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      Non-Photochemical Quenching Capacity in Arabidopsis thaliana Affects Herbivore Behaviour

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          Abstract

          Under natural conditions, plants have to cope with numerous stresses, including light-stress and herbivory. This raises intriguing questions regarding possible trade-offs between stress defences and growth. As part of a program designed to address these questions we have compared herbivory defences and damage in wild type Arabidopsis thaliana and two “photoprotection genotypes”, npq4 and oePsbS, which respectively lack and overexpress PsbS (a protein that plays a key role in qE-type non-photochemical quenching). In dual-choice feeding experiments both a specialist ( Plutella xylostella) and a generalist ( Spodoptera littoralis) insect herbivore preferred plants that expressed PsbS most strongly. In contrast, although both herbivores survived equally well on each of the genotypes, for oviposition female P. xylostella adults preferred plants that expressed PsbS least strongly. However, there were no significant differences between the genotypes in levels of the 10 most prominent glucosinolates; key substances in the Arabidopsis anti-herbivore chemical defence arsenal. After transfer from a growth chamber to the field we detected significant differences in the genotypes’ metabolomic profiles at all tested time points, using GC-MS, but no consistent “metabolic signature” for the lack of PsbS. These findings suggest that the observed differences in herbivore preferences were due to differences in the primary metabolism of the plants rather than their contents of typical “defence compounds”. A potentially significant factor is that superoxide accumulated most rapidly and to the highest levels under high light conditions in npq4 mutants. This could trigger changes in planta that are sensed by herbivores either directly or indirectly, following its dismutation to H 2O 2.

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          Most cited references20

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          A pigment-binding protein essential for regulation of photosynthetic light harvesting.

          Photosynthetic light harvesting in plants is regulated in response to changes in incident light intensity. Absorption of light that exceeds a plant's capacity for fixation of CO2 results in thermal dissipation of excitation energy in the pigment antenna of photosystem II by a poorly understood mechanism. This regulatory process, termed nonphotochemical quenching, maintains the balance between dissipation and utilization of light energy to minimize generation of oxidizing molecules, thereby protecting the plant against photo-oxidative damage. To identify specific proteins that are involved in nonphotochemical quenching, we have isolated mutants of Arabidopsis thaliana that cannot dissipate excess absorbed light energy. Here we show that the gene encoding PsbS, an intrinsic chlorophyll-binding protein of photosystem II, is necessary for nonphotochemical quenching but not for efficient light harvesting and photosynthesis. These results indicate that PsbS may be the site for nonphotochemical quenching, a finding that has implications for the functional evolution of pigment-binding proteins.
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            The chemical diversity and distribution of glucosinolates and isothiocyanates among plants.

            Glucosinolates (beta-thioglucoside-N-hydroxysulfates), the precursors of isothiocyanates, are present in sixteen families of dicotyledonous angiosperms including a large number of edible species. At least 120 different glucosinolates have been identified in these plants, although closely related taxonomic groups typically contain only a small number of such compounds. Glucosinolates and/or their breakdown products have long been known for their fungicidal, bacteriocidal, nematocidal and allelopathic properties and have recently attracted intense research interest because of their cancer chemoprotective attributes. Numerous reviews have addressed the occurrence of glucosinolates in vegetables, primarily the family Brassicaceae (syn. Cruciferae; including Brassica spp and Raphanus spp). The major focus of much previous research has been on the negative aspects of these compounds because of the prevalence of certain "antinutritional" or goitrogenic glucosinolates in the protein-rich defatted meal from widely grown oilseed crops and in some domesticated vegetable crops. There is, however, an opposite and positive side of this picture represented by the therapeutic and prophylactic properties of other "nutritional" or "functional" glucosinolates. This review addresses the complex array of these biologically active and chemically diverse compounds many of which have been identified during the past three decades in other families. In addition to the Brassica vegetables, these glucosinolates have been found in hundreds of species, many of which are edible or could provide substantial quantities of glucosinolates for isolation, for biological evaluation, and potential application as chemoprotective or other dietary or pharmacological agents.
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              Imaging of photo-oxidative stress responses in leaves.

              High resolution digital imaging was used to identify sites of photo-oxidative stress responses in Arabidopsis leaves non-invasively, and to demonstrate the potential of using a suite of imaging techniques for the study of oxidative metabolism in planta. Tissue-specific photoinhibition of photosynthesis in individual chloroplasts in leaves was imaged by chlorophyll fluorescence microscopy. Singlet oxygen production was assessed by imaging the quenching of the fluorescence of dansyl-2,2,5,5-tetramethyl-2,5-dihydro-1H-pyrrole (DanePy) that results from its reaction with singlet oxygen. Superoxide and hydrogen peroxide accumulation were visualized by the reduction of nitroblue tetrazolium (NBT) to formazan deposits and by polymerization with 3,3'-diaminobenzidine (DAB), respectively. Stress-induced expression of a gene involved with antioxidant metabolism was imaged from the bioluminescence from leaves of an Arabidopsis APX2-LUC transformant, which co-expresses an ascorbate peroxidase (APX2) with firefly luciferase. Singlet oxygen and superoxide production were found to be primarily located in mesophyll tissues whereas hydrogen peroxide accumulation and APX2 gene expression were primarily localized in the vascular tissues.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                2 January 2013
                : 8
                : 1
                : e53232
                Affiliations
                [1 ]Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, Umeå, Sweden
                [2 ]Department of Ecology and Environmental Science, Umeå University, Umeå, Sweden
                [3 ]Department of Molecular Biology, Pusan National University, Busan, Republic of Korea
                [4 ]Institute of Botany, Azerbaijan National Academy of Sciences, Baku, Azerbaijan
                [5 ]Department of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, Germany
                [6 ]CEA, Institut de Biologie et Technologies de Saclay, Service de Bioénergétique Biologie Structurale et Mécanisme, Gif-sur-Yvette, France
                RIKEN Plant Science Center, Japan
                Author notes

                Competing Interests: One of the authors (Jon Moen) is an academic editor of PLOS ONE. This does not alter the authors' adherence to all the PLOS ONE policies on sharing data and materials. Apart from this, the authors declare that no competing interests exist.

                Conceived and designed the experiments: HJJ MF JM SJ IZ CHL AKL MR JG. Performed the experiments: HJJ MF IZ AKL MR. Analyzed the data: HJJ MF IZ AKL MR. Wrote the first version of the manuscript: MF JM SJ. Coordinated the completion of the second version of the manuscript: HJJ SJ. Contributed with specific parts and edited and commented on the manuscript: HJJ MF IZ MR AKL YM JG JM CHL SJ.

                Article
                PONE-D-12-09506
                10.1371/journal.pone.0053232
                3534670
                23301046
                cd6460de-7c3b-4e8f-993e-fa5644cd78f5
                Copyright @ 2013

                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
                : 6 February 2012
                : 29 November 2012
                Page count
                Pages: 12
                Funding
                Funders are The Swedish Research Council (VR), The Max Planck Society, Agence Nationale de la Recherche (reference ANR-09-BLAN-0005-01), and Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (2009-0071776). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Biochemistry
                Metabolism
                Metabolic Pathways
                Plant Biochemistry
                Secondary Metabolism
                Ecology
                Plant Ecology
                Model Organisms
                Plant and Algal Models
                Arabidopsis Thaliana
                Molecular Cell Biology
                Signal Transduction
                Signaling Pathways
                Plant Science
                Plant Biochemistry
                Photosynthesis
                Plant Biotechnology
                Transgenic Plants
                Plant Physiology

                Uncategorized
                Uncategorized

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