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.

Fungi in the genus Metarhizium (Hypocreales: Clavicipitaceae) are insect pathogens that can establish as endophytes and can benefit their host plant. In field experiments, we observed a positive correlation between the prevalence of M. robertsii and legume cover crops, and a negative relationship with brassicaceous cover crops and with increasing proportion of cereal rye in mixtures. Here, we report the effects of endophytic M. robertsii on three cover crop species under greenhouse conditions. We inoculated seeds of Austrian winter pea (Pisum sativum L., AWP), cereal rye (Secale cereale L.), and winter canola (Brassica napus L.) with conidia of M. robertsii to assess the effects of endophytic colonization on cover crop growth. We recovered M. robertsii from 59%, 46%, and 39% of seed-inoculated AWP, cereal rye, and canola plants, respectively. Endophytic M. robertsii significantly increased height and above-ground biomass of AWP and cereal rye but did not affect chlorophyll content of any of the cover crop species. Among inoculated plants from which we recovered M. robertsii, above-ground biomass of AWP was positively correlated with the proportion of colonized root but not leaf tissue sections. Our results suggest that winter cover crops may help to conserve Metarhizium spp. in annual cropping systems.

Fungi in the genus Metarhizium (Hypocreales: Clavicipitaceae) are insect-pathogens and endophytes that can benefit their host plant through growth promotion and protection against stresses. Cochliobolus heterostrophus (Drechsler) Drechsler (Pleosporales: Pleosporaceae) is an economically-significant phytopathogenic fungus that causes Southern Corn Leaf Blight (SCLB) in maize. We conducted greenhouse and lab-based experiments to determine the effects of endophytic M. robertsii J.F. Bisch., Rehner & Humber on growth and defense in maize (Zea mays L.) infected with C. heterostrophus. We inoculated maize seeds with spores of M. robertsii and, at the 3 to 4-leaf stage, the youngest true leaf of M. robertsii-treated and untreated control plants with spores of C. heterostrophus. After 96 h, we measured maize height, above-ground biomass, endophytic colonization by M. robertsii, severity of SCLB, and expression of plant defense genes and phytohormone content. We recovered M. robertsii from 74% of plants grown from treated seed. The severity of SCLB in M. robertsii-treated maize plants was lower than in plants inoculated only with C. heterostrophus. M. robertsii-treated maize inoculated or not inoculated with C. heterostrophus showed greater height and above-ground biomass compared with untreated control plants. Height and above-ground biomass of maize co-inoculated with M. robertsii and C. heterostrophus were not different from M. robertsii-treated maize. M. robertsii modulated the expression of defense genes and the phytohormone content in maize inoculated with C. heterostrophus compared with plants not inoculated with C. heterostrophus and control plants. These results suggest that endophytic M. robertsii can promote maize growth and reduce development of SCLB, possibly by induced systemic resistance mediated by modulation of phytohormones and expression of defense and growth-related genes in maize.