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Key Message: This review provides an overview, analysis, and reflection on insect elicitors and effectors (particularly from oral secretions) in the context of the 'arms race' with host plants. Following injury by an insect herbivore, plants rapidly activate induced defenses that may directly or indirectly affect the insect. Such defense pathways are influenced by a multitude of factors; however, cues from the insect's oral secretions are perhaps the most well studied mediators of such plant responses. The relationship between plants and their insect herbivores is often termed an 'evolutionary arms race' of strategies for each organism to either overcome defenses or to avoid attack. However, these compounds that can elicit a plant defense response that is detrimental to the insect may also benefit the physiology or metabolism of an insect species. Indeed, several insect elicitors of plant defenses (such as the fatty acid-amino acid conjugate, volicitin) are known to enhance an insect's ability to obtain nutritionally important compounds from plant tissue. Here we re-examine the well-known elicitors and effectors from chewing insects to demonstrate not only our incomplete understanding of the specific biochemical and molecular cascades involved in these interactions but also to consider the role of these compounds for the insect species itself. Finally, this overview discusses opportunities for research in the field of plant-insect interactions by utilizing tools such as genomics and proteomics to integrate the future study of these interactions through ecological, physiological, and evolutionary disciplines., (© 2021. The Author(s), under exclusive licence to Springer Nature B.V.)

Plants possess a suite of traits that make them challenging to consume by insect herbivores. Plant tissues are recalcitrant, have low levels of protein, and may be well defended by chemicals. Insects use diverse strategies for overcoming these barriers, including co-opting metabolic activities from microbial associates. In this review, we discuss the co-option of bacteria and fungi in the herbivore gut. We particularly focus upon chewing, folivorous insects (Coleoptera and Lepidoptera) and discuss the impacts of microbial co-option on herbivore performance and plant responses. We suggest that there are two components to microbial co-option: fixed and plastic relationships. Fixed relationships are involved in integral dietary functions and can be performed by microbial enzymes co-opted into the genome or by stably transferred associates. In contrast, the majority of gut symbionts appear to be looser and perform more facultative, context-dependent functions. This more plastic, variable co-option of bacteria likely produces a greater number of insect phenotypes, which interact differently with plant hosts. By altering plant detection of herbivory or mediating insect interactions with plant defensive compounds, microbes can effectively improve herbivore performance in real time within and between generations., (© 2018 John Wiley & Sons Ltd.)

It is becoming abundantly clear that the microbes associated with plants and insects can profoundly influence plant-insect interactions. Here, we focus on recent findings and propose directions for future research that involve microbe-induced changes to plant defenses and nutritive quality as well as the consequences of these changes for the behavior and fitness of insect herbivores. Insect (herbivore and parasitoid)-associated microbes can favor or improve insect fitness by suppressing plant defenses and detoxifying defensive phytochemicals. Phytopathogens can influence or manipulate insect behavior and fitness by altering plant quality and defense. Plant-beneficial microbes can promote plant growth and influence plant nutritional and phytochemical composition that can positively or negatively influence insect fitness. Lastly, we suggest that entomopathogens have the potential to influence plant defenses directly as endophytes or indirectly by altering insect physiology.

The vasculature of plants act as a channel for transport of signal(s) that facilitate long-distance intraplant communication. In maize, Maize insect resistance1-Cysteine Protease (Mir1-CP), which has homology to papain-like proteases, provides defense to different feeding guilds of insect pests. Furthermore, accumulation of Mir1-CP in the vasculature suggests that Mir1-CP can potentially function as a phloem-mobile protein. In a recent study, we provided evidence that Mir1-CP can curtail the growth of phloem-sap sucking insect, corn leaf aphid (CLA; Rhopalosiphum maidis). Our current study further examined whether aboveground feeding by CLA can induce resistance to subsequent herbivory by belowground feeding western corn rootworm (WCR; Diabrotica virgifera virgifera). Aboveground feeding by CLA systemically induced the accumulation of Mir1-CP in the roots. Furthermore, foliage feeding by CLA provided enhanced resistance to subsequent herbivory by belowground feeding of WCR. Taken together, our previous findings and results presented here indicate that long-distance transport of Mir1-CP is critical for providing enhanced resistance to insect attack in maize.

Chewing herbivores cause massive damage when crushing plant tissues with their mandibles, thus releasing a vast array of cues that may be perceived by the plant to mobilize defenses. Besides releasing damage cues in wounded tissues, herbivores deposit abundant cues from their saliva, regurgitant and feces that trigger herbivore specific responses in plants. Herbivores can manipulate the perception mechanisms and defense signals to suppress plant defenses by secreting effectors and/or by exploiting their associated oral microbes. Recent studies indicate that both the composition of herbivore cues and the plant's ability to recognize them are highly dependent upon the specific plant-herbivore system. There is a growing amount of work on identifying herbivore elicitors and effectors, but the most significant bottleneck in the discipline is the identification and characterization of plant receptors that perceive these herbivore-specific cues., (Copyright © 2015 Elsevier Ltd. All rights reserved.)

Plants express inducible direct and indirect defenses in response to herbivory. The plant hormone jasmonic acid (JA) and related signaling compounds referred to as jasmonates play a central role in regulating defense responses to a wide range of herbivores.We assessed whether treating tomato seeds with 0.8 mM of methyl jasmonate (MeJA) affected the performance of the leaf miner Tuta absoluta, and whether possible changes in volatile profiles altered the behavior of its predator Chrysoperla externa. MeJA-treatment significantly lengthened larval development and decreased the pupal weight of T. absoluta. Herbivory alone increased the emissions of α-pinene, 6-methyl 5-hepten-2-one, β-myrcene, (E)-β-ocimene, isoterpinolene, TMTT, (Z)-3-hexenyl butyrate, and hexyl salicylate. MeJA seed treatment significantly decreased the emissions of α-cubebene from undamaged and herbivore-infested plants. In addition, the emissions of several compounds were lower in the absence of herbivory. Chrysoperla. externa preferred odors from herbivore-infested plants over those from control plants, regardless of the MeJA-treatment, and they did not show any preference for herbivore-infested plants for any of the MeJA-treatments. Our results show preliminary evidence that the treatment of tomato seeds with MeJA can reduce the performance of Tuta absoluta, and that the chemical differences observed in plant VOC profiles do not alter the behavior of the model predator.

Defense priming is defined as increased readiness of defense induction. A growing body of literature indicates that plants (or intact parts of a plant) are primed in anticipation of impending environmental stresses, both biotic and abiotic, and upon the following stimulus, induce defenses more quickly and strongly. For instance, some plants previously exposed to herbivore-inducible plant volatiles (HIPVs) from neighboring plants under herbivore attack show faster or stronger defense activation and enhanced insect resistance when challenged with secondary insect feeding. Research on priming of antiherbivore defense has been limited to the HIPV-mediated mechanism until recently, but significant advances were made in the past three years, including non-HIPV-mediated defense priming, epigenetic modifications as the molecular mechanism of priming, and others. It is timely to consider the advances in research on defense priming in the plant-insect interactions., (© 2012 Institute of Zoology, Chinese Academy of Sciences.)

Inducible defenses, which provide enhanced resistance after initial attack, are nearly universal in plants. This defense signaling cascade is mediated by the synthesis, movement, and perception of jasmonic acid and related plant metabolites. To characterize the long-term persistence of plant immunity, we challenged Arabidopsis (Arabidopsis thaliana) and tomato (Solanum lycopersicum) with caterpillar herbivory, application of methyl jasmonate, or mechanical damage during vegetative growth and assessed plant resistance in subsequent generations. Here, we show that induced resistance was associated with transgenerational priming of jasmonic acid-dependent defense responses in both species, caused caterpillars to grow up to 50% smaller than on control plants, and persisted for two generations in Arabidopsis. Arabidopsis mutants that are deficient in jasmonate perception (coronatine insensitive1) or in the biogenesis of small interfering RNA (dicer-like2 dicer-like3 dicer-like4 and nuclear RNA polymerase d2a nuclear RNA polymerase d2b) do not exhibit inherited resistance. The observation of inherited resistance in both the Brassicaceae and Solanaceae suggests that this trait may be more widely distributed in plants. Epigenetic resistance to herbivory thus represents a phenotypically plastic mechanism for enhanced defense across generations.

Our understanding of induced resistance against herbivores has grown immeasurably during the last several decades. Based upon the emerging literature, we argue that induced resistance represents a continuum of phenotypes that is determined by the plant's ability to integrate multiple suites of signals of plant and herbivore origin. We present a model that illustrates the range of signals arising from early detection through herbivore feeding, and then through subsequent plant generations., (Published by Elsevier Ltd.)

The psocid, Liposcelis paeta Pearman, is an increasingly important polyphagous pest of stored products worldwide. Intensive use of organophosphorous insecticides for pest control has facilitated resistance development in psocids in China. Three insecticide-resistant field populations of L. paeta were collected from Nanyang city of Henan Province (NY), and Wuzhou (WZ) and Hezhou (HZ) cities of Guangxi Province, China. Previous studies have shown that psocids have different susceptibilities to insecticides. In addition, their AChE susceptibilities to paraoxon-ethyl and demeton-S-methyl also differed from each other. Acetylcholinesterase 1, which is one of the major targets for organophosphate insecticides, has been fully cloned and sequenced from these populations of L. paeta. Comparison of both nucleotide and deduced amino acid sequences revealed nucleotide polymorphisms among L. paeta ace 1 genes from different populations, but none of these polymorphisms correspond to the active sites in AChE 1 from other insects. The results of comparative quantitative real-time PCR indicated that the relative expression level of HZ ace 1 gene was the highest among three populations, which was 1.20 and 1.02-fold higher than those of NY and WZ populations, respectively. This may due to an epigenetic inheritance phenomenon, which allows organisms to respond to a particular environment through changes in gene expression., (Copyright 2010 Elsevier Ltd. All rights reserved.)

The dramatic movements of some carnivorous plants species are triggered by sensory structures derived from trichomes. While unusual plant species such as the Venus fly trap and sundews may be expected to have elaborate sensors to capture their insect prey, more modest plant species might not be expected to have similar sensory capabilities. Our recent work, however, has revealed that glandular trichomes on tomato (Solanum lycopersicum) appear to have a function similar to trigger hairs of carnivorous species, acting as "early warning" sensors. Using a combination of behavioral, molecular, and biochemical techniques, we determined that caterpillars, moths and mechanical disruption upregulate signaling molecules and defensive genes found in glandular trichomes. Importantly, we discovered that plants whose trichomes have been broken respond more vigorously when their defenses were induced. Taken together, our results suggest that glandular trichomes can act as sensors that detect activity on the leaf surface, and ready plants for herbivore attack.

Although five different classes of insect herbivore-produced elicitors of plant volatiles have been identified, this is only a part of the complex, chemically mediated interactions between insect herbivores and their host plants. The defensive reactions of the plant, following physical injury by the herbivore, are influenced by a multitude of factors including, but not necessarily limited to, the elicitors and numerous other herbivore-associated molecules, as well as microbes on the plant surface that may alter plant defensive pathways. Ultimately, a thorough and accurate understanding of the chemical ecology of insect-plant interactions will require a more holistic approach, taking into consideration the ecological and physiological context in which a plant perceives and responds to herbivore-associated signals.

Pre-inoculation of plants with a pathogen that induces necrosis leads to the development of systemic acquired resistance (SAR) to subsequent pathogen attack [1]. The phenylpropanoid-derived compound salicylic acid (SA) is necessary for the full expression of both local resistance and SAR [2] [3]. A separate signaling pathway involving jasmonic acid (JA) is involved in systemic responses to wounding and insect herbivory [4] [5]. There is evidence both supporting and opposing the idea of cross-protection against microbial pathogens and insect herbivores [6] [7]. This is a controversial area because pharmacological experiments point to negative cross-talk between responses to systemic pathogens and responses to wounding [8] [9] [10], although this has not been demonstrated functionally in vivo. Here, we report that reducing phenylpropanoid biosynthesis by silencing the expression of phenylalanine ammonialyase (PAL) reduces SAR to tobacco mosaic virus (TMV), whereas overexpression of PAL enhances SAR. Tobacco plants with reduced SAR exhibited more effective grazing-induced systemic resistance to larvae of Heliothis virescens, but larval resistance was reduced in plants with elevated phenylpropanoid levels. Furthermore, genetic modification of components involved in phenylpropanoid synthesis revealed an inverse relationship between SA and JA levels. These results demonstrate phenylpropanoid-mediated cross-talk in vivo between microbially induced and herbivore-induced pathways of systemic resistance.

Reducing phenylpropanoid biosynthesis in transgenic tobacco compromises systemic acquired resistance (SAR) to tobacco mosaic virus, while increasing phenylpropanoid biosynthesis enhances SAR. Surprisingly, transgenic tobacco plants compromised in SAR exhibit more effective grazing-induced systemic resistance to larvae of Heliothis virescens, whereas induced insect resistance is compromised in transgenic plants with elevated phenylpropanoid levels. Levels of the phenylpropanoid-derived signal salicylic acid are directly correlated with overall phenylpropanoid biosynthesis in this series of transgenic plants. Moreover, while pathogen-induced SAR is almost completely compromised in salicylic acid-deficient plants expressing the bacterial nahG salicylate hydroxylase gene, these plants show enhanced grazing-induced insect resistance compared to wild-type. Hence, suppression of grazing-induced insect resistance is mediated at least in part by salicylic acid and likely reflects salicylic acid inhibition of the synthesis and action of the wound signal jasmonic acid. We propose that the dual functions of salicylic acid contribute to a signal poise which constrains constitutive expression of disease and insect resistance mechanisms, and reciprocally switches their selective activation.

Insects possess a suite of antioxidant enzymes and small molecular weight antioxidants that may form a concatenated response to an onslaught of dietary and endogenously produced oxidants. Antioxidant enzymes such as superoxide dismutase, catalase, glutathione transferase, and glutathione reductase have been characterized in insects. Water-soluble and lipid-soluble antioxidants such as ascorbate, glutathione, tocopherols, and carotenoids have not been well studied in insects but may play very important antioxidant roles. Additionally, the peritrophic matrix and trehalose may possess important antioxidant functions in insects. The enzymatic recycling of ascorbate, first noted in green plants, may also exist in insects. A greater understanding of these antioxidant systems may provide greater understanding about the ecological relationships of insects with their hosts.

Dehydroascorbic acid reductase, which catalyses the regeneration of ascorbic acid from dehydroascorbic acid, is reported here to occur widely among insects. Due to the reported absence of glutathione peroxidase in insects and the generally low affinity of catalase for hydrogen peroxide, dehydroascorbic acid reductase may play a pivotal role in the elimination of hydrogen peroxide in insects.