Heat stress reprograms herbivory-induced defense responses in potato plants.

Climate change is predicted to increase the occurrence of extreme weather events such as heatwaves, which may thereby impact the outcome of plant-herbivore interactions. While elevated temperature is known to directly affect herbivore growth, it remains largely unclear if it indirectly influences herbivore performance by affecting the host plant they feed on. In this study, we investigated how transient exposure to high temperature influences plant herbivory-induced defenses at the transcript and metabolic level. To this end, we studied the interaction between potato (Solanum tuberosum) plants and the larvae of the potato tuber moth (Phthorimaea operculella) under different temperature regimes. We found that P. operculella larvae grew heavier on leaves co-stressed by high temperature and insect herbivory than on leaves pre-stressed by herbivory alone. We also observed that high temperature treatments altered phylotranscriptomic patterns upon herbivory, which changed from an evolutionary hourglass pattern, in which transcriptomic responses at early and late time points after elicitation are more variable than the ones in the middle, to a vase pattern. Specifically, transcripts of many herbivory-induced genes in the early and late defense stage were suppressed by HT treatment, whereas those in the intermediate stage peaked earlier. Additionally, we observed that high temperature impaired the induction of jasmonates and defense compounds upon herbivory. Moreover, using jasmonate-reduced (JA-reduced, irAOC) and -elevated (JA-Ile-elevated, irCYP94B3s) potato plants, we showed that high temperature suppresses JA signaling mediated plant-induced defense to herbivore attack. Thus, our study provides evidences on how temperature reprograms plant-induced defense to herbivores.

Sustainable scenarios in a plants-rhizobacteria-plant consumers system are in risk when biotic or abiotic factors change.

The ecological relationship among plants, rhizobacteria and plant consumers has attracted the attention of researchers due to its implications in field crops. It is known that, the rhizosphere is occupied not only by rhizobacteria which grant benefits to the plants but also by bacteria which are detrimental for them. In this work, we construct and analyze a plants-rhizobacteria-plant consumers system. In the modeling process, it is assumed that there is a conditioned interaction between plants and bacteria in the rhizosfera such that there is a mutualistic relationship at low densities of rhizobacteria and the relationship is parasitic or competitive at higher densities of them. Benefits granted by rhizobacteria include mechanisms that increase the plant growth and defense mechanisms against plant consumers. From the analysis of the model and its simplified version, we show that scenarios of coexistence of all populations can occur for a wide range of values of the parameters which describe biotic or abiotic factors; however, these scenarios are in risk since scenarios of exclusion of species can occur simultaneously due to the presence of bistability phenomena. The results obtained can be useful for the decision makers to design interventions strategies on field crops when plant growth-promoting rhizobacteria are used.

Disarming the defenses: Insect detoxification of plant defense-related specialized metabolites.

The ability of certain insects to feed on plants containing toxic specialized metabolites may be attributed to detoxification enzymes. Representatives of a few large families of detoxification enzymes are widespread in insect herbivores acting to functionalize toxins and conjugate them with polar substituents to decrease toxicity, increase water solubility and enhance excretion. Insects have also developed specific enzymes for coping with toxins that are activated upon plant damage. Another source of detoxification potential in insects lies in their microbiomes, which are being increasingly recognized for their role in processing plant toxins. The evolution of insect detoxification systems to resist toxic specialized metabolites in plants may in turn have selected for the great diversity of such metabolites found in nature.

Are day-flying moths more specialized in larval dietary breadth?-a test of the "Salient Aroma Hypothesis" in a predominantly nocturnal clade.

Although diurnality is widespread across Lepidoptera and has evolved many times independently, its causes and ecological implications are yet poorly understood. The "Salient Aroma Hypothesis" (SAH) postulates that diurnal insect herbivores are overall more specialized in dietary breadth than species active at night. It is furthermore assumed that diurnality evolved more frequently in species that live in cooler environments. Using European geometrid moths as a model group, we tested whether diurnal activity in adults is associated with an increased larval dietary breadth as predicted by the SAH. We further investigated whether species that exclusively occur in colder regions or whose flight period is restricted to cool seasons are more likely to exhibit a diurnal flight activity. Contrary to expectation, we found no consistent differences in larval dietary breadth between diurnal and nocturnal species, and thus no support for the SAH. Diurnal activity occurred more frequently in species restricted to cold regions but not in species restricted to cool seasons. We conclude that diurnality could serve as an advantageous adaptation in cold environments, depending on further factors such as resource availability or predation pressure, but has no immediate consequences for larval dietary breadth.

How do host plant use and seasonal life cycle relate to insect body size: A case study on European geometrid moths (Lepidoptera: Geometridae).

We used European geometrid moths (>630 species) as a model group to investigate how life history traits linked to larval host plant use (i.e., diet breadth and host-plant growth form) and seasonal life cycle (i.e., voltinism, overwintering stage and caterpillar phenology) are related to adult body size in holometabolous insect herbivores. To do so, we applied phylogenetic comparative methods to account for shared evolutionary history among herbivore species. We further categorized larval diet breadth based on the phylogenetic structure of utilized host plant genera. Our results indicate that species associated with woody plants are, on average, larger than herb feeders and increase in size with increasing diet breadth. Obligatorily univoltine species are larger than multivoltine species, and attain larger sizes when their larvae occur exclusively in the early season. Furthermore, the adult body size is significantly smaller in species that overwinter in the pupal stage compared to those that overwinter as eggs or caterpillars. In summary, our results indicate that the ecological niche of holometabolous insect herbivores is strongly interrelated with body size at maturity.

Tritrophic Interactions among Arthropod Natural Enemies, Herbivores and Plants Considering Volatile Blends at Different Scale Levels.

Herbivore-induced plant volatiles (HIPVs) are released by plants upon damaged or disturbance by phytophagous insects. Plants emit HIPV signals not merely in reaction to tissue damage, but also in response to herbivore salivary secretions, oviposition, and excrement. Although certain volatile chemicals are retained in plant tissues and released rapidly upon damaged, others are synthesized de novo in response to herbivore feeding and emitted not only from damaged tissue but also from nearby by undamaged leaves. HIPVs can be used by predators and parasitoids to locate herbivores at different spatial scales. The HIPV-emitting spatial pattern is dynamic and heterogeneous in nature and influenced by the concentration, chemical makeup, breakdown of the emitted mixes and environmental elements (e.g., turbulence, wind and vegetation) which affect the foraging of biocontrol agents. In addition, sensory capability to detect volatiles and the physical ability to move towards the source were also different between natural enemy individuals. The impacts of HIPVs on arthropod natural enemies have been partially studied at spatial scales, that is why the functions of HIPVs is still subject under much debate. In this review, we summarized the current knowledge and loopholes regarding the role of HIPVs in tritrophic interactions at multiple scale levels. Therefore, we contend that closing these loopholes will make it much easier to use HIPVs for sustainable pest management in agriculture.

Specialist root herbivore modulates plant transcriptome and downregulates defensive secondary metabolites in a brassicaceous plant.

Plants face attackers aboveground and belowground. Insect root herbivores can lead to severe crop losses, yet the underlying transcriptomic responses have rarely been studied. We studied the dynamics of the transcriptomic response of Brussels sprouts (Brassica oleracea var. gemmifera) primary roots to feeding damage by cabbage root fly larvae (Delia radicum), alone or in combination with aboveground herbivory by cabbage aphids (Brevicoryne brassicae) or diamondback moth caterpillars (Plutella xylostella). This was supplemented with analyses of phytohormones and the main classes of secondary metabolites; aromatic, indole and aliphatic glucosinolates. Root herbivory leads to major transcriptomic rearrangement that is modulated by aboveground feeding caterpillars, but not aphids, through priming soon after root feeding starts. The root herbivore downregulates aliphatic glucosinolates. Knocking out aliphatic glucosinolate biosynthesis with CRISPR-Cas9 results in enhanced performance of the specialist root herbivore, indicating that the herbivore downregulates an effective defence. This study advances our understanding of how plants cope with root herbivory and highlights several novel aspects of insect-plant interactions for future research. Further, our findings may help breeders develop a sustainable solution to a devastating root pest.

Not Only Systemin: Prosystemin Harbors Other Active Regions Able to Protect Tomato Plants.

Prosystemin is a 200-amino acid precursor expressed in Solanaceae plants which releases at the C-terminal part a peptidic hormone called Systemin in response to wounding and herbivore attack. We recently showed that Prosystemin is not only a mere scaffold of Systemin but, even when deprived of Systemin, is biologically active. These results, combined with recent discoveries that Prosystemin is an intrinsically disordered protein containing disordered regions within its sequence, prompted us to investigate the N-terminal portions of the precursor, which contribute to the greatest disorder within the sequence. To this aim, PS1-70 and PS1-120 were designed, produced, and structurally and functionally characterized. Both the fragments, which maintained their intrinsic disorder, were able to induce defense-related genes and to protect tomato plants against Botrytis cinerea and Spodoptera littoralis larvae. Intriguingly, the biological activity of each of the two N-terminal fragments and of Systemin is similar but not quite the same and does not show any toxicity on experimental non-targets considered. These regions account for different anti-stress activities conferred to tomato plants by their overexpression. The two N-terminal fragments identified in this study may represent new promising tools for sustainable crop protection.

Testing the role of local plant chemical diversity on plant-herbivore interactions and plant species coexistence.

Accumulating evidence suggests that herbivorous insects influence the local composition and richness of Neotropical plant species, particularly in species-rich genera. Species richness, phylogenetic diversity, and chemical diversity all influence the ability of insect herbivores to find and utilize their hosts. The relative impact of these components of diversity on species coexistence and plant-herbivore interactions is not well understood. We constructed 60 local communities of up to 13 species of Piper (Piperaceae) in native, mature forest at a lowland wet forest location in Costa Rica. The species composition of each community was chosen such that species richness, phylogenetic diversity, and GCMS-based chemical diversity were varied independently among communities. We predicted that chemical diversity would most strongly affect the communities across time, with smaller effects of taxonomic and phylogenetic diversity. At 13 months after the experimental planting, we assessed survivorship of each cutting, measured total leaf area loss of the survivors, leaf area loss to generalist and specialist herbivorous insect species, and local extinction of species. Generalist and specialist herbivory decreased with increasing levels of species richness and phylogenetic diversity, respectively. Surprisingly, there was no independent effect of chemical diversity on any of the three measures of herbivore damage. Nevertheless, plots with a higher chemical and phylogenetic diversity showed decreased plant mortality and local species extinction. Overall, our results suggested that both chemical and phylogenetic similarity are important factors in the assembly and maintenance of tropical plant communities. The fact that chemical diversity influences plant mortality suggests that leaf herbivores, and possibly other plant natural enemies, could increase plant diversity via the selective mortality of similar chemotypes.

Plant Secondary Metabolites as Defense Tools against Herbivores for Sustainable Crop Protection.

Plants have evolved several adaptive strategies through physiological changes in response to herbivore attacks. Plant secondary metabolites (PSMs) are synthesized to provide defensive functions and regulate defense signaling pathways to safeguard plants against herbivores. Herbivore injury initiates complex reactions which ultimately lead to synthesis and accumulation of PSMs. The biosynthesis of these metabolites is regulated by the interplay of signaling molecules comprising phytohormones. Plant volatile metabolites are released upon herbivore attack and are capable of directly inducing or priming hormonal defense signaling pathways. Secondary metabolites enable plants to quickly detect herbivore attacks and respond in a timely way in a rapidly changing scenario of pest and environment. Several studies have suggested that the potential for adaptation and/or resistance by insect herbivores to secondary metabolites is limited. These metabolites cause direct toxicity to insect pests, stimulate antixenosis mechanisms in plants to insect herbivores, and, by recruiting herbivore natural enemies, indirectly protect the plants. Herbivores adapt to secondary metabolites by the up/down regulation of sensory genes, and sequestration or detoxification of toxic metabolites. PSMs modulate multi-trophic interactions involving host plants, herbivores, natural enemies and pollinators. Although the role of secondary metabolites in plant-pollinator interplay has been little explored, several reports suggest that both plants and pollinators are mutually benefited. Molecular insights into the regulatory proteins and genes involved in the biosynthesis of secondary metabolites will pave the way for the metabolic engineering of biosynthetic pathway intermediates for improving plant tolerance to herbivores. This review throws light on the role of PSMs in modulating multi-trophic interactions, contributing to the knowledge of plant-herbivore interactions to enable their management in an eco-friendly and sustainable manner.

Great tits (Parus major) flexibly learn that herbivore-induced plant volatiles indicate prey location: An experimental evidence with two tree species.

When searching for food, great tits (Parus major) can use herbivore-induced plant volatiles (HIPVs) as an indicator of arthropod presence. Their ability to detect HIPVs was shown to be learned, and not innate, yet the flexibility and generalization of learning remain unclear.We studied if, and if so how, naïve and trained great tits (Parus major) discriminate between herbivore-induced and noninduced saplings of Scotch elm (Ulmus glabra) and cattley guava (Psidium cattleyanum). We chemically analyzed the used plants and showed that their HIPVs differed significantly and overlapped only in a few compounds.Birds trained to discriminate between herbivore-induced and noninduced saplings preferred the herbivore-induced saplings of the plant species they were trained to. Naïve birds did not show any preferences. Our results indicate that the attraction of great tits to herbivore-induced plants is not innate, rather it is a skill that can be acquired through learning, one tree species at a time.We demonstrate that the ability to learn to associate HIPVs with food reward is flexible, expressed to both tested plant species, even if the plant species has not coevolved with the bird species (i.e., guava). Our results imply that the birds are not capable of generalizing HIPVs among tree species but suggest that they either learn to detect individual compounds or associate whole bouquets with food rewards.

Plant Allelochemicals as Sources of Insecticides.

In this review, we describe the role of plant-derived biochemicals that are toxic to insect pests. Biotic stress in plants caused by insect pests is one of the most significant problems, leading to yield losses. Synthetic pesticides still play a significant role in crop protection. However, the environmental side effects and health issues caused by the overuse or inappropriate application of synthetic pesticides forced authorities to ban some problematic ones. Consequently, there is a strong necessity for novel and alternative insect pest control methods. An interesting source of ecological pesticides are biocidal compounds, naturally occurring in plants as allelochemicals (secondary metabolites), helping plants to resist, tolerate or compensate the stress caused by insect pests. The abovementioned bioactive natural products are the first line of defense in plants against insect herbivores. The large group of secondary plant metabolites, including alkaloids, saponins, phenols and terpenes, are the most promising compounds in the management of insect pests. Secondary metabolites offer sustainable pest control, therefore we can conclude that certain plant species provide numerous promising possibilities for discovering novel and ecologically friendly methods for the control of numerous insect pests.

The Multifunctional Roles of Polyphenols in Plant-Herbivore Interactions.

There is no argument to the fact that insect herbivores cause significant losses to plant productivity in both natural and agricultural ecosystems. To counter this continuous onslaught, plants have evolved a suite of direct and indirect, constitutive and induced, chemical and physical defenses, and secondary metabolites are a key group that facilitates these defenses. Polyphenols-widely distributed in flowering plants-are the major group of such biologically active secondary metabolites. Recent advances in analytical chemistry and metabolomics have provided an opportunity to dig deep into extraction and quantification of plant-based natural products with insecticidal/insect deterrent activity, a potential sustainable pest management strategy. However, we currently lack an updated review of their multifunctional roles in insect-plant interactions, especially focusing on their insect deterrent or antifeedant properties. This review focuses on the role of polyphenols in plant-insect interactions and plant defenses including their structure, induction, regulation, and their anti-feeding and toxicity effects. Details on mechanisms underlying these interactions and localization of these compounds are discussed in the context of insect-plant interactions, current findings, and potential avenues for future research in this area.

The fate of chlorophyll in phytophagous insects goes beyond nutrition.

Chlorophyll (Chl) is a natural compound that is found in all autotrophic plants. Since phytophagous insects ingest the photosynthetically active material with the plant leaves, the question arises if and how herbivores deal with Chl and its degradation products. Here we review findings on Chl degradation in phytophagous insects and highlight the role of these ubiquitous plant metabolites for plant-feeding insects. Due to the anaerobic gut of many insects, the degradation is limited to the removal of the peripheral substituents, while the tetrapyrrole core remains intact. Proteins, such as red fluorescent protein, P252 (a novel 252-kDa protein), and chlorophyllide binding protein have been reported to occur in the insect gut and might be indirectly connected to Chl degradation. Besides of an nutritional value, e.g., by taking up Mg2+ ions or by sequestration of carbon from the phytol side chain, the Chl degradation products may serve the insect, after binding to certain proteins, as antimicrobial, antifungal, and antiviral factors. The protein complexes may also confer protection against reactive oxygen species. The antibiotic potential of proteins and degradation products does not only benefit phytophagous insects but also human being in medical application of cancer treatment for instance. This review highlights these aspects from a molecular, biochemical, and ecological point of view.

A compilation of host plants and their gall-inducing insects for the Caatinga Biome / Uma compilação de plantas hospedeiras e seus insetos galhadores para o bioma Caatinga

Caatinga is a seasonally dry tropical forest, one of the richest in plant species. Unfortunately, many groups of herbivorous insects associated with these plants are poorly known. This study aimed to investigate the diversity of gall-inducing insects (GII) and host plants (HP) in the Caatinga. For this, we compiled the information available in the literature of inventories on GII and their HP communities, and the described gall midge species. We found 100 species, 72 genera, and 32 families of HP hosting a total of 156 morphospecies of GII and 12 species of described cecidomyiids. Plant species with only one GII species represented 74% of hosts, but in super HP (i.e., HP with a high number of GII), despite the small number of HP species, there were many GII species. Fabaceae was also the most specious family, with 30% of HP species and 40% of GII. Furthermore, our results showed a low number of species of HP and GII for the Brazilian Caatinga, that we discussed this pattern with the following arguments, first, it is likely that the number of galling insect inventories for the Caatinga is under-sampled, second the Caatinga has a relatively smaller number of plant species when compared to other biomes, and finally, we argue that the Caatinga is a seasonally dry tropical forest where the deciduousness represents a relevant factor in the colonization and performance rates of GII.

A Caatinga é uma floresta tropical sazonalmente seca, uma das mais ricas em espécies vegetais. Infelizmente, muitos grupos de insetos herbívoros associados a essas plantas são pouco conhecidos. Este estudo teve como objetivo investigar a diversidade de insetos galhadores (IG) e plantas hospedeiras (PH) na Caatinga. Para isso, nós compilamos as informações disponíveis na literatura de inventários sobre a comunidade de IG e suas PH, e as espécies descritas de cecidomiídeos. Nós encontramos 100 espécies, 72 gêneros e 32 famílias de PH abrigando um total de 156 morfoespécies de IG e 12 espécies descritas de cecidomiídeos. Espécies de plantas com apenas uma espécie de IG representaram 74% das hospedeiras, mas para as super PH (ou seja, PH com alto número de IG), apesar do pequeno número de espécies de PH, havia muitas espécies de IG. Fabaceae foi a família mais rica, com 30% das espécies de PH e 40% dos IG. Além disso, nossos resultados mostraram um baixo número de espécies de PH e IG para a Caatinga brasileira, e discutimos esse padrão com os seguintes argumentos, primeiro, é provável que o número de inventários de insetos galhadores para a Caatinga seja subamostrado, segundo a Caatinga possui um número relativamente menor de espécies vegetais quando comparada a outros biomas e, por fim, argumentamos que a Caatinga é uma floresta tropical sazonalmente seca onde a deciduidade representa um fator relevante para as taxas de colonização e desempenho dos IG.

Silicon Alters Leaf Surface Morphology and Suppresses Insect Herbivory in a Model Grass Species.

Grasses accumulate large amounts of silicon (Si) which is deposited in trichomes, specialised silica cells and cell walls. This may increase leaf toughness and reduce cell rupture, palatability and digestion. Few studies have measured leaf mechanical traits in response to Si, thus the effect of Si on herbivores can be difficult to disentangle from Si-induced changes in leaf surface morphology. We assessed the effects of Si on Brachypodium distachyon mechanical traits (specific leaf area (SLA), thickness, leaf dry matter content (LDMC), relative electrolyte leakage (REL)) and leaf surface morphology (macrohairs, prickle, silica and epidermal cells) and determined the effects of Si on the growth of two generalist insect herbivores (Helicoverpa armigera and Acheta domesticus). Si had no effect on leaf mechanical traits; however, Si changed leaf surface morphology: silica and prickle cells were on average 127% and 36% larger in Si supplemented plants, respectively. Prickle cell density was significantly reduced by Si, while macrohair density remained unchanged. Caterpillars were more negatively affected by Si compared to crickets, possibly due to the latter having a thicker and thus more protective gut lining. Our data show that Si acts as a direct defence against leaf-chewing insects by changing the morphology of specialised defence structures without altering leaf mechanical traits.

Plant phylogeny drives arboreal caterpillar assemblages across the Holarctic.

Assemblages of insect herbivores are structured by plant traits such as nutrient content, secondary metabolites, physical traits, and phenology. Many of these traits are phylogenetically conserved, implying a decrease in trait similarity with increasing phylogenetic distance of the host plant taxa. Thus, a metric of phylogenetic distances and relationships can be considered a proxy for phylogenetically conserved plant traits and used to predict variation in herbivorous insect assemblages among co-occurring plant species.Using a Holarctic dataset of exposed-feeding and shelter-building caterpillars, we aimed at showing how phylogenetic relationships among host plants explain compositional changes and characteristics of herbivore assemblages.Our plant-caterpillar network data derived from plot-based samplings at three different continents included >28,000 individual caterpillar-plant interactions. We tested whether increasing phylogenetic distance of the host plants leads to a decrease in caterpillar assemblage overlap. We further investigated to what degree phylogenetic isolation of a host tree species within the local community explains abundance, density, richness, and mean specialization of its associated caterpillar assemblage.The overlap of caterpillar assemblages decreased with increasing phylogenetic distance among the host tree species. Phylogenetic isolation of a host plant within the local plant community was correlated with lower richness and mean specialization of the associated caterpillar assemblages. Phylogenetic isolation had no effect on caterpillar abundance or density. The effects of plant phylogeny were consistent across exposed-feeding and shelter-building caterpillars.Our study reveals that distance metrics obtained from host plant phylogeny are useful predictors to explain compositional turnover among hosts and host-specific variations in richness and mean specialization of associated insect herbivore assemblages in temperate broadleaf forests. As phylogenetic information of plant communities is becoming increasingly available, further large-scale studies are needed to investigate to what degree plant phylogeny structures herbivore assemblages in other biomes and ecosystems.