title: Plant elicitor peptides are conserved signals regulating direct and indirect antiherbivore defense.
abstract: Insect-induced defenses occur in nearly all plants and are regulated by conserved signaling pathways. As the first described plant peptide signal, systemin regulates antiherbivore defenses in the Solanaceae, but in other plant families, peptides with analogous activity have remained elusive. In the current study, we demonstrate that a member of the maize (Zea mays) plant elicitor peptide (Pep) family, ZmPep3, regulates responses against herbivores. Consistent with being a signal, expression of the ZmPROPEP3 precursor gene is rapidly induced by Spodoptera exigua oral secretions. At concentrations starting at 5 pmol per leaf, ZmPep3 stimulates production of jasmonic acid, ethylene, and increased expression of genes encoding proteins associated with herbivory defense. These include proteinase inhibitors and biosynthetic enzymes for production of volatile terpenes and benzoxazinoids. In accordance with gene expression data, plants treated with ZmPep3 emit volatiles similar to those from plants subjected to herbivory. ZmPep3-treated plants also exhibit induced accumulation of the benzoxazinoid phytoalexin 2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3-one glucoside. Direct and indirect defenses induced by ZmPep3 contribute to resistance against S. exigua through significant reduction of larval growth and attraction of Cotesia marginiventris parasitoids. ZmPep3 activity is specific to Poaceous species; however, peptides derived from PROPEP orthologs identified in Solanaceous and Fabaceous plants also induce herbivory-associated volatiles in their respective species. These studies demonstrate that Peps are conserved signals across diverse plant families regulating antiherbivore defenses and are likely to be the missing functional homologs of systemin outside of the Solanaceae.
authors.affiliation: Chemistry Research Unit, Center for Medical, Agricultural, and Veterinary Entomology, US Department of Agriculture-Agricultural Research Service, Gainesville, FL 32608, USA. alisa.huffaker@ars.usda.gov
authors.forename: Alisa
authors.initials: A
authors.lastname: Huffaker
authors.forename: Gregory
authors.initials: G
authors.lastname: Pearce
authors.forename: Nathalie
authors.initials: N
authors.lastname: Veyrat
authors.forename: Matthias
authors.initials: M
authors.lastname: Erb
authors.forename: Ted C J
authors.initials: TC
authors.lastname: Turlings
authors.forename: Ryan
authors.initials: R
authors.lastname: Sartor
authors.forename: Zhouxin
authors.initials: Z
authors.lastname: Shen
authors.forename: Steven P
authors.initials: SP
authors.lastname: Briggs
authors.forename: Martha M
authors.initials: MM
authors.lastname: Vaughan
authors.forename: Hans T
authors.initials: HT
authors.lastname: Alborn
authors.forename: Peter E A
authors.initials: PE
authors.lastname: Teal
authors.forename: Eric A
authors.initials: EA
authors.lastname: Schmelz
mesh_terms: D000818:Animals; D012634:Bodily Secretions / Q000378:metabolism; D003517:Cyclopentanes / Q000378:metabolism; D005030:Ethylenes / Q000378:metabolism; D018506:Gene Expression Regulation, Plant / Q000187:drug effects* / Q000276:immunology; D060434:Herbivory / Q000276:immunology; D006790:Host-Parasite Interactions; D007113:Immunity, Innate / Q000276:immunology*; D054883:Oxylipins / Q000378:metabolism; D011480:Protease Inhibitors / Q000378:metabolism; D011498:Protein Precursors / Q000378:metabolism*; D015398:Signal Transduction / Q000235:genetics / Q000276:immunology*; D018411:Spodoptera / Q000737:chemistry; D003313:Zea mays / Q000737:chemistry* / Q000276:immunology*
chemical_list: D003517:Cyclopentanes; D005030:Ethylenes; D054883:Oxylipins; D011480:Protease Inhibitors; D011498:Protein Precursors; C011006:jasmonic acid; C036216:ethylene