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Soil bacteria that associate with plant roots promote host vigor. Legume plants form mutualisms with rhizobial bacteria, and legumes grown with rhizobia have more nutrients and defenses than those grown without rhizobia. However, few studies have tested how stressors such as herbivores affect soil rhizobia, and the mechanisms mediating these interactions. Here we tested reciprocal interactions between a chewing herbivore, Sitona lineatus (pea leaf weevil), and Pisum sativum (pea) plants grown with or without rhizobia (Rhizobium leguminosarum biovar. viciae), and the plant-defense and nutritional mechanisms mediating these interactions. We hypothesized that plants grown with rhizobia would have less feeding from S. lineatus due to greater expression of phytohormones or physical defenses. We also predicted that herbivory might impede the mutualism between P. sativum and rhizobia. Our experiments showed that leaf defoliation by S. lineatus was indeed lowest on plants with rhizobia. Plants grown with rhizobia had increased gene transcript expression associated with hormone-related defense (jasmonic acid, ethylene, abscisic acid) as well as physical and antioxidant-related defense, which may explain reduced feeding by S. lineatus. Conversely, S. lineatus feeding reduced the number of root nodules and nodule fresh weight, suggesting a disruption of the symbiosis between plants and rhizobia. Our study shows that aboveground herbivores can engage in mutually antagonistic interactions with soil microbes that are mediated through multiple plant-mediated pathways.

In agroecosystems, plants frequently confront multiple biotic stressors, including herbivores and pathogens. The nature of these interactions plays a crucial role in mediating the activation of plant defense mechanisms. However, induction of plant chemical defenses has been more well studied than the induction of physical defenses. Here, we assessed the physical and chemical defense responses of pea (Pisum sativum) plants after exposure to three stressors: a vector herbivore (pea aphid, Acrythosiphon pisum), a non-vector herbivore (pea leaf weevil, Sitona lineatus), and a virus (Pea enation mosaic virus, PEMV). We used various histochemical staining techniques show that viruliferous A. pisum (transmitting PEMV) strongly induced callose deposition (aniline blue staining) and antioxidant-mediated defenses (DAB and NBT staining) in peas, primarily through accumulating reactive oxygen species (ROS). High-throughput phenotyping showed that viruliferous aphids reduced plant photosynthetic efficiency, but plants infected with PEMV had increased cell death (trypan blue staining). However, herbivory by aphids and weevils did not strongly induce defenses in peas, even though weevil feeding significantly reduced pea leaf area. These results show that not all herbivores induce strong defensive responses, and plant responses to vector species depends on their virus infection status. More broadly, our results indicate that variable stressors differentially regulate various plant responses through intricate chemical and physical defense pathways.

Insect growth is interrupted by molts, during which the insect develops a new exoskeleton. The exoskeleton confers protection and undergoes shedding between each developmental stage through an evolutionarily conserved and ordered sequence of behaviors, collectively referred to as ecdysis. Ecdysis is triggered by Ecdysis triggering hormone (ETH) synthesized and secreted from peripheral Inka cells on the tracheal surface and plays a vital role in the orchestration of ecdysis in insects and possibly in other arthropod species. ETH synthesized by Inka cells then binds to ETH receptor (ETHR) present on the peptidergic neurons in the central nervous system (CNS) to facilitate synthesis of various other neuropeptides involved in ecdysis. The mechanism of ETH function on ecdysis has been well investigated in holometabolous insects such as moths Manduca sexta and Bombyx mori, fruit fly Drosophila melanogaster, the yellow fever mosquito Aedes aegypti and beetle Tribolium castaneum etc. In contrast, very little information is available about the role of ETH in sequential and gradual growth and developmental changes associated with ecdysis in hemimetabolous insects. Recent studies have identified ETH precursors and characterized functional and biochemical features of ETH and ETHR in a hemimetabolous insect, desert locust, Schistocerca gregaria. Recently, the role of ETH in Juvenile hormone (JH) mediated courtship short-term memory (STM) retention and long-term courtship memory regulation and retention have also been investigated in adult male Drosophila. Our review provides a novel synthesis of ETH signaling cascades and responses in various insects triggering diverse functions in adults and juvenile insects including their development and reproductive regulation and might allow researchers to develop sustainable pest management strategies by identifying novel compounds and targets.

Drought alters plant traits in ways that affect herbivore performance. However, we lack a comprehensive understanding of the plant-derived mechanisms that mediate insect responses to drought. Water stress occurs along gradients of intensity, and the impacts of drought intensity on plant-insect interactions is understudied. Here, we assessed aphid performance on wheat plants exposed to a gradient of water stress and measured plant nutrients and phytohormones that may mediate aphid response to drought. We show that water stress reduced aphid performance, and the negative effect grew stronger as the magnitude of water stress increased. The plant response to water limitation was not consistent across the stress gradient and was reliant on the trait measured. Water limitation did not affect whole-plant nitrogen; however, water limitation did reduce amino acid concentration and increase sugars, but only under high stress intensity. The phytohormones abscisic acid (ABA), jasmonic acid (JA), and salicylic acid (SA), and the expression of their associated gene transcripts, were also differentially affected by water stress intensity. In well-watered conditions, aphid feeding increased concentrations of the defense-related hormones SA and JA over time; however, any amount of water limitation prevented aphid induction of JA. Although aphids may experience a reprieve from JA-related defenses in stressed conditions, SA levels remain high in response to aphid feeding, indicating aphids are still vulnerable to SA-related defenses. Any level of water stress also increased the expression of a callose-associated gene transcript, a physical defense that impairs feeding. Thus, poor aphid performance on mildly-stressed plants was correlated with increased plant defenses, whereas poor performance on highly-stressed plants was correlated with stronger plant defense induction and reduced plant nutritional quality. Understanding the mechanisms driving aphid and plant performance under water stress conditions can improve our ability to predict how aphid populations will respond to climate change.

The European corn borer (ECB; Ostrinia nubilalis) is an economically damaging insect pest of maize (Zea mays L.), an important cereal crop widely grown globally. Among inbred lines, the maize genotype Mp708 has shown resistance to diverse herbivorous insects, although several aspects of the defense mechanisms of Mp708 plants are yet to be explored. Here, the changes in root physiology arising from short-term feeding by ECB on the shoot tissues of Mp708 plants was evaluated directly using transcriptomics, and indirectly by monitoring changes in growth of western corn rootworm (WCR; Diabrotica virgifera virgifera) larvae. Mp708 defense responses negatively impacted both ECB and WCR larval weights, providing evidence for changes in root physiology in response to ECB feeding on shoot tissues. There was a significant downregulation of genes in the root tissues following short-term ECB feeding, including genes needed for direct defense (e.g., proteinase inhibitors and chitinases). Our transcriptomic analysis also revealed specific regulation of the genes involved in hormonal and metabolite pathways in the roots of Mp708 plants subjected to ECB herbivory. These data provide support for the long-distance signaling-mediated defense in Mp708 plants and suggest that altered metabolite profiles of roots in response to ECB feeding of shoots likely negatively impacted WCR growth.

The Western corn rootworm (WCR; Diabrotica virgifera virgifera) is an economically important belowground pest of maize. Belowground feeding by WCR is damaging because it weakens the roots system, diminishes nutrient uptake, and creates entry points for fungal and bacterial pathogens and increases lodging, all of which can significantly suppress maize yields. Previously, it was demonstrated that belowground herbivory can trigger plant defense responses in the roots and the shoots, thereby impacting intraplant communication. Although several aspects of maize-WCR interactions have been reported, co-transcriptomic remodeling in the plant and insect are yet to be explored. We used a maize genotype, Mp708, that is resistant to a large guild of herbivore pests to study the underlying plant defense signaling network between below and aboveground tissues. We also evaluated WCR compensatory transcriptome responses. Using RNA-seq, we profiled the transcriptome of roots and leaves that interacted with WCR infestation up to 5 days post infestation (dpi). Our results suggest that Mp708 shoots and roots had elevated constitutive and WCR-feeding induced expression of genes related to jasmonic acid and ethylene pathways, respectively, before and after WCR feeding for 1 and 5 days. Similarly, extended feeding by WCR for 5 days in Mp708 roots suppressed many genes involved in the benzoxazinoid pathway, which is a major group of indole-derived secondary metabolites that provides resistance to several insect pests in maize. Furthermore, extended feeding by WCR on Mp708 roots revealed several genes that were downregulated in WCR, which include genes related to proteolysis, neuropeptide signaling pathway, defense response, drug catabolic process, and hormone metabolic process. These findings indicate a dynamic transcriptomic dialog between WCR and WCR-infested maize plants.

Chewing herbivores, such as caterpillars and beetles, while feeding on the host plant, cause extensive tissue damage and release a wide array of cues to alter plant defenses. Consequently, the cues can have both beneficial and detrimental impacts on the chewing herbivores. Herbivore-associated molecular patterns (HAMPs) are molecules produced by herbivorous insects that aid them to elicit plant defenses leading to impairment of insect growth, while effectors suppress plant defenses and contribute to increased susceptibility to subsequent feeding by chewing herbivores. Besides secretions that originate from glands (e.g., saliva) and fore- and midgut regions (e.g., oral secretions) of chewing herbivores, recent studies have shown that insect frass and herbivore-associated endosymbionts also play a critical role in modulating plant defenses. In this review, we provide an update on a growing body of literature that discusses the chewing insect HAMPs and effectors and the mechanisms by which they modulate host defenses. Novel “omic” approaches and availability of new tools will help researchers to move forward this discipline by identifying and characterizing novel insect HAMPs and effectors and how these herbivore-associated cues are perceived by host plant receptors.

Switchgrass (Panicum virgatum L.) is a low input, high biomass perennial grass being developed for the bioenergy sector. Upland and lowland cultivars can differ in their responses to insect herbivory. Fall armyworm [FAW; Spodoptera frugiperda JE Smith (Lepidoptera: Noctuidae)] is a generalist pest of many plant species and can feed on switchgrass as well. Here, in two different trials, FAW larval mass were significantly reduced when fed on lowland cultivar Kanlow relative to larvae fed on upland cultivar Summer plants after 10 days. Hormone content of plants indicated elevated levels of the plant defense hormone jasmonic acid (JA) and its bioactive conjugate JA-Ile although significant differences were not observed. Conversely, the precursor to JA, 12-oxo-phytodienoic acid (OPDA) levels were significantly different between FAW fed Summer and Kanlow plants raising the possibility of differential signaling by OPDA in the two cultivars. Global transcriptome analysis revealed a stronger response in Kanlow plant relative to Summer plants. Among these changes were a preferential upregulation of several branches of terpenoid and phenylpropanoid biosynthesis in Kanlow plants suggesting that enhanced biosynthesis or accumulation of antifeedants could have negatively impacted FAW larval mass gain on Kanlow plants relative to Summer plants. A comparison of the switchgrass-FAW RNA-Seq dataset to those from maize-FAW and switchgrass-aphid interactions revealed that key components of plant responses to herbivory, including induction of JA biosynthesis, key transcription factors and JA-inducible genes were apparently conserved in switchgrass and maize. In addition, these data affirm earlier studies with FAW and aphids that the cultivar Kanlow can provide useful genetics for the breeding of switchgrass germplasm with improved insect resistance.