Plant Molecular Biology

, Volume 61, Issue 1–2, pp 195–213 | Cite as

Overexpression of Farnesyl Diphosphate Synthase in Arabidopsis Mitochondria Triggers Light-dependent Lesion Formation and Alters Cytokinin Homeostasis

  • David Manzano
  • Antoni Busquets
  • Marta Closa
  • Klára Hoyerová
  • Hubert Schaller
  • Miroslav Kamínek
  • Montserrat Arró
  • Albert Ferrer
Article

Abstract

To investigate the role of mitochondrial farnesyl diphosphate synthase (FPS) in plant isoprenoid biosynthesis we characterized transgenic Arabidopsis thaliana plants overexpressing FPS1L isoform. This overexpressed protein was properly targeted to mitochondria yielding a mature and active form of the enzyme of 40 kDa. Leaves from transgenic plants grown under continuous light exhibited symptoms of chlorosis and cell death correlating to H2O2 accumulation, and leaves detached from the same plants displayed accelerated senescence. Overexpression of FPS in mitochondria also led to altered leaf cytokinin profile, with a reduction in the contents of physiologically active trans-zeatin- and isopentenyladenine-type cytokinins and their corresponding riboside monophosphates as well as enhanced levels of cis-zeatin 7-glucoside and storage cytokinin O-glucosides. Overexpression of 3-hydroxy-3-methylglutaryl coenzyme A reductase did not prevent chlorosis in plants overexpressing FPS1L, but did rescue accelerated senescence of detached leaves and restored wild-type levels of cytokinins. We propose that the overexpression of FPS1L leads to an enhanced uptake and metabolism of mevalonic acid-derived isopentenyl diphosphate and/or dimethylallyl diphosphate by mitochondria, thereby altering cytokinin homeostasis and causing a mitochondrial dysfunction that renders plants more sensitive to the oxidative stress induced by continuous light.

Keywords

Arabidopsis thaliana cytokinin farnesyl diphosphate synthase isoprenoid mevalonic acid mitochondria 

Abbreviations

AOX

alternative oxidase

CaMV

cauliflower mosaic virus

Cox

cytochrome oxidase

DAB

3,3′-diaminobenzidine

DMAPP

dimethylallyl diphosphate

ER

endoplasmic reticulum

FPP

farnesyl diphosphate

FPS

farnesyl diphosphate synthase

GFP

green fluorescent protein

HMGR

3-hydroxy-3-methylglutaryl coenzyme A reductase

IP

isopentenyladenine

iP7G

N6-(Δ2-isopentenyl)adenine 7-glucoside

iPR

N6-(Δ2-isopentenyl)adenosine

iPRMP

N6-(Δ2-isopentenyl)adenosine 5′-monophosphate

IPP

isopentenyl diphosphate

IPT

isopentenyltransferase

MEP

methylerythritol phosphate

MVA

mevalonic acid

ROS

reactive oxygen species

c-Z

cis-zeatin

t-Z

trans-zeatin

c-Z7G

cis-zeatin 7-glucoside

t-Z7G

trans-zeatin 7-glucoside

t-Z9G

trans-zeatin 9-glucoside

t-ZOG

trans-zeatin O-glucoside

c-ZR

cis-zeatin riboside

t-ZR

trans-zeatin riboside

t-ZRMP

trans-zeatin riboside 5′-monophosphate

t-ZROG

trans-zeatin 9-riboside O-glucoside

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References

  1. Allen, L.J., MacGregor Koop, K.B. R.S., Bruce, D.H., Karner, J., Bown, A.W. 1999The relationship between photosynthesis and a mastoparan-induced hypersensitive response in isolated mesophyll cellsPlant Physiol.11912331241PubMedCrossRefGoogle Scholar
  2. Araus, J.L., Bort, J., Brown, R.H., Bassett, C.L., Cortadellas, N. 1993Immunocytochemical localization of phosphoenolpyruvate carboxylase and photosynthetic gas-exchange characteristics in ears of Triticum durum DesfPlanta191507514CrossRefGoogle Scholar
  3. Astot, C., Dolezal, K., Nordström, A., Wang, Q., Kunkel, T., Moritz, T., Chua, N.-H., Sandberg, G. 2000An alternative cytokinin biosynthesis pathwayProc. Natl. Acad. Sci. USA971477814783PubMedCrossRefGoogle Scholar
  4. Bach, T.J., Boronat, A., Campos, N., Ferrer, A., Vollack, K.U. 1999Mevalonate biosynthesis in plantsCrit. Rev. Biochem. Mol. Biol.3107122CrossRefGoogle Scholar
  5. Bassil, N.V., Mok, D.W.S., Mok, M.C. 1993Partial purification of cistrans- isomerase of zeatin from immature seed of Phaseolus vulgaris LPlant Physiol.102867872PubMedGoogle Scholar
  6. Bechtold, N., Ellis, J., Pelletier, G. 1993In planta Agrobacterium-mediated gene transfer by infiltration of adult Arabidopsis thaliana plantsCR Acad. Sci. Paris/Life Sci.31611941199Google Scholar
  7. Benko, A.L., Valduva, G., Martin, N.C., Hopper, A.K. 2000Competition between a sterol biosynthetic enzyme and tRNA modification in addition to changes in the protein synthesis machinery causes altered nonsense suppressionProc. Natl. Acad. Sci. USA976166PubMedCrossRefGoogle Scholar
  8. Bradford, M.M. 1976A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye bindingAnal. Biochem.72248254PubMedCrossRefGoogle Scholar
  9. Castillo-García, M., Couillaud, F. 1999Molecular cloning and tissue expression of an insect farnesyl diphosphate synthaseEur. J. Biochem.262365370CrossRefGoogle Scholar
  10. Champenoy, S., Tourte, M. 1998Expression of the yeast mevalonate kinase gene in transgenic tobaccoMol. Breeding4291300CrossRefGoogle Scholar
  11. Courdavault, V., Thiersault, M., Courtois, M., Gantet, P., Oudin, A., Doireau, P., St-Pierre, B., Giglioli-Guivarc’h, N. 2005CaaX-prenyltransferases are essential for expression of genes involved in the early stages of monoterpenoid biosynthetic pathway in Catharanthus roseus cellsPlant Mol. Biol.57855870PubMedCrossRefGoogle Scholar
  12. Crowell, D.N., Salaz, M.S. 1992Inhibition of growth of cultured tobacco cells at low concentrations of lovastatin is reversed by cytokininPlant Physiol.10020902095PubMedCrossRefGoogle Scholar
  13. Cunillera, N., Arró, M., Delourme, D., Karst, F., Boronat, A., Ferrer, A. 1996Arabidopsis thaliana contains two differentially expressed farnesyl-diphosphate synthase genesJ.Biol.Chem.27177747780PubMedCrossRefGoogle Scholar
  14. Cunillera, N., Boronat, A., Ferrer, A. 1997The Arabidopsis thaliana FPS1 gene generates a novel mRNA that encodes a mitochondrial farnesyl-diphosphate synthase isoformJ. Biol. Chem.2721538115388PubMedCrossRefGoogle Scholar
  15. Cunillera, N., Boronat, A., Ferrer, A. 2000Spatial and temporal patterns of GUS expression directed by 5′ regions of the Arabidopsis thaliana farnesyl diphosphate synthase genes FPS1 and FPS2Plant Mol. Biol.44747758PubMedCrossRefGoogle Scholar
  16. Dale, S., Arró, M., Becerra, B., Morrice, N., Boronat, A., Hardie, D.G., Ferrer, A. 1995Bacterial expression of the catalytic domain of 3-hydroxy-3-methylglutaryl coenzyme A reductase (isoform HMGR1) from Arabidopsis thaliana, and its inactivation by phosphorylation at Ser577 by Brassica oleracea 3-hydroxy-3-methylglutaryl coenzyme A reductase kinaseEur. J. Biochem.233506513PubMedCrossRefGoogle Scholar
  17. Dean, L., Elzen, B., Tamaki, S., Dunsmuir, P., Bedbrook, J. 1985Differential expression of the eight genes of the petunia ribulose bisphosphate carboxylase small subunit multigene familyEMBO J.530553061Google Scholar
  18. Disch, A., Hemmerlin, A., Bach, T.J., Rohmer, M. 1998Mevalonate-derived isopentenyl diphosphate is the biosynthetic precursor of ubiquinone prenyl-chain in tobacco BY-2 cellsBiochem. J.331615621PubMedGoogle Scholar
  19. Dobrev, P.I., Kamínek, M. 2002Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extractionJ. Chromatogr. A9502129PubMedCrossRefGoogle Scholar
  20. Dutilleul, C., Garmier, M., Noctor, G., Mathieu, C., Chétrit, P., Foyer, C.H., Paepe, R. 2003Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulationPlant Cell.1512121226PubMedCrossRefGoogle Scholar
  21. Eisenreich, W., Rohdich, F., Bacher, A. 2001Deoxyxylulose phosphate pathway to terpenoidsTrends Plant Sci.67884PubMedCrossRefGoogle Scholar
  22. Faust, J.R., Brown, M.S., Goldstein, J.L. 1980Synthesis of delta 2-isopentenyl tRNA from mevalonate in cultured human fibroblastsJ. Biol. Chem.25565466548PubMedGoogle Scholar
  23. Fryer, M., Oxborough, K., Mullineaux, P., Baker, N.R. 2002Imaging of photo-oxidative stress responses in leavesJ. Exp. Bot.5312491254PubMedCrossRefGoogle Scholar
  24. Gan, S., Amasino, R.M. 1995Inhibition of leaf senescence by autoregulated production of cytokininScience27019861988PubMedGoogle Scholar
  25. Gechev, T.S., Hille, J. 2005Hydrogen peroxide as a signal controlling plant programmed cell deathJ. Cell Biol.1681720PubMedCrossRefGoogle Scholar
  26. Haberer, G., Kieber, J.J. 2002Cytokinins. New insights into a classic phytohormonePlant Physiol.128354362PubMedCrossRefGoogle Scholar
  27. Harborne, J.B. 1991

    Recent advances in the ecological chemistry of plant terpenoids

    Harborne, J.B.Tomas-Barberan, R.A. eds. Ecological Chemistry and Biochemistry of Plant TerpenoidsClarendonOxford399426
    Google Scholar
  28. Harker, M., Hellyer, A., Clayton, J.C., Duvoix, A., Lanot, A., Safford, R. 2002Co-ordinate regulation of sterol biosynthesis enzyme activity during accumulation of sterols in developing rape and tobacco seedPlanta216707715PubMedGoogle Scholar
  29. Hemmerlin, A., Bach, T.J. 2000Farnesol-induced cell death and stimulation of 3-hydroxy-3-methylglutaryl-coenzyme A reductase activity in tobacco cv bright yellow-2 cellsPlant Physiol.12312571268PubMedCrossRefGoogle Scholar
  30. Hemmerlin, A., Hoeffler, J.F., Meyer, O., Tritsch, D., Kagan, I., Grosdemange-Billiard, C., Rohmer, M., Bach, T.J. 2003Crosstalk between the cytosolic and the plastidial methylerythritol phosphate pathways in tobacco Bright Yellow-2 cellsJ. Biol. Chem.2782666626676PubMedCrossRefGoogle Scholar
  31. Imbault, N., Thiersault, M., Dupéron, P., Benabdelmouna, A., Doireau, P. 1996Pravastatine: a tool for investigating the availability of mevalonate metabolites for primary and secondary metabolism in Catharanthus roseus cell suspensionsPhysiol. Plant98803809CrossRefGoogle Scholar
  32. Jones, A. 2000Does the plant mitochondrion integrate cellular stress and regulate programmed cell death?Trends Plant Sci.5225230PubMedCrossRefGoogle Scholar
  33. Kasahara, H., Takei, K., Ueda, N., Hishiyama, S., Yamaya, T., Kamiya, Y., Yamaguchi, S., Sakakibara, H. 2004Distinct isoprenoid origins of cis- and trans-zeatin biosyntheses in ArabidopsisJ. Biol. Chem.2791404914054PubMedCrossRefGoogle Scholar
  34. Koch, E., Slusarenko, A. 1990Arabidopsis is susceptible to infection by a downy mildew fungusPlant Cell2437445PubMedCrossRefGoogle Scholar
  35. Köhler, R., Zipfel, W.R., Webb, W.W., Hanson, M.R. 1997The green fluorescent protein as a marker to visualise plant mitochondria in vivoPlant J.11613621PubMedCrossRefGoogle Scholar
  36. Laule, O., Fürholz, A., Chang, H.-S., Zhu, T., Wang, X., Heifetz, P.B., Gruissem, W., Lange, M. 2003Cross-talk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thalianaProc. Natl. Acad. Sci. USA10068666871PubMedCrossRefGoogle Scholar
  37. Laureys, F., Dewitte, W., Witters, E., Montagu, M., Inzé, D., Onckelen, H. 1998Zeatin is dispensable for the G2-M transition in tobacco BY-2 cellsFEBS Lett.4262932PubMedCrossRefGoogle Scholar
  38. Lütke-Brinkhaus, F., Liedvogel, B., Kleinig, H. 1984On the biosynthesis of ubiquinones in plant mitochondriaEur. J. Biochem.141537541PubMedCrossRefGoogle Scholar
  39. Manzano, D., Fernández-Busquets, X., Schaller, H., González, V., Boronat, A., Arró, M., Ferrer, A. 2004The metabolic imbalance underlying lesion formation in Arabidopsis thaliana overexpressing farnesyl diphosphate synthase (isoform 1S) leads to oxidative stress and is triggered by the developmental decline of endogenous HMGR activityPlanta219982992PubMedCrossRefGoogle Scholar
  40. Masferrer, A., Arró, M., Manzano, D., Schaller, H., Fernández-Busquets, X., Moncaleán, P., Fernández, B., Cunillera, N., Boronat, A., Ferrer, A. 2002Overexpression of Arabidopsis thaliana farnesyl diphosphate synthase (FPS1S) in transgenic Arabidopsis induces a cell death/senescence-like response and reduced cytokinin levelsPlant J.30123132PubMedCrossRefGoogle Scholar
  41. Maxwell, D.P., Wang, Y., McIntosh, L. 1999The alternative oxidase lowers mitochondrial reactive oxigen production in plant cellsProc. Natl. Acad. Sci. USA9682718276PubMedCrossRefGoogle Scholar
  42. Maxwell, D.P., Nickels, R., McIntosh, L. 2002Evidence of mitochondrial involvement in the transduction of signals required for the induction of genes associated with pathogen attack and senescencePlant J.29269279PubMedCrossRefGoogle Scholar
  43. McGarvey, D.J., Croteau, R. 1995Terpenoid metabolismPlant Cell710151026PubMedCrossRefGoogle Scholar
  44. Menand, B., Maréchal-Drouard, L., Sakamoto, W., Dietrich, A., Wintz, H. 1998A single gene of chloroplast origin codes for a mitochondrial and chloroplastic methionyl-tRNA synthetase in Arabidopsis thalianaProc. Natl. Acad. Sci. USA951110411019CrossRefGoogle Scholar
  45. Mireau, H., Lancelin, D., Small, I.D. 1996The same Arabidopsis gene encodes both cytosolic and mitochondrial alanyl-tRNA synthetasesPlant Cell810271039PubMedCrossRefGoogle Scholar
  46. Mok, D.W.S., Mok, M.C. 2001Cytokinin metabolism and actionAnnu. Rev. Plant Physiol. Plant Mol. Biol.5289118PubMedCrossRefGoogle Scholar
  47. Newman, J.D., Chappell, J. 1997Isoprenoid biosynthesis in plants: carbon partitioning within the cytoplasmic pathwayCrit. Rev. Biochem. Mol. Biol.3495106CrossRefGoogle Scholar
  48. Peeters, N.M., Chapron, A., Giritch, A., Grandjean, O., Lancelin, D., Lhomme, T., Vivrel, A., Small, I. 2000Duplication and quadruplication of Arabidopsis thaliana cysteinyl- and asparaginyl-tRNA synthetase genes of organellar originJ. Mol. Evol.50413423PubMedGoogle Scholar
  49. Quail, P.H. 1979Plant cell fractionationAnnu. Rev. Plant. Physiol.30425489CrossRefGoogle Scholar
  50. Rodríguez-Concepción, M., Boronat, A. 2002Elucidation of the methylerythritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastids. A metabolic milestone achieved through genomicsPlant Physiol.13010791089PubMedCrossRefGoogle Scholar
  51. Rodríguez-Concepción, M., Forés, O., Martínez-García, J.F., González, V., Phillips, M., Ferrer, A., Boronat, A. 2004Distinct light-mediated pathways regulate the biosynthesis and exchange of isoprenoid precursors during Arabidopsis seedling developmentPlant Cell16144156PubMedCrossRefGoogle Scholar
  52. Runquist, M., Ericsson, J., Thelin, A., Chojnacki, T., Dallner, G. 1994Isoprenoid biosynthesis in rat liver mitochondriaJ. Biol. Chem.26958045809PubMedGoogle Scholar
  53. Saisho, D., Nambar, E., Naito, S., Tsutsumi, N., Hirai, A., Nakazono, M. 1997Characterization of the gene family for alternative oxidase from Arabidopsis thalianaPlant Mol. Biol.35585596PubMedCrossRefGoogle Scholar
  54. Sakakibara, H., Kasahara, H., Ueda, N., Kojima, M., Takei, K., Hishiyama, S., Asami, T., Okada, K., Kamiya, Y., Yamaya, T., Yamaguchi, S. 2005Agrobacterium tumefaciens increases cytokinin production in plastids by modifying the biosynthetic pathway in the host plantProc. Natl. Acad. Sci. USA10299729977PubMedCrossRefGoogle Scholar
  55. Shipton, C.A., Parmryd, I., Swiezewska, E., Andersson, B., Dallner, G. 1995Isoprenylation of plant proteins in vivo. Isoprenylated proteins are abundant in the mitochondria and nuclei of spinachJ. Biol. Chem.270566572PubMedCrossRefGoogle Scholar
  56. Stone, J.M., Heard, J.E., Asai, T., Ausubel, F.M. 2000Simulation of fungal-mediated cell death by fumonisin B1 and selection of fumonisin B1-resistant (fbr) Arabidopsis mutantsPlant Cell1218111822PubMedCrossRefGoogle Scholar
  57. Taverner, E., Letham, D.S., Wang, J., Cornish, E., Willcocks, D.A. 1999Influence of ethylene on cytokinin metabolism in relation to Petunia corolla senescencePhytochemistry51341347CrossRefGoogle Scholar
  58. Thordal-Christensen, H., Zhang, Z., Wei, Y., Collinge, D.B. 1997Sucellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interactionPlant J.1111871194CrossRefGoogle Scholar
  59. Staden, J. 1996Changes in foliar cytokinins of Salix babilonica and Gingo biloba prior and during leaf senescenceSouth Afr. J. Bot.62110Google Scholar
  60. Vranová, E., Inzé, D., Breusegem, F. 2002Signal transduction during oxidative stressJ. Exp. Bot.5312271236PubMedCrossRefGoogle Scholar
  61. Wang, K.C., Ohnuma, S. 2000Isoprenyl diphosphate synthasesBiochim. Biophys. Acta15293348PubMedGoogle Scholar
  62. Zhu, X.F., Suzuki, K., Saito, T., Okada, K., Tanaka, K., Nakagawa, T., Matsuda, H., Kawamukai, M. 1997Geranylgeranyl pyrophosphate synthase encoded by the newly isolated gene GGPS6 from Arabidopsis thaliana is localized in mitochondriaPlant Mol. Biol.35331341PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • David Manzano
    • 1
    • 4
  • Antoni Busquets
    • 1
  • Marta Closa
    • 1
  • Klára Hoyerová
    • 2
  • Hubert Schaller
    • 3
  • Miroslav Kamínek
    • 2
  • Montserrat Arró
    • 1
  • Albert Ferrer
    • 1
  1. 1.Departament de Bioquímica i Biologia Molecular, Facultat de FarmàciaUniversitat de BarcelonaBarcelonaSpain
  2. 2.Institute of Experimental BotanyAcademy of Sciences of the Czech RepublicPrague 6Czech Republic
  3. 3.Département IsoprénoïdesInstitut de Biologie Moléculaire des Plantes (IBMP/CNRS), Institut de BotaniqueStrasbourgFrance
  4. 4.Department of Cell and Developmental BiologyJohn Innes CentreNorwichUK

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