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Emissions of Putative Isoprene Oxidation Products from Mango Branches Under Abiotic Stress

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Emissions of Putative Isoprene Oxidation Products from Mango Branches Under Abiotic Stress UC Irvine UC Irvine Previously Published Works Title Emissions of putative isoprene oxidation products from mango branches under abiotic stress. Permalink https://escholarship.org/uc/item/3ds8t64n Journal Journal of experimental botany, 64(12) ISSN 0022-0957 Authors Jardine, Kolby J Meyers, Kimberly Abrell, Leif et al. Publication Date 2013-09-01 DOI 10.1093/jxb/ert202 Supplemental Material https://escholarship.org/uc/item/3ds8t64n#supplemental License https://creativecommons.org/licenses/by/4.0/ 4.0 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Journal of Experimental Botany, Vol. 64, No. 12, pp. 3697–3709, 2013 doi:10.1093/jxb/ert202 Advance Access publication 23 July, 2013 This paper is available online free of all access charges (see http://jxb.oxfordjournals.org/open_access.html for further details) RESEARCH PAPER Emissions of putative isoprene oxidation products from mango branches under abiotic stress Kolby J. Jardine1,*, Kimberly Meyers2, Leif Abrell3, Eliane G. Alves4, Ana Maria Yanez Serrano4,5, Jürgen Kesselmeier5, Thomas Karl6, Alex Guenther6, Jeffrey Q. Chambers1 and Claudia Vickers7 1 Climate Science Department, Earth Science Division, Lawrence Berkeley National Laboratory, 1 Cyclotron Rd, Building 64, Room 241, Berkeley, CA 94720, USA 2 US Department of Agriculture, Agriculture Research Service, 2000 East Allen Rd, Tucson, AZ 85719, USA Downloaded from 3 Department of Chemistry & Biochemistry and Department of Soil, Water and Environmental Science, University of Arizona, PO Box 210038, Tucson, AZ 85721-0038, USA 4 Large-Scale Biosphere-Atmosphere Experiment (LBA), Instituto Nacional de Pesquisas da Amazônia, Av. André Araújo, 2936, Aleixo, CEP 69060-001, Manaus, Brazil 5 Biogeochemistry Department, Max Planck Institute for Chemistry, PO Box 3060, 55020 Mainz, Germany http://jxb.oxfordjournals.org/ 6 Atmospheric Chemistry Division, National Center for Atmospheric Research, PO Box 3000, Boulder, CO 80307-3000, USA 7 Australian Institute for Bioengineering and Nanotechnology, The University of Queensland, Building 75, Cnr Cooper and College Rds, St Lucia, QLD 4072, Australia * To whom correspondence should be addressed. Email: [email protected] Received 17 May 2013; Revised 17 May 2013; Accepted 5 June 2013 at University of California, Irvine on August 17, 2015 Abstract Although several per cent of net carbon assimilation can be re-released as isoprene emissions to the atmosphere by many tropical plants, much uncertainty remains regarding its biological significance. In a previous study, we detected emissions of isoprene and its oxidation products methyl vinyl ketone (MVK) and methacrolein (MACR) from tropical plants under high temperature/light stress, suggesting that isoprene is oxidized not only in the atmosphere but also within plants. However, a comprehensive analysis of the suite of isoprene oxidation products in plants has not been performed and production relationships with environmental stress have not been described. In this study, putative isoprene oxidation products from mango (Mangifera indica) branches under abiotic stress were first identified. High temperature/light and freeze–thaw treatments verified direct emissions of the isoprene oxidation products MVK and MACR together with the first observations of 3-methyl furan (3-MF) and 2-methyl-3-buten-2-ol (MBO) as putative novel isoprene oxidation products. Mechanical wounding also stimulated emissions of MVK and MACR. Photosynthesis 13 under CO2 resulted in rapid (<30 min) labelling of up to five carbon atoms of isoprene, with a similar labelling pattern observed in the putative oxidation products. These observations highlight the need to investigate further the mecha- nisms of isoprene oxidation within plants under stress and its biological and atmospheric significance. Keywords: 2-Methyl-3-buten-2-ol, 3-methyl furan, methacrolein, methyl vinyl ketone, reactive oxygen species, volatile organic compounds. Introduction Isoprene (C5H8) is emitted in large quantities by many terres- atmospheric chemistry leading to the formation of a num- trial plants directly into the atmosphere, where it acts to fuel ber of species with high relevance to air quality and climate Abbreviations: 3-MF, 3-methyl furan; 3-MT, 3-methyl thiophene; GC-MS, gas chromatography/mass spectrometry; GLV, green leaf volatiles; MACR, methacr- olein; MBO, 2-methyl-3-buten-2-ol; MVK, methyl vinyl ketone; NIST, the National Institute of Standards and Technology; PAR, photosynthetically active radiation; PTR-MS, proton transfer reaction/mass spectrometry; ROS, reactive oxygen species; sccm, standard cm3 min–1; slpm, standard l min–1; TD, thermal desorption. © The Author [2013]. Published by Oxford University Press on behalf of the Society for Experimental biology. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http:// creativecommons.org/licenses/by-nc/3.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected] 3698 | Jardine et al. including organic nitrates (Lockwood et al., 2010), ground presence of α,β-unsaturated carbonyl groups, and therefore level ozone (Pierce et al., 1998), and secondary organic aero- show high reactivity with nucleophiles (Uchida et al., 1998). sols (Kroll et al., 2006) that may act as effective cloud conden- Reactive electrophiles may potentially affect gene expression sation nuclei (Engelhart et al., 2011). Due to its high annual at all levels by chemically reacting with nucleic acids, proteins, global emission rate of 500–750 Tg year–1 (Guenther et al., and small molecules as well as by indirectly lowering pools of 2006) and high reactivity to atmospheric oxidants such as cellular reductants (Farmer and Davoine, 2007). the OH radical (Atkinson and Arey, 2003), isoprene emis- Recently, we obtained evidence that isoprene is oxidized sions from terrestrial vegetation exert a controlling effect on not only in the atmosphere but also within plants. Using gas the oxidative power of the lower atmosphere. Once emitted, chromatography/mass spectrometry (GC-MS) and proton isoprene is rapidly oxidized in the atmosphere (1–2 h lifetime transfer reaction/mass spectrometry (PTR-MS), we detected with respect to oxidation by OH radicals) with first-order gas-phase emissions of isoprene and its oxidation products oxidation products dominated by formaldehyde (50–70%), MVK and MACR from high temperature/light-stressed methyl vinyl ketone (MVK, 25–39%), methacrolein (MACR, desert (Jardine et al., 2010a) and tropical (Jardine et al., 2012) 17–27%), and 3-methyl furan (3-MF, 4.2–5.4%) (Atkinson plants. We demonstrated at the leaf, branch, and enclosed and Arey, 2003). However, efforts to quantify the magnitude mesocosm scales that higher emissions of MVK+MACR of isoprene chemistry–climate feedbacks have been hindered relative to isoprene occurred during high temperature/light Downloaded from by major uncertainties as to why plants dedicate a significant stress. In addition, leaf feeding of pyruvate-2-13C (a precur- fraction (a few per cent under normal physiological condi- sur of isoprene) through the transpiration stream was used tions) of assimilated carbon to isoprene emissions in the first to track 13C into de novo isoprene biosynthesis and its oxida- place (Pacifico et al., 2009). In contrast to its role in atmos- tion products MVK and MACR, suggesting that these com- pheric chemistry, very little is known about the behaviour and pounds are produced directly from isoprene reactions. http://jxb.oxfordjournals.org/ effects of isoprene in planta, including potential redox reac- In this study, using a coupled PTR-MS, GC-MS, and pho- tions and products. tosynthesis system, we first investigated branch-level emissions Reactive oxygen species (ROS) including singlet oxygen of isoprene and putative isoprene oxidation products MVK 1 – ( O2), superoxide anion (O2 ), hydrogen peroxide (H2O2), and MACR from a high isoprene-emitting species, Mangifera and the hydroxyl radical (OH) are continuously generated indica (mango), and a non-isoprene-emitting species Annona in plants due to the incomplete reduction of oxygen. While muricata (soursop) under abiotic stress including high tem- initially considered toxic byproducts of aerobic metabolism, perature/light, freeze–thaw/dehydration, and mechanical ROS are now widely recognized to play a multitude of signal- wounding. Next, we quantified emissions of the putative at University of California, Irvine on August 17, 2015 ling roles during the regulation of biological processes includ- novel isoprene oxidation products 3-MF, 3-methyl thiophene ing growth and development (Foreman et al., 2003), cell cycle (3-MT), and 2-methyl-3-buten-2-ol (MBO) from mango (Feher et al., 2008), programmed cell death (Overmyer et al., branches in response to abiotic stress. Finally, we explored the 2003), hormone signalling and stomatal regulation (Kwak possibility that these compounds derive from isoprene oxida- et al., 2003; Pei et al., 2000), and biotic and abiotic stress tion within plants (Fig. 1) by tracking isoprene biosynthesis 13 responses (Mittler, 2002; Mullineaux and Karpinski, 2002). and volatile emissions during photosynthesis under CO2. While ROS concentrations within plants are generally kept low by cellular antioxidant defence systems, ROS accumula- tion during stress can overwhelm
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