Increasing atmospheric CO2 reduces metabolic and physiological differences between isoprene- and non-isoprene-emitting poplars

New Phytologist

Volumn 200, Issue 2, 2013, Pages 534-546

  Way, Danielle A ^a,b   Ghirardo, Andrea ^c   Kanawati, Basem ^c   Esperschütz, Jürgen ^c,d   Monson, Russell K ^e   Jackson, Robert B ^a   Schmitt Kopplin, Philippe ^c   Schnitzler, Jörg Peter ^c  

^a DUKE UNIVERSITY   (United States)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^e UNIVERSITY OF ARIZONA   (United States)

Author keywords

CO 2; Fourier transform ion cyclotron resonance mass spectrometer (FT ICR MS); Isoprene; Nontargeted metabolomics; Poplar

Indexed keywords

ANTIOXIDANT; ATMOSPHERIC CHEMISTRY; BIOGENIC EMISSION; CARBON DIOXIDE; DICOTYLEDON; FOURIER TRANSFORM; ISOPRENE; MASS SPECTROMETRY; METABOLISM; PHYSIOLOGICAL RESPONSE; PIGMENT; TOLERANCE; VOLATILE ORGANIC COMPOUND;

1,3 BUTADIENE DERIVATIVE; CARBON DIOXIDE; FATTY ACID; HEMITERPENE; ISOPRENE; PENTANE; PHOSPHOLIPID;

ARTICLE; CO 2; CONFOCAL MICROSCOPY; DRUG EFFECT; EVAPOTRANSPIRATION; FOURIER TRANSFORM ION CYCLOTRON RESONANCE MASS SPECTROMETER (FT-ICR-MS); GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METABOLOME; NONTARGETED METABOLOMICS; PHOTOSYNTHESIS; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT LEAF; POPULUS; RNA INTERFERENCE; SPECIES DIFFERENCE; UPREGULATION; DRUG EFFECTS;

CO 2; FOURIER TRANSFORM ION CYCLOTRON RESONANCE MASS SPECTROMETER (FT-ICR-MS); ISOPRENE; NONTARGETED METABOLOMICS; POPLAR;

BUTADIENES; CARBON DIOXIDE; FATTY ACIDS; GENE EXPRESSION REGULATION, PLANT; HEMITERPENES; METABOLOME; MICROSCOPY, CONFOCAL; PENTANES; PHOSPHOLIPIDS; PHOTOSYNTHESIS; PLANT LEAVES; PLANT TRANSPIRATION; POPULUS; RNA INTERFERENCE; SPECIES SPECIFICITY; STRESS, PHYSIOLOGICAL; UP-REGULATION;

EID: 84884381315     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12391     Document Type: Article

References (72)

1. Aharoni A, Giri AP, Deuerlein S, Griepink F, de Kogel WJ, Verstappen FWA, Verhoeven HA, Jongsma MA, Schwab W, Bouwmeester HJ. 2003. Terpenoid metabolism in wild-type and transgenic Arabidopsis plants. Plant Cell 15: 2866-2884.
2. Archibald AT, Levine JG, Abraham NL, Cooke MC, Edwards PM, Heard DE, Jenkin ME, Kurunaharan A, Pike RC, Monks PS et al. 2011. Impacts of HOx regeneration and recycling in the oxidation of isoprene: consequences for the composition of past, present and future atmospheres. Geophysical Research Letters 38: L05804.
3. Barta C, Loreto F. 2006. The relationship between the methyl-erythritol phosphate (MEP) pathway leading to emission of volatile isoprenoids and abscisic acid content in leaves. Plant Physiology 141: 1676-1683.
4. 2 history. Nature Geoscience 4: 418-420.
5. Behnke K, Ehlting B, Teuber M, Bauerfeind M, Louis S, Hänsch R, Polle A, Bohlmann J, Schnitzler JP. 2007. Transgenic, non-isoprene emitting poplars don't like it hot. Plant Journal 51: 485-499.
6. Behnke K, Grote R, Brüggemann N, Zimmer I, Zhou G, Eolbeid M, Janz D, Polle A, Schnitzler JP. 2012. Isoprene emission-free poplars - a chance to reduce the impact from poplar plantations on the atmosphere. New Phytologist 194: 70-82.
7. Behnke K, Kaiser A, Bauernfeind M, Zimmer I, Meier R, Janz D, Polle A, Schmitt-Kopplin P, Hänsch R, Hampp R et al. 2010b. RNAi-mediated suppression of isoprene emission in poplar transiently impacts phenolic metabolism under high temperature and high light intensities: a transcriptomic and metabolomic analysis. Plant Molecular Biology 74: 61-75.
8. Behnke K, Loivamäki M, Zimmer I, Rennenberg H, Schnitzler JP, Louis S. 2010a. Isoprene emission protects photosynthesis in sunfleck exposed Grey poplar. Photosynthesis Research 104: 5-17.
9. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, Series B (Methodological) 57: 289-300.
10. Benjamini Y, Krieger AM, Yekutieli D. 2006. Adaptive linear step-up procedures that control the false discovery rate. Biometrika 93: 491-507.
11. Burgos A, Szymanski J, Seiwert B, Degenkolbe T, Hannah MA, Giavalisco P, Willmitzer L. 2011. Analysis of short-term changes in the Arabidopsis thaliana glycerolipidome in response to temperature and light. Plant Journal 66: 656-668.
12. Cho MH, Chen Q, Okpodu CM, Boss WF. 1992. Separation and quantification of [3H] inositol phospholipids using thin-layer-chromatography and a computerized 3H imaging scanner. LC-GC 10: 464-468.
13. Cinege G, Louis S, Hänsch R, Schnitzler JP. 2009. Regulation of isoprene synthase promoter by environmental and internal factors. Plant Molecular Biology 69: 593-604.
14. Crowell DN. 2000. Functional implications of protein isoprenylation in plants. Progress in Lipid Research 39: 393-408.
15. Demmig-Adams B, Adams WW III. 2006. Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytologist 172: 11-21.
16. Durand T, Bultetl-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: 875-888.
17. Eastmond PJ, Quettier A-L, Kroon JTM, Christian Craddock C, Adams N, Slabas AR. 2010. PHOSPHATIDIC ACID PHOSPHOHYDROLASE1 and 2 regulate phospholipid synthesis at the endoplasmic reticulum in Arabidopsis. The Plant Cell 22: 2796-2811.
18. 4 photosynthesis. Trends in Ecology and Evolution 6: 95-99.
19. Estévez JM, Cantero A, Reindl A, Reichler S, Leon P. 2001. 1-Deoxy-d-xylulose-5-phosphate synthase, a limiting enzyme for plastidic isoprenoid biosynthesis in plants. The Journal of Biological Chemistry 25: 22901-22909.
20. Fuentes JD, Lerdau M, Atkinson R, Baldocchi D, Bottenheim JW, Ciccioli P, Lamb B, Geron C, Gu L, Guenther A et al. 2000. Biogenic hydrocarbons in the atmosphere boundary layer: a review. Bulletin of the American Meteorological Society 81: 1537-1575.
21. Gerber E, Hemmerlin A, Hartmann M, Heintz D, Hartmann MA, Mutterer J, Rodriguez-Concepcion M, Boronat A, Van Dorsselaer A, Rohmer M et al. 2009. The plastidial 2-C-methyl-d-erythritol 4-phosphate pathway provides the isoprenyl moiety for protein geranylgeranylation in tobacco BY-2 cells. Plant Cell 21: 285-300.
22. Ghirardo A, Zimmer I, Brüggemann N, Schnitzler JP. 2010. Analysis of 1-deoxy-d-xylulose 5-phosphate synthase activity in Grey poplar leaves using isotope ratio mass spectrometry. Phytochemistry 71: 918-922.
23. Gombos Z, Wada H, Hideg E, Murata N. 1994. The unsaturation of membrane-lipids stabilizes photosynthesis against heat stress. Plant Physiology 104: 563-567.
24. Guevara-Garcia A, San Roman C, Arroyo A, Cortes ME, Gutierrez-Nava M, Leon P. 2005. Characterization of the Arabidopsis clb6 mutant illustrates the importance of posttranslational regulation of the methyl-d-erythritol 4-phosphate pathway. Plant Cell 17: 628-643.
25. Harley PC, Monson RK, Lerdau MT. 1999. Ecological and evolutionary aspects of isoprene emission from plants. Oecologia 118: 109-123.
26. Hill AJ, Fall R, Monson RK. 1991. Methods for the analysis of isoprene emission from leaves. In: Liskin H, Jackson J, eds. Plant toxin analysis. Modern methods of plant analysis, new series, vol 13. Berlin, Germany: Springer, 297-313.
27. Holt NE, Fleming GR, Niyogi KK. 2004. Toward an understanding of the mechanism of nonphotochemical quenching in green plants. Biochemistry 43: 8281-8289.
28. Hong Y, Zhang W, Wang X. 2010. Phospholipase D and phosphatidic acid signalling in plant response to drought and salinity. Plant, Cell & Environment 33: 627-635.
29. Janowski BA, Willy PJ, Devi TR, Falck JR, Mangelsdorf DJ. 1996. An oxysterol signalling pathway mediated by the nuclear receptor LXR alpha. Nature 383: 728-731.
30. Jardine KJ, Monson RK, Abrell L, Saleska SR, Arneth A, Jardine A, Ishida FY, Serrano AMY, Artaxo P, Karl T et al. 2012. Within-plant isoprene oxidation confirmed by direct emissions of oxidation products methyl vinyl ketone and methacrolein. Global Change Biology 18: 973-984.
31. Kiendler-Scharr A, Andres S, Bachner M, Behnke K, Broch S, Hofzumahaus A, Holland F, Kleist E, Mentel TF, Rubach F et al. 2012. Isoprene in poplar emissions: effects on new particle formation and OH concentrations. Atmospheric Chemistry and Physics 12: 1021-1030.
32. Laothawornkitkul J, Paul ND, Vickers CE, Possell M, Taylor JE, Mullineaux PM, Hewitt CN. 2008. Isoprene emissions influence herbivore-feeding decisions. Plant, Cell & Environment 31: 1410-1415.
33. Laule O, Furholz A, Chang HS, Zhu T, Wang X, Heifetz PB, Gruissem W, Lange M. 2003. Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 100: 6866-6871.
34. Lerdau M. 2007. A positive feedback with negative consequences. Science 316: 212-213.
35. 2 during the last ice age from an Antarctic ice core. Nature 357: 488-490.
36. Liljenberg C, Kates M. 1985. Changes in lipid composition of oat root membranes as a function of water-deficit stress. Canadian Journal of Biochemistry and Cell Biology 63: 77-84.
37. Lois LM, Campos N, Rosa Putra S, Danielsen K, Rohmer M, Boronat A. 1998. Cloning and characterization of a gene from Escherichia coli encoding a transketolase-like enzyme that catalyzes the synthesis of d-1-deoxyxylulose 5-phosphate, a common precursor for isoprenoid, thiamin, and pyridoxol biosynthesis. Proceedings of the National Academy of Sciences, USA 95: 2105-2110.
38. Lois LM, Rodríguez-Concepción M, Gallego F, Campos N, Boronat A. 2000. Carotenoid biosynthesis during tomato fruit development: regulatory role of 1-deoxy-D-xylulose 5-phosphate synthase. Plant Journal 22: 503-513.
39. Loreto F, Schnitzler JP. 2010. Abiotic stresses and induced BVOCs. Trends in Plant Science 15: 154-166.
40. Mahmoud SS, Croteau R. 2001. Metabolic engineering of essential oil yield and composition in mint by altering expression of deoxyxylulose phosphate reductoisomerase and menthofuran synthase. Proceedings of the National Academy of Sciences, USA 98: 8915-8920.
41. Meehl GA, Stocker TF, Collins WD, Friedlingstein P, Gaye AT, Gregory JM, Kitoh A, Knutti R, Murphy JM, Noda A et al. 2007. Global climate projections. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL, eds. Climate change 2007: the physical science basis. Contribution of Working Group I to the fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge, UK: Cambridge University Press, 747-845.
42. Méne-Saffrané L, Dubungon L, Chételat A, Stolz S, Gauhier-Darimont C, Farmer EE. 2008. Nonenzymatic oxidation of trienoic fatty acids contributes to reactive oxygen species management in Arabidopsis. Journal of Biological Chemistry 284: 1702-1708.
43. Monson RK, Jones RT, Rosenstiel TN, Schnitzler JP. 2013. Why only some plants emit isoprene. Plant, Cell & Environment 36: 503-516.
44. Müller JF, Stavrakou T, Wallens S, De Smedt I, Van Roozendael M, Potosnak MJ, Rinne J, Munger A, Guenther AB. 2008. Global isoprene emissions estimated using MEGAN, ECMWF analyses and a detailed canopy environment model. Atmospheric Chemistry and Physics 8: 1329-1341.
45. Munné-Bosch S. 2005. The role of α-tocopherol in plant stress tolerance. Journal of Plant Physiology 162: 743-748.
46. Munoz-Bertomeu J, Arrillaga I, Ros R, Segura J. 2006. Up-regulation of 1-deoxy-d-xylulose-5-phosphate synthase enhances production of essential oils in transgenic spike lavender. Plant Physiology 142: 890-900.
47. Navari-Izzo F, Ricci F, Vazzana C, Quartacci MF. 2006. Unusual composition of thylakoid membranes of the resurrection plant Boea hygroscopica: changes in lipids upon dehydration and rehydration. Physiologia Plantarum 94: 135-142.
48. Niinemets U, Tenhunen JD, Harley PC, Steinbrecher R. 1999. A model of isoprene emission based on energetic requirements for isoprene synthesis and leaf photosynthetic properties for Liquidambar and Quercus. Plant, Cell & Environment 22: 1319-1335.
49. 2 and water relations mediated by plant hydraulics. Philosophical Transactions of the Royal Society B 367: 583-600.
50. Pacifico F, Folberth GA, Jones CD, Harrison SP, Collins WJ. 2012. Sensitivity of biogenic isoprene emissions to past, present and future environmental conditions and implications for atmospheric chemistry. Journal of Geophysical Research - Atmospheres 117: D22302.
51. Poisson N, Kanakidou M, Crutzen PJ. 2000. Impact of non-methane hydrocarbons on tropospheric chemistry and the oxidizing power of the global troposphere: 3-dimensional modelling results. Journal of Atmospheric Chemistry 36: 157-230.
52. 2 concentrations. Global Change Biology 17: 1595-1610.
53. 2 uncouples growth from isoprene emission in an agriforest ecosystem. Nature 421: 256-259.
54. 4 plants. Photosynthesis Research 77: 209-225.
55. 4 photosynthesis. Annual Review of Plant Biology 63: 19-47.
56. Sato N, Sonoike K, Kawaguchi A, Tsuzuki M. 1996. Contribution of lowered unsaturation levels of chloroplast lipids to high temperature tolerance of photosynthesis in Chlamydomonas reinhardtii. Journal of Photochemistry and Photobiology B: Biology 36: 333-337.
57. Schnitzler JP, Zimmer I, Bachl A, Arend M, Fromm J, Fischbach RJ. 2005. Biochemical properties of isoprene synthase in poplar (Populus × canescens). Planta 222: 777-786.
58. Sharkey TD, Singsaas EL. 1995. Why plants emit isoprene. Nature 374: 769.
59. Sharkey TD, Yeh S. 2001. Isoprene emission from plants. Annual Review of Plant Physiology and Plant Molecular Biology 52: 407-436.
60. Singsaas EL, Lerdau M, Winter K, Sharkey TD. 1997. Isoprene increases thermotolerance in isoprene-emitting species. Plant Physiology 115: 1413-1420.
61. Suhre K, Schmitt-Kopplin P. 2008. MassTRIX: mass translator into pathways. Nucleic Acids Research 36: W481-W484.
62. Tans P, Keeling R. 2012. National oceanic and atmospheric administration, earth system research laboratory. URL www.esrl.noaa.gov/gmd/ccgg/trends/ [accessed 7 June 2012].
63. Tunc-Özdemir M, Miller G, Song L, Kim J, Sodek A, Koussevitzky S, Misra AN, Mittler R, Shintani D. 2009. Thiamin confers enhanced tolerance to oxidative stress in Arabidopsis. Plant Physiology 151: 421-432.
64. Vallabhaneni R, Wurtzel ET. 2009. Timing and biosynthetic potential for carotenoid accumulation in genetically diverse germplasm of maize. Plant Physiology 150: 562-572.
65. Velikova V, Sharkey TD, Loreto F. 2012. Stabilization of thylakoid membranes in isoprene-emitting plants reduces formation of reactive oxygen species. Plant Signaling & Behavior 7: 139-141.
66. Velikova V, Varkonyl Z, Szabo M, Maslenkova L, Nogues I, Kovacs L, Peeva V, Busheva M, Garab G, Sharkey TD et al. 2011. Increased thermostability of thylakoid membranes in isoprene-emitting leaves probed with three biophysical techniques. Plant Physiology 157: 905-916.
67. Vickers CE, Possell M, Cojocariu CI, Laothawornkitkul J, Ryan A, Mullineaux PM, Hewitt CN. 2009. Isoprene synthesis protects tobacco plants from oxidative stress. Plant, Cell & Environment 32: 520-531.
68. 2 concentrations. Oecologia 166: 273-282.
69. Wildermuth MC, Fall R. 1996. Light-dependent isoprene emission (characterization of a thylakoid-bound isoprene synthase in Salix discolor chloroplasts). Plant Physiology 112: 171-182.
70. 2 concentration. Global Change Biology 15: 1189-1200.
71. Wolfertz M, Sharkey TD, Boland W, Kühnemann F, Yeh S, Weise SE. 2004. Biochemical regulation of isoprene emission. Plant, Cell & Environment 26: 1357-1364.
72. Zelles L, Bai QY, Rackwitz R, Chadwick D, Beese F. 1995. Determination of phospholipid- and lipopolysaccharide-derived fatty acids as an estimate of microbial biomass and community structure in soils. Biology and Fertility of Soils 19: 115-123.