Indirect Defense Research Articles

Chemical and biological studies of natural and synthetic products for the highly selective control of pest insect species.

Tanacetum cinerariifolium was known to produce pyrethrins, but the mechanism of pyrethrin biosynthesis was largely unclear. The author showed that the nonmevalonate and oxylipin pathways underlie biosynthesis of the acid and alcohol moieties, respectively, and a GDSL lipase joins the products of these pathways. A blend of the green leaf volatiles and (E)-β-farnesene mediates the induction of wounding responses to neighboring intact conspecies by enhancing pyrethrin biosynthesis. Plants fight against herbivores underground as well as aboveground, and, in soy pulps, some fungi produce compounds selectively modulating ion channels in insect nervous system. The author proposed that indirect defense of plants occurs where microorganisms produce defense substances in the rhizosphere. Broad-spectrum pesticides, including neonicotinoids, may affect nontarget organisms. The author discovered cofactors enabling functional expression of insect nicotinic acetylcholine receptors (nAChRs). This led to understanding the mechanism of insect nAChR-neonicotinoid interactions, thus paving new avenues for controlling crop pests and disease vectors.

Comparative analyses of responses to exogenous and endogenous antiherbivore elicitors enable a forward genetics approach to identify maize gene candidates mediating sensitivity to herbivore-associated molecular patterns.

Crop damage by herbivorous insects remains a significant contributor to annual yield reductions. Following attack, maize (Zea mays) responds to herbivore-associated molecular patterns (HAMPs) and damage-associated molecular patterns (DAMPs), activating dynamic direct and indirect antiherbivore defense responses. To define underlying signaling processes, comparative analyses between plant elicitor peptide (Pep) DAMPs and fatty acid-amino acid conjugate (FAC) HAMPs were conducted. RNA sequencing analysis of early transcriptional changes following Pep and FAC treatments revealed quantitative differences in the strength of response yet a high degree of qualitative similarity, providing evidence for shared signaling pathways. In further comparisons of FAC and Pep responses across diverse maize inbred lines, we identified Mo17 as part of a small subset of lines displaying selective FAC insensitivity. Genetic mapping for FAC sensitivity using the intermated B73 × Mo17 population identified a single locus on chromosome 4 associated with FAC sensitivity. Pursuit of multiple fine-mapping approaches further narrowed the locus to 19 candidate genes. The top candidate gene identified, termed FAC SENSITIVITY ASSOCIATED (ZmFACS), encodes a leucine-rich repeat receptor-like kinase (LRR-RLK) that belongs to the same family as a rice (Oryza sativa) receptor gene previously associated with the activation of induced responses to diverse Lepidoptera. Consistent with reduced sensitivity, ZmFACS expression was significantly lower in Mo17 as compared to B73. Transient heterologous expression of ZmFACS in Nicotiana benthamiana resulted in a significantly increased FAC-elicited response. Together, our results provide useful resources for studying early elicitor-induced antiherbivore responses in maize and approaches to discover gene candidates underlying HAMP sensitivity in grain crops.

Feeding Volatiles of Larval Sparganothis pilleriana (Lepidoptera: Tortricidae) Attract Heterospecific Adults of the European Grapevine Moth.

Plants release volatiles in response to caterpillar feeding. These herbivore-induced plant volatiles (HIPVs) attract natural enemies of the herbivores and repel or attract conspecific adult herbivores in a tri-trophic interaction which has been considered to be an indirect plant defense against herbivores. Recently, we demonstrated the attraction of male and female European grapevine moth, Lobesia botrana (Denis & Schiffermüller) (Lepidoptera: Tortricidae) to a blend of phenylacetonitrile and acetic acid, two compounds identified as HIPVs in heterospecific apple-leafroller interactions. The ecological basis of our findings is not clearly understood. Thus, this work was undertaken to investigate HIPVs in the grapevine-leafroller interaction and study the response of heterospecific adults L. botrana, to these volatiles. We collected headspace volatiles emitted from uninfested grapevines and grapevines infested with larvae of a generalist herbivore, the grapevine leafroller moth, Sparganothis pilleriana (Denis & Schiffermüller), and analyzed them using gas chromatography/mass spectrometry. Infested grape leaves released three compounds (phenylacetonitrile, indole, and 2-phenylethanol) not found from uninfested leaves. Nine different blends, comprising a full factorial set of the three compounds with each blend containing acetic acid, were tested in a field-cage trial. Only lures containing phenylacetonitrile caused a significant increase in trap catches compared to the other lures and blank traps. Electroantennographic tests show that L. botrana can detect the compounds. The results confirm our hypothesis that phenylacetonitrile is released during grapevines infestation with herbivores, and attracts adult L. botrana.

Distance Dependent Contribution of Ants to Pollination but Not Defense in a Dioecious, Ambophilous Gymnosperm.

Dioecious plants are obligate outcrossers with separate male and female individuals, which can result in decreased seed set with increasing distance between the sexes. Wind pollination is a common correlate of dioecy, yet combined wind and insect pollination (ambophily) could be advantageous in compensating for decreased pollen flow to isolated females. Dioecious, ambophilous gymnosperms Ephedra (Gnetales) secrete pollination drops (PDs) in female cones that capture airborne pollen and attract ants that feed on them. Plant sugary secretions commonly reward ants in exchange for indirect plant defense against herbivores, and more rarely for pollination. We conducted field experiments to investigate whether ants are pollinators and/or plant defenders of South American Ephedra triandra, and whether their contribution to seed set and seed cone protection varies with distance between female and male plants. We quantified pollen flow in the wind and assessed the effectiveness of ants as pollinators by investigating their relative contribution to seed set, and their visitation rate in female plants at increasing distance from the nearest male. Ants accounted for most insect visits to female cones of E. triandra, where they consumed PDs, and pollen load was larger on bigger ants without reduction in pollen viability. While wind pollination was the main contributor to seed set overall, the relative contribution of ants was distance dependent. Ant contribution to seed set was not significant at shorter distances, yet at the farthest distance from the nearest male (23 m), where 20 times less pollen reached females, ants enhanced seed set by 30% compared to plants depending solely on wind pollination. We found no evidence that ants contribute to plant defense by preventing seed cone damage. Our results suggest that, despite their short-range movements, ants can offset pollen limitation in isolated females of wind-pollinated plants with separate sexes. We propose that ants enhance plant reproductive success via targeted delivery of airborne pollen, through frequent contact with ovule tips while consuming PDs. Our study constitutes the first experimental quantification of distance-dependent contribution of ants to pollination and provides a working hypothesis for ambophily in other dioecious plants lacking pollinator reward in male plants.

Herbivory-Induced Emission of Volatile Terpenes in Chrysanthemum morifolium Functions as an Indirect Defense against Spodoptera litura Larvae by Attracting Natural Enemies.

Indirect defense is an important strategy employed by sessile plants to defend against herbivorous insects by recruiting the natural enemies of herbivores mediated by herbivore-induced plant volatiles (HIPVs). We aimed to determine whether indirect defense occurs in Compositae with Chrysanthemum morifolium as the model and elucidate the mechanisms underlying the biosynthesis of HIPVs. Using two-choice olfactometer bioassays, we showed that C. morifolium plants following infestation by larvae of the tobacco cutworm (Spodoptera litura, TCW) were significantly more attractive to two natural enemies of TCW larvae than control plants, indicating that indirect defense is an active defense strategy of C. morifolium. The chemical cue responsible for indirect defense in C. morifolium was identified as a complex blend of volatiles predominated by sesquiterpenes and monoterpenes. A total of 11 candidate terpene synthase (TPS) genes were identified by comparing the transcriptomes of healthy and TCW-infested plants. Gene expression analysis confirmed that up-regulated CmjTPS genes are consistent with the elevated emission of terpenes after herbivory treatment. Our study showed that the herbivore-induced emission of JA-dependent volatile terpenes attracted both predatory and parasitic enemies of herbivores. Generally, our findings indicate that indirect defense might be an important defense mechanism against insects in C. morifolium.

Molecular Hydrogen as a Novel Antitumor Agent: Possible Mechanisms Underlying Gene Expression.

While many antitumor drugs have yielded unsatisfactory therapeutic results, drugs are one of the most prevalent therapeutic measures for the treatment of cancer. The development of cancer largely results from mutations in nuclear DNA, as well as from those in mitochondrial DNA (mtDNA). Molecular hydrogen (H2), an inert molecule, can scavenge hydroxyl radicals (·OH), which are known to be the strongest oxidizing reactive oxygen species (ROS) in the body that causes these DNA mutations. It has been reported that H2 has no side effects, unlike conventional antitumor drugs, and that it is effective against many diseases caused by oxidative stress and chronic inflammation. Recently, there has been an increasing number of papers on the efficacy of H2 against cancer and its effects in mitigating the side effects of cancer treatment. In this review, we demonstrate the efficacy and safety of H2 as a novel antitumor agent and show that its mechanisms may not only involve the direct scavenging of ·OH, but also other indirect biological defense mechanisms via the regulation of gene expression.

Effects of Prohydrojasmon on the Number of Infesting Herbivores and Biomass of Field-Grown Japanese Radish Plants.

Prohydrojasmon (PDJ), an analog of jasmonic acid (JA), was found to induce direct and indirect defenses against herbivores in non-infested plants. To test whether PDJ can be used for pest control in crop production, we conducted experiments in pesticide-free Japanese radish fields from October 4 to December 12 in 2015. Twenty-four Japanese radish plants in three plots were treated with a 100 times-diluted commercial formulation (5%) of PDJ (treated plants), and 24 plants in three different plots were treated with water (control plants) until November 29 every week. Throughout the observation period, the number of aphids, leaf-mining fly larvae, vegetable weevils, and thrips was significantly lower on the treated plants than on the control plants. In contrast, the number of lepidopteran larvae was not significantly different between the treated and control plants throughout the study period. Parasitized aphids (mummies) were also observed in both plots. Poisson regression analyses showed that a significantly higher number of mummies was recorded on the treated plants as compared to that on the control plants when the number of aphids increased. This suggested that PDJ application to Japanese radish plants attracted more parasitoid wasps on the treated plants than on the control plants. We also identified eight terpenoids and methyl salicylate as the PDJ-induced plant volatiles in the headspace of the treated plants. Some of these volatiles might be responsible for attracting aphid-parasitoid wasps in the field. However, for other insect pests, we did not find any natural enemies. Interestingly, the genes of the JA and salicylic acid signaling pathways were differentially upregulated in the treated plants. We also observed that the PDJ treatments induced the expression of the genes related to glucosinolate biosynthesis and the subsequent isothiocyanate formation. Additionally, the weights of both the aboveground and belowground parts of the treated plants were significantly lower than those of the respective parts of the control plants. These results indicated that the treatment of Japanese radish plants with a 100 times-diluted commercial formulation of PDJ induced their direct and indirect defenses against several insect pest species to reduce their numbers, and negatively affected their biomass.

The enemy of my enemy is not always my friend: Negative effects of carnivorous arthropods on plants

Abstract Plants are members of complex communities of which arthropods are the most speciose members. The role of carnivores in shaping the outcome of multi‐trophic interactions by top‐down control of herbivores has been well studied. Particularly, the positive impacts of natural enemies of herbivores on plants through direct (consumptive) and indirect (non‐consumptive) effects on their prey and hosts have received considerable interest, while multi‐trophic interactions that result in negative effects on plants have received little attention. Negative impacts of carnivorous arthropods have been documented and arise when carnivores directly affect plants and/or their interactions with beneficial arthropods. In general, negative effects may be compensated by positive effects of other carnivorous arthropods, but their presence and significance is likely to be underestimated in tri‐trophic interactions. Recent studies have revealed that the composition and dynamics of the plant and arthropod community have a significant effect on plant fitness. Therefore, we encourage an approach that accounts for a larger community of species and interactions associated with plants, including interaction types in which carnivores may negatively affect plants. This review highlights specific interaction types that ultimately lead to negative effects of carnivores on plants. This synthesis presents alternative hypotheses to those that predict that carnivores invariably benefit plants. Testing potential costs and benefits of carnivores to plants will advance our understanding of indirect plant defence. A free Plain Language Summary can be found within the Supporting Information of this article.

Endophytic Colonization by the Entomopathogenic Fungus Beauveria Bassiana Affects Plant Volatile Emissions in the Presence or Absence of Chewing and Sap-Sucking Insects.

Entomopathogenic fungi are gaining acceptance in Integrated Pest Management (IPM) systems as effective and environmental safety biological control agents to protect a great variety of crops against pest insects. Many of these insect-pathogenic fungi can establish themselves as endophytes and thereby may induce the plant immune system. The activation of plant defenses by the fungal endophytic colonization can have a direct impact on herbivores and plant pathogens. An integral component of many plant defense responses is also the release of volatile organic compounds, which may serve as an indirect defense by attracting the natural enemies of herbivores. Here we investigated the effect of endophytic colonization by the entomopathogenic fungus Beauveria bassiana on the volatile emission by melon and cotton plants, either unharmed or after being damaged by sap-sucking aphids or leaf chewing caterpillars. We found that when the plants are colonized by B. bassiana they emit a different blend of volatile compounds compared to uncolonized control plants. Some of the emitted compounds have been reported previously to be released in response to herbivory and have been implicated in natural enemy attraction. Several of the compounds are also known to have antimicrobial properties. Therefore, endophytic colonization by B. bassiana might help to not only direct control insect pests but also increase the resistance of plants against agronomically important pests and phytopathogens.

Volatile emission and biosynthesis in endophytic fungi colonizing black poplar leaves.

Plant volatiles play a major role in plant–insect interactions as defense compounds or attractants for insect herbivores. Recent studies have shown that endophytic fungi are also able to produce volatiles and this raises the question of whether these fungal volatiles influence plant–insect interactions. Here, we qualitatively investigated the volatiles released from 13 endophytic fungal species isolated from leaves of mature black poplar (Populus nigra) trees. The volatile blends of these endophytes grown on agar medium consist of typical fungal compounds, including aliphatic alcohols, ketones and esters, the aromatic alcohol 2-phenylethanol and various sesquiterpenes. Some of the compounds were previously reported as constituents of the poplar volatile blend. For one endophyte, a species of Cladosporium, we isolated and characterized two sesquiterpene synthases that can produce a number of mono- and sesquiterpenes like (E)-β-ocimene and (E)-β-caryophyllene, compounds that are dominant components of the herbivore-induced volatile bouquet of black poplar trees. As several of the fungus-derived volatiles like 2-phenylethanol, 3-methyl-1-butanol and the sesquiterpene (E)-β-caryophyllene, are known to play a role in direct and indirect plant defense, the emission of volatiles from endophytic microbial species should be considered in future studies investigating tree-insect interactions.

Ca2+ signal contributing to jasmonic acid‐induced direct and indirect defense against the whitefly Bemisia tabaci in tomato plants

AbstractThe phytophagous whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) causes serious crop yield losses around the world especially by vectoring viruses. Exogenous jasmonic acid (JA) induces direct plant resistance to B. tabaci, but the underlying mechanism of JA‐induced exogenous defenses is not well understood. Here, we demonstrate that exogenous JA not only increases the cytosolic Ca2+ concentration ([Ca2+]cyt) in tomato mesophyll cells but also induces the expression of Ca2+‐sensor genes and plant defense genes. Pre‐treatment with Ca2+ inhibitor (ruthenium red) significantly repressed the elevation of [Ca2+]cyt, expression of JA‐induced genes, and emission of plant volatiles induced by JA, thus reducing the JA‐induced direct (feeding choice and fitness of B. tabaci) and indirect [olfactory choice and parasitism by the parasitoid Encarsia formosa Gahan (Hymenoptera: Aphelinidae)] plant resistance to B. tabaci. These results indicate that the Ca2+ signal induced by JA mediates and directs the plants defenses against whitefly. Present results will not only give us a better understanding of how exogenous JA influences the crop community, but also deliver some clues for the potential application of exogenous JA, as a plant elicitor, in whitefly management.

Species diversity and biological trait function: Effectiveness of ant–plant mutualism decreases as ant species diversity increases

Abstract One of the major concerns of ecological and evolutionary research is the prediction of community function in relation to the degree of biodiversity. To clarify the relationship between biodiversity and the expression of plant defence traits, we investigated ant–plant defensive mutualism in the pioneer plant Mallotus japonicus at several sites across Japan. The plant bears ant‐attracting extrafloral nectar (EFN) and food bodies (FBs) as indirect defence traits. To reveal variations in ant–plant interactions in the field, we measured species richness of nectar‐feeding ants and interaction strength between each ant species and the plant (visiting frequency of each ant species to the plant). We also investigated the expression of EFNs and FBs in natural plant populations at the study sites. To assess the defensive quality of each ant species, we then experimentally estimated the aggressiveness of the dominant ant species. To examine the link between ant species richness and the defensive function of ants, we conducted an ant‐exclusion experiment and a common garden experiment to clarify whether the defence efficacy of ants varied in relation to ant species richness. Ant species richness differed among the study sites. We found negative relationships between ant species richness and the mean interaction strength of ant species, the interaction strength of aggressive ant species and the number of EFNs per leaf. The effectiveness of indirect defence by ants was poor at sites where ant species richness was high. When cultivated in the same environment, plants from sites with low ant species richness developed a larger number of EFNs per leaf than those from sites with high ant species richness. Our results suggest that facultative ant–plant defensive mutualism is weakened at sites where ant species richness is high, resulting in a decrease in the number of EFNs per leaf. Such a link between species richness and an indirect trait function may help us to understand the evolutionary patterns of various species traits in complex biological communities. A free Plain Language Summary can be found within the Supporting Information of this article.

Genome-Wide Association Study Reveals Genomic Region Associated with Mite-Recruitment Phenotypes in the Domesticated Grapevine (Vitis vinifera).

Indirect defenses are plant phenotypes that reduce damage by attracting natural enemies of plant pests and pathogens to leaves. Despite their economic and ecological importance, few studies have investigated the genetic underpinnings of indirect defense phenotypes. Here, we present a genome-wide association study of five phenotypes previously determined to increase populations of beneficial (fungivorous and predacious) mites on grape leaves (genus Vitis): leaf bristles, leaf hairs, and the size, density, and depth of leaf domatia. Using a common garden genetic panel of 399 V. vinifera cultivars, we tested for genetic associations of these phenotypes using previously obtained genotyping data from the Vitis9kSNP array. We found one single nucleotide polymorphism (SNP) significantly associated with domatia density. This SNP (Chr5:1160194) is near two genes of interest: Importin Alpha Isoform 1 (VIT_205s0077g01440), involved in downy mildew resistance, and GATA Transcription Factor 8 (VIT_205s0077g01450), involved in leaf shape development. Our findings are among the first to examine the genomic regions associated with ecologically important plant traits that facilitate interactions with beneficial mites, and suggest promising candidate genes for breeding and genetic editing to increase naturally occurring predator-based defenses in grapevines.

Silicon Supplementation of Maize Impacts Fall Armyworm Colonization and Increases Predator Attraction.

Supplementation with Silicon (Si) is well-known for increasing resistance of grasses to insect herbivores. Although the exact underlying mechanism remains unknown, Si accumulation interacts with the jasmonic acid-signalling pathway, which modulates herbivore-induced plant defences. We examined whether Si supplementation alters direct and induced indirect defences in maize plants in ways that deter the initial infestation by the fall armyworm Spodoptera frugiperda (JE Smith). We assessed the herbivore's oviposition preference, neonate and third-instar larval performance as well as the recruitment of a predator of young larvae, the flower bug Orius insidiosus (Say), by herbivore-induced plant volatiles (HIPVs). In choice tests, S. frugiperda deposited about two times more eggs on -Si than on +Si maize. The mortality of neonate S. frugiperda larvae was about sixfold higher in +Si compared to -Si plants, even though they consumed similar leaf area on both treatments. Although there were no mortality differences, Si supplementation also impacted third-instar larvae that gained about twofold less weight than those fed on -Si maize. In olfactometer assays, O. insidiosus was not attracted to volatiles of uninfested maize plants with or without Si supplementation, but it was attracted to those emitted by fall armyworm-infested plants, irrespective of whether plants received Si supplementation. However, when the flower bug could choose between the volatiles released from -Si and +Si fall armyworm-infested plants, it preferentially oriented to +Si fall armyworm-infested plant. Our results show that Si supplementation in maize may deter fall armyworm colonization because of greater direct defences and attractiveness of HIPVs to the flower bug.

Feeding guild determines strength of top-down forces in multitrophic system experiencing bottom-up constraints

Nitrogen (N) and water are crucial in crop production but increasingly scarce environmental resources. Reducing their inputs can affect the whole plant-arthropod community including biocontrol agents. In a multitrophic system, we studied the interaction of the bottom-up effects of moderately reduced N concentration and/or water supply as well as the top-down effects of pests of different feeding guilds on plant nutritional quality (N and carbon concentration), direct defense (alkaloids and phenolics), and indirect defense (plant volatile organic compounds); on herbivore performance and host quality (N and carbon) to parasitoids and the latter's performance. Studied organisms were tomato plants, the sap feeders Macrosiphum euphorbiae and Bemisia tabaci, the leaf chewers Tuta absoluta and Spodoptera littoralis, and the parasitic wasps Aphelinus abdominalis and Necremnus tutae. Resource limitation affected plant quality, triggering bottom-up effects on herbivore and parasitoid performance, except for T. absoluta and N. tutae. Feeding guild had a major influence: bottom-up effects were stronger on sap feeders; N effects were stronger on sap feeders while water effects were stronger with leaf chewers (S. littoralis). Top-down effects of leaf chewer herbivory partly attenuated bottom-up effects and partly suppressed plant defenses. Bottom-up effects weakened when cascading up trophic levels. In summary, the interaction between plants, pests, and beneficial insects was modulated by abiotic factors, affecting insect performance. Simultaneous abiotic and biotic impact shaped plant biochemistry depending on the feeding guild: the biotic top-down effect of leaf chewer herbivory attenuated the bottom-up effects of plant nutrition and hence dominated the plant biochemical profile whereas in sap feeder infested leaves, it corresponded to the abiotic impact. This study highlights the plant's finely tuned regulatory system facilitating response prioritization. It offers perspectives on how smart manipulation of plant nutrient solutions might save resources while maintaining efficient biocontrol in crop production.

Evolutionary changes in an invasive plant support the defensive role of plant volatiles

SummaryIt is increasingly evident that plants interact with their outside world through the production of volatile organic compounds,1, 2, 3, 4, 5 but whether the volatiles have evolved to serve in plant defense is still a topic of considerable debate.3,6, 7, 8 Unharmed leaves constitutively release small amounts of volatiles, but when the leaves are damaged by herbivorous arthropods, they emit substantially more volatiles. These herbivore-induced plant volatiles (HIPVs) attract parasitoids and predators that kill insect herbivores,9, 10, 11, 12 and this can benefit the plants.13,14 As yet, however, there is no tangible evolutionary evidence that this tritrophic interplay contributes to the selection forces that have shaped the volatile emissions of plants.2,3,5, 6, 7, 8,15 With this in mind, we investigated the evolutionary changes in volatile emissions in invasive common ragwort and the respective defensive roles of its constitutive and inducible volatiles. This Eurasian plant has invaded other continents, where it evolved for many generations in the absence of specialized herbivores and their natural enemies. We found that, compared to native ragworts, invasive plants release higher levels of constitutive volatiles but considerably lower levels of herbivore-induced volatiles. As a consequence, invasive ragwort is more attractive to a specialist moth but avoided by an unadapted generalist moth. Importantly, conforming to the indirect defense hypothesis, a specialist parasitoid was much more attracted to caterpillar-damaged native ragwort, which was reflected in higher parasitism rates in a field trial. The evolution of foliar volatile emissions appears to be indeed driven by their direct and indirect roles in defenses against insects.

Intentional and unintentional selection during plant domestication: herbivore damage, plant defensive traits and nutritional quality of fruit and seed crops.

Greater susceptibility to herbivory can arise as an effect of crop domestication. One proposed explanation is that defenses decreased intentionally or unintentionally during the domestication process, but evidence for this remains elusive. An alternative but nonexclusive explanation is presumed selection for higher nutritional quality. We used a metaanalytical approach to examine susceptibility to herbivores in fruit and seed crops and their wild relatives. Our analyses provide novel insights into the mechanisms of increased susceptibility by evaluating whether it can be attributed to either a reduction in herbivore defensive traits, including direct/indirect and constitutive/inducible defenses, or an increase in the nutritional content of crops. The results confirm higher herbivory and lower levels of all types of defenses in crops compared to wild relatives, although indirect defenses were more affected than direct ones. Contrary to expectations, nutritional quality was lower in crops than in wild relatives, which may enhance biomass loss to herbivores if they increase consumption to meet nutritional requirements. Our findings represent an important advance in our understanding of how changes in defensive and nutritional traits following domestication could influence, in combination or individually, crop susceptibility to herbivore attacks.

α-Linolenic acid in Papilio machaon larvae regurgitant induces a defensive response in Apiaceae

Papilio machaon hippocrates C. Felder et R. Felder, 1864 (Papilionidae) larvae are pests of plants of the family Apiaceae. It is unclear whether Apiaceae plants show induced defensive responses against P. machaon hippocrates larvae, and if so, how these responses are induced. Comparison of the fatty acid (FA) composition of the leaves of host plants and the regurgitant of P. machaon hippocrates larvae by LC–MS revealed a great increase in α-linolenic acid (α-LA) in the regurgitant compared with the FAs contained in the leaves. However, specific FA amino acid conjugates, known as elicitor compounds, such as volicitin, were not detected. Sterile host plants (Saposhnikovia divaricata (Turcz.) Schischk., Apiaceae) were treated with α-LA to mimic the damage made by P. machaon hippocrates larvae. After α-LA treatment to leaves, induced defensive reactions, i.e., release of volatile compounds such as α- and β-pinene and camphene (possible induced indirect defense) and the accumulation of specialized metabolites such as (R)-falcarinol and bergapten (possible induced direct defense) were observed. These findings highlight the role of α-LA in the interaction between P. machaon hippocrates larvae and Apiaceae host plants.

Indirect plant defenses: volatile organic compounds and extrafloral nectar

Indirect plant defense is an important component in regulating population dynamics and the structure of numerous communities in different ecosystems. These defenses mainly involve the emission of volatile organic compounds (VOCs) induced after damage by an herbivore. VOCs can play several ecological roles, such as help natural enemies locate prey or hosts, attract or repel other herbivores, mediate communication between neighboring plants and among different parts of the same plant, and affect the behavior of pollinators and seed dispersers. In addition to VOCs, some plants produce extrafloral nectar, which can enhance plant defense, by attracting, retaining, and increasing the efficiency of some natural enemies; however, among the associated costs, these compounds can attract other herbivorous species and exclude some natural enemies due to competition. Many factors can influence the production of indirect defenses by plants, such as the individual species, life stage, density of herbivores, age, abiotic factors, as well as the association of plants with symbiotic microorganisms. The potential of indirect plant defenses to reduce herbivory and increase the plant fitness has been well demonstrated. Indirect plant defenses may have ecological costs but can express phenotypic plasticity, as plants can reduce or increase the production of defenses according to the associated herbivory rate. Such variable expression of characteristics provides a barrier against the evolution of resistance by the associated herbivores. In this article, we intend to provide a review on volatile organic compounds and extrafloral nectar as indirect plant defenses, including some costs and benefits of these defense mechanisms.

Silicon suppresses a ubiquitous mite herbivore and promotes natural enemy attraction by altering plant volatile blends

Silicon (Si) accumulation in plants is widely recognised as an effective physical defence against chewing herbivores. However, its effects on some feeding guilds such as cell-content feeders are understudied despite being severe economic pests (e.g. Tetranychus urticae). Moreover, most studies focus on direct impacts of Si, but there is growing evidence that Si also impacts indirect defence. We examined the effects of Si on French bean, Phaseolus vulgaris, defences against the two-spotted spider mite, T. urticae. We grew plants hydroponically with (+ Si) or without (–Si) silicon, assessed T. urticae performance and tested the preference of the predatory mite, Phytoseiulus persimilis, for volatiles from T. urticae-infested (+ M) or uninfested (–M) plants. The provision of Si to plants suppressed T. urticae egg-laying, population growth and leaflet damage, and partially ameliorated T. urticae-induced reductions in stomatal conductance and net photosynthesis. Furthermore, T. urticae infestation increased foliar Si accumulation. Predatory mites were more attracted (64%) to volatiles from + Si plants experiencing herbivory than to –Si plants. The relative emissions (%) of volatile compounds, viz. E-2-hexanyl benzoate, hexanal, E-trans-β-ocimene, D-limonene, β-caryophyllene and methyl salicylate were elevated from + Si + M plants, while the relative emissions of 3-hexanol, trans-calamenene, o-xylene and o-cymene were lowered compared to –Si + M plants. Our results show, for the first time, that Si defences are inducible and effective even in low Si-accumulating plants against T. urticae and suggest that Si could play a role in pest biocontrol.