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ARS Home » Southeast Area » Gainesville, Florida » Center for Medical, Agricultural and Veterinary Entomology » Chemistry Research » Research » Publications at this Location » Publication #282481

Title: An amino acid substitution inhibits specialist herbivore production of an antagonist effector and recovers insect-induced plant defenses

item Schmelz, Eric
item Huffaker, Alisa
item Carroll, Mark
item Alborn, Hans
item ALI, JARED - Cornell University
item Teal, Peter

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/21/2012
Publication Date: 9/24/2012
Citation: Schmelz, E.A., Huffaker, A., Carroll, M.J., Alborn, H.T., Ali, J.G., Teal, P.E. 2012. An amino acid substitution inhibits specialist herbivore production of an antagonist effector and recovers insect-induced plant defenses . Plant Physiology. 160(3):1468-1478.

Interpretive Summary: Following attack by pests, plants activate a wide range of protective biochemical defenses. Insect herbivores are often recognized by plants through the presence of elicitor molecules in larval oral secretions that greatly amplify the wound-induced plant responses. The existence of negative insect-derived effectors that suppress plant defenses is also predictable yet very few specific biochemicals with inhibitory activity have been characterized. By examining the interactions of generalist (Fall armyworm; Spodoptera frugiperda) and specialist (Velvetbean caterpillar; Anticarsia gemmatalis) pests on cowpea (Vigna unguiculata), scientists at the Center for Medical, Agricultural and Veterinary Entomology in Gainesville, FL, have discovered that Velvetbean caterpillars convert a potent plant elicitor into a competitive inhibitor of plant recognition. Importantly biochemical screens identified a simple alteration of the plant-derived elicitor precursor that was resistant to further Velvetbean caterpillar modification. When Velvetbean caterpillars ingested trace amounts of a modified plant protein sequence they elicited significantly greater plant defenses in cowpea herbivory assays. Velvetbean caterpillars are one of the single most problematic defoliators of tropical legume crops. We demonstrate a biochemical mechanism by which these legume crop pests avoid plant defense activation and demonstrate a simple strategy to recover the natural protective responses.

Technical Abstract: Plants respond to insect herbivory through the production of biochemicals that function as either direct defenses or indirect defenses via the attraction of natural enemies. Curiously, attack by even closely related insect pests can result in distinctive levels of induced plant defenses. Despite these observations, precise biochemical mechanisms responsible for differing plant responses remain largely unknown. Cowpea (Vigna unguiculata) plants respond to Fall armyworm (FAW; Spodoptera frugiperda) herbivory through the detection of fragments of ATP synthase '-subunit (cATPC) proteins, termed inceptin-related peptides, present in larval oral secretions (OS). In contrast to generalists like FAW, OS of the legume specializing Velvetbean caterpillar (VBC; Anticarsia gemmatalis) does not elicit ethylene production and demonstrates significantly lower induced volatile emission in direct herbivory comparisons. Unlike all other Lepidoptera examined which preferentially harbor the inceptin [Vu-In; +ICDINGVCVDA-] elicitor, VBC OS contains predominantly a C-terminal truncated peptide Vu-In-A [+ICDINGVCVD-]. Vu-In-A is both inactive and functions as potent naturally occurring competitive antagonist of Vu-In induced responses. Amino acid substitutions at the Vu-In C-terminus were screened for differences in VBC gut proteolysis and revealed a valine substituted peptide [Vu-In'V; +ICDINGVCVDV-] that retained full activity. Compared to the native polypeptide, VBC that previously ingested 500 pmols of a modified cATPC precursor elicited significantly stronger plant responses in herbivory assays. We demonstrate that a specialist herbivore minimizes the activation of defenses by converting an elicitor into a competitive antagonist effector and identify an amino acid substitution that recovers these induced plant defenses to a level observed with generalist herbivores.