title: Induction and detoxification of maize 1,4-benzoxazin-3-ones by insect herbivores.
abstract: In monocotyledonous plants, 1,4-benzoxazin-3-ones, also referred to as benzoxazinoids or hydroxamic acids, are one of the most important chemical barriers against herbivores. However, knowledge about their behavior after attack, mode of action and potential detoxification by specialized insects remains limited. We chose an innovative analytical approach to understand the role of maize 1,4-benzoxazin-3-ones in plant-insect interactions. By combining unbiased metabolomics screening and simultaneous measurements of living and digested plant tissue, we created a quantitative dynamic map of 1,4-benzoxazin-3-ones at the plant-insect interface. Hypotheses derived from this map were tested by specifically developed in vitro assays using purified 1,4-benzoxazin-3-ones and active extracts from mutant plants lacking 1,4-benzoxazin-3-ones. Our data show that maize plants possess a two-step defensive system that effectively fends off both the generalist Spodoptera littoralis and the specialist Spodoptera frugiperda. In the first step, upon insect attack, large quantities of 2-β-d-glucopyranosyloxy-4,7-dimethoxy-1,4-benzoxazin-3-one (HDMBOA-Glc) are formed. In the second step, after tissue disruption by the herbivores, highly unstable 2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3-one (HDMBOA) is released by plant-derived β-glucosidases. HDMBOA acts as a strong deterrent to both S. littoralis and S. frugiperda. Although constitutively produced 1,4-benzoxazin-3-ones such as 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) are detoxified via glycosylation by the insects, no conjugation of HDMBOA in the insect gut was found, which may explain why even the specialist S. frugiperda has not evolved immunity against this plant defense. Taken together, our results show the benefit of using a plant-insect interface approach to elucidate plant defensive processes and unravel a potent resistance mechanism in maize.
authors.affiliation: Laboratory for Fundamental and Applied Research in Chemical Ecology, University of Neuchâtel, Rue Emile-Argand 11, CH-2009 Neuchâtel, Switzerland.
authors.forename: Gaétan
authors.initials: G
authors.lastname: Glauser
authors.forename: Guillaume
authors.initials: G
authors.lastname: Marti
authors.forename: Neil
authors.initials: N
authors.lastname: Villard
authors.forename: Gwladys A
authors.initials: GA
authors.lastname: Doyen
authors.forename: Jean-Luc
authors.initials: JL
authors.lastname: Wolfender
authors.forename: Ted C J
authors.initials: TC
authors.lastname: Turlings
authors.forename: Matthias
authors.initials: M
authors.lastname: Erb
mesh_terms: D000818:Animals; D048588:Benzoxazines / Q000276:immunology / Q000378:metabolism* / Q000633:toxicity; D041981:Gastrointestinal Tract / Q000276:immunology / Q000378:metabolism; D005960:Glucosides / Q000276:immunology / Q000378:metabolism* / Q000633:toxicity; D006031:Glycosylation; D060434:Herbivory / Q000276:immunology*; D006790:Host-Parasite Interactions; D007814:Larva / Q000276:immunology / Q000378:metabolism / Q000502:physiology; D025341:Principal Component Analysis; D055550:Protein Stability; D013045:Species Specificity; D018411:Spodoptera / Q000276:immunology* / Q000378:metabolism / Q000502:physiology; D018675:Toxicity Tests; D003313:Zea mays / Q000276:immunology* / Q000378:metabolism / Q000469:parasitology* / Q000633:toxicity
chemical_list: C430218:2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3-one glucoside; D048588:Benzoxazines; D005960:Glucosides; C050733:2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one