Mechanisms of plant defense against insect herbivores

Plants respond to herbivory through various morphological, biochemicals, and molecular mechanisms to counter/offset the effects of herbivore attack. The biochemical mechanisms of defense against the herbivores are wide-ranging, highly dynamic, and are mediated both by direct and indirect defenses. The defensive compounds are either produced constitutively or in response to plant damage, and affect feeding, growth, and survival of herbivores. In addition, plants also release volatile organic compounds that attract the natural enemies of the herbivores. These strategies either act independently or in conjunction with each other. However, our understanding of these defensive mechanisms is still limited. Induced resistance could be exploited as an important tool for the pest management to minimize the amounts of insecticides used for pest control. Host plant resistance to insects, particularly, induced resistance, can also be manipulated with the use of chemical elicitors of secondary metabolites, which confer resistance to insects. By understanding the mechanisms of induced resistance, we can predict the herbivores that are likely to be affected by induced responses. The elicitors of induced responses can be sprayed on crop plants to build up the natural defense system against damage caused by herbivores. The induced responses can also be engineered genetically, so that the defensive compounds are constitutively produced in plants against are challenged by the herbivory. Induced resistance can be exploited for developing crop cultivars, which readily produce the inducible response upon mild infestation, and can act as one of components of integrated pest management for sustainable crop production.     

Herbivore induced plant volatiles: Their role in plant defense for pest management

Plants respond to herbivory through different defensive mechanisms. The induction of volatile emission is one of the important and immediate response of plants to herbivory. Herbivore-induced plant volatiles (HIPVs) are involved in plant communication with natural enemies of the insect herbivores, neighboring plants, and different parts of the damaged plant. Release of a wide variety of HIPVs in response to herbivore damage and their role in plant-plant, plant-carnivore and intraplant communications represents a new facet of the complex interactions among different trophic levels. HIPVs are released from leaves, flowers, and fruits into the atmosphere or into the soil from roots in response to herbivore attack. Moreover, HIPVs act as feeding and/or oviposition deterrents to insect pests. HIPVs also mediate the interactions between the plants and the microorganisms. This review presents an overview of HIPVs emitted by plants, their role in plant defense against herbivores and their implications for pest management.     

Natural selection and the joint evolution of toleranceand resistance as plant defenses

Plants can defend themselves against the damaging effects of herbivory in at least two ways. Resistant plants avoid or deter herbivores and are therefore fed upon less than susceptible plants. Tolerant plants are not eaten less than plants with little tolerance, but the effects of herbivore damage are not so detrimental to a tolerant plant as they are to a less tolerant plant. Biologists have suggested that these two strategies might represent two alternative and redundant defenses against herbivory since they appear to serve the same function for plants. I explore the relationship between resistance and tolerance, particularly with regards to how the joint evolution of these two traits will influence the evolution of plant defense. Although I briefly review some of the contributions of theory to the study of tolerance, I concentrate on an empirical, ecological genetic approach to the study of the evolution of these characters and the coevolution of tolerance and herbivores. In order to understand the evolution of any trait, we must understand the evolutionary forces acting on the trait. Specifically, we must understand how natural selection acts on tolerance. I review several studies that have specifically measured the form of selection acting on tolerance and tested the hypothesis that resistance and tolerance are alternative strategies. I also present a statistical analysis that does not support the hypothesis that herbivores are selective agents on tolerance. Finally, I consider a variety of constraints that possibly restrict the evolution of tolerance. This revised version was published online in July 2006 with corrections to the Cover Date.     

Associational effects and the maintenance of polymorphism in plant defense against herbivores: review and evidence

Many plant species have evolved defense traits against herbivores. Associational effects (AEs) refer to a kind of apparent interaction where the herbivory risk to a focal plant species depends on the composition of other plant species in a neighborhood. Despite ample evidence for AEs between different plant species, this point of view has rarely been applied to polymorphism in defense traits within a plant species. The purpose of this review is to highlight an overlooked role of conspecific AEs in maintaining polymorphism in antiherbivore defense. First, I present a general review of AE between plant species and its role in the coexistence of plant species. This viewpoint of AE can be applied to genetic polymorphism within a plant species, as it causes frequency‐ and density‐dependent herbivory between multiple plant types. Second, I introduce a case study of conspecific AEs in the trichome‐producing (hairy) and glabrous plants of Arabidopsis halleri subsp. gemmifera. Laboratory and semi‐field experiments illustrated that AEs against the brassica leaf beetle Phaedon brassicae mediate a minority advantage in defense and fitness between hairy and glabrous plants. Combined with a statistical modeling approach, field observation revealed that conspecific AEs can maintain the trichome dimorphism via negative frequency‐dependent selection in a plant population. Finally, I discuss spatial and temporal scales at which AEs contribute to shaping genetic variation in antiherbivore defense in a plant metapopulation. Based on the review and evidence, I suggest that AEs play a key role in the maintenance of genetic variation within a plant species.     

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.     

Plant defenses against parasitic plants show similarities to those induced by herbivores and pathogens

Herbivores and pathogens come quickly to mind when one thinks of the biotic challenges faced by plants. Important but less appreciated enemies are parasitic plants, which can have important consequences for the fitness and survival of their hosts. Our knowledge of plant perception, signaling and response to herbivores and pathogens has expanded rapidly in recent years, but information is generally lacking for parasitic species. In a recent paper we reported that some of the same defense responses induced by herbivores and pathogens—notably increases in jasmonic acid (JA), salicylic acid (SA), and a hypersensitive-like response (HLR)—also occur in tomato plants upon attack by the parasitic plant Cuscuta pentagona (field dodder). Parasitism induced a distinct pattern of JA and SA accumulation, and growth trials using genetically-altered tomato hosts suggested that both JA and SA govern effective defenses against the parasite, though the extent of the response varied with host plant age. Here we discuss similarities between the induced responses we observed in response to Cuscuta parasitism to those previously described for herbivores and pathogens and present new data showing that trichomes should be added to the list of plant defenses that act against multiple enemies and across kingdoms.Key words: Cuscuta, induced defenses, parasitic plant, jasmonic acid, salicylic acid, phytohormones, hypersensitive response, trichomes, defense signalingSeveral thousand species of plants are parasitic, stealing water and nutrients from other plants through a specialized feeding structure, the haustorium.¹ Haustoria are thought to be modified roots that grow into tissues and fuse with the vascular system of their photosynthetic hosts.¹ Considering that these parasites include some of the world''s most devastating agricultural pests² and are influential, fascinating components of natural communities,^1,3 surprisingly little is known about host defenses induced by parasitic plants. To address this shortcoming, we used a metabolomics approach to track biochemical changes induced in tomato shoots by invasion of C. pentagona haustoria.⁴We found that parasitism induced large increases in both JA and SA beginning about 24 hr after formation of haustoria began, but that production of JA and SA was largely separated in time. Host production of JA was transitory and reached a maximum at 36 hr, whereas SA peaked 12 hr later and remained elevated 5 d later. We also found that C. pentagona grew larger on mutant tomato plants in which the SA (NahG) or JA (jasmonic acid-insensitive1) pathways were disrupted, suggesting that these hormones can act independently to reduce parasite growth. Taken together, these findings suggest the staggered production of JA and SA may be an adaptive response to parasitism—by sequentially activating the JA and SA pathways, tomato plants may minimize the potential for cross-talk between these sometimes antagonistic pathways^5,6 and utilize both signaling molecules.^6,7 Thus, defenses against C. pentagona contain elements characteristic of responses to both herbivores (primarily JA-mediated⁸) and pathogens (primarily SA-mediated⁹)—though it should be noted that some herbivores induce SA¹⁰ and some pathogens JA.¹¹ It is worth noting that parasitism induced predominately cis-JA, the same jasmonate isomer induced by herbivore feeding.¹² Host responses to Cuscuta seem to most resemble that of known plant responses to some pathogens in which a similar sequence of JA and SA production is required to limit disease.¹³C. pentagona also triggered a hypersensitive-like response (HLR) localized around the points of parasite attachment. Using a trypan blue staining technique, we verified host cell death in these parasite-induced lesions. The deposition of eggs by some insect herbivores can elicit the formation of necrotic tissue,¹⁴ but localized cell death is most widely associated with the hypersensitive response (HR) of plants to pathogens. This complex early defense response can restrict the growth and spread of viruses, fungi and bacteria.⁹ Our work adds to existing evidence¹⁵ that the Cuscuta-induced HLR can play a similar role by preventing or limiting the growth of the parasite.An interesting discovery was that the first attachment by C. pentagona elicited almost no response from young 10-day-old hosts, whereas a subsequent attachment after 10 days induced the wholesale changes discussed above (we also found changes in abscisic acid and free fatty acids). Trials in which we varied the age of the host and parasite indicated that host age, rather than a priming effect on defenses, determined the magnitude of response. We have previously observed that Cuscuta spp. in natural populations germinate very early in the growing season, and hypothesized that this tactic promotes successful parasitism by ensuring the presence of young hosts; recent field work seems to corroborate this.¹⁶ As with the response to Cuscuta parasitism, levels of host plant defenses against insects¹⁷ and pathogens¹⁸ are known to be vary with host age.In an earlier paper we reported that tomato plants parasitized by C. pentagona released greater amounts of volatiles than did unparasitized control plants.¹⁹ The production and release of volatiles is a hallmark of plant responses to feeding by herbivores.²⁰ Herbivore-induced volatiles serve as an indirect plant defense by attracting herbivores'' natural enemies,²¹ repelling herbivores,²² or acting as intra-plant signals that prime systemic responses.²³ Although less well documented, pathogen attack can also induce emissions of volatile compounds,²⁴ some of which are antimicrobial and may serve as a direct defense against infection.²⁵ The same volatile compounds induced by Cuscuta (e.g., 2-carene, α-pinene, limonene, β-phellandrene) were also induced by caterpillar feeding and application of JA.¹⁹ Like herbivores, the JA induced by C. pentagona may regulate the emissions of plant volatiles. Whether or how parasitic plant-induced volatiles might function in defense is unknown, but they presumably could affect host plant choice by Cuscuta seedlings, which use plant volatiles to locate and select hosts.²⁶Following on from our previous studies we examined the potential role of host trichomes in resistance to parasitism by C. pentagona. Plant trichomes have been long appreciated as the first line of defense against insect herbivores^27,28 and more recently pathogens.²⁹ We hypothesized that trichomes could also defend against parasitic plants based on our observations that (1) tomato trichomes become denser with age (Fig. 1), notably on hypocotyls which is the first area contacted by Cuscuta seedlings, and (2) these trichomes can act as a physical barrier to C. pentagona seedlings. To test this hypothesis we allowed seedlings of C. pentagona to attach to 25-day-old tomato plants (Solanum lycopersicum ‘Halley 3155’) in a climate controlled growth chamber. Of 20 trials conducted, in six (30%) the parasite seedling was completely blocked by trichomes and was unable to reach the host stem—the parasite perished in each of these. Type I glandular trichomes, which are several millimeters long with a glandular tip,³⁰ were primarily responsible for the blocking effect. Thus, trichomes can defend against parasitic plants in a manner analogous to herbivores by physically obstructing their movement. Interestingly, the effectiveness of trichomes is also dependent on age of the host since those on younger tomato plants (<20 days old) are too sparse to impede Cuscuta seedlings (Fig. 1).Open in a separate windowFigure 1A newly germinated Cuscuta pentagona seedling encircles and attaches to the hypocotyl of a 10-day-old tomato seedling; the early development of haustoria are visible as nod-like swellings. The trichomes on hypocotyls of young tomato seedlings are not dense enough to affect C. pentagona seedlings, but the increased density of trichomes on 25-day-old plants can act as a physical barrier that blocks parasite seedlings (inset).Considering that the majority of plant defenses are mediated by only a small number of master regulators (e.g., JA, SA, ethylene),⁷ it is not surprising that plant responses to parasitic plants share commonalities with those induced by herbivores and pathogens. These few molecules mediate complex, interacting signaling networks that can be variously activated and modified by plants to tune defenses against a seemingly endless variety of attackers.⁷ Our finding that JA and SA act to defend plants from attack by other plants, further support these phytohormones as ‘global’ defense signals. It is also apparent that constitutive defenses, such as trichomes, can be effective against diverse antagonists (e.g., herbivores and parasitic plants). These new insights into host defenses against parasitic plants suggest many avenues of needed research including the molecular events induced by parasitic plant attack, the parasite-derived cues that elicit responses, and the ways in which JA and SA act to reduce parasite growth. Finally, our findings suggest it might be possible to manipulate induced responses or host plant age by varying planting date to control parasitic plants in agriculture.     

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.     

Gall insects can avoid and alter indirect plant defenses

Parasitic species can dramatically alter host traits. Some of these parasite-induced changes can be considered adaptive manipulations that benefit the parasites. Gall-inducing insects are parasites well known for their ability to alter host-plant morphology and physiology, including the distribution of plant defensive compounds. Here it was investigated whether gall-inducing species alter indirect plant defenses, involving the release of volatile compounds that are attractive to foraging natural enemies. Using field and factorial laboratory experiments, volatile production by goldenrod (Solidago altissima) plants was examined in response to attack by two gall-inducing species, the tephritid fly Eurosta solidaginis and the gelechiid moth Gnorimoschema gallaesolidaginis, as well as the meadow spittlebug, Philaenus spumarius, and the generalist caterpillar Heliothis virescens. Heliothis virescens elicited strong indirect defensive responses from S. altissima, but the gall-inducing species and spittlebugs did not. More significantly, infestation by E. solidaginis appeared to suppress volatile responses to subsequent attack by the generalist caterpillar. The extensive control that E. solidaginis apparently exerts over host-plant defense responses may reduce the predation risk for the gall inducer and the subsequent herbivore, and could influence community-level dynamics, including the distribution of herbivorous insect species associated with S. altissima parasitized by E. solidaginis.     

Relationships among Key deer, insect herbivores, and plant quality

Deer can have severe effects on plant communities, which in turn can affect insect communities. We studied the effects of Key deer herbivory on the incidence of insect herbivores that occur within deer habitats in the lower Florida Keys, within the National Key Deer Refuge (NKDR). We analyzed plant chemistry (tannins, nitrogen) and surveyed for the occurrence of insects (above the browse tier) among plant species that were either deer-preferred or less-preferred. Results indicated higher levels of foliar tannins on islands with fewer Key deer and larger amounts of foliar nitrogen on islands with a high density of Key deer. Consequently, leaf miners were significantly more abundant on islands with high deer density, irrespective of deer-preference of plant species. On islands with a high deer density, incidence of leaves damaged by chewing insects was lower on preferred plant species but greater on less-preferred species than on islands with fewer deer. No apparent patterns were evident in the distribution of leaf gallers among plant species or islands with different deer density. Our results imply that plant nutrition levels—either preexisting or indirectly affected by deer deposition—are more important than plant defenses in determining the distribution of insect herbivores in the NKDR. Although high densities of the endangered Key deer have negative effects on some plant species in the NKDR, it seems Key deer might have an indirect positive influence on insect incidence primarily above the browse tier. Further research is warranted to enable fuller understanding of the interactions between Key deer and the insect community.     

Positive interactions between herbivores and plant diversity shape forest regeneration

The effects of herbivores and diversity on plant communities have been studied separately but rarely in combination. We conducted two concurrent experiments over 3 years to examine how tree seedling diversity, density and herbivory affected forest regeneration. One experiment factorially manipulated plant diversity (one versus 15 species) and the presence/absence of deer (Odocoileus virginianus). We found that mixtures outperformed monocultures only in the presence of deer. Selective browsing on competitive dominants and associational protection from less palatable species appear responsible for this herbivore-driven diversity effect. The other experiment manipulated monospecific plant density and found little evidence for negative density dependence. Combined, these experiments suggest that the higher performance in mixture was owing to the acquisition of positive interspecific interactions rather than the loss of negative intraspecific interactions. Overall, we emphasize that realistic predictions about the consequences of changing biodiversity will require a deeper understanding of the interaction between plant diversity and higher trophic levels. If we had manipulated only plant diversity, we would have missed an important positive interaction across trophic levels: diverse seedling communities better resist herbivores, and herbivores help to maintain seedling diversity.     

A conserved pattern in plant‐mediated interactions between herbivores

Plant‐mediated interactions between herbivores are important determinants of community structure and plant performance in natural and agricultural systems. Current research suggests that the outcome of the interactions is determined by herbivore and plant identity, which may result in stochastic patterns that impede adaptive evolution and agricultural exploitation. However, few studies have systemically investigated specificity versus general patterns in a given plant system by varying the identity of all involved players. We investigated the influence of herbivore identity and plant genotype on the interaction between leaf‐chewing and root‐feeding herbivores in maize using a partial factorial design. We assessed the influence of leaf induction by oral secretions of six different chewing herbivores on the response of nine different maize genotypes and three different root feeders. Contrary to our expectations, we found a highly conserved pattern across all three dimensions of specificity: The majority of leaf herbivores elicited a negative behavioral response from the different root feeders in the large majority of tested plant genotypes. No facilitation was observed in any of the treatment combinations. However, the oral secretions of one leaf feeder and the responses of two maize genotypes did not elicit a response from a root‐feeding herbivore. Together, these results suggest that plant‐mediated interactions in the investigated system follow a general pattern, but that a degree of specificity is nevertheless present. Our study shows that within a given plant species, plant‐mediated interactions between herbivores of the same feeding guild can be stable. This stability opens up the possibility of adaptations by associated organisms and suggests that plant‐mediated interactions may contribute more strongly to evolutionary dynamics in terrestrial (agro)ecosystems than previously assumed.     

虫害诱导的植物挥发物:植物与植食性昆虫及其天敌相互作用的进化产物

综述了植物、植食性昆虫及其天敌相互作用的进化过程。虫害诱导的植物挥发物的特征和功能是植物-植食性昆虫-天敌之间长期进化的结果。在植物、植食性昆虫与天敌相互作用的进化过程中,3个不同营养级,包括植物、植食性昆虫和天敌有着各自的调节和利用虫害诱导的植物挥发物的策略。但有一些问题,如通过实验研究得出的诱导防御在田间是否真正能起到保护作用等需进一步研究、阐明。     

植物病原物的群体遗传学

品种单一化、生产密集型和一年多茬的现代农业特点导致病原物呈现出进化速度加快、致病力增强及流行风险增大趋势。深入研究病原物群体遗传学对认识病害的流行、有效选育和使用抗性品种乃至控制病害具有重要意义。文章阐述了植物病原物群体遗传学的研究目标和内容、突变、基因迁移、基因重组、随机遗传漂变和自然选择5大遗传机制在植物病原物进化过程中的作用,以及目前植物病原物群体遗传学研究的现状。     

Induced resistance to herbivores and the information content of early season attack

Current models of induced plant defenses all assume that herbivory is predictable. Present damage must provide information about the likelihood of future attack. We tested this assumption by measuring the relationship between damage early in the season and the number of subsequent attacks by cotton leaf perforators, Bucculatrix thurberiella, to plants of wild cotton, Gossypium thurberi, at three sites in the Sonoran desert. Damage early in the season was a good predictor of the number of new mines initiated throughout the season for plants in Florida Canyon. This result was neither evidence for nor against induced resistance nor was it a consequence of induced resistance. This is because induced resistance has been found to affect survival of miners but previous damage did not affect the initiation of new mines. At two other sites, early damage was not related to future attacks. This difference in predictability of attack may be related to inducibility of plants since Florida Canyon was the only site that provided evidence of induced resistance in a previous study. We found no evidence that the usefulness of information based on early season damage decreased as the season progressed. Assessment of attacks on all shoots of the plant was more useful at predicting later damage to an assay shoot than was assessment of solely the assay shoot. Number of mines, produced only by G. thurberiella, was a better predictor of subsequent attacks by G. thurberiella than were chews and rasps which were made by many different herbivores. However, general chewing damage was a better indicator of the level of induction against G. thurberiella than was the more specific mining damage. Plants may respond more to chewing damage even though mining damage is a better predictor of future attacks.