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

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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.

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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:

N 6-(Δ2-isopentenyl)adenine 7-glucoside

iPR:

N 6-(Δ2-isopentenyl)adenosine

iPRMP:

N 6-(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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Authors and Affiliations

  1. Departament de Bioquímica i Biologia Molecular, Facultat de Farmàcia, Universitat de Barcelona, Avda. Diagonal 643, Barcelona, 08028, Spain

    David Manzano, Antoni Busquets, Marta Closa, Montserrat Arró & Albert Ferrer

  2. Institute of Experimental Botany, Academy of Sciences of the Czech Republic, Rozvojova 135, Prague 6, CZ-165 02, Czech Republic

    Klára Hoyerová & Miroslav Kamínek

  3. Département Isoprénoïdes, Institut de Biologie Moléculaire des Plantes (IBMP/CNRS), Institut de Botanique, 28, rue Goethe, Strasbourg, 67083, France

    Hubert Schaller

  4. Department of Cell and Developmental Biology, John Innes Centre, Colney Lane, Norwich, NR4 7UH, UK

    David Manzano

Authors
  1. David Manzano
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  2. Antoni Busquets
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  3. Marta Closa
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  4. Klára Hoyerová
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  5. Hubert Schaller
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  6. Miroslav Kamínek
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  7. Montserrat Arró
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  8. Albert Ferrer
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Corresponding author

Correspondence to Albert Ferrer.

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Manzano, D., Busquets, A., Closa, M. et al. Overexpression of Farnesyl Diphosphate Synthase in Arabidopsis Mitochondria Triggers Light-dependent Lesion Formation and Alters Cytokinin Homeostasis. Plant Mol Biol 61, 195–213 (2006). https://doi.org/10.1007/s11103-006-6263-y

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  • DOI: https://doi.org/10.1007/s11103-006-6263-y

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