title: Priming by airborne signals boosts direct and indirect resistance in maize.
abstract: Plants counteract attack by herbivorous insects using a variety of inducible defence mechanisms. The production of toxic proteins and metabolites that instantly affect the herbivore's development are examples of direct induced defence. In addition, plants may release mixtures of volatile organic compounds (VOCs) that indirectly protect the plant by attracting natural enemies of the herbivore. Recent studies suggest that these VOCs can also prime nearby plants for enhanced induction of defence upon future insect attack. However, evidence that this defence priming causes reduced vulnerability to insects is sparse. Here we present molecular, chemical and behavioural evidence that VOC-induced priming leads to improved direct and indirect resistance in maize. A differential hybridization screen for inducible genes upon attack by Spodoptera littoralis caterpillars identified 10 defence-related genes that are responsive to wounding, jasmonic acid (JA), or caterpillar regurgitant. Exposure to VOCs from caterpillar-infested plants did not activate these genes directly, but primed a subset of them for earlier and/or stronger induction upon subsequent defence elicitation. This priming for defence-related gene expression correlated with reduced caterpillar feeding and development. Furthermore, exposure to caterpillar-induced VOCs primed for enhanced emissions of aromatic and terpenoid compounds. At the peak of this VOC emission, primed plants were significantly more attractive to parasitic Cotesia marginiventris waSPS. This study shows that VOC-induced priming targets a specific subset of JA-inducible genes, and links these responses at the molecular level to enhanced levels of direct and indirect resistance against insect attack.
authors.affiliation: Laboratory of Evolutionary Entomology, Institute of Zoology, University of Neuchâtel, Neuchâtel, Switzerland. j.ton@bio.uu.nl
authors.forename: Jurriaan
authors.initials: J
authors.lastname: Ton
authors.forename: Marco
authors.initials: M
authors.lastname: D'Alessandro
authors.forename: Violaine
authors.initials: V
authors.lastname: Jourdie
authors.forename: Gabor
authors.initials: G
authors.lastname: Jakab
authors.forename: Danielle
authors.initials: D
authors.lastname: Karlen
authors.forename: Matthias
authors.initials: M
authors.lastname: Held
authors.forename: Brigitte
authors.initials: B
authors.lastname: Mauch-Mani
authors.forename: Ted C J
authors.initials: TC
authors.lastname: Turlings
mesh_terms: D000818:Animals; D005247:Feeding Behavior; D018506:Gene Expression Regulation, Plant / Q000502:physiology*; D007814:Larva / Q000502:physiology; D009930:Organic Chemicals / Q000378:metabolism*; D018411:Spodoptera / Q000502:physiology; D014835:Volatilization; D014863:Wasps / Q000502:physiology; D003313:Zea mays / Q000502:physiology*
chemical_list: D009930:Organic Chemicals