The role of the jasmonate response in plant susceptibility to diverse pathogens with a range of lifestyles

Plants defend themselves against attack from insects and pathogens with various resistance strategies. The jasmonate and salicylate signaling pathways are two induced responses that protect plants against these attackers. Knowledge of the range of organisms that are affected by each response is important for understanding how plants coordinate their defenses against multiple attackers and the generality of effect of different resistance mechanisms. The jasmonate response is known to protect plants against a wide range of insect herbivores; in this study, we examined the role of the jasmonate response in susceptibility to eight pathogens with diverse lifestyles in the laboratory and field. Recent biochemical models suggest that the lifestyle of the pathogen (necrotroph versus biotroph) should predict whether the jasmonate response will be involved in resistance. We tested this by examining the susceptibility of wild-type (cv Castlemart with no known genes for resistance to the pathogens used) and jasmonate-deficient mutant tomato (Lycopersicon esculentum) plants (def1) and by employing rescue treatments of the mutant. Plant susceptibility to five of the eight pathogens we examined was reduced by the jasmonate response, including two bacteria (Pseudomonas syringae and Xanthomonas campestris), two fungi (Verticillium dahliae and Fusarium oxysporum f. sp. lycopersici), and an oomycete (Phytophthora infestans). Susceptibility to three fungi was unaffected (Cladosporium fulvum, Oidium neolycopersici, and Septoria lycopersici). Our results indicate that the jasmonate response reduces damage by a wide range of pathogens from different lifestyles, a result that contrasts with the emerging picture of diseases on Arabidopsis. Thus, the generality of jasmonate-based resistance of tomato challenges the view that ecologically distinct plant parasites are resisted via different mechanisms.     

Vector and virus induce plant responses that benefit a non-vector herbivore

The negative cross-talk between induced plant defences against pathogens and arthropod herbivores is exploited by vectors of plant pathogens: a plant challenged by pathogens reduces investment in defences that would otherwise be elicited by herbivores. This negative cross-talk may also be exploited by non-vector herbivores which elicit similar anti-herbivore defences in the plant. We studied how damage by the thrips Frankliniella occidentalis and/or infection with Tomato spotted wilt virus (TSWV) affect the performance of a non-vector arthropod: the two-spotted spider mite Tetranychus urticae, a parenchym feeder just like F. occidentalis. Juvenile survival of spider mites on plants inoculated with TSWV by thrips was higher than on control and on thrips-damaged plants. However, thrips damage did not reduce spider-mite survival as compared to the control, suggesting that the positive effect of TSWV on spider-mite survival is independent of anti-thrips defence. Developmental and oviposition rates were enhanced on plants inoculated with TSWV by thrips and on plants with thrips damage. Therefore, spider mites benefit from TSWV-infection of pepper plants, but also from the response of plants to thrips damage. We suggest that the positive effects of TSWV on this non-vector species cannot be explained exclusively by cross-talk between anti-herbivore and anti-pathogen plant defences.     

Jasmonate-dependent plant defense restricts thrips performance and preference

Background  

The western flower thrips (Frankliniella occidentalis [Pergande]) is one of the most important insect herbivores of cultivated plants. However, no pesticide provides complete control of this species, and insecticide resistance has emerged around the world. We previously reported the important role of jasmonate (JA) in the plant's immediate response to thrips feeding by using an Arabidopsis leaf disc system. In this study, as the first step toward practical use of JA in thrips control, we analyzed the effect of JA-regulated Arabidopsis defense at the whole plant level on thrips behavior and life cycle at the population level over an extended period. We also studied the effectiveness of JA-regulated plant defense on thrips damage in Chinese cabbage (Brassica rapa subsp. pekinensis).     

Plant volatiles as method of communication

Plants emit volatile compounds that can act as a communication method to insects, neighboring plants and pathogens. Plants respond to leaf and root damage by herbivores and pathogens by emitting these compounds. The volatile compounds can deter the herbivores or pathogens directly or indirectly by attracting their natural enemies to kill them. The simultaneous damage of plants by herbivores and pathogens can influence plant defense. The induced plant volatiles can also make neighboring plants ready for defense or induce defense in parts distant from the damaged area of the same plant. Belowground root herbivory can alter the defense response to aboveground leaf herbivory. In addition, most plants normally emit volatile compounds from their flowers that directly attract foraging mutualistic insects for nectar, which in turn perform the very important function of pollination for subsequent reproduction. The volatile compounds emitted from the floral and vegetative parts of plants belong to three main classes of compounds: terpenoids, phenylpropanoids/benzenoids, and C6-aldehydes (green-leaf volatiles). The volatile phytohormones methyl salicylate and methyl jasmonate serve as important signaling molecules for communication purposes, and interact with each other to optimize the plant defense response. Here we discuss and integrate the current knowledge on all types of communication between plants and insects, neighboring plants and pathogens that are mediated through plant volatiles.     

Jasmonate-dependent plant defenses mediate soybean thrips and soybean aphid performance on soybean

Insect herbivores from different feeding guilds induce different signaling pathways in plants. In this study, we examined the effects of salicylic acid (SA)- and jasmonic acid (JA)-mediated defenses on performance of insect herbivores from two different feeding guilds: cell-content feeders, soybean thrips and phloem feeders, soybean aphids. We used a combination of RT-qPCR analysis and elicitor-induced plant resistance to determine induction of SA and JA signaling pathways and the impact on herbivore performance. In the early interaction between the host plant and the two herbivores, SA and JA signaling seems to occur simultaneously. But overall, soybean thrips induced JA-related marker genes, whereas soybean aphids increased SA and ABA-related marker genes over a 24-h period. Populations of both soybean thrips and soybean aphids were reduced (47 and 25 %, respectively) in methyl jasmonate (MeJA)-pretreated soybean plants. SA treatment has no effect on either herbivore performance. A combination pretreatment of SA and MeJA did not impact soybean thrips population but reduced soybean aphid numbers which was comparable with MeJA treatment. Our data suggest that SA–JA antagonism could be responsible for the effect of hormone pretreatment on thrips performance, but not on aphid performance. By linking plant defense gene expression and elicitor-induced resistance, we were able to pinpoint the role for JA signaling pathway in resistance to two herbivores from different feeding guilds.     

硅对植物抗虫性的影响及其机制

硅不是植物必需营养元素,但硅在提高植物对一系列非生物和生物胁迫的抗性方面都具有重要作用。综述了硅对植物抗虫性的影响及其机制。在多数植物中,增施硅肥可增强其抗虫性;所增强的抗性与硅肥种类和施用方式之间存在关系。植物组织中沉积的硅可增加其硬度和耐磨度,降低植物可消化性,从而增强植物组成性防御,包括延缓昆虫生长发育、降低繁殖力、减轻植物受害程度;植物体内的硅含量以及硅沉积的位点和排列方式影响组成性防御作用的强度。此外,硅可以调节植物诱导性防御,包括直接防御和间接防御,直接防御涉及增加有毒物质含量、产生局部过敏反应或系统获得抗性、产生有毒化合物和防御蛋白,从而延缓昆虫发育;间接防御主要通过释放挥发性化合物吸引植食性昆虫的捕食性和寄生性天敌而导致植食性昆虫种群下降。     

Perception, signaling and molecular basis of oviposition-mediated plant responses

Eggs deposited on plants by herbivorous insects represent a threat as they develop into feeding larvae. Plants are not a passive substrate and have evolved sophisticated mechanisms to detect eggs and induce direct and indirect defenses. Recent years have seen exciting development in molecular aspects of egg-induced responses. Some egg-associated elicitors have been identified, and signaling pathways and egg-induced expression profiles are being uncovered. Depending on the mode of oviposition, both the jasmonic acid and salicylic acid pathways seem to play a role in the induction of defense responses. An emerging concept is that eggs are recognized like microbial pathogens and innate immune responses are triggered. In addition, some eggs contain elicitors that induce highly specific defenses in plants. Examples of egg-induced suppression of defense or, on the contrary, egg-induced resistance highlight the complexity of plant–egg interactions in an on-going arms race between herbivores and their hosts. A major challenge is to identify plant receptors for egg-associated elicitors, to assess the specificity of these elicitors and to identify molecular components that underlie various responses to oviposition.     

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.     

Are Defenses of Wild Radish Populations Well Matched with Variability and Predictablity of Herbivory?

Theory predicts that plants should employ constitutive (fixed) defenses when herbivory is consistently strong among years and induced (plastic) defenses when herbivory varies among years but is predictable within a season. We tested this theory by examining the herbivore species and damage censused over three seasons for 20 populations of wild radish in northern California. We conducted assays of constitutive resistance by challenging undamaged plants from these 20 populations with their common herbivores in the greenhouse. We assayed induced resistance by comparing the performance of herbivores on plants that had been experimentally damaged to undamaged plants from the same populations. Following damage, plants generally became more resistant to chewing herbivores (caterpillars) but more susceptible to sucking herbivores (aphids). Constitutive resistance to caterpillars was not stronger for populations that had high levels of herbivory that varied little among years, contrary to theory. Induced resistance may be stronger for plants from populations where herbivory varied more among years, consistent with expectations, although low power makes this conclusion equivocal. Induced resistance was not stronger for populations where early herbivory was a good predictor of late season herbivory. This lack of support for theory could have been caused by inadequacies with the experimental tests or with the theory and its assumptions. The theory assumes a coevolutionary equilibrium; however, high gene flow that has been reported for wild radish could disrupt matches between risk of herbivory and plant defense. The theory also assumes that resistance traits evolved as defenses against herbivory although these traits also serve other functions. Finally, the correlation we measured between early and late season herbivory may be at a temporal scale that is irrelevant since wild radish appears to adjust its defenses very rapidly.     

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.     

The Myriad Plant Responses to Herbivores

Abstract Plant responses to herbivores are complex. Genes activated on herbivore attack are strongly correlated with the mode of herbivore feeding and the degree of tissue damage at the feeding site. Phloem-feeding whiteflies and aphids that produce little injury to plant foliage are perceived as pathogens and activate the salicylic acid (SA)-dependent and jasmonic acid (JA)/ethylene-dependent signaling pathways. Differential expression of plant genes in response to closely related insect species suggest that some elicitors generated by phloem-feeding insects are species-specific and are dependent on the herbivore's developmental stage. Other elicitors for defense-gene activation are likely to be more ubiquitous. Analogies to the pathogen-incompatible reactions are found. Chewing insects such as caterpillars and beetles and cell-content feeders such as mites and thrips cause more extensive tissue damage and activate wound-signaling pathways. Herbivore feeding is not equivalent to mechanical wounding. Wound responses are a part of the induced responses that accompany herbivore feeding. Herbivores induce direct defenses that interfere with herbivore feeding, growth and development, fecundity, and fertility. In addition, herbivores induce an array of volatiles that creates an indirect mechanism of defense. Volatile blends provide specific cues to attract herbivore parasites and predators to infested plants. The nature of the elicitors for volatile production is discussed.     

Host plant and the predator Podisus nigrispinus: when the defense compounds of the plant affect the third trophic level

Many herbivorous insects can overcome chemical plant defenses, using the plant's defensive products for their own good, as a defense against predators. Eucalyptus spp. (Myrtaceae), recently introduced in Brazil, are rich in secondary compounds; however, there are reports that these plants have been suffering from population outbreaks of defoliating Lepidoptera in Brazil. The predator Podisus nigrispinus (Dallas) (Hemiptera: Pentatomidae) has been used against herbivorous insects in eucalyptus plantations, but little is known about its establishment in the field. This study aims to investigate whether the effectiveness of this predator may be affected indirectly by compounds of eucalyptus plants, when compared to guava, Psidium guajava L., a Brazilian native species of Myrtaceae. Thus, we evaluated the performance of P. nigrispinus on larvae of Thyrinteina arnobia (Stoll) (Lepidoptera: Geometridae) reared on eucalyptus (exotic species) or guava plants (native species). Podisus nigrispinus performance (reproduction and survival) was better on larvae fed on guava than on larvae fed on eucalyptus. It is possible that the negative effect on the predator's development occurred because of the plants’ secondary compounds appropriated by caterpillars, due to the short coevolutionary history between eucalyptus and the predator. The data suggest that the chemical compounds that could help the plant's defenses against herbivores may also affect their natural enemies, especially when the interaction between plant and natural enemy involves an exotic plant recently introduced into the insect's habitat.     

Jasmonate-mediated induced plant resistance affects a community of herbivores

1. The negative effect of induced plant resistance on the preference and performance of herbivores is a well‐documented ecological phenomenon that is thought to be important for both plants and herbivores. This study links the well‐developed mechanistic understanding of the biochemistry of induced plant resistance in the tomato system with an examination of how these mechanisms affect the community of herbivores in the field. 2. Several proteins that are induced in tomato foliage following herbivore damage have been linked causally to reductions in herbivore performance under laboratory conditions. Application of jasmonic acid, a natural elicitor of these defensive proteins, to tomato foliage stimulates induced responses to herbivory. 3. Jasmonic acid was sprayed on plants in three doses to generate plants with varying levels of induced responses, which were measured as increases in the activities of proteinase inhibitors and polyphenol oxidase. 4. Field experiments conducted over 3 years indicated that induction of these defensive proteins is associated with decreases in the abundance of all four naturally abundant herbivores, including insects in three feeding guilds, caterpillars, flea beetles, aphids, and thrips. Induced resistance killed early instars of noctuid caterpillars. Adult flea beetles strongly preferred control plants over induced plants, and this effect on host plant preference probably contributed to differences in the natural abundance of flea beetles. 5. The general nature of the effects observed in this study suggests that induced resistance will suppress many members of the herbivore community. By linking plant biochemistry, insect preference, performance, and abundance, tools can be developed to manipulate plant resistance sensibly and to predict its outcome under field conditions.     

The jasmonate pathway alters herbivore feeding behaviour: consequences for plant defences

The jasmonate pathway is a highly conserved defensive cascade in plants that regulates the induction of resistance against herbivores; however, its role in herbivore feeding behaviour remains unknown. We used a mutant tomato plant (def‐1) deficient in the production of jasmonate‐related defensive proteins to test the hypothesis that genotypes with a reduced ability to induce resistance have a higher and more concentrated pattern of herbivore damage. Wild‐type and def‐1 plants received either damage by Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae) caterpillars or no damage. After treatment, we tested for systemic responses by allowing a free roaming S. exigua caterpillar to feed on the undamaged portions of plants. Weight‐gain and leaf consumption of S. exigua were highest on def‐1 plants, regardless of prior herbivore damage. Def‐1 plants also had fewer numbers of leaves and leaflets eaten, and fewer feeding holes, which was indicative of a more concentrated distribution of damage on mutant compared to wild‐type plants. Following these results, we mimicked the amount and distribution of feeding damage that wild‐type or jasmonate‐deficient plants would receive on wild‐type plants to test whether changes in feeding behaviour may feedback to influence the expression of induced resistance. We mimicked the distribution of damage in wild‐type and jasmonate‐deficient plants by allowing caterpillars to feed on either one (leaf 1 or 2) or two leaves (leaf 1 and 2). Increased herbivore damage resulted in higher proteinase inhibitor (PI) activity, a jasmonate‐regulated defensive protein, and lower S. exigua performance on wild‐type but not jasmonate‐deficient plants. Compared to undamaged plants, a concentrated pattern of herbivore damage increased systemic resistance; these induced responses were greater on leaflets with stronger vascular connections to the damaged leaf. A more dispersed pattern of caterpillar damage altered the expression of induced responses, but the outcome depended on the specific pattern of damage. When leaf 1 was damaged and then leaf 2, the undamaged (third) leaf (which is more strongly connected to leaf 1 than 2) expressed reduced the PI activity compared to plants receiving concentrated damage to leaf 1; whereas in plants where leaf 2 was first damaged and then leaf 1, there were no differences in PI activity in leaf 3 compared to plants receiving concentrated damage to leaf 2. Thus, induction of the jasmonate pathway may not only determine the amount and distribution of feeding damage by herbivores, but this may feedback to affect the subsequent expression of plant defence.     

Jasmonate-induced defenses: a tale of intelligence, collaborators and rascals

Plants have sophisticated defense systems to protect their tissues against the attack of herbivorous organisms. Many of these defenses are orchestrated by the oxylipin jasmonate. A growing body of evidence indicates that the expression of jasmonate-induced responses is tightly regulated by the ecological context of the plant. Ecological information is provided by molecular signals that indicate the nature of the attacker, the value of the attacked organs, phytochrome status and thereby proximity of competing plants, association with beneficial organisms and history of plant interactions with pathogens and herbivores. This review discusses recent advances in this field and highlights the need to map the activities of informational modulators to specific control points within our emerging model of jasmonate signaling.     

Ecological and Evolutionary Interactions between Wild Crucifers and Their Herbivorous Insects

Abstract Insects feeding on ten species of wild crucifer were investigated. Differences in host plant range and insect community structure were examined with regard to anti-herbivore defense mechanisms. Most of the crucifer species deterred insect herbivory by disappearing in the summer or by lowering their intrinsic quality as food for insects. Species with these defense mechanisms were exploited by only a few specialized herbivorous insects that seemed to have counter defenses. The plants without these defense mechanisms were used by many herbivorous insect species. Rorippa indica lacked direct defenses, but supported a low total density of herbivore individuals. This crucifer has an indirect defense mechanism: ants attracted to floral nectar defended the plant from deleterious herbivores. Crucifers that disappeared seasonally lacked other anti-herbivore defense mechanisms. This suggests that the phonological response is an alternative other responses to herbivore attack.     

Contrasting consequences of plant domestication for the chemical defenses of leaves and seeds in lima bean plants

Plant domestication is assumed to result in reduced levels of defensive compounds in crops, because this makes the plants more suitable for consumption by humans and livestock. We argue that this should mainly be reflected in the concentrations of defense compounds in the plant parts that are used for consumption and not necessarily for other parts of crop plants. We tested this hypothesis for domesticated lima bean (Phaseolus lunatus), by comparing its chemical defenses against a leaf herbivore, the beet armyworm (Spodoptera exigua), and a seed predator, the beetle Zabrotes subfasciatus. For seeds and leaves we determined the concentrations of cyanogenic glycosides (CNGs) in cultivated varieties and wild populations and evaluated the preference and performance of the herbivores when exposed to leaves and seeds from wild and cultivated plants. Concentrations of CNGs were significantly different between wild and cultivated plants. In the leaves the concentration of CNGs in the cultivated varieties were more than double that of the wild leaves. In contrast, seeds from cultivated plants had up to 20 times lower CNG concentration compared to seeds from the wild populations. Insect preference and performance do not parallel the chemical data. Larvae of S. exigua preferred wild leaves but had higher survival on cultivated leaves. The beetles, however, strongly preferred seeds from cultivated plants and females developed more quickly on these seeds. We conclude that domestication of P. lunatus has altered the concentration of CNGs in both the seeds and the leaves in opposite directions. This results in differential effects on the herbivores that attack these two plant structures. The contrasting effect of domestication on different plant tissues can be explained by the fact that bean plants have been specifically selected for human consumption of the seeds. Tissue-specific effects of plant domestication on plant defenses can be expected for other crops as well.     

Indirect defence of plants against herbivores: using Arabidopsis thaliana as a model plant

In their defence against pathogens, herbivorous insects, and mites, plants employ many induced responses. One of these responses is the induced emission of volatiles upon herbivory. These volatiles can guide predators or parasitoids to their herbivorous prey, and thus benefit both plant and carnivore. This use of carnivores by plants is termed indirect defence and has been reported for many plant species, including elm, pine, maize, Lima bean, cotton, cucumber, tobacco, tomato, cabbage, and Arabidopsis thaliana. Herbivory activates an intricate signalling web and finally results in defence responses such as increased production of volatiles. Although several components of this signalling web are known (for example the plant hormones jasmonic acid, salicylic acid, and ethylene), our understanding of how these components interact and how other components are involved is still limited. Here we review the knowledge on elicitation and signal transduction of herbivory-induced volatile production. Additionally, we discuss how use of the model plant Arabidopsis thaliana can enhance our understanding of signal transduction in indirect defence and how cross-talk and trade-offs with signal transduction in direct defence against herbivores and pathogens influences plant responses.