title: An amino acid substitution inhibits specialist herbivore production of an antagonist effector and recovers insect-induced plant defenses.
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. While attack by closely related insect pests can result in distinctive levels of induced plant defenses, precise biochemical mechanisms responsible for differing responses remain largely unknown. Cowpea (Vigna unguiculata) responds to Fall armyworm (Spodoptera frugiperda) herbivory through the detection of fragments of chloroplastic ATP synthase γ-subunit proteins, termed inceptin-related peptides, present in larval oral secretions (OS). In contrast to generalists like Fall armyworm, OS of the legume-specializing velvetbean caterpillar (VBC; Anticarsia gemmatalis) do not elicit ethylene production and demonstrate significantly lower induced volatile emission in direct herbivory comparisons. Unlike all other Lepidoptera OS examined, which preferentially contain inceptin (Vu-In; +ICDINGVCVDA-), VBC OS contain predominantly a C-terminal truncated peptide, Vu-In(-A) (+ICDINGVCVD-). Vu-In(-A) is both inactive and functions as a potent naturally occurring antagonist of Vu-In-induced responses. To block antagonist production, amino acid substitutions at the C terminus were screened for differences in VBC gut proteolysis. A valine-substituted peptide (Vu-In(ΔV); +ICDINGVCVDV-) retaining full elicitor activity was found to accumulate in VBC OS. Compared with the native polypeptide, VBC that previously ingested 500 pmol of the valine-modified chloroplastic ATP synthase γ-subunit 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 an antagonist effector and identify an amino acid substitution that recovers these induced plant defenses to a level observed with generalist herbivores.
authors.affiliation: Chemistry Research Unit, Agricultural Research Service, Center of Medical, Agricultural, and Veterinary Entomology, United States Department of Agriculture, Gainesville, Florida 32608, USA. eric.schmelz@ars.usda.gov
authors.forename: Eric A
authors.initials: EA
authors.lastname: Schmelz
authors.forename: Alisa
authors.initials: A
authors.lastname: Huffaker
authors.forename: Mark J
authors.initials: MJ
authors.lastname: Carroll
authors.forename: Hans T
authors.initials: HT
authors.lastname: Alborn
authors.forename: Jared G
authors.initials: JG
authors.lastname: Ali
authors.forename: Peter E A
authors.initials: PE
authors.lastname: Teal
mesh_terms: D000595:Amino Acid Sequence; D019943:Amino Acid Substitution / Q000235:genetics*; D000818:Animals; D025222:Chloroplast Proton-Translocating ATPases / Q000378:metabolism; D007887:Fabaceae / Q000187:drug effects / Q000276:immunology* / Q000469:parasitology*; D060434:Herbivory / Q000187:drug effects / Q000502:physiology*; D007814:Larva / Q000187:drug effects / Q000502:physiology; D008954:Models, Biological; D008969:Molecular Sequence Data; D009036:Moths / Q000187:drug effects / Q000201:enzymology / Q000502:physiology*; D010455:Peptides / Q000737:chemistry / Q000494:pharmacology; D018411:Spodoptera / Q000187:drug effects
chemical_list: D010455:Peptides; D025222:Chloroplast Proton-Translocating ATPases