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Within-plant isoprene oxidation confirmed by direct emissions

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Within-plant isoprene oxidation confirmed by directemissions of oxidation products methyl vinyl ketone andmethacroleinKOLBY J. JARDINE*, RUSSELL K. MONSON† , LEIF ABRELL‡ § , SCOTT R. SALESKA¶ ,ALMUT ARNETH**††, ANGELA JARDINE*, FRANC¸ OISE YOKO ISHIDA‡‡,ANAMARIAYANEZ SERRANO‡‡, PAULO ARTAXO§§,THOMASKARL¶¶, SILVANO FARES***, ALLENGOLDSTEIN†††, FRANCESCO LORETO‡‡‡ and TRAVIS HUXMAN*¶*The University of Arizona-Biosphere 2, PO Box 8746, Tucson, AZ 85738, USA, †School of Natural Resources and theEnvironment, University of Arizona, Biological Sciences East, Tucson, AZ 85721, USA, ‡Department of Chemistry &Biochemistry, University of Arizona, P.O. Box 210041, 1306 East University Blvd., Tucson, AZ 85721-0041, USA, §Departmentof Soil, Water & Environmental Science, University of Arizona, P.O. Box 210038, Tucson, AZ 85721-0038, USA, ¶Department ofEcology and Evolutionary Biology, University of Arizona, P.O. Box 210088, BioSciences West 310, Tucson, AZ 85721, USA,**Department of Physical Geography and Ecosystems Analysis, Lund University, So¨lvegatan 12, S-223 62, Lund, Sweden,††Research Centre Karlsruhe, Institute for Meteorology and Climate Research (IMK-IFU), 82467, Garmisch-Partenkirchen,Germany, ‡‡Large Biosphere-Atmosphere Experiment (LBA), Instituto Nacional de Pesquisas da Amazoˆnia, Av. Andre´Arau´jo,2936, Aleixo, CEP 69060-001, Manaus, Brazil, §§Instituto de Fisica Rua do Matao, Universidade de Sao Paulo, Travessa R Nr.187, CEP 05508-090, Cidade Universita´ria, Sa˜o Paulo, Brazil, ¶¶Atmospheric Chemistry Division, National Center forAtmospheric Research, P.O. Box 3000, Boulder, CO 80307-3000, USA, ***Agricultural Research Council (CRA), Research Centerfor the Soil Plant System, Via della Navicella 2-4, 00184, Rome, Italy, †††Department of Environmental Science, Policy, andManagement, University of California, 130 Mulford Hall #3114, Berkeley, CA 94720, USA, ‡‡‡National Research Council,Institute for Plant Protection, Via Madonna del Piano 10, 50132, Sesto Fiorentino (Firenze), ItalyAbstractIsoprene is emitted from many terrestrial plants at high rates, accounting for an estimated 1/3 of annual globalvolatile organic compound emissions from all anthropogenic and biogenic sources combined. Through rapidphotooxidation reactions in the atmosphere, isoprene is converted to a variety of oxidized hydrocarbons, provid-ing higher order reactants for the production of organic nitrates and tropospheric ozone, reducing the availabil-ity of oxidants for the breakdown of radiatively active trace gases such as methane, and potentially producinghygroscopic particles that act as effective cloud condensation nuclei. However, the functional basis for plant pro-duction of isoprene remains elusive. It has been hypothesized that in the cell isoprene mitigates oxidative dam-age during the stress-induced accumulation of reactive oxygen species (ROS), but the products of isoprene-ROSreactions in plants have not been detected. Using pyruvate-2-13C leaf and branch feeding and individual branchand whole mesocosm flux studies, we present evidence that isoprene (i) is oxidized to methyl vinyl ketone andmethacrolein (iox) in leaves and that iox/i emission ratios increase with temperature, possibly due to an increasein ROS production under high temperature and light stress. In a primary rainforest in Amazonia, we inferredsignificant in plant isoprene oxidation (despite the strong masking effect of simultaneous atmospheric oxidation),from its influence on the vertical distribution of ioxuptake fluxes, which were shifted to low isoprene emittingregions of the canopy. These observations suggest that carbon investment in isoprene production is larger thanthat inferred from emissions alone and that models of tropospheric chemistry and biota–chemistry–climate inter-actions should incorporate isoprene oxidation within both the biosphere and the atmosphere with potentialimplications for better understanding both the oxidizing power of the troposphere and forest response to climatechange.Keywords: Amazon, biosphere–atmosphere interactions, isoprene oxidation, methacrolein, methyl vinyl ketone, reactive oxy-gen species, temperature stress, thermotoleranceReceived 18 October 2011; revised version received 18 October 2011 and accepted 3 November 2011Correspondence: Kolby J. Jardine, tel. + 520 603 6096, fax + 520 838 6162, e-mail: [email protected]© 2011 Blackwell Publishing Ltd 973Global Change Biology (2012) 18, 973–984, doi: 10.1111/j.1365-2486.2011.02610.xIntroductionThe oxidative power of the lower atmosphere is con-trolled to a large extent by the emission of biogenichydrocarbons, especially those that contain carbon–car-bon double bonds, and is thus available for oxidationthrough reaction with hydroxyl radicals, ozone, andnitrate radicals (Monson, 2002). The first-generationproducts formed from the oxidation of isoprene, themost abundantly emitted plant hydrocarbon, are domi-nated by methyl vinyl ketone and methacrolein, collec-tively referred to here as iox(Pierotti et al., 1990). Todate, it has been assumed that most of the ioxin theatmosphere is produced by atmospheric oxidation ofisoprene, at the expense of atmospheric oxidants (Pier-otti et al., 1990; Montzka et al., 1993; Warneke et al.,2001; Tani et al., 2010). This assumption has influencedthe form of the current generation of atmosphericchemistry models that are used to study issues rangingfrom the oxidizing capacity of the atmosphere (Stav-rakou et al., 2010), the production of tropospheric ozone(Dreyfus et al., 2002), and the tropospheric lifetime ofmethane (Young et al., 2009).A wide variety of biotic (e.g. microbes, insects) andabiotic (e.g. thermal, radiative, drought) stressors causeaccumulation of reactive oxygen species (ROS), includ-ing hydrogen peroxide, singlet oxygen, superoxideanion, and the hydroxyl radical, in plant tissues. Exces-sive ROS accumulation can overwhelm cellular antioxi-dant defenses, including enzyme-mediated ROSquenching reactions, antioxidant systems for ROS scav-enging, and defense gene activation (Moller, 2001). Fol-lowing ROS accumulation, extensive oxidation ofimportant components such as nucleic acids, proteins,and lipids can further exacerbate ROS accumulationleading to programmed cell death (Apel & Hirt, 2004).Thus, plants with a diverse suite of antioxidantdefenses are expected to better tolerate stressful envi-ronmental


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