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Plant Biol (Stuttg) 2004; 6(1): 12-21
DOI: 10.1055/s-2003-44722
Original Paper

Georg Thieme Verlag Stuttgart · New York

Induction of Poplar Leaf Nitrate Reductase: A Test of Extrachloroplastic Control of Isoprene Emission Rate

T. N. Rosenstiel 1 , A. L. Ebbets 2 , W. C. Khatri 2 , R. Fall 2 , 3 , R. K. Monson 1 , 3
  • 1Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, USA
  • 2Department of Chemistry and Biochemistry, University of Colorado, Boulder, USA
  • 3Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, USA
Further Information

Publication History

Publication Date:
17 February 2004 (online)

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Abstract

Several recent studies have suggested that control of isoprene emission rate is in part exerted by supply of extrachloroplastic phosphoenolpyruvate to the chloroplast. To test this hypothesis, we altered PEP supply by differential induction of cytosolic nitrate reductase (NR) and PEP carboxylase (PEPC) in plants of Populus deltoides grown with NO3 - or NH4 + as the sole nitrogen source. Growth with 8 mM NH4 + produced a high leaf nitrogen concentration, compared with 8 mM NO3 -, as well as slightly elevated rates of photosynthesis and significantly enhanced rates of isoprene emission and content of dimethylallyl diphosphate (DMAPP, a precursor to isoprene biosynthesis), chlorophyll (a+b) and carotenoids. Growth with 8 mM NO3 - resulted in parallel reductions in both leaf isoprene emission rate and DMAPP. The differential effects of growth with NH4 + or NO3 - were not observed when plants were grown with 4 mM nitrogen. The effects of reduced DMAPP availability were specific to isoprene emission and were not propagated to higher isoprenoids, as the correlations between nitrogen content and either leaf chlorophyll (a+b) or total carotenoids were unaffected by nitrogen source. Biochemical analysis revealed significantly higher levels of NR and PEPC activity in leaves of 8 mM NO3 --grown plants, consistent with their fundamental roles in nitrate assimilation. Taken together, these results support the hypothesis that foliar assimilation of NO3 - reduces isoprene emission rate by competing for carbon skeletons (mediated by PEPC) within the cytosol and possibly reductant within the chloroplast. Cytosolic competition for PEP is a major regulator of chloroplast DMAPP supply, and we offer a new “safety valve” hypothesis to explain why plants emit isoprene.

Key words

VOC - volatile organic compound - photosynthesis - nitrate reductase - ammonium - metabolism - isoprene.

References

  • 1 Adams W. W. III., Demmig-Adams B.. Operation of the xanthophyll cycle in higher plants in response to diurnal changes in incident sunlight.  Planta. (1992);  186 390-398
    PubMedGoogle Scholar
  • 2 Affek H. P., Yakir D.. Protection by isoprene against singlet oxygen in leaves.  Plant Physiol.. (2002);  129 269-277
    CrossrefPubMedGoogle Scholar
  • 73 Affek H. P., Yakir D.. Natural abundance carbon isotope composition of isoprene reflects incomplete coupling between isoprene synthesis and photosynthetic carbon flow.  Plant Physiol.. (2003);  131 1727-1736
    CrossrefPubMedGoogle Scholar
  • 3 Black B. L., Fuchigami L. H., Coleman G. D.. Partitioning of nitrate assimilation among leaves, stems and roots of poplar.  Tree Physiol.. (2002);  22 717-724
    PubMedGoogle Scholar
  • 4 Bloom A. J.. Ammonium and nitrate as nitrogen sources for plant growth. ISI Atlas of Science.  Animal and Plant Sciences. (1988);  1 55-59
    PubMedGoogle Scholar
  • 5 Bradford M. M.. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding.  Analyt. Biochem.. (1976);  72 248-254
    CrossrefPubMedGoogle Scholar
  • 6 Brüggemann N., Schnitzler J. P.. Comparison of isoprene emission, intercellular isoprene concentration and photosynthetic performance in water-limited oak (Quercus pubescens Willd. and Quercus robur L.) saplings.  Plant Biol.. (2002);  4 456-463
    Article in Thieme ConnectPubMedGoogle Scholar
  • 7 Champigny M. L., Brauer M., Bismuth E., ThiManh C., Siegl G., Van Quy L., Stitt M.. The short term effects of NO3 - and NH4 + assimilation on sucrose synthesis in leaves.  J. Plant Physiol.. (1992);  139 361-368
    PubMedGoogle Scholar
  • 8 Chapin F. S.. The mineral nutrition of wild plants.  Annu. Rev. Ecol. Syst.. (1980);  11 233-260
    CrossrefPubMedGoogle Scholar
  • 9 Delwiche C. F., Sharkey T. D.. Rapid appearance of 13C in biogenic isoprene when 13CO2 is fed to intact leaves.  Plant Cell Environ.. (1993);  16 587-591
    PubMedGoogle Scholar
  • 10 Duff M. G., Chollet R.. In vivo regulation of wheat-leaf phosphoenolpyruvate carboxylase by reversible phosphorylation.  Plant Physiol.. (1995);  107 775-782
    PubMedGoogle Scholar
  • 11 Fehsenfeld F. C., Calvert J., Fall R., Goldan P., Guenther A. B., Hewitt C. N., Lamb B., Liu S., Trainer M., Westberg H.. et al. . Emissions of volatile organic compounds from vegetation and the implications for atmospheric chemistry.  Global Biogeochem. Cycles. (1992);  6 389-430
    PubMedGoogle Scholar
  • 12 Fuentes J. D., Lerdau M., Atkinson R., Baldocchi D., Bottenheim J. W., Ciccioli P., Lamb B., Geron C., Gu L., Guenther A., Sharkey T. D., Stockwell W.. Biogenic hydrocarbons in the atmospheric boundary layer: a review.  Bulletin of the American Meteorological Society. (2000);  81 1537-1575
    CrossrefPubMedGoogle Scholar
  • 13 Fisher A. J., Rosenstiel T. N., Shirk M. C., Fall R.. Nonradioactive assay for cellular dimethylallyl diphosphate.  Analyt. Biochem.. (2001);  292 272-279
    PubMedGoogle Scholar
  • 14 Flügge U. I.. Metabolite transport across the chloroplast envelope of C3-plants. Leegood, R. C., Sharkey, T. D., and von Caemmerer, S., eds. Photosynthesis: Physiology and Metabolism, Advances in Photosynthesis, Vol. 9. Dordrecht; Kluwer Academic Publishers (2000): 137-152
    Google Scholar
  • 15 Foyer C. H., Ferrario-Méry S., Huber S. C.. Regulation of carbon fluxes in the cytosol: coordination of sucrose synthesis, nitrate reduction and organic acid and amino acid biosynthesis. Leegood, R. C., Sharkey, T. D., and von Caemmerer, S., eds. Photosynthesis: Physiology and Metabolism, Advances in Photosynthesis, Vol. 9. Dordrecht; Kluwer Academic Publishers (2000): 177-203
    Google Scholar
  • 16 Foyer C. H., Noctor G., Lelandais M., Lescure J. C., Valadier M. H., Boutin J. P., Horton P.. Short-term effects of nitrate, nitrite and ammonium assimilation on photosynthesis, carbon partitioning and protein phosphorylation in maize.  Plant Physiol.. (1994);  192 211-220
    PubMedGoogle Scholar
  • 17 Foyer C. H., Ferrario S.. Modulation of carbon and nitrogen metabolism in transgenic plants with a view to improved biomass production.  Biochem. Soc. Trans.. (1994);  22 909-915
    PubMedGoogle Scholar
  • 18 Gilmore A. M., Yamamoto H. Y.. Resolution of lutein and zeaxanthin using a non-endcapped, lightly carbon-loaded C18 high-performance liquid chromatographic column.  J. of Chromatography. (1991);  543 137-145
    PubMedGoogle Scholar
  • 19 Glynn C., Herms D. A., Egawa M., Hansenn R., Mattson W. J.. Effects of nutrient availability on biomass allocation as well as constitutive and rapid induced herbivore resistance in poplar.  Oikos. (2003);  101 385-397
    CrossrefPubMedGoogle Scholar
  • 20 Harley P., Litvak M., Sharkey T., Monson R.. Isoprene emission from velvet bean leaves.  Plant Physiol.. (1994);  105 279-285
    PubMedGoogle Scholar
  • 21 Harley P., Guenther A., Zimmerman P.. Effects of light, temperature and canopy position on net photosynthesis and isoprene emission from sweetgum (Liquidambar styraciflua L.) leaves.  Tree Physiol.. (1996);  16 25-32
    PubMedGoogle Scholar
  • 22 Harley P. C., Monson R. K., Lerdau M. T.. Ecological and evolutionary aspects of isoprene emission by plants.  Oecologia. (1999);  118 109-123
    CrossrefPubMedGoogle Scholar
  • 23 Hills A. J., Fall R. R., Monson R. K.. Methods for the analysis of isoprene emission from leaves. Linskens, H. F. and Jackson, J. F., eds. Modern Methods of Plant Analysis, New Series, Vol. 13, Plant Toxin Analysis. Berlin; Springer Verlag (1992): 297-315
    Google Scholar
  • 24 Jaworski E. G.. Nitrate reductase assay in intact plant tissues.  Biochem. Biophys. Res. Commun.. (1971);  43 1274-1279
    CrossrefPubMedGoogle Scholar
  • 25 Kaiser W. M., Forster J.. Low CO2 prevents nitrate reduction in leaves.  Plant Physiol.. (1989);  91 970-974
    PubMedGoogle Scholar
  • 26 Karl T., Fall R., Rosenstiel T. N., Prazeller P., Larsen B., Duane M., Seufert G., Lindinger W.. On-line analysis of the 13CO2 labeling of leaf isoprene suggests multiple subcellular origins of isoprene precursors.  Planta. (2002);  215 894-905
    CrossrefPubMedGoogle Scholar
  • 27 Kreuzwieser J., Graus M., Wisthaler A., Hansel A., Rennenberg H., Schnitzler J. P.. Xylem-transported glucose as an additional carbon source for leaf isoprene formation in Quercus robur. .  New Phytol.. (2002);  156 171-178
    CrossrefPubMedGoogle Scholar
  • 28 Kronzucker H. J., Siddiqi M. Y., Glass  M A. D.. Conifer root discrimination against soil nitrate and the ecology of forest succession.  Nature. (1997);  385 59-61
    CrossrefPubMedGoogle Scholar
  • 29 Kuzma J., Fall R.. Leaf isoprene emission rate is dependent on leaf development and the level of isoprene synthase.  Plant Physiol.. (1993);  101 435-440
    PubMedGoogle Scholar
  • 30 Lehning A., Zimmer I., Steinbrecher R., Brüggemann N., Schnitzler J. P.. Isoprene synthase activity and its relation to isoprene emission in Quercus robur L-leaves.  Plant Cell Environ.. (1999);  22 495-504
    CrossrefPubMedGoogle Scholar
  • 31 Lichtenthaler H. K.. The 1-deoxy-D-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants.  Ann. Rev. Plant Physiol. Plant Mol. Biol.. (1999);  50 47-65
    PubMedGoogle Scholar
  • 32 Litvak M. E., Loreto F., Harley P. C., Sharkey T. D., Monson R. K.. The response of isoprene emission rate and photosynthetic rate to photon flux and nitrogen supply in aspen and white oak trees.  Plant Cell Environ.. (1996);  19 549-559
    PubMedGoogle Scholar
  • 33 Logan B. A., Monson R. K.. Thermotolerance of leaf discs from four isoprene-emitting species is not enhanced by exposure to exogenous isoprene.  Plant Physiol.. (1999);  120 821-825
    CrossrefPubMedGoogle Scholar
  • 34 Logan B. A., Anchodoquy T. J., Monson R. K., Pan R.. The effect of isoprene on the properties of spinach thylakoids and phosphatidylcholine liposomes.  Plant Biol.. (1999);  1 602-606
    PubMedGoogle Scholar
  • 35 Logan B. A., Monson R., Potosnak M.. Biochemistry and physiology of foliar isoprene production.  Trends in Plant Science. (2000);  5 477-481
    CrossrefPubMedGoogle Scholar
  • 36 Loreto F., Sharkey T. D.. A gas exchange study of photosynthesis and isoprene emission in Quercus rubra L.  Planta. (1990);  182 523-531
    PubMedGoogle Scholar
  • 37 Loreto F., Delfine S.. Emission of isoprene from salt-stressed Eucalyptus globulus leaves.  Plant Physiol.. (2000);  123 1605-1610
    CrossrefPubMedGoogle Scholar
  • 38 Loreto F., Mannozzi M., Maris C., Nascetti P., Ferranti F., Pasqualini S.. Ozone quenching properties of isoprene and its antioxidant role in leaves.  Plant Physiol.. (2001);  126 993-1000
    CrossrefPubMedGoogle Scholar
  • 39 Miller B., Oschinski C., Zimmer W.. First isolation of an isoprene synthase gene from poplar and successful expression of the gene in Escherichia coli. .  Planta. (2001);  213 483-487
    CrossrefPubMedGoogle Scholar
  • 40 Min X., Siddiqi M. Y., Guy R. D., Glass A. D. M., Kronzucker H. J.. Induction of nitrate uptake and nitrate reductase activity in trembling aspen and lodgepole pine.  Plant Cell Environ.. (1998);  21 1039-1046
    CrossrefPubMedGoogle Scholar
  • 41 Min X., Siddiqi M. Y., Guy R. D., Glass A. D. M., Kronzucker H. J.. A comparative kinetic analysis of nitrate and ammonium influx in two early-successional tree species of temperate and boreal forest ecosystems.  Plant Cell Environ.. (2000);  23 321-328
    CrossrefPubMedGoogle Scholar
  • 42 Molinas S. M., Altabe S. G., Opperdoes F. R., Rider M. H., Michels P. A. M., Uttaro A. D.. The multifunctional isopropyl alcohol dehydrogenase of Phytomonas sp. could be the result of a horizontal gene transfer from a bacterium to the trypanosomatid lineage.  J. of Biol. Chem.. (2003);  278 36169-36175
    PubMedGoogle Scholar
  • 43 Monson R. K., Fall R.. Isoprene emissions from aspen leaves. Influence of environment and relation to photosynthesis and photorespiration.  Plant Physiol.. (1989);  90 267-274
    PubMedGoogle Scholar
  • 44 Monson R. K., Jaeger C. H., Adams W. W. III., Driggers E. M., Silver G. M., Fall R.. Relationships among isoprene emission rate, photosynthesis, and isoprene synthase activity as influenced by temperature.  Plant Physiol.. (1992);  98 1175-1180
    PubMedGoogle Scholar
  • 45 Monson R. K., Harley P. C., Litvak M. E., Wildermuth M., Guenther A. B., Zimmermann P. R., Fall R.. Environmental and developmental controls over the seasonal pattern of isoprene emission from aspen leaves.  Oecologia. (1994);  9 260-270
    PubMedGoogle Scholar
  • 46 Monson R. K., Holland E. A.. Biospheric trace gas fluxes and their control over tropospheric chemistry.  Ann. Rev. Ecol. Syst.. (2001);  32 547-576
    CrossrefPubMedGoogle Scholar
  • 47 Monson R. K.. Volatile organic compound emissions from terrestrial ecosystems: a primary biological control over atmospheric chemistry.  Israel Journal of Chemistry. (2002);  42 29-42
    CrossrefPubMedGoogle Scholar
  • 48 Nelson D. W., Sommers L. E.. Total carbon, organic carbon, and organic matter. Sumner, M. E., ed. Methods of Soil Analysis: Chemical Methods, Part 3. Madison, Wisconsin, USA; Soil Science Society of America, Inc. (1996): 961-1010
    Google Scholar
  • 49 Niinemets U., Tenhunen J., Harley P., Steinbrecher R.. A model of isoprene emission based on energetic requirements for isoprene synthesis and lead photosynthetic properties for Liquidambar and Quercus. .  Plant Cell and Environ.. (1999);  22 1319-1335
    CrossrefPubMedGoogle Scholar
  • 50 Niyogi K. K.. Safety valves for photosynthesis.  Curr Opinion Plant Biol. (2000);  3 455-460
    CrossrefPubMedGoogle Scholar
  • 51 Peñuelas J., Llusià J.. Linking photorespiration, monoterpenes and thermotolerance in Quercus.  New Phytol.. (2002);  155 227-237
    CrossrefPubMedGoogle Scholar
  • 52 Raven J. A., Wollenweber B., Handley L. L.. A comparison of ammonium and nitrate as nitrogen sources for photolithotrophs.  New Phytol.. (1992);  121 19-32
    PubMedGoogle Scholar
  • 53 Rosenstiel T. N., Fisher A. J., Fall R., Monson R. K.. Differential accumulation of dimethylallyl diphosphate in leaves and needles of isoprene-emitting, methylbutenol-emitting, and non-emitting species.  Plant Physiol.. (2002);  129 1276-1284
    CrossrefPubMedGoogle Scholar
  • 54 Rosenstiel T. N., Potosnak M. J., Griffin K. L., Fall R., Monson R. K.. Increased CO2 uncouples growth from isoprene emission in an agriforest ecosystem.  Nature. (2003);  421 256-259
    CrossrefPubMedGoogle Scholar
  • 55 Rothstein D. E., Zaj D. R., Pregitzer K. S., Curtis P. S.. Kinetics of nitrogen uptake by Populus tremuloides in relation to atmospheric CO2 and soil nitrogen availability.  Tree Physiol.. (2000);  20 265-270
    PubMedGoogle Scholar
  • 56 Scheibe R.. Light-dark modulation regulation of chloroplast metabolism in a new light.  Bot Acta. (1990);  103 327-334
    PubMedGoogle Scholar
  • 57 Scheible W. R., Krapp A., Stitt M.. Reciprocal diurnal changes of phosphoenolpyruvate carboxylase expression and cytosolic pyruvate kinase, citrate synthase and NADP-isocitrate dehydrogenase expression regulate organic acid metabolism during nitrate assimilation in tobacco leaves.  Plant Cell and Environ.. (2000);  23 1155-1167
    PubMedGoogle Scholar
  • 58 Schnitzler J. P., Arenz R., Steinbrecher R., Lehning A.. Characterization of an isoprene synthase from leaves of Quercus petraea (Mattuschka) Liebl.  Bot Acta. (1996);  109 216-221
    PubMedGoogle Scholar
  • 59 Schwender J., Zeidler J., Groner R., Müller C., Frocke M., Braun S., Lichtenthaler F. W., Lichtenthaler H. K.. Incorporation of 1-deoxy-D-xylulose into isoprene and phytol by higher plants and algae.  FEBS Lett.. (1997);  414 129-134
    CrossrefPubMedGoogle Scholar
  • 60 Sharkey T., Singsaas E.. Why plants emit isoprene.  Nature. (1995);  374 769
    PubMedGoogle Scholar
  • 61 Sharkey T. D., Yeh S.. Isoprene emission from plants.  Ann. Rev. Plant Physiol. Plant Mol. Biol.. (2001);  52 407-436
    PubMedGoogle Scholar
  • 62 Shen B., Hohmann S., Jensen R. G., Bohnert H. J.. Roles of sugar alcohols in osmotic stress adaptation: replacement of glycerol by mannitol and sorbitol in yeast.  Plant Physiol.. (1999);  121 45-52
    CrossrefPubMedGoogle Scholar
  • 63 Shirk M. C., Wagner W. P., Fall R.. Isoprene formation in Bacillus subtilis: a barometer of central carbon assimilation in a bioreactor?.  Biotechnol. Prog.. (2002);  18 1109-1115
    CrossrefPubMedGoogle Scholar
  • 64 Siebrecht S., Tischner R.. Changes in the xylem exudates composition of poplar (Populus tremula × P. alba) dependent on the nitrogen and potassium supply.  J. Exp. Bot.. (1999);  50 1797-1806
    CrossrefPubMedGoogle Scholar
  • 65 Silver G. M., Fall R.. Enzymatic synthesis of isoprene from dimethylallyl diphosphate in aspen leaf extracts.  Plant Physiol.. (1991);  97 1588-1591
    PubMedGoogle Scholar
  • 66 Silver G. M., Fall R.. Characterization of aspen isoprene synthase, an enzyme responsible for leaf isoprene emission to the atmosphere.  J. Biol. Chem.. (1995);  270 13010-13016
    CrossrefPubMedGoogle Scholar
  • 67 Smith J. A. C., Raven J. A.. Intracellular pH and its regulation.  Ann. Rev. Plant Physiol.. (1979);  30 289-311
    PubMedGoogle Scholar
  • 68 Stitt M., Muller C., Matt P., Gibon Y., Carillo P., Morcuende R., Scheible W. R., Krapp A.. Steps towards an integrated view of nitrogen metabolism.  J. of Exp. Bot.. (2002);  53 959-970
    CrossrefPubMedGoogle Scholar
  • 69 Traux B., Lambert F., Gagnon D., Chevrier N.. Nitrate reductase and glutamine synthetase activities in relation to growth and nitrogen assimilation in red oak and red ash seedlings: effects of N-forms, N concentration and light intensity.  Trees. (1994);  9 12-18
    PubMedGoogle Scholar
  • 70 Wolfertz M., Sharkey T. D., Boland W., Kühnemann F., Yeh S., Weise S. E.. Biochemical regulation of isoprene emission.  Plant Cell and Environ.. (2003);  26 1357-1364
    PubMedGoogle Scholar
  • 71 Woolfolk W. T. M., Friend A. L.. Growth response of cottonwood roots to varied NH4:NO3 ratios in enriched patches.  Tree Physiol.. (2003);  23 427-432
    PubMedGoogle Scholar
  • 72 Zimmer W., Brüggemann N., Emeis S., Giersch C., Lehning A., Steinbrecher R., Schnitzler J. P.. Process-based modelling of isoprene emission by oak leaves.  Plant Cell Environ.. (2000);  23 585-595
    CrossrefPubMedGoogle Scholar

T. N. Rosenstiel

Department of Ecology and Evolutionary Biology
University of Colorado

Campus Box 334

Boulder, CO 80309

USA

Email: todd.rosenstiel@colorado.edu

Section Editor: H. Rennenberg