to the defence mechanisms of elms to other biotic stressors. This review highlights knowledge of direct and indirect elm defences against biotic stressors focusing on morphological, chemical and gene regulation aspects. First, we report how morphological defence mechanisms via barrier formation and vessel occlusion prevent colonisation and spread of wood- and bark-inhabiting fungi and bacteria. Second, we outline how secondary metabolites such as terpenoids (volatile terpenoids, mansonones and triterpenoids) and phenolics (lignans, coumarins, flavonoids) in leaves and bark are involved in constitutive and induced chemical defence mechanisms of elms. Third, we address knowledge on how the molecular regulation of elm defence is orchestrated through the interaction of a huge variety of stress- and defence-related genes. We conclude by pointing to the gaps of knowledge on the chemical and molecular mechanisms of elm defence against pest insects and diseases. An in-depth understanding of defence mechanisms of elms will support the development of sustainable integrated management of pests and diseases attacking elms.     

The multifaceted function of BAK1/SERK3: Plant immunity to pathogens and responses to insect herbivores

Almost a decade ago BRI1-associated kinase 1 (BAK1) was identified as a co-receptor of brassinosteroid (BR) insensitive 1 (BRI1), the receptor for BRs, which plays an essential role in transducing BR signaling to regulate plant development. BAK1 is also critical in resistance to various pathogens. BAK1 rapidly binds to certain receptors for pathogen/microbe-associated molecular patterns (PAMPs/MAMPs) after the perception of pathogen elicitors and is required for the full elicitation of pathogen-induced defense responses, such as the activation of the mitogen-activated protein kinase 6 (MPK6) and production of reactive oxygen species. Thus, BAK1 functions in both BR signaling and PAMP-triggered immunity (PTI). Recently BAK1 was also found to play an important role in mediating defense responses against an insect herbivore (Manduca sexta) of Nicotiana attenuata. In this interaction, BAK1 positively modulates wound- or herbivore feeding-induced accumulation of jasmonic acid (JA) and JA-isoleucine (JA-Ile). This mini-review summarizes recent advances in our understanding of the functions of BAK1 in resistance to pathogens and herbivores.Key words: BAK1, defense, herbivore, immunity, insect, jasmonate, pathogen, wounding