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.     

Antiherbivore defenses alter natural selection on plant reproductive traits

While many studies demonstrate that herbivores alter selection on plant reproductive traits, little is known about whether antiherbivore defenses affect selection on these traits. We hypothesized that antiherbivore defenses could alter selection on reproductive traits by altering trait expression through allocation trade‐offs, or by altering interactions with mutualists and/or antagonists. To test our hypothesis, we used white clover, Trifolium repens, which has a Mendelian polymorphism for the production of hydrogen cyanide—a potent antiherbivore defense. We conducted a common garden experiment with 185 clonal families of T. repens that included cyanogenic and acyanogenic genotypes. We quantified resistance to herbivores, and selection on six floral traits and phenology via male and female fitness. Cyanogenesis reduced herbivory but did not alter the expression of reproductive traits through allocation trade‐offs. However, the presence of cyanogenic defenses altered natural selection on petal morphology and the number of flowers within inflorescences via female fitness. Herbivory influenced selection on flowers and phenology via female fitness independently of cyanogenesis. Our results demonstrate that both herbivory and antiherbivore defenses alter natural selection on plant reproductive traits. We discuss the significance of these results for understanding how antiherbivore defenses interact with herbivores and pollinators to shape floral evolution.     

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.     

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。     

Insect eggs suppress plant defence against chewing herbivores

Plants activate direct and indirect defences in response to insect egg deposition. However, whether eggs can manipulate plant defence is unknown. In Arabidopsis thaliana, oviposition by the butterfly Pieris brassicae triggers cellular and molecular changes that are similar to the changes caused by biotrophic pathogens. In the present study, we found that the plant defence signal salicylic acid (SA) accumulates at the site of oviposition. This is unexpected, as the SA pathway controls defence against fungal and bacterial pathogens and negatively interacts with the jasmonic acid (JA) pathway, which is crucial for the defence against herbivores. Application of P. brassicae or Spodoptera littoralis egg extract onto leaves reduced the induction of insect‐responsive genes after challenge with caterpillars, suggesting that egg‐derived elicitors suppress plant defence. Consequently, larval growth of the generalist herbivore S. littoralis, but not of the specialist P. brassicae, was significantly higher on plants treated with egg extract than on control plants. In contrast, suppression of gene induction and enhanced S. littoralis performance were not seen in the SA‐deficient mutant sid2‐1, indicating that it is SA that mediates this phenomenon. These data reveal an intriguing facet of the cross‐talk between SA and JA signalling pathways, and suggest that insects have evolved a way to suppress the induction of defence genes by laying eggs that release elicitors. We show here that egg‐induced SA accumulation negatively interferes with the JA pathway, and provides an advantage for generalist herbivores.     

不同土壤线虫功能团对水稻生长及地上部植食者的影响

探明土壤生物多营养级相互作用是了解生态功能调控机制的核心。本研究通过调控土壤线虫的典型功能团的完全交互设计(食微线虫有无、植食线虫有无、捕杂食线虫有无)探索了线虫功能团对水稻(Oryza sativa)生长及褐飞虱(Nilaparvata lugens)数量的影响。结果表明, 与不接种线虫相比, 植食线虫显著增加水稻根系生物量(P < 0.05), 显著增加其茎叶总酚含量(P < 0.05); 单独的食微线虫增加了褐飞虱数量(P < 0.05), 但显著降低水稻根系生物量(P < 0.05); 捕杂食线虫促进水稻茎叶生长, 降低了褐飞虱数量; 当食微、植食和捕杂食线虫同时存在时, 植物茎叶及根系总酚含量均处于较高水平, 暗示其抗虫潜力更强。总之, 处于较高营养级的捕杂食线虫能够通过调控植食和食微线虫的数量, 提高植物的防御能力, 暗示土壤生物调控措施在植物地上部病原物防控方面有重要的前景。     

Indirect plant defense against insect herbivores: a review

Plants respond to herbivore attack by launching 2 types of defenses: direct defense and indirect defense. Direct defense includes all plant traits that increase the resistance of host plants to insect herbivores by affecting the physiology and/or behavior of the attackers. Indirect defense includes all traits that by themselves do not have significant direct impact on the attacking herbivores, but can attract natural enemies of the herbivores and thus reduce plant loss. When plants recognize herbivore‐associated elicitors, they produce and release a blend of volatiles that can attract predators, parasites, and other natural enemies. Known herbivore‐associated elicitors include fatty acid–amino acid conjugates, sulfur‐containing fatty acids, fragments of cell walls, peptides, esters, and enzymes. Identified plant volatiles include terpenes, nitrogenous compounds, and indoles. In addition, constitive traits including extrafloral nectars, food bodies, and domatia can be further induced to higher levels and attract natural enemies as well as provide food and shelter to carnivores. A better understanding of indirect plant defense at global and componential levels via advanced high throughput technologies may lead to utilization of indirect defense in suppression of herbivore damage to plants.     

Interactions among fungal endophytes,grasses and herbivores

The interaction between two species often depends on the presence or absence of a third species. One widespread three-species interaction involves fungal endophytes infecting grasses and the herbivores that feed upon them. The endophytes are allied with the fungal family Clavicipitaceae and grow systemically in intercellular spaces in above-ground plant tissues including seeds. Like relatedClaviceps species, the endophytes produce a variety of alkaloids that make the host plants toxic or distasteful to herbivores. A large number of grass species are infected, especially cool-season grasses in temperate areas. Field and laboratory studies have shown that herbivores avoid infected plants in choice trials and suffer increased mortality and decreased growth on infected grasses in feeding experiments. Resistance to herbivores may provide a selective advantage to infected plants in competitive interactions with noninfected plants. Recent studies have shown that differential herbivory can reverse competitive hierarchies among plant species. Both endophyte-infected and noninfected tall fescue grass (Festuca arundinacea) are outcompeted by orchardgrass (Dactylis glomerata) in the absence of insect herbivory. However, when herbivores are present infected tall fescue outcompetes orchardgrass. These results suggest that the frequency of infection in grass species and grassland communities will increase over time. Several studies are reviewed illustrating increases in infection frequency within grass populations subject to herbivore pressure. Endophytic fungi may be important regulators of plant-herbivore interactions and so indirectly affect the structure and dynamics of plant communities.     

Diversity protects plant communities against generalist molluscan herbivores

Wildflower strips are used to increase natural enemies of crop pests and to conserve insect diversity on farmland. Mollusks, especially slugs, can affect the vegetation development in these strips considerably. Although recent theoretical work suggests that more diverse plant communities will exhibit greater resistance against herbivore pressure, empirical studies are scarce. We conducted a semi‐natural experiment in wildflower strips, manipulating trophic structure (reduction in herbivorous mollusks and reduction in major predators) and plant diversity (2, 6, 12, 20 and 24 sown species). This design allowed us to assess the effect of plant diversity, biomass and composition on mollusks, and vice versa, the effect of mollusc abundance on vegetation. Seven species of mollusks were found in the strips, with the slugs Arion lusitanicus, Deroceras reticulatum and Deroceras panormitanum being most frequent. We found a negative relationship between plant diversity and mollusk abundance, which was due predominantly to a decrease in the agricultural pest species A. lusitanicus. These results are consistent with the hypothesis that plant diversity can reduce the impact of herbivores. However, plant identity also had an effect on mollusks, and accounted for a much larger fraction of the variation in mollusk communities than biodiversity effects. While overall plant diversity decreased during the 3 years of the study, in the final year the highest plant diversity was found in the plots where mollusk populations were experimentally reduced. We conclude that selective feeding by generalist herbivores leads to changes in plant community composition and hence reduced plant diversity. Our results highlight the importance of plant biodiversity as protection against generalist herbivores, which if abundant can in the long term negatively impact plant diversity, driving the system along a “low plant diversity – high mollusk abundance” trajectory.     

Herbivore performance and plant defense after sequential attacks by inducing and suppressing herbivores

It is well known that herbivore-induced plant defenses alter host plant quality and can affect the behavior and performance of later arriving herbivores.Effects of sequential attacks by herbivores that either suppress or induce plant defenses are less well studied.We sequentially infested leaves of tomato plants with a strain of the phytophagous spider mite Tetranychus urticae that induces plant defenses and the closely related Tetranychus evansi, which suppresses plant defenses.Plant quality was quantified through oviposifion of both spider mite species and by measuring proteinase inhibitor activity using plant material that had been sequentially attacked by both herbivore species.Spider-mite oviposifion data show that T.evansi could suppress an earlier induction of plant defenses by T.urticae,and T.urticae could induce defenses in plants previously attacked by T.evansi in 1 day.Longer attacks by the second species did not result in further changes in oviposifion.Proteinase inhibitor activity levels showed that T.evansi suppressed the high activity levels induced by T.urticae to constitutive levels in 1 day,and further suppressed activity to levels similar to those in plants attacked by T.evansi alone.Attacks by T.urticae induced proteinase inhibitor activity in plants previously attacked by T.evansi,eventually to similar levels as induced by T.urticae alone.Hence,plant quality and plant defenses were significantly affected by sequential attacks and the order of attack does not affect subsequent performance,but does affect proteinase inhibitor activity levels.Based on our results,we discuss the evolution of suppression of plant defenses.     

Will plant vigor and tolerance be genetically correlated? Effects of intrinsic growth rate and self-limitation on regrowth

Plants are known to maintain fitness despite herbivore attack by a variety of damage-induced mechanisms. These mechanisms are said to confer tolerance, which can be measured as the slope of fitness over the proportion of plant biomass removed by herbivore damage. It was recently supposed by Stowe et al. (2000) that another plant property, general vigor, has little effect on tolerance. We developed simple models of annual monocarpic plants to determine if a genetic change in components of growth vigor will also change the fitness reaction to damage. We examined the impact of intrinsic growth rate on the tolerance reaction norm slope assuming plants grow geometrically, i.e., without self-limitation. In this case an increase in intrinsic growth rate decreases tolerance (the reaction norm slope becomes more negative). A logistic growth model was used to examine the impact of self-limiting growth on the relationship between intrinsic growth rate and the tolerance reaction norm slope. With self-limitation, the relationship is sensitive to the timing of attack. When attack is early and there is time for regrowth, increasing growth rate increases tolerance (slope becomes less negative). The time limitations imposed by late attack prevent appreciable regrowth and induce a negative relationship between growth rate and tolerance. In neither of these simple cases will the correlation between vigor and tolerance constrain selection on either trait. However, a positive correlation between growth rate and self-limitation will favor fast growth/strong self-limitation in a high-damage environment, but slow growth/weak self-limitation in a low-damage environment. Thus, fundamental growth rules that determine vigor have constitutive effects on tolerance. The net costs and benefits of damage-induced tolerance mechanisms will thus be influenced by the background imposed by fundamental growth rules. This revised version was published online in July 2006 with corrections to the Cover Date.     

Molecular aspects of plant responses to pathogens

Plants respond to infection by accumulating many compounds some of which may function in disease resistance. These include: phytoalexins, antifungal proteins, chitinases, glucanases, esterases, proteaes, phospholipases, lipoxygenases, ribonucleases, peroxidases, phenoloxidases, lignin, callose, hydroxyproline and glycine-rich glycoproteins, phenolic cross-linked polysachcarides, melanin-like pigments, salicylic acid, jasmonic acid, ethylene, peptides, oligosaccharides, hydrogen peroxide and active oxygen species. Though specific avirulence genes, elicitors and elicitor receptors have been reported, the production of defense-related compounds is nonspecific and can be elicited by pathogens, pathogen products and many organics and inorganics. The molecular implications of this specificity/nonspecificity and their significance to disease resistance and practical disease control will be discussed.     

Large herbivores facilitate an insect herbivore by modifying plant community composition in a temperate grassland

Large herbivores often co‐occur and share plant resources with herbivorous insects in grassland ecosystems; yet, how they interact with each other remains poorly understood. We conducted a series of field experiments to investigate whether and how large domestic herbivores (sheep; Ovis aries) may affect the abundance of a common herbivorous insect (aphid; Hyalopterus pruni) in a temperate grassland of northeast China. Our exclosure experiment showed that 3 years (2010–2012) of sheep grazing had led to 86% higher aphid abundance compared with ungrazed sites. Mechanistically, this facilitative effect was driven by grazing altering the plant community, rather than by changes in food availability and predator abundance for aphids. Sheep significantly altered plant community by reducing the abundance of unpalatable forbs for the aphids. Our small‐scale forb removal experiment revealed an “associational plant defense” by forbs which protect the grass Phragmites australis from being attacked by the aphids. However, selective grazing on forbs by sheep indirectly disrupted such associational plant defense, making P. australis more susceptible to aphids, consequentially increasing the density of aphids. These findings provide a novel mechanistic explanation for the effects of large herbivores on herbivorous insects by linking selective grazing to plant community composition and the responses of insect populations in grassland ecosystems.     

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.