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      Waterborne Signaling Primes the Expression of Elicitor-Induced Genes and Buffers the Oxidative Responses in the Brown Alga Laminaria digitata

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          Abstract

          As marine sessile organisms, seaweeds must respond efficiently to biotic and abiotic challenges in their natural environment to reduce the fitness consequences of wounds and oxidative stress. This study explores the early steps of the defense responses of a large marine brown alga (the tangle kelp Laminaria digitata) and investigates its ability to transmit a warning message to neighboring conspecifics. We compared the early responses to elicitation with oligoguluronates in laboratory-grown and harvested wild individuals of L. digitata. We followed the release of H 2O 2 and the concomitant production of volatile organic compounds. We also monitored the kinetics of expression of defense-related genes following the oxidative burst. Laboratory-grown algae were transplanted in kelp habitats to further evaluate their responses to elicitation after a transient immersion in natural seawater. In addition, a novel conditioning procedure was established to mimic field conditions in the laboratory. Our experiments showed that L. digitata integrates waterborne cues present in the kelp bed and/or released from elicited neighboring plants. Indeed, the exposure to elicited conspecifics changes the patterns of oxidative burst and volatile emissions and potentiates this kelp for faster induction of genes specifically regulated in response to oligoguluronates. Thus, waterborne signals shape the elicitor-induced responses of kelps through a yet unknown mechanism reminiscent of priming in land plants.

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          Most cited references65

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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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            Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature.

            Plants respond to herbivore attack with the release of volatile organic compounds (VOCs), which can attract predatory arthropods and/or repel herbivores and thus serve as a means of defense against herbivores. Such VOCs might also be perceived by neighboring plants to adjust their defensive phenotype according to the present risk of attack. We exposed lima bean plants at their natural growing site to volatiles of beetle-damaged conspecific shoots. This reduced herbivore damage and increased the growth rate of the exposed plants. To investigate whether VOCs also can serve in signaling processes within the same individual plant we focused on undamaged "receiver" leaves that were either exposed or not exposed to VOCs released by induced "emitter" leaves. Extrafloral nectar secretion by receiver leaves increased when they were exposed to VOCs of induced emitters of neighboring plants or of the same shoot, yet not when VOCs were removed from the system. Extrafloral nectar attracts predatory arthropods and represents an induced defense mechanism. The volatiles also primed extrafloral nectar secretion to show an augmented response to subsequent damage. Herbivore-induced VOCs elicit a defensive response in undamaged plants (or parts of plants) under natural conditions, and they function as external signal for within-plant communication, thus serving also a physiological role in the systemic response of a plant to local damage.
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              Long-distance signalling in plant defence.

              Plants use inducible defence mechanisms to fend off harmful organisms. Resistance that is induced in response to local attack is often expressed systemically, that is, in organs that are not yet damaged. In the search for translocated defence signals, biochemical studies follow the physical movement of putative signals, and grafting experiments use mutants that are impaired in the production or perception of these signals. Long-distance signals can directly activate defence or can prime for the stronger and faster induction of defence. Historically, research has focused on the vascular transport of signalling metabolites, but volatiles can play a crucial role as well. We compare the advantages and constraints of vascular and airborne signals for the plant, and discuss how they can act in synergy to achieve optimised resistance in distal plant parts.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2011
                24 June 2011
                : 6
                : 6
                : e21475
                Affiliations
                [1 ]Marine Plants and Biomolecules Laboratory, Unité Mixte de Recherche 7139, Station Biologique de Roscoff, Université Pierre et Marie Curie, Roscoff, France
                [2 ]Unité Mixte de Recherche 7139, Station Biologique, Centre National de la Recherche Scientifique (CNRS), Roscoff, France
                [3 ]Laboratoire de Biochimie, Epissage, Cancer, Lipides et Apoptose, Unit 613, Institut National de la Santé et de la Recherche Médicale, Faculté de Médecine, Université de Bretagne Occidentale, Brest, France
                [4 ]Adaptation et Diversité en Milieu Marin, Unité Mixte de Recherche 7144, Station Biologique, Université Pierre et Marie Curie, Roscoff, France
                [5 ]Unité Mixte de Recherche 7144, Adaptation et Diversité en Milieu Marin, Station Biologique, Centre National de la Recherche Scientifique (CNRS), Roscoff, France
                Biodiversity Insitute of Ontario - University of Guelph, Canada
                Author notes

                Conceived and designed the experiments: FT AC CL PP. Performed the experiments: FT AC SG SR. Analyzed the data: FT AC MV. Contributed reagents/materials/analysis tools: SG SR PM. Wrote the paper: FT AC CL PP. Supervised SG and FT Ph.D. thesis: PP CL. Supervised SR Ph.D. thesis: PM.

                Article
                PONE-D-11-04055
                10.1371/journal.pone.0021475
                3123347
                21731761
                09db8e0e-3903-46e4-aec2-236c126750c1
                Thomas et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 28 February 2011
                : 1 June 2011
                Page count
                Pages: 12
                Categories
                Research Article
                Biology
                Marine Biology
                Phycology
                Model Organisms
                Plant and Algal Models
                Plant Science
                Plants
                Algae

                Uncategorized
                Uncategorized

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