Gene network reconstruction identifies the authentic trans-prenyl diphosphate synthase that makes the solanesyl moiety of ubiquinone-9 in Arabidopsis

Anne Lise Ducluzeau, Yashitola Wamboldt, Christian G. Elowsky, Sally A. MacKenzie, Robert C. Schuurink, Gilles J.C. Basset

Research output: Contribution to journalArticle

33 Citations (Scopus)

Abstract

Summary Ubiquinone (coenzyme Q) is the generic name of a class of lipid-soluble electron carriers formed of a redox active benzoquinone ring attached to a prenyl side chain. The length of the latter varies among species, and depends upon the product specificity of a trans-long-chain prenyl diphosphate synthase that elongates an allylic diphosphate precursor. In Arabidopsis, this enzyme is assumed to correspond to an endoplasmic reticulum-located solanesyl diphosphate synthase, although direct genetic evidence was lacking. In this study, the reconstruction of the functional network of Arabidopsis genes linked to ubiquinone biosynthesis singled out an unsuspected solanesyl diphosphate synthase candidate - product of gene At2g34630 - that, extraordinarily, had been shown previously to be targeted to plastids and to contribute to the biosynthesis of gibberellins. Green fluorescent protein (GFP) fusion experiments in tobacco and Arabidopsis, and complementation of a yeast coq1 knockout lacking mitochondrial hexaprenyl diphosphate synthase demonstrated that At2g34630 is also targeted to mitochondria. At2g34630 is the main - if not sole - contributor to solanesyl diphosphate synthase activity required for the biosynthesis of ubiquinone, as demonstrated by the dramatic (75-80%) reduction of the ubiquinone pool size in corresponding RNAi lines. Overexpression of At2g34630 gave up to a 40% increase in ubiquinone content compared to wild-type plants. None of the silenced or overexpressing lines, in contrast, displayed altered levels of plastoquinone. Phylogenetic analyses revealed that At2g34630 is the only Arabidopsis trans-long-chain prenyl diphosphate synthase that clusters with the Coq1 orthologs involved in the biosynthesis of ubiquinone in other eukaryotes.

Original languageEnglish (US)
Pages (from-to)366-375
Number of pages10
JournalPlant Journal
Volume69
Issue number2
DOIs
StatePublished - Jan 1 2012

Fingerprint

Ubiquinone
ubiquinones
Gene Regulatory Networks
Arabidopsis
Diphosphates
biosynthesis
Plastoquinone
Gibberellins
benzoquinones
Plastids
RNA Interference
Green Fluorescent Proteins
ubiquinone 9
trans-octaprenyltranstransferase
prenyl
gene regulatory networks
Eukaryota
green fluorescent protein
gibberellins
Endoplasmic Reticulum

Keywords

  • Arabidopsis
  • isoprenoid
  • mitochondria
  • prenyl diphosphate synthase
  • ubiquinone

ASJC Scopus subject areas

  • Genetics
  • Plant Science
  • Cell Biology

Cite this

Gene network reconstruction identifies the authentic trans-prenyl diphosphate synthase that makes the solanesyl moiety of ubiquinone-9 in Arabidopsis. / Ducluzeau, Anne Lise; Wamboldt, Yashitola; Elowsky, Christian G.; MacKenzie, Sally A.; Schuurink, Robert C.; Basset, Gilles J.C.

In: Plant Journal, Vol. 69, No. 2, 01.01.2012, p. 366-375.

Research output: Contribution to journalArticle

Ducluzeau, Anne Lise ; Wamboldt, Yashitola ; Elowsky, Christian G. ; MacKenzie, Sally A. ; Schuurink, Robert C. ; Basset, Gilles J.C. / Gene network reconstruction identifies the authentic trans-prenyl diphosphate synthase that makes the solanesyl moiety of ubiquinone-9 in Arabidopsis. In: Plant Journal. 2012 ; Vol. 69, No. 2. pp. 366-375.
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abstract = "Summary Ubiquinone (coenzyme Q) is the generic name of a class of lipid-soluble electron carriers formed of a redox active benzoquinone ring attached to a prenyl side chain. The length of the latter varies among species, and depends upon the product specificity of a trans-long-chain prenyl diphosphate synthase that elongates an allylic diphosphate precursor. In Arabidopsis, this enzyme is assumed to correspond to an endoplasmic reticulum-located solanesyl diphosphate synthase, although direct genetic evidence was lacking. In this study, the reconstruction of the functional network of Arabidopsis genes linked to ubiquinone biosynthesis singled out an unsuspected solanesyl diphosphate synthase candidate - product of gene At2g34630 - that, extraordinarily, had been shown previously to be targeted to plastids and to contribute to the biosynthesis of gibberellins. Green fluorescent protein (GFP) fusion experiments in tobacco and Arabidopsis, and complementation of a yeast coq1 knockout lacking mitochondrial hexaprenyl diphosphate synthase demonstrated that At2g34630 is also targeted to mitochondria. At2g34630 is the main - if not sole - contributor to solanesyl diphosphate synthase activity required for the biosynthesis of ubiquinone, as demonstrated by the dramatic (75-80{\%}) reduction of the ubiquinone pool size in corresponding RNAi lines. Overexpression of At2g34630 gave up to a 40{\%} increase in ubiquinone content compared to wild-type plants. None of the silenced or overexpressing lines, in contrast, displayed altered levels of plastoquinone. Phylogenetic analyses revealed that At2g34630 is the only Arabidopsis trans-long-chain prenyl diphosphate synthase that clusters with the Coq1 orthologs involved in the biosynthesis of ubiquinone in other eukaryotes.",
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