Maize Plants Recognize Herbivore-Associated Cues from Caterpillar Frass

Abstract

Caterpillar behaviors such as feeding, crawling, and oviposition are known to induce defenses in maize and other plant species. We examined plant defense responses to another important caterpillar behavior, their defecation. Fall armyworms (FAW, Spodoptera frugiperda), a major threat to maize (Zea mays), are voracious eaters and deposit copious amounts of frass in the enclosed whorl tissue surrounding their feeding site, where it remains for long periods of time. FAW frass is composed of molecules derived from the host plant, the insect itself, and associated microbes, and hence provides abundant cues that may alter plant defense responses. We observed that proteins from FAW frass initially induced wound-responsive defense genes in maize; however, a pathogenesis-related (pr) defense gene was induced as the time after application increased. Elicitation of pathogen defenses by frass proteins was correlated with increased herbivore performance and reduced fungal pathogen performance over time. These responses differ from the typical plant response to oral secretions of the FAW. The results pave the way for identification of protein molecule(s) from the excretion of an herbivore that elicits pathogen defense responses while attenuating herbivore defenses in plants.

Turnabout Is Fair Play: Herbivory-Induced Plant Chitinases Excreted in Fall Armyworm Frass Suppress Herbivore Defenses in Maize

“…Plants respond to insect herbivory with an arsenal of defenses, both direct defenses, when plants synthesize molecules that are detrimental to the insect pests, and indirect defenses, when plants emit volatiles after insect attack that recruit natural enemies of the pests (Chen, 2008). The recognition of herbivory by plants has been attributed to different insect behaviors, such as feeding, crawling, oviposition, and even defecation (Pechan et al, 2002;Felton and Tumlinson, 2008;Peiffer et al, 2009;Hilfiker et al, 2014;Ray et al, 2015). Herbivory not only mechanically damages the host tissue but also includes secretions such as insect saliva, regurgitant, or frass (Felton and Tumlinson, 2008;Ray et al, 2015).…”

“…The recognition of herbivory by plants has been attributed to different insect behaviors, such as feeding, crawling, oviposition, and even defecation (Pechan et al, 2002;Felton and Tumlinson, 2008;Peiffer et al, 2009;Hilfiker et al, 2014;Ray et al, 2015). Herbivory not only mechanically damages the host tissue but also includes secretions such as insect saliva, regurgitant, or frass (Felton and Tumlinson, 2008;Ray et al, 2015). The molecules deposited from these secretions that trigger herbivore defenses have been referred to as elicitors or herbivore-associated molecular patterns (HAMPs) that are analogous to pathogen-associated molecular patterns (Bent and Mackey, 2007;Felton and Tumlinson, 2008;Acevedo et al, 2015;Schmelz, 2015).…”

Lessons from the Far End: Caterpillar FRASS-Induced Defenses in Maize, Rice, Cabbage, and Tomato

“…Herbivore frass is composed of a complex blend of biomolecules arising from the insect, host plant, and microbes present in the gut or frass (Chen et al, 2005, Chen et al, 2007Ray et al, 2015). We have only begun to understand how endophytic symbionts in the insect gut can alter plant defenses (Chung et al, 2013).…”

“…Plant defense responses to insect herbivory have been attributed to several insect behaviors such as feeding, crawling, oviposition, and even defecation (Alborn et al 1997;Felton and Tumlinson 2008;Hilfiker et al 2014;Kim et al 2012;Mithöfer et al 2005;Peiffer et al 2009;Ray et al 2015). Insect feeding is associated with deposition of oral secretions and/ or saliva on plant tissue, which leaves chemical cues of et al 2013b;Musser et al 2002;Tian et al 2012).…”

Two New Polyphenol Oxidase Genes of Tea Plant (Camellia sinensis) Respond Differentially to the Regurgitant of Tea Geometrid, Ectropis obliqua

“…The collected regurgitant was centrifuged for 5 min at 10,000× g , after which the supernatant was collected and stored at −80 °C for leaf treatment. Preliminary separation of the regurgitant was carried out according to the method described in Ray et al [65] (2015) with minor revision. The collected regurgitant was diluted 1:4 v / v with water and filtered through Miracloth (EMD Millipore, Billerica, MA, USA) to remove debris.…”