Photosynthesis Research

, Volume 113, Issue 1–3, pp 321–333 | Cite as

Green leaf volatiles and oxygenated metabolite emission bursts from mesquite branches following light–dark transitions

  • K. Jardine
  • G. A. Barron-Gafford
  • J. P. Norman
  • L. Abrell
  • R. K. Monson
  • K. T. Meyers
  • M. Pavao-Zuckerman
  • K. Dontsova
  • E. Kleist
  • C. Werner
  • T. E. Huxman
Regular Paper

Abstract

Green leaf volatiles (GLVs) are a diverse group of fatty acid-derived compounds emitted by all plants and are involved in a wide variety of developmental and stress-related biological functions. Recently, GLV emission bursts from leaves were reported following light–dark transitions and hypothesized to be related to the stress response while acetaldehyde bursts were hypothesized to be due to the ‘pyruvate overflow’ mechanism. In this study, branch emissions of GLVs and a group of oxygenated metabolites (acetaldehyde, ethanol, acetic acid, and acetone) derived from the pyruvate dehydrogenase (PDH) bypass pathway were quantified from mesquite plants following light–dark transitions using a coupled GC–MS, PTR-MS, and photosynthesis system. Within the first minute after darkening following a light period, large emission bursts of both C5 and C6 GLVs dominated by (Z)-3-hexen-1-yl acetate together with the PDH bypass metabolites are reported for the first time. We found that branches exposed to CO2-free air lacked significant GLV and PDH bypass bursts while O2-free atmospheres eliminated the GLV burst but stimulated the PDH bypass burst. A positive relationship was observed between photosynthetic activity prior to darkening and the magnitude of the GLV and PDH bursts. Photosynthesis under 13CO2 resulted in bursts with extensive labeling of acetaldehyde, ethanol, and the acetate but not the C6-alcohol moiety of (Z)-3-hexen-1-yl acetate. Our observations are consistent with (1) the “pyruvate overflow” mechanism with a fast turnover time (<1 h) as part of the PDH bypass pathway, which may contribute to the acetyl-CoA used for the acetate moiety of (Z)-3-hexen-1-yl acetate, and (2) a pool of fatty acids with a slow turnover time (>3 h) responsible for the C6 alcohol moiety of (Z)-3-hexen-1-yl acetate via the 13-lipoxygenase pathway. We conclude that our non-invasive method may provide a new valuable in vivo tool for studies of acetyl-CoA and fatty acid metabolism in plants at a variety of spatial scales.

Keywords

Green leaf volatiles Pyruvate dehydrogenase bypass Light–dark transitions Photosynthesis Pyruvate overflow 

Supplementary material

11120_2012_9746_MOESM1_ESM.doc (256 kb)
Supplementary material 1 (DOC 256 kb)

References

  1. Andreou A, Feussner I (2009) Lipoxygenases—structure and reaction mechanism. Phytochemistry 70(13–14):1504–1510PubMedCrossRefGoogle Scholar
  2. Anstis PJP, Friend J (1974) Effect of light on lipoxygenase activity in dwarf pea-seedlings. Phytochemistry 13(12):2709–2712CrossRefGoogle Scholar
  3. Arimura G, Matsui K, Takabayashi J (2009) Chemical and molecular ecology of herbivore-induced plant volatiles: proximate factors and their ultimate Functions. Plant Cell Physiol 50(5):911–923PubMedCrossRefGoogle Scholar
  4. Bao XM, Focke M, Pollard M, Ohlrogge J (2000) Understanding in vivo carbon precursor supply for fatty acid synthesis in leaf tissue. Plant J 22(1):39–50PubMedCrossRefGoogle Scholar
  5. Barron-Gafford G, Scott R, Jenerette D, Hamerlynck EP, Huxman T (2012) Temperature and precipitation controls over leaf- and ecosystem-level CO2 flux along a woody plant encroachment gradient. Glob Chang Biol 18:1389–1400. doi:10.1111/j.1365-2486.2011.02599.x CrossRefGoogle Scholar
  6. Beauchamp J, Wisthaler A, Hansel A et al (2005) Ozone induced emissions of biogenic VOC from tobacco: relationships between ozone uptake and emission of LOX products. Plant, Cell Environ 28(10):1334–1343CrossRefGoogle Scholar
  7. Brilli F, Ruuskanen TM, Schnitzhofer R et al (2011) Detection of plant volatiles after leaf wounding and darkening by proton transfer reaction “time-of-flight” mass spectrometry (PTR-TOF). PLoS ONE 6(5):e20419PubMedCrossRefGoogle Scholar
  8. Broun P, Gettner S, Somerville C (1999) Genetic engineering of plant lipids. Annu Rev Nutr 19:197–216PubMedCrossRefGoogle Scholar
  9. Chang WC (2003) Identification of an endogenous inhibitor of arachidonate metabolism in human epidermoid carcinoma A431 cells. J Biomed Sci 10(6):599–606PubMedCrossRefGoogle Scholar
  10. Chehab EW, Kaspi R, Savchenko T, Rowe H, Negre-Zakharov F, Kliebenstein D, Dehesh K (2008) Distinct roles of jasmonates and aldehydes in plant-defense responses. PLoS ONE 3(4):e1904PubMedCrossRefGoogle Scholar
  11. Chehab W, Kaspi R, Savchenko T, Dehesh K (2010) Hexenyl acetate mediates indirect plant defense responses. Proc ANAS (Biol Sci) 66(5–6):145–151Google Scholar
  12. Connor EC, Rott AS, Zeder M, Juttner F, Dorn S (2008) (13)C-labelling patterns of green leaf volatiles indicating different dynamics of precursors in Brassica leaves. Phytochemistry 69(6):1304–1312PubMedCrossRefGoogle Scholar
  13. Cook HW, Lands WEM (1975) Further studies of the kinetics of oxygenation of arachidonic acid by soybean lipoxygenase. Can J Biochem 53:1220–1231PubMedCrossRefGoogle Scholar
  14. D’Auria JC, Pichersky E, Schaub A, Hansel A, Gershenzon J (2007) Characterization of a BAHD acyltransferase responsible for producing the green leaf volatile (Z)-3-hexen-1-yl acetate in Arabidopsis thaliana. Plant J 49(2):194–207PubMedCrossRefGoogle Scholar
  15. De Gouw JA, Howard CJ, Custer TG, Baker BM, Fall R (2000) Proton-transfer chemical-ionization mass spectrometry allows real-time analysis of volatile organic compounds released from cutting and drying of crops. Environ Sci Technol 34(12):2640–2648CrossRefGoogle Scholar
  16. Durand T, Bultel-Ponce V, Guy A, Berger S, Mueller MJ, Galano JM (2009) New bioactive oxylipins formed by non-enzymatic free-radical-catalyzed pathways: the phytoprostanes. Lipids 44(10):875–888PubMedCrossRefGoogle Scholar
  17. Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH (2004) Airborne signals prime plants against insect herbivore attack. Proc Nat Acad Sci USA 101(6):1781–1785PubMedCrossRefGoogle Scholar
  18. Fall R, Karl T, Hansel A, Jordan A, Lindinger W (1999) Volatile organic compounds emitted after leaf wounding: on-line analysis by proton-transfer-reaction mass spectrometry. J Geophys Res-Atmos 104(D13):15963–15974CrossRefGoogle Scholar
  19. Fall R, Karl T, Jordon A, Lindinger W (2001) Biogenic C5VOCs: release from leaves after freeze-thaw wounding and occurrence in air at a high mountain observatory. Atmos Environ 35(22):3905–3916CrossRefGoogle Scholar
  20. Farmer EE, Davoine C (2007) Reactive electrophile species. Curr Opin Plant Biol 10(4):380–386PubMedCrossRefGoogle Scholar
  21. Fatland BL, Nikolau BJ, Wurtele ES (2005) Reverse genetic characterization of cytosolic acetyl-CoA generation by ATP-citrate lyase in Arabidopsis. Plant Cell 17(1):182–203PubMedCrossRefGoogle Scholar
  22. Gigot C, Ongena M, Fauconnier ML, Wathelet JP, Du Jardin P, Thonart P (2010) The lipoxygenase metabolic pathway in plants: potential for industrial production of natural green leaf volatiles. Biotechnol Agron Soc Environ 14(3):451–460Google Scholar
  23. Graus M, Schnitzler JP, Hansel A, Cojocariu C, Rennenberg H, Wisthaler A, Kreuzwieser J (2004) Transient release of oxygenated volatile organic compounds during light-dark transitions in grey poplar leaves. Plant Physiol 135(4):1967–1975PubMedCrossRefGoogle Scholar
  24. Guenther A, Hewitt CN, Erickson D et al (1995) A global-model of natural volatile organic-compound emissions. J Geophys Res-Atmos 100(D5):8873–8892CrossRefGoogle Scholar
  25. Guss PL, Macko V, Richards T, Stahmann MA (1968) Lipoxidase in early growth of wheat. Plant Cell Physiol 9(3):415–422Google Scholar
  26. Hatanaka A (1993) Studies on biogeneration and physiological-role of green odor by plant. Nippon Nogeikagaku Kaishi-Nippon Nogeikagaku Kaishi-J Jpn Soc Biosci Biotechnol Agrochem 67(10):1391–1398CrossRefGoogle Scholar
  27. Heiden AC, Kobel K, Langebartels C, Schuh-Thomas G, Wildt J (2003) Emissions of oxygenated volatile organic compounds from plants—part I: emissions from lipoxygenase activity. J Atmos Chem 45(2):143–172CrossRefGoogle Scholar
  28. Holopainen JK, Gershenzon J (2010) Multiple stress factors and the emission of plant VOCs. Trends Plant Sci 15(3):176–184PubMedCrossRefGoogle Scholar
  29. Holopainen JK, Heijari J, Oksanen E, Alessio GA (2010) Leaf volatile emissions of Betula pendula during autumn coloration and leaf fall. J Chem Ecol 36(10):1068–1075PubMedCrossRefGoogle Scholar
  30. Holzinger R, Sandoval-Soto L, Rottenberger S, Crutzen PJ, Kesselmeier J (2000) Emissions of volatile organic compounds from Quercus ilex L. measured by proton transfer reaction mass spectrometry under different environmental conditions. J Geophys Res-Atmos 105(D16):20573–20579CrossRefGoogle Scholar
  31. Huang HS, Chen CJ, Lu HS, Chang WC (1998) Identification of a lipoxygenase inhibitor in A431 cells as a phospholipid hydroperoxide glutathione peroxidase. FEBS Lett 424(1–2):22–26PubMedCrossRefGoogle Scholar
  32. Jansen RMC, Miebach M, Kleist E, van Henten EJ, Wildt J (2009) Release of lipoxygenase products and monoterpenes by tomato plants as an indicator of Botrytis cinerea-induced stress. Plant Biol 11(6):859–868PubMedCrossRefGoogle Scholar
  33. Jardine K, Sommer E, Saleska S, Huxman T, Harley P, Abrell L (2010a) Gas phase measurements of pyruvic acid and its volatile metabolites. Environ Sci Technol 44:2454–2460PubMedCrossRefGoogle Scholar
  34. Jardine KJ, Henderson WM, Huxman TE, Abrell L (2010b) Dynamic solution injection: a new method for preparing pptv-ppbv standard atmospheres of volatile organic compounds. Atmos Meas Tech 3(6):1569–1576CrossRefGoogle Scholar
  35. Jardine KJ, Sommer ED, Saleska SR, Huxman TE, Harley PC, Abrell L (2010c) Gas phase measurements of pyruvic acid and its volatile metabolites. Environ Sci Technol 44(7):2454–2460PubMedCrossRefGoogle Scholar
  36. Joo E, Dewulf J, Demarcke M et al (2010) Quantification of interferences in PTR-MS measurements of monoterpene emissions from Fagus sylvatica L. using simultaneous TD-GC–MS measurements. Int J Mass Spectrom 291(1–2):90–95Google Scholar
  37. Karl T, Curtis AJ, Rosenstiel TN, Monson RK, Fall R (2002) Transient releases of acetaldehyde from tree leaves—products of a pyruvate overflow mechanism? Plant, Cell Environ 25(9):1121–1131CrossRefGoogle Scholar
  38. Kulkarni AP, Cook DC (1988) Hydroperoxidase activity of lipoxygenase—hydrogen peroxide-dependent oxidation of xenobiotics. Biochem Biophys Res Commun 155(2):1075–1081PubMedCrossRefGoogle Scholar
  39. Lin M, Behal R, Oliver DJ (2003) Disruption of plE2, the gene for the E2 subunit of the plastid pyruvate dehydrogenase complex, in Arabidopsis causes an early embryo lethal phenotype. Plant Mol Biol 52(4):865–872PubMedCrossRefGoogle Scholar
  40. Loreto F, Schnitzler JP (2010) Abiotic stresses and induced BVOCs. Trends Plant Sci 15(3):154–166PubMedCrossRefGoogle Scholar
  41. Loreto F, Barta C, Brilli F, Nogues I (2006) On the induction of volatile organic compound emissions by plants as consequence of wounding or fluctuations of light and temperature. Plant, Cell Environ 29(9):1820–1828CrossRefGoogle Scholar
  42. Maccarrone M, Van Zadelhoff G, Veldink GA, Vliegenthart JFG, Finazzi-Agro A (2000) Early activation of lipoxygenase in lentil (Lens culinaris) root protoplasts by oxidative stress induces programmed cell death. Eur J Biochem 267(16):5078–5084PubMedCrossRefGoogle Scholar
  43. Mellema S, Eichenberger W, Rawyler A, Suter M, Tadege M, Kuhlemeier C (2002) The ethanolic fermentation pathway supports respiration and lipid biosynthesis in tobacco pollen. Plant J 30(3):329–336PubMedCrossRefGoogle Scholar
  44. Mene-Saffrane L, Dubugnon L, Chetelat A, Stolz S, Gouhier-Darimont C, Farmer EE (2009) Nonenzymatic oxidation of trienoic fatty acids contributes to reactive oxygen species management in Arabidopsis. J Biol Chem 284(3):1702–1708PubMedCrossRefGoogle Scholar
  45. Nam KH, Minami C, Kong FJ, Matsuura H, Takahashi K, Yoshihara T (2005) Relation between environmental factors and the LOX activities upon potato tuber formation and flower-bud formation in morning glory. Plant Growth Regul 46(3):253–260CrossRefGoogle Scholar
  46. Nelson MJ, Chase DB, Seitz SP (1995) Photolysis of purple lipoxygenase—implications for the structure of the chromophore. Biochemistry 34(18):6159–6163PubMedCrossRefGoogle Scholar
  47. Ohlrogge JB (1994) Design of new plant-products—engineering of fatty-acid metabolism. Plant Physiol 104(3):821–826PubMedGoogle Scholar
  48. Oliver DJ, Nikolau BJ, Wurtele ES (2009) Acetyl-CoA-life at the metabolic nexus. Plant Sci 176(5):597–601CrossRefGoogle Scholar
  49. Smith WL, Lands WEM (1972) Oxygenation of unsaturated fatty-acids by soybean lipoxygenase. J Biol Chem 247(4):1038–1047PubMedGoogle Scholar
  50. Tadege M, Kuhlemeier C (1997) Aerobic fermentation during tobacco pollen development. Plant Mol Biol 35(3):343–354PubMedCrossRefGoogle Scholar
  51. Wan CG, Sosebee RE (1990) Characteristics of photosynthesis and conductance in early and late leaves of honey mesquite. Bot Gaz 151(1):14–20CrossRefGoogle Scholar
  52. Wei Y, Lin M, Oliver DJ, Schnable PS (2009) The roles of aldehyde dehydrogenases (ALDHs) in the PDH bypass of Arabidopsis. BMC Biochem 10:7PubMedCrossRefGoogle Scholar
  53. Zhang L, Qiu ZM, Hu Y et al (2011) ABA treatment of germinating maize seeds induces VP1 gene expression and selective promoter-associated histone acetylation. Physiol Plant 143(3):287–296PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • K. Jardine
    • 1
  • G. A. Barron-Gafford
    • 1
  • J. P. Norman
    • 1
  • L. Abrell
    • 2
    • 3
  • R. K. Monson
    • 4
  • K. T. Meyers
    • 1
  • M. Pavao-Zuckerman
    • 1
  • K. Dontsova
    • 1
  • E. Kleist
    • 5
  • C. Werner
    • 6
  • T. E. Huxman
    • 1
    • 7
  1. 1.The University of Arizona-Biosphere 2TucsonUSA
  2. 2.Department of Chemistry & BiochemistryUniversity of ArizonaTucsonUSA
  3. 3.Department of Soil, Water and Environmental ScienceUniversity of ArizonaTucsonUSA
  4. 4.School of Natural Resources and the EnvironmentUniversity of ArizonaTucsonUSA
  5. 5.Institut für Chemie und Dynamik der Geosphäre (ICG)JülichGermany
  6. 6.Experimental and Systems EcologyUniversity of BielefeldBielefeldGermany
  7. 7.Department of Ecology and Evolutionary BiologyUniversity of ArizonaTucsonUSA

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