Functional Analysis of Two Solanesyl Diphosphate Synthases from Arabidopsis thaliana

Solanesyl diphosphate (SPP) is regarded as the precursor of the side-chains of both plastoquinone and ubiquinone in Arabidopsis thaliana. We previously analyzed A. thaliana SPP synthase (At-SPS1) (Hirooka et al., Biochem. J., 370, 679–686 (2003)). In this study, we cloned a second SPP synthase (At-SPS2) gene from A. thaliana and characterized the recombinant protein. Kinetic analysis indicated that At-SPS2 prefers geranylgeranyl diphosphate to farnesyl diphosphate as the allylic substrate. Several of its features, including the substrate preference, were similar to those of At-SPS1. These data indicate that At-SPS1 and At-SPS2 share their basic catalytic machinery. Moreover, analysis of the subcellular localization by the transient expression of green fluorescent protein-fusion proteins showed that At-SPS2 is transported into chloroplasts, whereas At-SPS1 is likely to be localized in the endoplasmic reticulum in the A. thaliana cells. It is known that the ubiquinone side-chain originates from isopentenyl diphosphate derived from the cytosolic mevalonate pathway, while the plastoquinone side-chain is synthesized from isopentenyl diphosphate derived from the plastidial methylerythritol phosphate pathway. Based on this information, we propose that At-SPS1 contributes to the biosynthesis of the ubiquinone side-chain and that At-SPS2 supplies the precursor of the plastoquinone side-chain in A. thaliana.

[1]  K. Yazaki,et al.  The AtPPT1 gene encoding 4-hydroxybenzoate polyprenyl diphosphate transferase in ubiquinone biosynthesis is required for embryo development in Arabidopsis thaliana , 2004, Plant Molecular Biology.

[2]  A. Hemmerlin,et al.  Cross-talk between the Cytosolic Mevalonate and the Plastidial Methylerythritol Phosphate Pathways in Tobacco Bright Yellow-2 Cells* , 2003, Journal of Biological Chemistry.

[3]  C. Clarke,et al.  The Saccharomyces cerevisiae COQ6 Gene Encodes a Mitochondrial Flavin-dependent Monooxygenase Required for Coenzyme Q Biosynthesis* , 2003, Journal of Biological Chemistry.

[4]  A. Fürholz,et al.  Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[5]  E. Fukusaki,et al.  Cloning and kinetic characterization of Arabidopsis thaliana solanesyl diphosphate synthase. , 2003, The Biochemical journal.

[6]  A. Hemmerlin,et al.  Isoprenoid biosynthesis in higher plants and in Escherichia coli: on the branching in the methylerythritol phosphate pathway and the independent biosynthesis of isopentenyl diphosphate and dimethylallyl diphosphate. , 2002, The Biochemical journal.

[7]  R. Backhaus,et al.  Molecular cloning of geranyl diphosphate synthase and compartmentation of monoterpene synthesis in plant cells. , 2000, The Plant journal : for cell and molecular biology.

[8]  T. Saito,et al.  Five geranylgeranyl diphosphate synthases expressed in different organs are localized into three subcellular compartments in Arabidopsis. , 2000, Plant physiology.

[9]  E. Swiezewska,et al.  Subcellular localization of plastoquinone and ubiquinone synthesis in spinach cells. , 2000, Biochimica et biophysica acta.

[10]  K. Wang,et al.  Chain-length determination mechanism of isoprenyl diphosphate synthases and implications for molecular evolution. , 1999, Trends in biochemical sciences.

[11]  A. Frankel,et al.  Yeast and Rat Coq3 and Escherichia coli UbiG Polypeptides Catalyze Both O-Methyltransferase Steps in Coenzyme Q Biosynthesis* , 1999, The Journal of Biological Chemistry.

[12]  T. Nishino,et al.  A Pathway Where Polyprenyl Diphosphate Elongates in Prenyltransferase , 1998, The Journal of Biological Chemistry.

[13]  R. Croteau,et al.  Truncation of limonene synthase preprotein provides a fully active 'pseudomature' form of this monoterpene cyclase and reveals the function of the amino-terminal arginine pair. , 1998, Biochemistry.

[14]  K. Tanaka,et al.  Molecular cloning and mutational analysis of the ddsA gene encoding decaprenyl diphosphate synthase from Gluconobacter suboxydans. , 1998, European journal of biochemistry.

[15]  T. Koyama,et al.  Enzymatic Aspects of Isoprenoid Chain Elongation. , 1998, Chemical reviews.

[16]  A. Hemmerlin,et al.  Mevalonate-derived isopentenyl diphosphate is the biosynthetic precursor of ubiquinone prenyl side chain in tobacco BY-2 cells. , 1998, The Biochemical journal.

[17]  J. Joyard,et al.  Cloning and functional expression of AtCOQ3, the Arabidopsis homologue of the yeast COQ3 gene, encoding a methyltransferase from plant mitochondria involved in ubiquinone biosynthesis. , 1998, The Plant journal : for cell and molecular biology.

[18]  Y. Kamiya,et al.  Cloning of the sdsA gene encoding solanesyl diphosphate synthase from Rhodobacter capsulatus and its functional expression in Escherichia coli and Saccharomyces cerevisiae , 1997, Journal of bacteriology.

[19]  P. Beyer,et al.  Chloroplast import of four carotenoid biosynthetic enzymes in vitro reveals differential fates prior to membrane binding and oligomeric assembly. , 1997, European journal of biochemistry.

[20]  E. Dibrov,et al.  The COQ5 Gene Encodes a Yeast Mitochondrial Protein Necessary for Ubiquinone Biosynthesis and the Assembly of the Respiratory Chain* , 1997, The Journal of Biological Chemistry.

[21]  Jörg Schwender,et al.  Biosynthesis of isoprenoids in higher plant chloroplasts proceeds via a mevalonate‐independent pathway , 1997, FEBS letters.

[22]  F. Karst,et al.  Arabidopsis thaliana Contains Two Differentially Expressed Farnesyl-Diphosphate Synthase Genes (*) , 1996, The Journal of Biological Chemistry.

[23]  Takanori Hirano,et al.  Engineered GFP as a vital reporter in plants , 1996, Current Biology.

[24]  C. Clarke,et al.  The COQ7 Gene Encodes a Protein in Saccharomyces cerevisiae Necessary for Ubiquinone Biosynthesis (*) , 1996, The Journal of Biological Chemistry.

[25]  F. Karst,et al.  Cloning of an Arabidopsis thaliana cDNA coding for farnesyl diphosphate synthase by functional complementation in yeast , 1994, Plant Molecular Biology.

[26]  G. Bartley,et al.  Nucleotide Sequence of an Arabidopsis cDNA for Geranylgeranyl Pyrophosphate Synthase , 1994, Plant physiology.

[27]  A. Theologis,et al.  Transient transformation of Arabidopsis leaf protoplasts: a versatile experimental system to study gene expression. , 1994, The Plant journal : for cell and molecular biology.

[28]  A. B. Hope.  The chloroplast cytochrome bf complex: a critical focus on function. , 1993, Biochimica et biophysica acta.

[29]  E. Swiezewska,et al.  Biosynthesis of ubiquinone and plastoquinone in the endoplasmic reticulum-Golgi membranes of spinach leaves. , 1993, The Journal of biological chemistry.

[30]  P. Edwards,et al.  COQ2 is a candidate for the structural gene encoding para-hydroxybenzoate:polyprenyltransferase. , 1992, The Journal of biological chemistry.

[31]  P. Hugueney,et al.  Purification and characterization of farnesyl pyrophosphate synthase from Capsicum annuum , 1990, FEBS letters.

[32]  P. Edwards,et al.  Elucidation of the deficiency in two yeast coenzyme Q mutants. Characterization of the structural gene encoding hexaprenyl pyrophosphate synthetase. , 1990, The Journal of biological chemistry.

[33]  M. Block,et al.  Localization and synthesis of prenylquinones in isolated outer and inner envelope membranes from spinach chloroplasts. , 1985, Archives of biochemistry and biophysics.

[34]  R. Casey,et al.  Membrane reconstitution of the energy-conserving enzymes of oxidative phosphorylation. , 1984, Biochimica et biophysica acta.

[35]  Fujii Hiroshi,et al.  Efficient enzymatic hydrolysis of polyprenyl pyrophosphates. , 1982, Biochimica et biophysica acta.

[36]  M. M. Bradford.  A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. , 1976, Analytical biochemistry.

[37]  U. K. Laemmli,et al.  Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4 , 1970, Nature.

[38]  D. Threlfall,et al.  Biosynthesis of ubiquinone—a search for polyprenyl phenol and quinone precursors , 1970 .

[39]  D. Andrews,et al.  Membrane-bound fatty acid desaturases are inserted co-translationally into the ER and contain different ER retrieval motifs at their carboxy termini. , 2004, The Plant journal : for cell and molecular biology.

[40]  E. Swiezewska,et al.  Isoprenoid biosynthesis via 1-deoxy-D-xylulose 5-phosphate/2-C-methyl-D-erythritol 4-phosphate (DOXP/MEP) pathway. , 2001, Acta biochimica Polonica.

[41]  A. Szkopińska.  Ubiquinone. Biosynthesis of quinone ring and its isoprenoid side chain. Intracellular localization. , 2000, Acta biochimica Polonica.

[42]  Shigeki Mitaku,et al.  SOSUI: classification and secondary structure prediction system for membrane proteins , 1998, Bioinform..

[43]  T. Koyama,et al.  Efficient enzymatic hydrolysis of polyprenyl pyrophosphates. , 1982, Biochimica et biophysica acta.