Two independent biochemical pathways for isopentenyl diphosphate and isoprenoid biosynthesis in higher plants

In the early times of isoprenoid research, a single pathway was found for the formation of the C5 monomer, isopentenyl diphosphate (IPP), and this acetate/mevalonate pathway was supposed to occur ubiquitously in all living organisms. Now, 40 years later, a totally different IPP biosynthesis route has been detected in eubacteria, green algae and higher plants. In this new pathway glyceraldehyde 3-phosphate (GAP) and pyruvate are precursors of isopentenyl diphosphate, but not acetyl-CoA and mevalonic acid. In green tissues of three higher plants it was shown that all chloroplastbound isoprenoids (β-carotene, phytyl chains of chlorophylls and nona-prenyl chain of plastoquinone-9) are formed via the GAP/pyruvate pathway, whereas the cytoplasmic sterols are formed via the acetate/mevalonate pathway. Also, isoprene, emitted by various plants at high light conditions by action of the plastid-bound isoprene synthase, is formed via the new GAP/pyruvate pathway. Thus, in higher plants, there exist two separate and biochemically different IPP biosynthesis pathways: (1) the novel alternative GAP/pyruvate pathway apparently bound to the plastidic compartment and (2) the classical cytoplasmic acetate/mevalonate pathway. This new GAP/pyruvate pathway for IPP formation allows a reasonable interpretation of previous odd results concerning the biosynthesis of chloroplast isoprenoids, which, so far, had mainly been interpreted assuming compartmentation differences. The novel GAP/pyruvate pathway for IPP formation in plastids appears as a heritage of their prokaryotic, endosymbiotic ancestors.

[1]  J. Schwender,et al.  Biosynthesis of isoprenoids (carotenoids, sterols, prenyl side-chains of chlorophylls and plastoquinone) via a novel pyruvate/glyceraldehyde 3-phosphate non-mevalonate pathway in the green alga Scenedesmus obliquus. , 1996, The Biochemical journal.

[2]  G. Märkl,et al.  Bildung und Vorkommen von Phytol, III. Einbau von Essigsäure- und Mevalonsäure-[2-14C] in Chlorophyll, Sterine und Carotinoide von Gerstenkeimlingen† , 1962 .

[3]  H. Lichtenthaler,et al.  Mevinolin: A Highly Specific Inhibitor of Microsomal 3-Hydroxy-3-Methylglutaryl-Coenzyme A Reductase of Radish Plants , 1982, Zeitschrift fur Naturforschung. Section C, Biosciences.

[4]  H. Seto,et al.  Simultaneous operation of the mevalonate and non-mevalonate pathways in the biosynthesis of isopentenly diphosphate in Streptomyces aeriouvifer , 1996 .

[5]  J. Porter,et al.  The incorporation of mevalonic acid-2-C14 and dimethylacrylic acid-3-C14 into carotenes. , 1960, Archives of biochemistry and biophysics.

[6]  J. Görlach,et al.  Plastidic Isoprenoid Synthesis during Chloroplast Development : Change from Metabolic Autonomy to a Division-of-Labor Stage. , 1990, Plant physiology.

[7]  H. Sahm,et al.  Glyceraldehyde 3-Phosphate and Pyruvate as Precursors of Isoprenic Units in an Alternative Non-mevalonate Pathway for Terpenoid Biosynthesis , 1996 .

[8]  H. Lichtenthaler,et al.  Is Isoprene Emitted by Plants Synthesized via the Novel Isopentenyl Pyrophosphate Pathway? , 1997 .

[9]  H. Yamashita,et al.  A High Activity of 3-Hydroxy-3-methylglutaryl Coenzyme A Reductase in Chloroplasts of Stevia rebaudiana Bertoni , 1996 .

[10]  R. Douce,et al.  Biosynthesis of the thiazole moiety of thiamin (vitamin B1) in higher plant chloroplasts. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[11]  R. Fall,et al.  Light-Dependent Isoprene Emission (Characterization of a Thylakoid-Bound Isoprene Synthase in Salix discolor Chloroplasts) , 1996, Plant physiology.

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

[13]  R. Hill,et al.  Biosynthesis of vitamins B1 and B6 in Escherichia coli: concurrent incorporation of 1-deoxy-D-xylulose into thiamin (B1) and pyridoxol (B6) , 1996 .

[14]  W. Eisenreich,et al.  Studies on the biosynthesis of taxol: the taxane carbon skeleton is not of mevalonoid origin. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[15]  T. Goodwin,et al.  Studies in carotenogenesis. 25. The incorporation of [1-14C]acetate, [2-14C]acetate and 14CO2 into lycopene by tomato slices , 1960 .

[16]  D. Hill,et al.  Direct Binding of the Proline-rich Region of Protein Tyrosine Phosphatase 1B to the Src Homology 3 Domain of p130Cas* , 1996, The Journal of Biological Chemistry.

[17]  T. Goodwin,et al.  Studies in carotenogenesis. 27. Incorporation of [2-14C]acetate, dl-[2-14C]mevalonate and 14CO2 into carrot-root preparations , 1960 .

[18]  H. Lichtenthaler,et al.  QUINONE AND PIGMENT COMPOSITION OF CHLOROPLASTS AND QUANTASOME AGGREGATES FROM SPINACIA OLERACEA. , 1964, Biochimica et biophysica acta.

[19]  J. Gray Control of Isoprenoid Biosynthesis in Higher Plants , 1988 .

[20]  H. Lichtenthaler Regulation of Prenylquinone Synthesis in Higher Plants , 1977 .

[21]  H. Kleinig The Role of Plastids in Isoprenoid Biosynthesis , 1989 .

[22]  H. Sahm,et al.  Isoprenoid biosynthesis in bacteria: two different pathways? , 1993, FEMS Microbiology Letters.

[23]  T. Sharkey,et al.  Isoprene synthesis by plants and animals. , 1996, Endeavour.

[24]  H. Sahm,et al.  Bacterial sterol surrogates. Biosynthesis of the side-chain of bacteriohopanetetrol and of a carbocyclic pseudopentose from 13C-labelled glucose in Zymomonas mobilis , 1989 .

[25]  H. Okuyama,et al.  Sesqui- and di-terpene biosynthesis from 13C labelled acetate and mevalonate in cultured cells of Heteroscyphus planus , 1995 .

[26]  H. Kleinig,et al.  On the biosynthesis of ubiquinones in plant mitochondria. , 1984, European journal of biochemistry.

[27]  M. Rohmer,et al.  Prokaryotic hopanoids: the biosynthesis of the bacteriohopane skeleton. Formation of isoprenic units from two distinct acetate pools and a novel type of carbon/carbon linkage between a triterpene and D-ribose. , 1988, European journal of biochemistry.

[28]  H. Sahm,et al.  Isoprenoid biosynthesis in bacteria: a novel pathway for the early steps leading to isopentenyl diphosphate. , 1993, The Biochemical journal.

[29]  H. Lichtenthaler,et al.  Inhibition by mevinolin of plant growth, sterol formation and pigment accumulation , 1983 .

[30]  T. Goodwin The Prenyllipids of the Membranes of Higher Plants , 1977 .