Mechanical damage caused by insect feeding along with components present in insect saliva and oral secretions are known to induce jasmonic acid–mediated defense responses in plants. This study investigated the effects of bacteria from oral secretions of the fall armyworm Spodoptera frugiperda on herbivore-induced defenses in tomato and maize plants. Using culture-dependent methods, we identified seven different bacterial isolates belonging to the family Enterobacteriacea from the oral secretions of field-collected caterpillars. Two isolates, Pantoea ananatis and Enterobacteriaceae-1, downregulated the activity of the plant defensive proteins polyphenol oxidase and trypsin proteinase inhibitors (trypsin PI) but upregulated peroxidase (POX) activity in tomato. A Raoultella sp. and a Klebsiella sp. downregulated POX but upregulated trypsin PI in this plant species. Conversely, all of these bacterial isolates upregulated the expression of the herbivore-induced maize proteinase inhibitor (mpi) gene in maize. Plant treatment with P. ananatis and Enterobacteriaceae-1 enhanced caterpillar growth on tomato but diminished their growth on maize plants. Our results highlight the importance of herbivore-associated microbes and their ability to mediate insect plant interactions differently in host plants fed on by the same herbivore.

Stomata play a central role in plant responses to abiotic and biotic stresses. Existing knowledge regarding the roles of stomata in plant stress is centered on abiotic stresses and plant-pathogen interactions, but how stomata influence plant-herbivore interactions remains largely unclear. Here, we summarize the functions of stomata in plant-insect interactions and highlight recent discoveries of how herbivores manipulate plant stomata. Because stomata are linked to interrelated physiological processes in plants, herbivory-induced changes in stomatal dynamics might have cellular, organismic, and/or even community-level impacts. We summarize our current understanding of how stomata mediate plant responses to herbivory and environmental stimuli, propose how herbivores may influence these responses, and identify key knowledge gaps in plant-herbivore interactions.

Obligate symbioses occur when organisms require symbiotic relationships to survive. Some parasitic wasps of caterpillars possess obligate mutualistic viruses called “polydnaviruses.” Along with eggs, wasps inject polydnavirus inside their caterpillar hosts where the hatching larvae develop inside the caterpillar. Polydnaviruses suppress the immune systems of their caterpillar hosts, which enables egg hatch and wasp larval development. It is unknown whether polydnaviruses also manipulate the salivary proteins of the caterpillar, which may affect the elicitation of plant defenses during feeding by the caterpillar. Here, we show that a polydnavirus of the parasitoid Microplitis croceipes, and not the parasitoid larva itself, drives the regulation of salivary enzymes of the caterpillar Helicoverpa zea that are known to elicit tomato plant-defense responses to herbivores. The polydnavirus suppresses glucose oxidase, which is a primary plant-defense elicitor in the saliva of the H. zea caterpillar. By suppressing plant defenses, the polydnavirus allows the caterpillar to grow at a faster rate, thus improving the host suitability for the parasitoid. Remarkably, polydnaviruses manipulate the phenotypes of the wasp, caterpillar, and host plant, demonstrating that polydnaviruses play far more prominent roles in shaping plant–herbivore interactions than ever considered. Significance The role of herbivore-associated microbes in mediating plant–herbivore interactions has gained recent attention. We show that a parasitoid associated with its caterpillar host not only suppresses the immune system of the caterpillar but also suppresses the induced defenses of the caterpillar’s host plant. Parasitoids inject eggs into their hosts but also inject polydnaviruses that suppress the caterpillar’s immunity. Immunosuppression enables eggs to hatch and develop as larvae within caterpillars. Additionally, the polydnavirus reduces salivary glucose oxidase, the primary elicitor found in the caterpillar’s oral secretions. Caterpillars injected with polydnavirus induce lower plant defenses than untreated caterpillars. Our results reveal a dimension to the complexity of plant–herbivore interactions indicating that polydnaviruses mediate the phenotypes of the parasitoid, herbivore, and plant.

In addition to feeding damage, herbivores release cues that are recognized by plants to elicit defenses. Caterpillar oral secretions have been shown to trigger herbivore defense responses in several different plant species. In this study, the effects of two fall armyworm (Spodoptera frugiperda) oral secretions (saliva and regurgitant) on caterpillar defense responses in maize (Zea mays) were examined. Only minute amounts of regurgitant were deposited on the maize leaf during larval feeding bouts and its application to leaves failed to induce the expression of several herbivore defense genes. On the other hand, caterpillars consistently deposited saliva on leaves during feeding and the expression of several maize defense genes significantly increased in response to saliva application and larval feeding. However, feeding by ablated caterpillars with impaired salivation did not induce these defenses. Furthermore, bioassays indicated that feeding by unablated caterpillars significantly enhanced defenses when compared with that of ablated caterpillars. Another critical finding was that the maize genotype and stage of development affected the expression of defense genes in response to wounding and regurgitant treatments. These results demonstrate that fall armyworm saliva contains elicitors that trigger herbivore defenses in maize.

The perception of herbivory by plants is known to be triggered by the deposition of insect-derived factors such as saliva and oral secretions, oviposition materials, and even feces. Such insect-derived materials harbor chemical cues that may elicit herbivore and/or pathogen-induced defenses in plants. Several insect-derived molecules that trigger herbivore-induced defenses in plants are known; however, insect-derived molecules suppressing them are largely unknown. In this study, we identified two plant chitinases from fall armyworm (Spodoptera frugiperda) larval frass that suppress herbivore defenses while simultaneously inducing pathogen defenses in maize (Zea mays). Fall armyworm larvae feed in enclosed whorls of maize plants, where frass accumulates over extended periods of time in close proximity to damaged leaf tissue. Our study shows that maize chitinases, Pr4 and Endochitinase A, are induced during herbivory and subsequently deposited on the host with the feces. These plant chitinases mediate the suppression of herbivore-induced defenses, thereby increasing the performance of the insect on the host. Pr4 and Endochitinase A also trigger the antagonistic pathogen defense pathway in maize and suppress fungal pathogen growth on maize leaves. Frass-induced suppression of herbivore defenses by deposition of the plant-derived chitinases Pr4 and Endochitinase A is a unique way an insect can co-opt the plant’s defense proteins for its own benefit. It is also a phenomenon unlike the induction of herbivore defenses by insect oral secretions in most host-herbivore systems.