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The pds2 mutation is a lesion in the Arabidopsis homogentisate solanesyltransferase gene involved in plastoquinone biosynthesis

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Abstract

Plastoquinone plays critical roles in photosynthesis, chlororespiration and carotenoid biosynthesis. The previously isolated pds2 mutant from Arabidopsis was deficient in tocopherol and plastoquinone accumulation, and the biochemical phenotype of this mutant could not be reversed by externally applied homogentisate, suggesting a later step in tocopherol and/or plastoquinone biosynthesis had been disrupted. Recently, the protein encoded by At3g11950 (AtHST) was shown to condense homogentisate with solanesyl diphosphate (SDP), the substrate for plastoquinone synthesis, but not phytyl diphosphate (PDP), the substrate for tocopherol biosynthesis. We have sequenced the AtHST allele in the pds2 mutant background and identified an in-frame 6 bp (2 aa) deletion in the gene. The pds2 mutation could be functionally complemented by constitutive expression of AtHST, demonstrating that the molecular basis for the pds2 mutation is this 6 bp-lesion in the AtHST gene. Confocal microscopy of EGFP tagged AtHST suggested that AtHST is localized to the chloroplast envelope, supporting the hypothesis that plastoquinone synthesis occurs in the plastid.

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Fig. 1
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Abbreviations

EGFP:

Enhanced green fluorescence protein

HGA:

Homogentisate

HGGT:

Homogentisate geranylgeranyltransferase

HPP:

Hydroxyphenylpyruvate

HPPDase:

Hydroxyphenylpyruvate dioxygenase

HPT:

Homogentisate phytyltransferase

HST:

Homogentisate solanesyltransferase

PDP:

Phytyl diphosphate

PQ-9:

Plastoquinone-9

SDP:

Solanesyl diphosphate

SPS:

Solanesyl diphosphate synthase

References

  • Bräuer L, Brandt W, Wessjohann LA (2004) Modeling the E. coli 4-hydroxybenzoic acid oligoprenyltransferase (UbiA transferase) and characterization of potential active sites. J Mol Model 10:317–327

    Article  PubMed  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  Google Scholar 

  • Collakova E, DellaPenna D (2001) Isolation and functional analysis of homogentisate phytyltransferase from Synechocystis sp. PCC 6803 and Arabidopsis Plant Physiol 127:1113–1124

    Article  PubMed  CAS  Google Scholar 

  • Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300:1005–1016

    Article  PubMed  CAS  Google Scholar 

  • Garcia I, Rodgers M, Lenne C, Rolland A, Sailland A, Matringe M (1997) Subcellular localization and purification of a p-hydroxyphenylpyruvate dioxygenase from cultured carrot cells and characterization of the corresponding cDNA. Biochem J 325:761–769

    PubMed  CAS  Google Scholar 

  • Hirooka K, Bamba T, Fukusaki E, Kobayashi A (2003) Cloning and kinetic characterization of Arabidopsis thaliana solanesyl diphosphate synthase. Biochem J 370:679–686

    Article  PubMed  CAS  Google Scholar 

  • Hirooka K, Izumi Y, An C, Nakazawa Y, Fukusaki E, Kobayashi A (2005) Functional analysis of two solanesyl diphosphate synthases from Arabidopsis thaliana. Biosci Biotechnol Biochem 69:592–601

    Article  PubMed  CAS  Google Scholar 

  • Liu CJ, Dixon RA (2001) Elicitor-induced association of isoflavone O-methyltransferase with endomembranes prevents formation and 7-O-methylation of daidzein during isoflavonoid phytoalexin biosynthesis. Plant Cell 13:2643–2658

    Article  PubMed  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Nicholas KB, Nicholas HB Jr, Deerfield DW II (1997) GeneDoc: analysis and visualization of gene variation. Embnet News 4:1–4

    Google Scholar 

  • Nielsen H, Engelbrecht J, Brunak S, von Heijne G (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10:1–6

    Article  PubMed  CAS  Google Scholar 

  • Nievelstein V, Vandekerckhove J, Tadros MH, von Lintig J, Nitschke W, Beyer P (1995) Carotene desaturation is linked to a respiratory redox pathway in Narcissus pseudonarcissus chromoplast membranes. Involvement of a 23-KDa oxygen-evolving-complex-like protein. Eur J Biochem 233:864–872

    Article  PubMed  CAS  Google Scholar 

  • Norris SR, Barrette TR, DellaPenna D (1995) Genetic dissection of carotenoid synthesis in Arabidopsis defines plastoquinone as an essential component of phytoene desaturation. Plant Cell 7:2139–2149

    Article  PubMed  CAS  Google Scholar 

  • Norris SR, Shen X, DellaPenna D (1998) Complementation of the Arabidopsis pds1 mutation with the gene encoding p-Hydroxyphenylpyruvate dioxygenase. Plant Physiol 117:1317–1323

    Article  PubMed  CAS  Google Scholar 

  • Osowska-Rogers S, Swiezewska E, Andersson B, Dallner G (1994) The endoplasmic reticulum–Golgi system is a major site of plastoquinone synthesis in Spinach leaves. Biochem Biophys Res Comm 205:714–721

    Article  PubMed  CAS  Google Scholar 

  • Restrepo MA, Freed DD, Carrington JC (1990) Nuclear transport of plant potyviral proteins. Plant Cell 2:987–998

    Article  PubMed  CAS  Google Scholar 

  • Sadre R, Gruber J, Frentzen M (2006) Characterization of homogentisate prenyltransferases involved in plastoquinone-9 and tocopherol biosynthesis. FEBS Lett 580:5357–5362

    Article  PubMed  CAS  Google Scholar 

  • Savidge B, Weiss JD, Wong YH, Lassner MW, Mitsky TA, Shewmaker CK, Post-Beittenmiller D, Valentin HE (2002) Isolation and characterization of homogentisate phytyltransferase genes from Synechocystis sp. PCC 6803 and Arabidopsis Plant Physiol 129:321–332

    Article  PubMed  CAS  Google Scholar 

  • Siebert M, Bechthold A, Melzer M, May U, Berger U, Schroder G, Schroder J, Severin K, Heide L (1992) Ubiquinone biosynthesis. Cloning of the genes coding for chorismate pyruvate-lyase and 4-hydroxybenzoate octaprenyl transferase from Escherichia coli FEBS Lett 307:347–350

    Article  PubMed  CAS  Google Scholar 

  • Soll J, Kemmerling M, Schultz G (1980) Tocopherol and plastoquinone synthesis in spinach chloroplasts subfractions. Arch Biochem Biophys 204:544–550

    Article  PubMed  CAS  Google Scholar 

  • Soll J, Schultz G, Joyard J, Douce R, Block MA (1985) Localization and synthesis of prenylquinones in isolated outer and inner membranes from spinach chloroplasts. Arch Biochem Biophys 238:290–299

    Article  PubMed  CAS  Google Scholar 

  • Swiezewska E (2004) Ubiquinone and plastoquinone metabolism in plants. Methods Enzymol 378:124–131

    Article  PubMed  CAS  Google Scholar 

  • Swiezewska E, Dallner G, Andersson B, Ernster L (1993) Biosynthesis of ubiquinone and plastoquinone in the endoplasmic reticulum–Golgi membranes of spinach leaves. J Biol Chem 268:1494–1499

    PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic acid Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Tian L, Dixon RA (2006) Engineering isoflavone metabolism with an artificial bifunctional enzyme. Planta 224:496–507

    Article  PubMed  CAS  Google Scholar 

  • Venkatesh T, Karunanandaa B, Free D, Rottnek J, Baszis S, Valentin HE (2006) Identification and characterization of an Arabidopsis homogentisate phytyltransferase paralog. Planta 223:1134–1144

    Article  PubMed  CAS  Google Scholar 

  • Wanke M, Dallner G, Swiezewska E (2000) Subcellular localization of plastoquinone and ubiquinone synthesis in spinach cells. Biochim Biophys Acta 1463:188–194

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. Aline Vaster for assistance with confocal microscopy and Drs. Rujin Chen and Ping Xu for critical reading of the manuscript. This work was supported by the Samuel Roberts Noble Foundation.

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Authors and Affiliations

  1. Plant Biology Division, The Samuel Roberts Noble Foundation, 2510 Sam Noble Parkway, Ardmore, OK, 73401, USA

    Li Tian & Richard A. Dixon

  2. Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI, 48824, USA

    Dean DellaPenna

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  1. Li Tian
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  2. Dean DellaPenna
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  3. Richard A. Dixon
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Correspondence to Richard A. Dixon.

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Tian, L., DellaPenna, D. & Dixon, R.A. The pds2 mutation is a lesion in the Arabidopsis homogentisate solanesyltransferase gene involved in plastoquinone biosynthesis. Planta 226, 1067–1073 (2007). https://doi.org/10.1007/s00425-007-0564-5

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