Priming by airborne signals boosts direct and indirect resistance in maize

• Published in: The Plant journal : for cell and molecular biology Vol. 49; no. 1; pp. 16 - 26
• Main Authors: Ton, Jurriaan, D'Alessandro, Marco, Jourdie, Violaine, Jakab, Gabor, Karlen, Danielle, Held, Matthias, Mauch-Mani, Brigitte, Turlings, Ted C.J
• Format: Journal Article
• Language: English
• Published: Oxford, UK Oxford, UK : Blackwell Publishing Ltd 01.01.2007; Blackwell Publishing Ltd; Blackwell Science
• Subjects: Agronomy. Soil science and plant productions; Animals; Biological and medical sciences; Botany; Cell physiology; Cotesia marginiventris; Feeding Behavior; Fundamental and applied biological sciences. Psychology; Gene expression; Gene Expression Regulation, Plant - physiology; Genetics and breeding of economic plants; Herbivores; Hymenoptera; induced resistance; Insects; jasmonic acid; Larva - physiology; Molecular and cellular biology; Molecular biology; Organic Chemicals - metabolism; Pest resistance; Plant ecology; Plant pathogens; priming; Signal transduction; Spodoptera - physiology; Spodoptera littoralis; Varietal selection. Specialized plant breeding, plant breeding aims; VOCs; Volatile organic compounds; Volatilization; Wasps - physiology; Zea mays; Zea mays - physiology; priming; Monocotyledones; Zea mays; Cotesia marginiventris; volatile organic compounds; Volatile organic compound; Hybridization; Gene expression; Induced resistance; Spodoptera littoralis; Gene; Gramineae; Insect resistance; Angiospermae; Development; Spermatophyta; jasmonic acid
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/j.1365-313X.2006.02935.x

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.