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      Indole is an essential herbivore-induced volatile priming signal in maize

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          Abstract

          Herbivore-induced volatile organic compounds prime non-attacked plant tissues to respond more strongly to subsequent attacks. However, the key volatiles that trigger this primed state remain largely unidentified. In maize, the release of the aromatic compound indole is herbivore-specific and occurs earlier than other induced responses. We therefore hypothesized that indole may be involved in airborne priming. Using indole-deficient mutants and synthetic indole dispensers, we show that herbivore-induced indole enhances the induction of defensive volatiles in neighbouring maize plants in a species-specific manner. Furthermore, the release of indole is essential for priming of mono- and homoterpenes in systemic leaves of attacked plants. Indole exposure markedly increases the herbivore-induced production of the stress hormones jasmonate-isoleucine conjugate and abscisic acid, which represents a likely mechanism for indole-dependent priming. These results demonstrate that indole functions as a rapid and potent aerial priming agent that prepares systemic tissues and neighbouring plants for incoming attacks.

          Abstract

          Herbivore attack of plant tissue primes non-attacked tissue to respond more strongly to subsequent attacks. Here, Erb et al. identify indole as an airborne priming signal that enhances herbivore-induced defensive-volatile and stress-hormone production in systemic tissues and neighbouring plants.

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          Most cited references38

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          XCMS Online: a web-based platform to process untargeted metabolomic data.

          Recently, interest in untargeted metabolomics has become prevalent in the general scientific community among an increasing number of investigators. The majority of these investigators, however, do not have the bioinformatic expertise that has been required to process metabolomic data by using command-line driven software programs. Here we introduce a novel platform to process untargeted metabolomic data that uses an intuitive graphical interface and does not require installation or technical expertise. This platform, called XCMS Online, is a web-based version of the widely used XCMS software that allows users to easily upload and process liquid chromatography/mass spectrometry data with only a few mouse clicks. XCMS Online provides a solution for the complete untargeted metabolomic workflow including feature detection, retention time correction, alignment, annotation, statistical analysis, and data visualization. Results can be browsed online in an interactive, customizable table showing statistics, chromatograms, and putative METLIN identities for each metabolite. Additionally, all results and images can be downloaded as zip files for offline analysis and publication. XCMS Online is available at https://xcmsonline.scripps.edu.
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            Airborne signals prime plants against insect herbivore attack.

            Green leafy volatiles (GLV), six-carbon aldehydes, alcohols, and esters commonly emitted by plants in response to mechanical damage or herbivory, induced intact undamaged corn seedlings to rapidly produce jasmonic acid (JA) and emit sesquiterpenes. More importantly, corn seedlings previously exposed to GLV from neighboring plants produced significantly more JA and volatile sesquiterpenes when mechanically damaged and induced with caterpillar regurgitant than seedlings not exposed to GLV. The use of pure synthetic chemicals revealed that (Z)-3-hexenal, (Z)-3-hexen-1-ol, and (Z)-3-hexenyl acetate have nearly identical priming activity. Caterpillar-induced nocturnal volatiles, which are enriched in GLV, also exhibited a strong priming effect, inducing production of larger amounts of JA and release of greater quantities of volatile organic compounds after caterpillar regurgitant application. In contrast, GLV priming did not affect JA production induced by mechanical wounding alone. Thus, GLV specifically prime neighboring plants against impending herbivory by enhancing inducible chemical defense responses triggered during attack and may play a key role in plant-plant signaling and plant-insect interactions.
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              Volatile signaling in plant-plant interactions: "talking trees" in the genomics era.

              Plants may "eavesdrop" on volatile organic compounds (VOCs) released by herbivore-attacked neighbors to activate defenses before being attacked themselves. Transcriptome and signal cascade analyses of VOC-exposed plants suggest that plants eavesdrop to prime direct and indirect defenses and to hone competitive abilities. Advances in research on VOC biosynthesis and perception have facilitated the production of plants that are genetically "deaf" to particular VOCs or "mute" in elements of their volatile vocabulary. Such plants, together with advances in VOC analytical instrumentation, will allow researchers to determine whether fluency enhances the fitness of plants in natural communities.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Pub. Group
                2041-1723
                16 February 2015
                : 6
                : 6273
                Affiliations
                [1 ]Institute of Plant Sciences, Department of Biology, University of Bern , Altenbergrain 21, 3013 Bern, Switzerland
                [2 ]Laboratory for Fundamental and Applied Research in Chemical Ecology, Faculty of Science, University of Neuchâtel , Rue Emile-Argand 11, 2009 Neuchâtel, Switzerland
                [3 ]Lehrstuhl für Genetik, TU Munich , Emil-Ramann-Straβe 8, 85354 Freising, Germany
                [4 ]Department of Animal and Plant Sciences, University of Sheffield , Western Bank, S10 2TN Sheffield, UK
                Author notes
                [*]

                These authors contributed equally to the work.

                Article
                ncomms7273
                10.1038/ncomms7273
                4339915
                25683900
                4d364672-a426-4ab0-9393-ee36ffe3a820
                Copyright © 2015, Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 06 June 2014
                : 12 January 2015
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