Electrical signalling and plant response to herbivory: A short review.

For a long time, electrical signaling was neglected at the expense of signaling studies in plants being concentrated with chemical and hydraulic signals. Studies conducted in recent years have revealed that plants are capable of emitting, processing, and transmitting bioelectrical signals to regulate a wide variety of physiological functions. Many important biological and physiological phenomena are accompanied by these cellular electrical manifestations, which supports the hypothesis about the importance of bioelectricity as a fundamental 'model' for response the stresses environmental and for activities regeneration of these organisms. Electrical signals have also been characterized and discriminated against in genetically modified plants under stress mediated by sucking insects and/or by the application of systemic insecticides. Such results can guide future studies that aim to elucidate the factors involved in the processes of resistance to stress and plant defense, thus aiding in the development of successful strategies in integrated pest management. Therefore, this mini review includes the results of studies aimed at electrical signaling in response to biotic stress. We also demonstrated how the generation and propagation of electrical signals takes place and included a description of how these electrical potentials are measured.

A tripartite rheostat controls self-regulated host plant resistance to insects.

Plants deploy receptor-like kinases and nucleotide-binding leucine-rich repeat receptors to confer host plant resistance (HPR) to herbivores1. These gene-for-gene interactions between insects and their hosts have been proposed for more than 50 years2. However, the molecular and cellular mechanisms that underlie HPR have been elusive, as the identity and sensing mechanisms of insect avirulence effectors have remained unknown. Here we identify an insect salivary protein perceived by a plant immune receptor. The BPH14-interacting salivary protein (BISP) from the brown planthopper (Nilaparvata lugens Stål) is secreted into rice (Oryza sativa) during feeding. In susceptible plants, BISP targets O. satvia RLCK185 (OsRLCK185; hereafter Os is used to denote O. satvia-related proteins or genes) to suppress basal defences. In resistant plants, the nucleotide-binding leucine-rich repeat receptor BPH14 directly binds BISP to activate HPR. Constitutive activation of Bph14-mediated immunity is detrimental to plant growth and productivity. The fine-tuning of Bph14-mediated HPR is achieved through direct binding of BISP and BPH14 to the selective autophagy cargo receptor OsNBR1, which delivers BISP to OsATG8 for degradation. Autophagy therefore controls BISP levels. In Bph14 plants, autophagy restores cellular homeostasis by downregulating HPR when feeding by brown planthoppers ceases. We identify an insect saliva protein sensed by a plant immune receptor and discover a three-way interaction system that offers opportunities for developing high-yield, insect-resistant crops.

Drought impairs herbivore-induced volatile terpene emissions by ponderosa pine but not through constraints on newly assimilated carbon.

Volatile terpenes serve multiple biological roles including tree resistance against herbivores. The increased frequency and severity of drought stress observed in forests across the globe may hinder trees from producing defense-related volatiles in response to biotic stress. To assess how drought-induced physiological stress alters volatile emissions alone and in combination with a biotic challenge, we monitored pre-dawn water potential, gas-exchange, needle terpene concentrations and terpene volatile emissions of ponderosa pine (Pinus ponderosa) saplings during three periods of drought and in response to simulated herbivory via methyl jasmonate application. Although 3-, 6- and 7-week drought treatments reduced net photosynthetic rates by 20, 89 and 105%, respectively, the magnitude of volatile fluxes remained generally resistant to drought. Herbivore-induced emissions, however, exhibited threshold-like behavior; saplings were unable to induce emissions above constitutive levels when pre-dawn water potentials were below the approximate zero-assimilation point. By comparing compositional shifts in emissions to needle terpene concentrations, we found evidence that drought effects on constitutive and herbivore-induced volatile flux and composition are primarily via constraints on the de novo fraction, suggesting that reduced photosynthesis during drought limits the carbon substrate available for de novo volatile synthesis. However, results from a subsequent 13CO2 pulse-chase labeling experiment then confirmed that both constitutive (<3% labeled) and herbivore-induced (<8% labeled) de novo emissions from ponderosa pine are synthesized predominantly from older carbon sources with little contribution from new photosynthates. Taken together, we provide evidence that in ponderosa pine, drought does not constrain herbivore-induced de novo emissions through substrate limitation via reduced photosynthesis, but rather through more sophisticated molecular and/or biophysical mechanisms that manifest as saplings reach the zero-assimilation point. These results highlight the importance of considering drought severity when assessing impacts on the herbivore-induced response and suggest that drought-altered volatile metabolism constrains induced emissions once a physiological threshold is surpassed.

The legacy of the extinct Neotropical megafauna on plants and biomes.

Large mammal herbivores are important drivers of plant evolution and vegetation patterns, but the extent to which plant trait and ecosystem geography currently reflect the historical distribution of extinct megafauna is unknown. We address this question for South and Central America (Neotropical biogeographic realm) by compiling data on plant defence traits, climate, soil, and fire, as well as on the historical distribution of extinct megafauna and extant mammal herbivores. We show that historical mammal herbivory, especially by extinct megafauna, and soil fertility explain substantial variability in wood density, leaf size, spines and latex. We also identified three distinct regions (''antiherbiomes''), differing in plant defences, environmental conditions, and megafauna history. These patterns largely matched those observed in African ecosystems, where abundant megafauna still roams, and suggest that some ecoregions experienced savanna-to-forest shifts following megafauna extinctions. Here, we show that extinct megafauna left a significant imprint on current ecosystem biogeography.

Dietary influence on modulation of Helicoverpa armigera oral secretion composition leading to differential regulation of tomato plant defense.

Little is known about how different plant-based diets influence the insect herbivores' oral secretion (OS) composition and eventually the plant defense responses. We analyzed the OS composition of the generalist Lepidopteran insect, Helicoverpa armigera feeding on the host plant tomato (OSH), non-host plant capsicum (OSNH), and artificial diet (OSAD) using Liquid Chromatography-Quadrupole Time of Flight Mass Spectrometry. Higher numbers and levels of alkaloids and terpenoids were observed in OSH and OSNH, respectively while OSAD was rich in phospholipids. Interestingly, treatment of H. armigera OSAD, OSH and OSNH on wounded tomato leaves showed differential expression of (i) genes involved in JA and SA biosynthesis and their responsive genes, and (ii) biosynthetic pathway genes of chlorogenic acid (CGA) and trehalose, which exhibited increased accumulation along with several other plant defensive metabolites. Specifically, high levels of CGA were detected after OSH and OSNH treatments in tomato leaves. There was higher expression of the genes involved in phenylpropanoid biosynthesis, which may lead to the increased accumulation of CGA and related metabolites. In the insect bioassay, CGA significantly inhibited H. armigera larval growth. Our results underline the differential accumulation of plant and insect OS metabolites and identified potential plant metabolite(s) affecting insect growth and development.

Herbivore feeding preference corroborates optimal defense theory for specialized metabolites within plants.

Numerous plants protect themselves from attackers by using specialized metabolites. The biosynthesis of these deterrent, often toxic metabolites is costly, as their synthesis diverts energy and resources on account of growth and development. How plants diversify investments into growth and defense is explained by the optimal defense theory. The central prediction of the optimal defense theory is that plants maximize growth and defense by concentrating specialized metabolites in tissues that are decisive for fitness. To date, supporting physiological evidence relies on the correlation between plant metabolite presence and animal feeding preference. Here, we use glucosinolates as a model to examine the effect of changes in chemical defense distribution on feeding preference. Taking advantage of the uniform glucosinolate distribution in transporter mutants, we show that high glucosinolate accumulation in tissues important to fitness protects them by guiding larvae of a generalist herbivore to feed on other tissues. Moreover, we show that the mature leaves of Arabidopsis thaliana supply young leaves with glucosinolates to optimize defense against herbivores. Our study provides physiological evidence for the central hypothesis of the optimal defense theory and sheds light on the importance of integrating glucosinolate biosynthesis and transport for optimizing plant defense.

Exploring the role of soil types on defense and fitness traits of silverleaf nightshade (Solanum elaeagnifolium), a worldwide invasive species through a field survey in the native range.

Silverleaf nightshade (Solanum elaeagnifolium) is a highly successful invasive weed that has caused agricultural losses both in its home and invaded ranges. Surveying 50 sub-populations over 36,000 km2 in its native range in South Texas, we investigated the interactions among soil type, population size, plant height, herbivory, and plant defenses in its home range with the expectation that populations growing in the plant's preferred sandier soils would host larger colonies of healthier and better defended plants. At each sampling location, on randomly selected plants, we measured height, insect herbivore damage, and presence, and density of internode spines. Soil type was determined using the NRCS Web Soil Survey and primarily grouped into sand, clay, or urban. Our results show a tradeoff between growth and defense with larger colonies and taller plants in clay soils, but smaller colonies of shorter, spinier plants in sandy soils. We also observed decreased herbivory in urban soils, further confirming the plant's ability to survive and even be strengthened by highly disturbed conditions. This study is a starting point for a better understanding of silverleaf nightshade's ecology in its home range and complicates the assumption that it thrives best in sandy soils.

Production of complementary defense metabolites reflects a co-evolutionary arms race between a host plant and a mutualistic bark beetle-fungal complex.

Intra-specific variation in conifers has been extensively studied with respect to defense against herbivores and pathogens. While studies have shown the ability of individual or specific mixtures of compounds to influence insects and microbes, research testing biologically relevant mixtures of defense compounds reflecting intra-specific variation amongst tree populations to enemy complexes is needed. We characterized the variations in lodgepole pine monoterpenes from a progeny trial in western Canada and grouped trees in four clusters using their monoterpene profiles. We then selected 11 representative families across four clusters and amended their entire monoterpene profiles (with the exception of ß-phellandrene) in media to determine how representative families affect the performance of the mountain pine beetle or its fungal symbiont. We placed adult beetles or inoculated fungus on the amended media and measured beetle performance and fungal growth as a proxy to host suitability. We found that different clusters or families differentially influenced beetle or fungal responses. However, monoterpene profiles of trees suitable to the beetle or the fungus were dissimilar. These outcomes reflect a co-evolutionary arms-race between the host and the bark beetle-fungus complex, which has resulted in the production of complementary defense metabolites among different pine populations to enhance tree survival.

Cardenolides, toxicity, and the costs of sequestration in the coevolutionary interaction between monarchs and milkweeds.

For highly specialized insect herbivores, plant chemical defenses are often co-opted as cues for oviposition and sequestration. In such interactions, can plants evolve novel defenses, pushing herbivores to trade off benefits of specialization with costs of coping with toxins? We tested how variation in milkweed toxins (cardenolides) impacted monarch butterfly (Danaus plexippus) growth, sequestration, and oviposition when consuming tropical milkweed (Asclepias curassavica), one of two critical host plants worldwide. The most abundant leaf toxin, highly apolar and thiazolidine ring-containing voruscharin, accounted for 40% of leaf cardenolides, negatively predicted caterpillar growth, and was not sequestered. Using whole plants and purified voruscharin, we show that monarch caterpillars convert voruscharin to calotropin and calactin in vivo, imposing a burden on growth. As shown by in vitro experiments, this conversion is facilitated by temperature and alkaline pH. We next employed toxin-target site experiments with isolated cardenolides and the monarch's neural Na+/K+-ATPase, revealing that voruscharin is highly inhibitory compared with several standards and sequestered cardenolides. The monarch's typical >50-fold enhanced resistance to cardenolides compared with sensitive animals was absent for voruscharin, suggesting highly specific plant defense. Finally, oviposition was greatest on intermediate cardenolide plants, supporting the notion of a trade-off between benefits and costs of sequestration for this highly specialized herbivore. There is apparently ample opportunity for continued coevolution between monarchs and milkweeds, although the diffuse nature of the interaction, due to migration and interaction with multiple milkweeds, may limit the ability of monarchs to counteradapt.

Feeding of pea leafminer larvae simultaneously activates jasmonic and salicylic acid pathways in plants to release a terpenoid for indirect defense.

The pea leafminer, Liriomyza huidobrensis, is an important pest species affecting ornamental crops worldwide. Plant damage consists of oviposition and feeding punctures created by female adult flies as well as larva-bored mines in leaf mesophyll tissues. How plants indirectly defend themselves from these two types of leafminer damage has not been sufficiently investigated. In this study, we compared the indirect defense responses of bean plants infested by either female adults or larvae. Puncturing of leaves by adults released green leaf volatiles and terpenoids, while larval feeding caused plants to additionally emit methyl salicylate and (E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene (TMTT). Puncturing of plants by female adults induced increases in jasmonic acid (JA) and JA-related gene expressions but reduced the expressions of salicylic acid (SA)-related genes. In contrast, JA and SA and their-related gene expression levels were increased significantly by larval feeding. The exogenous application of JA+SA significantly triggered TMTT emission, thereby significantly inducing the orientation behavior of parasitoids. Our study has confirmed that larval feeding can trigger TMTT emission through the activation of both JA and SA pathways to attract parasitoids; however, TMTT alone is less attractive than the complete blend of volatiles released by infested plants.

Long non-coding RNAs associate with jasmonate-mediated plant defence against herbivores.

Long non-coding RNA (lncRNA) are important regulators of many biological processes in plants, including defence against pathogens; whether lncRNAs mediate defence against herbivore attack is yet to be explored. With wild tobacco, Nicotiana attenuata, and its well-characterized interactions with herbivores, we identified a total of 1,290 significantly up- or down-regulated lncRNAs in response to a precise herbivore elicitation treatment. Of these, long intergenic non-coding RNAs (lincRNAs) were the most abundant. Based on their expression patterns, these up-regulated lincRNAs were classified as early (<1 hr) or late (>3 hr) responders. The early responding lincRNAs had accumulation patterns that tracked the herbivore-elicited burst of bioactive jasmonates (JAs) and the expression of regulator genes in JA signalling which regulate plant defences against herbivores. Silencing two of these early responders in N. attenuata (JAL1 and JAL3) significantly attenuated the accumulation of JAs, JA-mediated defensives and the plant's resistance to M. sexta attack, suggesting roles in regulating JA-mediated plant defence. By lincRNA sequencing of JA-deficient lines, many late responder lincRNAs were found to be transcriptionally regulated by JA signalling. This study uncovers a new role of lncRNAs in JA-mediated herbivore resistance.

Arabidopsis, tobacco, nightshade and elm take insect eggs as herbivore alarm and show similar transcriptomic alarm responses.

Plants respond to insect eggs with transcriptional changes, resulting in enhanced defence against hatching larvae. However, it is unknown whether phylogenetically distant plant species show conserved transcriptomic responses to insect eggs and subsequent larval feeding. We used Generally Applicable Gene set Enrichment (GAGE) on gene ontology terms to answer this question and analysed transcriptome data from Arabidopsis thaliana, wild tobacco (Nicotiana attenuata), bittersweet nightshade (Solanum dulcamara) and elm trees (Ulmus minor) infested by different insect species. The different plant-insect species combinations showed considerable overlap in their transcriptomic responses to both eggs and larval feeding. Within these conformable responses across the plant-insect combinations, the responses to eggs and feeding were largely analogous, and about one-fifth of these analogous responses were further enhanced when egg deposition preceded larval feeding. This conserved transcriptomic response to eggs and larval feeding comprised gene sets related to several phytohormones and to the phenylpropanoid biosynthesis pathway, of which specific branches were activated in different plant-insect combinations. Since insect eggs and larval feeding activate conserved sets of biological processes in different plant species, we conclude that plants with different lifestyles share common transcriptomic alarm responses to insect eggs, which likely enhance their defence against hatching larvae.

Improved host-plant resistance to Phytophthora rot and powdery mildew in soybean (Glycine max (L.) Merr.).

Soybean is an important oilseed cum vegetable crop, susceptible to various biotic stresses which is attributed to recent decline in crop productivity. The emergence of virulent biotypes/strains of different plant pathogens necessitates the development of new crop varieties with enhanced host resistance mechanisms. Pyramiding of multiple disease-resistant genes is one of the strategies employed to develop durable disease-resistant cultivars to the prevailing and emerging biotypes of pathogens. The present study, reports the successful introgression of two major R-genes, including Rps2 (Phytophthora rot resistance), Rmd-c (complete-powdery mildew resistance) and effective nodulating gene (rj2) through functional Marker-Assisted Backcross Breeding (MABB) in the genetic background of well-adapted and high yielding soybean varieties, CO 3 and JS 335. We have identified several promising introgressed lines with enhanced resistance to Phytophthora rot and powdery mildew. The improved soybean lines have exhibited medium to high level of resistance against powdery mildew and Phytophthora rot as well as displayed effective nodulation capacity. Our study has proven the generation of resistant genotypes to realize the potential of MABB for achieving host plant resistance in soybean. The improved lines developed can greatly assist the soybean breeding programs in India and other soybean growing countries for evolving disease-resistant varieties.

Persistence and Oscillations of Plant-Pollinator-Herbivore Systems.

This paper considers plant-pollinator-herbivore systems where the plant produces food for the pollinator, the pollinator provides pollination service for the plant in return, while the herbivore consumes both the food and the plant itself without providing pollination service. Based on these resource-consumer interactions, we form a plant-pollinator-herbivore model which includes the intermediary food. Using qualitative method and Kuznetsov theorem, we show global dynamics of the subsystems, uniform persistence of the whole system and periodic oscillation by Hopf bifurcation. Rigorous analysis on the system demonstrates mechanisms by which varying parameters could make the system transition between extinction of herbivore, coexistence of the three species at steady states, coexistence in periodic oscillations and extinction of pollinator. It is shown that (i) in plant-pollinator interactions, the plant would produce food; (ii) in plant-herbivore interactions, the plant would produce toxin; (iii) in the presence of both pollinator and herbivore, the plant would produce both food and toxin, and intermediate productions are analytically given by which the plant can reach its maximal density; and (iv) an appropriate toxin production could drive the herbivore into extinction, an unappropriate one would drive the pollinator into extinction, while too much toxin production will drive the plant itself into extinction. The analysis leads to explanations for experimental observations and provides new insights.

Host plants alter their volatiles to help a solitary egg parasitoid distinguish habitats with parasitized hosts from those without.

When attacked by herbivores, plants emit volatiles to attract parasitoids and predators of herbivores. However, our understanding of the effect of plant volatiles on the subsequent behaviour of conspecific parasitoids when herbivores on plants are parasitized is limited. In this study, rice plants were infested with gravid females of the brown planthopper (BPH) Nilaparvata lugens for 24 hr followed by another 24 hr in which the BPH eggs on plants were permitted to be parasitized by their egg parasitoid, Anagrus nilaparvatae; volatiles from rice plants that underwent such treatment were less attractive to subsequent conspecific parasitoids compared to the volatiles from plants infested with gravid BPH females alone. Chemical analysis revealed that levels of JA and JA-Ile as well as of four volatile compounds-linalool, MeSA, α-zingiberene and an unknown compound-from plants infested with BPH and parasitized by wasps were significantly higher than levels of these compounds from BPH-infested plants. Laboratory and field bioassays revealed that one of the four increased chemicals-α-zingiberene-reduced the plant's attractiveness to the parasitoid. These results suggest that host plants can fine-tune their volatiles to help egg parasitoids distinguish host habitats with parasitized hosts from those without.

Evolution of phenotypic plasticity: Genetic differentiation and additive genetic variation for induced plant defence in wild arugula Eruca sativa.

Phenotypic plasticity is the primary mechanism of organismal resilience to abiotic and biotic stress, and genetic differentiation in plasticity can evolve if stresses differ among populations. Inducible defence is a common form of adaptive phenotypic plasticity, and long-standing theory predicts that its evolution is shaped by costs of the defensive traits, costs of plasticity and a trade-off in allocation to constitutive versus induced traits. We used a common garden to study the evolution of defence in two native populations of wild arugula Eruca sativa (Brassicaceae) from contrasting desert and Mediterranean habitats that differ in attack by caterpillars and aphids. We report genetic differentiation and additive genetic variance for phenology, growth and three defensive traits (toxic glucosinolates, anti-nutritive protease inhibitors and physical trichome barriers) as well their inducibility in response to the plant hormone jasmonic acid. The two populations were strongly differentiated for plasticity in nearly all traits. There was little evidence for costs of defence or plasticity, but constitutive and induced traits showed a consistent additive genetic trade-off within each population for the three defensive traits. We conclude that these populations have evolutionarily diverged in inducible defence and retain ample potential for the future evolution of phenotypic plasticity in defence.