Loss of function of 3-hydroxy-3-methylglutaryl coenzyme A reductase 1 (HMG1) in Arabidopsis leads to dwarfing, early senescence and male sterility, and reduced sterol levels

Plant Journal

Volumn 37, Issue 5, 2004, Pages 750-761

  Suzuki, Masashi ^a   Kamide, Yukiko ^a   Nagata, Noriko ^a,e   Seki, Hikaru ^a   Ohyama, Kiyoshi ^a,b   Kato, Hisashi ^a,f   Masuda, Kazuo ^c   Sato, Shusei ^d   Kato, Tomohiko ^d   Tabata, Satoshi ^d   Yoshida, Shigeo ^a   Muranaka, Toshiya ^a  

^a RIKEN Center for Sustainable Resource Science   (Japan)

^b Plantech Research Institute   (Japan)

^c SHOWA PHARMACEUTICAL UNIVERSITY   (Japan)

^d KAZUSA DNA RESEARCH INSTITUTE   (Japan)

^e JAPAN WOMEN'S UNIVERSITY   (Japan)

^f KEIO UNIVERSITY   (Japan)

Author keywords

3 hydroxy 3 methylglutaryl CoA reductase; Dwarfing; Male sterile; Mevalonate pathway; Senescence; Sterol

Indexed keywords

BIOMARKERS; BIOSYNTHESIS; CATALYSIS; COENZYMES; DNA; ENZYME INHIBITION; ENZYME KINETICS; GENETIC ENGINEERING; GROWTH KINETICS; HORMONES; MUTAGENESIS;

GENE EXPRESSION; SENESCENCE;

PLANT CELL CULTURE;

ARABIDOPSIS PROTEIN; BRASSINOLIDE; CHOLESTANOL; CYSTEINE PROTEINASE; CYTOKININ; ENZYME INHIBITOR; HETEROCYCLIC STEROID; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; MEVALONIC ACID; MEVINOLIN; PHYTOSTEROL; SAG12 PROTEIN, ARABIDOPSIS; SQUALENE; TRITERPENE;

ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; CELL DIVISION; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; FERTILITY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PHENOTYPE; PHYSIOLOGY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL DIVISION; CHOLESTANOLS; CYSTEINE ENDOPEPTIDASES; CYTOKININS; ENZYME INHIBITORS; FERTILITY; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; HYDROXYMETHYLGLUTARYL COA REDUCTASES; LOVASTATIN; MEVALONIC ACID; MUTATION; PHENOTYPE; PHYTOSTEROLS; SQUALENE; STEROIDS, HETEROCYCLIC; TRITERPENES;

ARABIDOPSIS; EMBRYOPHYTA; INSERTION SEQUENCES;

EID: 10744224664     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2004.02003.x     Document Type: Article

References (60)

1. Asami, T., Mizutani, M., Fujioka, S. et al. (2001) Selective interaction of triazole derivatives with DWF4, a cytochrome P450 monooxygenase of the brassinosteroid biosynthetic pathway, correlates with brassinosteroid deficiency in planta. J. Biol. Chem. 276, 25687-25691.
2. Brown, M.S., Faust, J.R., Goldstein, J.L., Kaneko, I. and Eodo, A. (1978) Induction of 3-hydroxy-3-methylglutaryl coenzyme-A reductase-activity in human fibroblasts incubated with compactin (ML-236B), a competitive inhibitor of reductase. J. Biol. Chem. 253, 1121-1128.
3. Caelles, C., Ferrer, A., Balcells, L., Hegardt, F.G. and Boronat, A. (1989) Isolation and structural characterization of a cDNA encoding Arabidopsis thaliana 3-hydroxy-3-methylglutaryl coenzyme A reductase. Plant Mol. Biol. 13, 627-638.
4. Carland, F.M., Fujioka, S., Takatsuto, S., Yoshida, S. and Nelson, T. (2002) The identification of CVP1 reveals a role for sterols in vascular patterning. Plant Cell, 14, 2045-2058.
5. Chen, X., Goodwin, S.M., Boroff, V.L., Liu, X. and Jenks, M.A. (2003) Cloning and characterization of the WAX2 gene of Arabidopsis involved in cuticle membrane and wax production. Plant Cell, 15, 1170-1185.
6. Choe, S., Dilkes, B.P., Fujioka, S., Takatsuto, S., Sakurai, A. and Feldmann, K.A. (1998) The DWF4 gene of Arabidopsis encodes a cytochrome P450 that mediates multiple 22α-hydroxylation steps in brassinosteroid biosynthesis. Plant Cell, 10, 231-243.
7. Chomczynski, P. (1992) One-hour downward alkaline capillary transfer for blotting of DNA and RNA. Anal. Biochem. 201, 134-139.
8. Clarke, P.R. and Hardie, D.G. (1990) Regulation of HMG-CoA reductase: identification of the site phosphorylated by the AMP-activated protein kinase in vitro and intact rat liver. EMBO J. 9, 2439-2446.
9. Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
10. Clouse, S.D. (1997) Molucular genetics of brassinosteroid action. Physiol. Plant. 100, 702-709.
11. Crowell, D.N. and Salaz, M.S. (1992) Inhibition of growth of cultured tobacco cells at low concentrations of lovastatin is reversed by cytokinin. Plant Physiol. 100, 2090-2095.
12. Daraselia, N.D., Tarchevskaya, S. and Narita, J.O. (1996) The promoter for tomato 3-hydroxy-3-methylglutaryl coenzyme A reductase gene 2 has unusual regulatory elements that direct high-level expression. Plant Physiol. 112, 727-733.
13. Diener, A.C., Li, H., Zhou, W., Whoriskey, W.J., Nes, W.D. and Fink, G.R. (2000) STEROL METHYLTRANSFERASE 1 controls the level of cholesterol in plants. Plant Cell, 12, 853-870.
14. Enjuto, M., Balcells, L., Campos, N., Caelles, C., Arró, M. and Boronat, A. (1994) Arabidopsis thaliana contains two differentially expressed 3-hydroxy-3-methylglutaryl-CoA reductase genes, which encode microsomal forms of the enzyme. Proc. Natl. Acad. Sci. USA, 91, 927-931.
15. Enjuto, M., Lumbreras, V., Marin, C. and Boronat, A. (1995) Expression of the Arabidopsis HMG2 gene, encoding 3-hydroxy-3-methylglutaryl coenzyme A reductase, is restricted to meristematic and floral tissues. Plant Cell, 7, 517-527.
16. Estévez, J.M., Cantero, A., Romero, C., Kawaide, H., Jiménez, L.F., Kuzuyama, T., Seto, H., Kamiya, Y. and León, P. (2000) Analysis of the expression of CLA1, a gene that encodes the 1-deoxyxylulose 5-phosphate synthase of the 2-C-methyl-D-erythritol-4-phosphate pathway in Arabidopsis. Plant Physiol. 124, 95-103.
17. Fujioka, S., Li, J., Choi, Y.-H. et al. (1997) The Arabidopsis deetiolated2 mutant is blocked early in brassinosteroid biosynthesis. Plant Cell, 9, 1951-1962.
18. Gan, S. and Amasino, R.M. (1995) Inhibition of leaf senescence by autoregulated production of cytokinin. Science, 270, 1986-1988.
19. Goda, H., Shimada, Y., Asami, T., Fujioka, S. and Yoshida, S. (2002) Microarray analysis of brassinosteroid-regulated genes in Arabidopsis. Plant Physiol. 130, 1319-1334.
20. Goldstein, J.L. and Brown, M.S. (1990) Regulation of the mevalonate pathway. Nature, 343, 425-430.
21. Hartmann, M.A., Wentzinger, L., Hemmerlin, A. and Bach, T.J. (2000) Metabolism of farnesyl diphosphate in tobacco BY-2 cells treated with squalestatin. Biochem. Soc. Trans. 28, 794-796.
22. He, J.-X., Fujioka, S., Li, T.-C., Kang, S.G., Seto, H., Takatsuto, S., Yoshida, S. and Jang, J.-C. (2003) Sterols regulate development and gene expression in Arabidopsis. Plant Physiol. 131, 1258-1269.
23. Hemmerlin, A. and Bach, T.J. (1998) Effects of mevinolin on cell cycle progression and viability of tobacco BY-2 cells. Plant J. 14, 65-74.
24. Hernández-Pinzón, I., Ross, J.H.E., Barnes, K.A., Damant A.P. and Murphy, D.J. (1999) Composition and role of tapetal lipid bodies in the biogenesis of the pollen coat of Brassica napus. Planta, 208, 588-598.
25. Husselstein-Muller, T., Schaller, H. and Benveniste, P. (2001) Molecular cloning and expression in yeast of 2,3-oxidosqualene-triterpenoid cyclases from Arabidopsis thaliana. Plant Mol. Biol. 45, 75-92.
26. Jang, J.-C., Fujioka, S., Tasaka, M., Seto, H., Takatsuto, S., Ishii, A., Aida, M., Yoshida, S. and Sheen. J. (2000) A critical role of sterols in embryonic patterning and meristem programming revealed by the fackel mutants of Arabidopsis thaliana. Genes Dev. 14, 1485-1497.
27. Jefferson, R.J. (1987) Assaying chimeric genes in plants: the GUS gene fusion systems. Plant Mol. Biol. Rep. 5, 387-405.
28. Kasahara, H., Hanada, A., Kuzuyama, T., Takagi, M., Kamiya, Y. and Yamaguchi, S. (2002) Contribution of the mevalonate and methylerythritol phosphate pathways to the biosynthesis of gibberellins in Arabidopsis. J. Biol. Chem. 277, 45188-45194.
29. Korth, K.L., Stermer, B.A., Bhattacharyya, M.K. and Dixon, R.A. (1997) HMG-CoA reductase gene families that differentially accumulate transcripts in potato tubers are developmentally expressed in floral tissues. Plant Mol. Biol. 33, 545-551.
30. Kushiro, T., Shibuya, M. and Ebizuka, Y. (1998) β-Amyrin synthase. Eur. J. Biochem. 256, 238-244.
31. Laule, O., Fürholz, A., Chang, H.-S., Zhu, T., Wang, X., Heifetz, P.B., Gruissem, W. and Lange, B.M. (2003) Cross-talk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA, 100, 6866-6871.
32. 2-M transition in tobacco BY-2 cells. FEBS Lett. 426, 29-32.
33. Learned, R.M. (1996) Light suppresses 3-hydroxy-3-methylglutaryl coenzyme A reductase gene expression in Arabidopsis thaliana. Plant Physiol. 110, 645-655.
34. Learned, R.M. and Fink, G.R. (1989) 3-Hydroxy-3-methylglutaryl-coenzyme A reductase from Arabidopsis thaliana is structurally distinct from the yeast and animal enzymes. Proc. Natl. Acad. Sci. USA, 86, 2779-2783.
35. Learned, R.M. and Connolly, E.L. (1997) Light modulates the spatial patterns of 3-hydroxy-3-methylglutaryl coenzyme A reductase gene expression in Arabidopsis thaliana. Plant J. 11, 499-511.
36. Lichtenthaler, H.K. (1999) The 1-deoxy-D-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 47-65.
37. Lohman, K.M., Gan, S., John, M.C. and Amasino, R.M. (1994) Molecular analysis of natural leaf senescence in Arabidopsis thaliana. Physiol. Plant. 92, 322-328.
38. Lumbreras, V., Campos, N. and Boronat, A. (1995) The use of an alternative promoter in the Arabidopsis thaliana HMG1 gene generates an mRNA that encodes a novel 3-hydroxy-3-methylglutaryl coenzyme A reductase isoform with an extended N-terminal region. Plant J. 8, 541-549.
39. Mandel, M.A., Feldmann, K.A., Herrera-Estrella, L., Rocha-Sosa, M. and León, P. (1996) CLA1, a novel gene required for chloroplast development, is highly conserved in evolution. Plant J. 9, 649-658.
40. Masferrer, A., Arró, M., Manzano, D., Schaller, H., Fernández-Busquets, X., Moncaleán, P., Fernández, B., Cunillera, N., Boronat, A. and Ferrer, A. (2002) Overexpression of Arabidopsis thaliana farnesyl diphosphate synthase (FPS1S) in transgenic Arabidopsis induces a cell death/senescence-like response and reduced cytokinin levels. Plant J. 30, 123-132.
41. Miyazawa, Y., Kato, H., Muranaka, T. and Yoshida, S. (2002) Amyloplast formation in cultured tobacco BY-2 cells requires a high cytokinin content. Plant Cell Physiol. 43, 1534-1541.
42. Nagata, N., Suzuki, M., Yoshida, S. and Muranaka, T. (2002) Mevalonic acid partially restores chloroplast and etioplast development in Arabidopsis lacking the non-mevalonate pathway. Planta, 216, 345-350.
43. Newman, J.D. and Chappell, J. (1999) Isoprenoid biosynthesis in plants: carbon partitioning within the cytoplasmic pathway. Crit. Rev. Biochem. Mol. Biol. 34, 95-106.
44. Ori, N., Juarez, M.T., Jackson, D., Yamaguchi, J., Banowetz, G.M. and Hake, S. (1999) Leaf senescence is delayed in tobacco plants expressing the maize homeobox gene knotted1 under the control of a senescence-activated promoter. Plant Cell, 11, 1073-1080.
45. Piffanelli, P. and Murphy, D.J. (1998) Novel organelles and targeting mechanisms in the anther tapetum. Trends Plant Sci. 3, 250-253.
46. Porat, R., Lu, P. and O'Neil, S.D. (1998) Arabidopsis SKP1, a homologue of a cell cycle regulator gene, is predominantly expressed in meristematic cells. Planta, 204, 345-351.
47. Re, E.B., Jones, D. and Learned, R.M. (1995) Co-expression of native and introduced genes reveals cryptic regulation of HMG CoA reductase expression in Arabidopsis. Plant J. 7, 771-784.
48. Rodríguez-Conceptión, M. and Boronat, A. (2002) Elucidation of methylerythritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastids. A metabolic milestone achieved through genomics. Plant Physiol. 130, 1079-1089.
49. Schaeffer, A., Bronner, R., Benveniste, P. and Schaller, H. (2001) The ratio of campesterol to sitosterol that modulates growth in Arabidopsis is controlled by STEROL METHYLTRANSFERASE 2;1. Plant J. 25, 605-615.
50. Schrick, K., Mayer, U., Horrichs, A., Kuhnt, C., Bellini, C., Dangl, J., Schmidt J. and Jürgens. G. (2000) FACKEL is a sterol C-14 reductase required for organized cell division and expansion in Arabidopsis embryogenesis. Genes Dev. 14, 1471-1484.
51. Segura, M.J.R., Meyer, M.M. and Matsuda, S.P.T. (2000) Arabidopsis thaliana LUP1 converts oxidosqualene to multiple triterpene alcohols and a triterpene diol. Orga. L. 2, 2257-2259.
52. Sekimata, K., Kimura, T., Kaneko, I., Nakano, T., Yoneyama, K., Takeuchi, Y., Yoshida, S. and Asami, T. (2001) A specific brrasinosteroid biosynthesis inhibitor, Brz2001: evaluation of its effects on Arabidopsis, cress, tobacco, and rice. Planta, 213, 716-721.
53. Shibuya, M., Zhang, H., Endo, A., Shishikura, K., Kushiro, T. and Ebizuka, Y. (1999) Two branches of the lupeol synthase gene in the molecular evolution of plant oxidosqualene cyclases. Eur. J. Biochem. 266, 302-307.
54. Souter, M., Topping, J., Pullen, M., Friml, J., Palme, K., Hackett, R., Grierson, D. and Lindsey, K. (2002) Hydra mutants of Arabidopsis are defective in sterol profiles and auxin and ethylene signaling. Plant Cell, 14, 1017-1031.
55. Sugden, C., Donaghy, P.G., Halford, N.G. and Hardie, D.G. (1999) Two SNF1-related protein kinases from spinach leaf phosphorylate and inactivate 3-hydroxy-3-methylglutaryl-coenzyme A reductase, nitrate reductase, and sucrose phosphate synthase in vitro. Plant Physiol. 120, 257-274.
56. Suzuki, M., Nagata, N., Kamide, Y., Yoshida, S. and Muranaka, T. (2003) The study of the mechanism of cell elongation using an inhibitor of 3-hydroxy-3-methylglutaryl-CoA reductase. In Advanced Research on Plant Lipids (Murata, N., Yamada, M., Nishida, I., Okuyama, H., Sekiya, J. and Wada, H., eds). Dordrecht: Kluwer Academic Publishers, pp. 249-252.
57. Weaver, L.M., Gan, S., Quirino, B. and Amasino, R.M. (1998) A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment. Plant Mol. Biol. 37, 455-469.
58. Willemsen, V., Friml, J., Grebe, M., Toorn, A.V.D., Palme, K. and Scheres, B. (2003) Cell polarity and PIN protein positioning in Arabidopsis require STEROL METHYLTRANSFERASE1 function. Plant Cell, 15, 612-625.
59. Worters-Arts, M., Lush, W.M. and Mariani, C. (1998) Lipids are required for directional pollen-tube growth. Nature, 392, 818-821.
60. Yokoyama, R. and Nishitani, K. (2001) A comprehensive expression analysis of all members of a gene family encoding cell-wall enzymes allowed us to predict cis-regulatory regions involved in cell-wall construction in specific organs of Arabidopsis. Plant Cell Physiol. 42, 1025-1033.