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From inhibitors to target site genes and beyond—herbicidal inhibitors as powerful tools for functional genomics

Published online by Cambridge University Press:  20 January 2017

Rui-Guang Zhen  and
Bijay K. Singh
Bijay K. Singh
Affiliation:
BASF Plant Science, BASF Corporation, P.O. Box 400, Princeton, NJ 08543-0400
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Abstract

With rapid progress being made in deciphering plant genomic sequences, determining the function of these genes is one of the main challenges that plant molecular biologists face today. Herbicidal inhibitors have been very useful for understanding gene function in at least two examples, represented by herbicidal inhibitors of hydroxyphenylpyruvate dioxygenase (HPPD) and deoxyxylulosephosphate reductoisomerase (DXR). In the first, an albino mutant of Arabidopsis isolated during the study of carotenoid biosynthesis was found to have an intact carotenoid biosynthetic pathway. A number of “bleaching herbicides” in development at about the same time (e.g., sulcotrione) produced similar symptoms by strongly inhibiting HPPD, a key enzyme in plastoquinone biosynthesis. Examination of the Arabidopsis mutant revealed that the HPPD gene had been inactivated in the albino plants. Inhibition of the HPPD pathway also led to reduced levels of tocopherol (vitamin E), an end product of the pathway. Further studies and manipulation of the pathway produced plants with significantly higher levels of vitamin E. This result is a clear demonstration of how an herbicidal inhibitor was able to lead to the identification of a gene that was responsible for a particular phenotype. As a second example, identification of fosmidomycin as a specific inhibitor of DXR in the recently elucidated nonmevalonate pathway of isopentenyl pyrophosphate (IPP) biosynthesis was instrumental in furthering the understanding of an important route to synthesis of many important terpenoid products.

Keywords

Fosmidomycin, 3-(N-formyl-N-hydroxyamino)propylphosphonic acidsulcotrioneArabidopsis mutantHerbicidemutantphytoene desaturasenorflurazonHPPDplastoquinonetocopherolnonmevalonate pathwayIPP
Type
Symposium
Information
Weed Science , Volume 49 , Issue 2 , April 2001 , pp. 266 - 272
Copyright
Copyright © Weed Science Society of America 

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References

Literature Cited

Araki, N., Kusumi, K., Masamoto, K., Niwa, Y., and Iba, K. 2000. Temperature-sensitive Arabidopsis mutant defective in 1-deoxy-D-xylulose 5-phosphate synthase within the plastid non-mevalonate pathway of isoprenoid biosynthesis. Physiol. Plant. 108:19–24.Google Scholar
Aulabaugh, A. and Schloss, J. V. 1990. Oxalyl hydroxamates as reaction intermediate analogs for ketol acid reductoisomerase. Biochemistry 29:2824–2830.CrossRefGoogle ScholarPubMed
Bishop, N. I. and Wong, J. 1974. Photochemical characteristics of a vitamin E deficient mutant of Scenedesmus obliquus . Ber. Dtsch. Bot. Ges. 87:359–371.Google Scholar
Bouvier, F., d’Harlingue, A., Suire, C., Backhaus, R. A., and Camara, B. 1998. Dedicated roles of plastid transketolases during the early onset of isoprenoid biogenesis in pepper fruits. Plant Physiol. 117:1423–1431.Google Scholar
Cunningham, F. X. Jr. and Gantt, E. 1998. Genes and enzymes of carotenoid biosynthesis in plants. Ann. Rev. Plant Physiol. Plant Mol. Biol. 49:557–583.Google Scholar
Duvold, T., Calí, P., Bravo, J., and Rohmer, M. 1997. Incorporation of 2-C-methyl-D-erythritol, a putative isoprenoid precursor in the mevalonate-independent pathway, into ubiquinone and menaquinone of Escherichia coli . Tetrahedron Lett. 38:6181–6184.CrossRefGoogle Scholar
Gai, X., Lal, S., Xing, L., Brendel, V., and Walbot, V. 2000. Gene discovery using the maize genome database ZmDB. Nucleic Acids Res. 28:94–96.Google Scholar
Goodwin, T.W. and Mercer, E. I. 1963. The regulation of sterol and carotenoid metabolism in germinating seedlings. Pages 37–40. In Grant, J. K., ed. The Control of Lipid Metabolism. London: Academic Press.Google Scholar
Gura, T. 2000. Reaping the plant gene harvest. Science 287:412–414.Google Scholar
Henry, A., Powls, R., and Pennock, J. F. 1986. Scenedesmus obliquus PS28: a tocopherol-free mutant which cannot form phytol. Biochem. Soc. Trans. 14:958–959.CrossRefGoogle Scholar
Herz, S., Wungsintaweekul, J., Schuhr, C. A., et al. 2000. Biosynthesis of terpenoids: YgbB protein converts 4-diphosphocytidyl-2C-methyl-Derythritol 2-phosphate to 2C-methyl-D-erythritol 2,4-cyclodiphosphate. Proc. Natl. Acad. Sci. USA 97:2486–2490.Google Scholar
Horbach, S., Sahm, H., and Welle, R. 1993. Isoprenoid biosynthesis in bacteria: two different pathways. FEMS Microbiol. Lett. 111:135–140.Google Scholar
Jomaa, H., Wiesner, J., Sanderbrand, S., et al. 1999. Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science 285:1573–1576.CrossRefGoogle ScholarPubMed
Julliard, J. H. 1992. Biosynthesis of the pyridoxal ring (vitamin B6) in higher plant chloroplasts and its relationship with the biosynthesis of the thiazol ring (vitamin B1). C.R. Acad. Sci. Ser. 314:285–290.Google Scholar
Julliard, J. H. and Douce, R. 1991. Biosynthesis of the thiazole moiety of thiamin (vitamin B1) in higher plant chloroplasts. Proc. Natl. Acad. Sci. USA 88:2041–2045.CrossRefGoogle ScholarPubMed
Kamuro, Y., Kawai, T., and Kakiuchi, T., inventors; Fujisawa Pharmaceuticals, assignee. 1990 Dec 27. Herbicide. European Patent 0256785B1.Google Scholar
Kaneko, T., Sato, S., Kotani, H., et al. 1996. Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res. 3:109–136.Google Scholar
Kreuz, K. and Kleinig, H. 1984. Synthesis of prenyl lipids in cells of spinach leaf. Compartmentation of enzymes for formation of isopentenyl diphosphate. Eur. J. Biochem. 141:531–535.Google Scholar
Kuzuyama, T., Shimizu, T., Takahashi, S., and Seto, H. 1998. Fosmidomycin, a specific inhibitor of 1-deoxy-D-xylulose 5-phosphate reductoisomerase in the nonmevalonate pathway for terpenoid biosynthesis. Tetrahedron Lett. 39:7913–7916.Google Scholar
Lange, B. M., Wildung, M. R., McCaskill, D., and Croteau, R. 1998. A family of transketolases that directs isoprenoids via a mevalonate-independent pathway. Proc. Natl. Acad. Sci. USA 95:2100–2104.Google Scholar
Lichtenthaler, H. K. 1999. The 1-deoxy-D-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants. Ann. Rev. Plant Physiol. Plant Mol. Biol. 50:47–65.Google Scholar
Lois, L. M., Campos, N., Putra, S. R., Danielsen, K., Rohmer, M., and Boronat, A. 1998. Cloning and characterization of a gene from Escherichia coli encoding a transketolase-like enzyme that catalyzes the synthesis of D-1-deoxyxylulose 5-phosphate, a common precursor for isoprenoid, thiamin, and pyridoxol biosynthesis. Proc. Natl. Acad. Sci. USA 95:2105–2110.Google Scholar
Lüttgen, H., Rohdich, F., Herz, S., et al. 2000. Biosynthesis of terpenoids: YchB protein of Escherichia coli phosphorylates the 2-hydroxy group of 4-diphosphocytidyl-2C-methyl-D-erythritol. Proc. Natl. Acad. Sci. USA 97:1062–1067.Google Scholar
Mandel, M. A., Feldmann, K. A., Herrera-Estrella, L., Rocha-Sosa, M., and Leon, P. 1996. CLA1, a novel gene required for chloroplast development, is highly conserved in evolution. Plant J. 9:649–658.Google Scholar
Mayer, M. P., Beyer, P., and Kleinig, H. 1990. Quinone compounds are able to replace molecular oxygen as terminal electron acceptor in phytoene desaturation in chrmoplasts of Narcissus pseudonarcissus L. Eur. J. Biochem. 191:359–363.Google Scholar
Norris, S. R., Barrette, T. R., and DellePenna, D. 1995. Genetic dissection of carotenoid synthesis in Arabidopsis defines plastoquinone as an essential component of phytoene desaturation. Plant Cell 7:2139–2149.Google Scholar
Norris, S. R., Shen, X., and DellaPenna, D. 1998. Complementation of the Arabidopsis pds1 mutation with the gene encoding ρ-hydroxyphenylpyruvate dioxygenase. Plant Physiol. 117:1317–1323.Google Scholar
Okuhara, M., Kuroda, Y., Goto, T., Okamoto, M., Terano, H., Kosanobu, M., Aoki, H., and Imanaka, H. 1980. Studies of new phosphonic acid antibiotics. III. Isolation and characterization of FR-31564, FR-32863 and FR-33289. J. Antibiot. 33:24–28.Google Scholar
Patterson, D. R., inventor; Rohm and Hass Co., assignee. 1987 Sep 15. Herbicidal hydroxyamino phosphonic acids and derivatives. U.S. patent 4,693,742.Google Scholar
Rohdich, F., Wungsintaweekul, J., Fellermeier, M., Sagner, S., Herz, S., Kis, K., Eisenreich, W., Bacher, A., and Zenk, M. H. 1999. Cytidine 5'-triphosphate-dependent biosynthesis of isoprenoids: YgbP protein of Escherichia coli catalyzes the formation of 4-diphosphocytidyl-2-Cmethylerythritol. Proc. Natl. Acad. Sci. USA 96:11758–11763.Google Scholar
Rohmer, M., Knani, M., Simonin, P., Sutter, B., and Sahm, H. 1993. Isoprenoid biosynthesis in bacteria: a novel pathway for the early steps leading to isopentenyl diphosphate. Biochem. J. 295:517–524.Google Scholar
Sasaki, T. 1998. The rice genome project in Japan. Proc. Natl. Acad. Sci. USA 95:2027–2028.CrossRefGoogle ScholarPubMed
Schulz, A., Ort, O., Beyer, P., and Kleinig, H. 1993. SC-0051, a 2-benzoylcyclohexane-1,3-dione bleaching herbicide, is a potent inhibitor of the enzyme ρ-hydroxyphenylpyruvate dioxygenase. FEBS Lett. 318:162–166.CrossRefGoogle Scholar
Schwender, J., Müller, C., Zeidler, J., and Lichtenthaler, H. K. 1999. Cloning and heterologous expression of a cDNA encoding 1-deoxy-D-xylulose-5-phosphate reductoisomerase of Arabidopsis thaliana . FEBS Lett. 455:140–144.Google Scholar
Secor, J. 1994. Inhibition of barnyardgrass 4-hydroxyphenylpyruvate dioxygenase by sulcotrione. Plant Physiol. 106:1429–1433.CrossRefGoogle ScholarPubMed
Seto, H., Watanabe, H., and Furihata, K. 1996. Simultaneous operation of the mevalonate and nonmevalonate pathways in the biosynthesis of isopentenyl diphosphate in Streptomyces aeriouvifer . Tetrahedron Lett. 37:7979–7982.Google Scholar
Shintani, D. and DellaPenna, D. 1998. Elevating the vitamin E content of plants through metabolic engineering. Science 282:2098–2100.Google Scholar
Somerville, C. and Somerville, S. 1999. Plant functional genomics. Science 285:380–383.CrossRefGoogle ScholarPubMed
Sprenger, G. A., Schörken, U., Wiegert, T., Grolle, S., and de Graaf, A. A. 1997. Identification of a thiamin-dependent synthase in Escherichia coli required for the formation of 1-deoxy D-xylulose-5-phosphate precursor to isoprenoids, thiamin, and pyridoxol. Proc. Natl. Acad. Sci. USA 94:1857–1862.Google Scholar
Takahashi, S., Kuzuyama, T., Watanabe, H., and Seto, H. 1998. A 1-deoxy-D-xylulose 5-phosphate reductoisomerase catalyzing the formation of 2- C-methyl-D-erythritol 4-phosphate in an alternative nonmevalonate pathway for terpenoid biosynthesis. Proc. Natl. Acad. Sci. USA 95:9879–9884.Google Scholar
Zerdler, J., Schwender, J., Müler, C., Wiesner, J., Weidemeyer, C., Beck, E., Jomaa, H., and Lichtenthaler, H. K. 1998 Inhibition of the non-mevalonate 1-deoxy-D-xylulose-5-phosphate pathway of plant isoprenoid biosynthesis by fosmidomycin. Z. Naturforsch 53c:980–986.CrossRefGoogle Scholar