Reverse genetic characterization of two paralogous acetoacetyl CoA thiolase genes in Arabidopsis reveals their importance in plant growth and development

Plant Journal

Volumn 70, Issue 6, 2012, Pages 1015-1032

  Jin, Huanan ^a   Song, Zhihong ^a,b   Nikolau, Basil J ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b U S DEPARTMENT OF ENERGY   (United States)

Author keywords

acetoacetyl CoA thiolases; Arabidopsis thaliana; embryo lethality; mevalonate pathway; phytosterol; pleiotropic phenotypes

Indexed keywords

ACETOACETYL COA THIOLASES; ARABIDOPSIS THALIANA; EMBRYO LETHALITY; MEVALONATE PATHWAY; PHYTOSTEROL; PLEIOTROPIC PHENOTYPES;

CARDIOVASCULAR SYSTEM; GENE EXPRESSION; GROWTH KINETICS;

PLANTS (BOTANY);

ACETYL COENZYME A ACETYLTRANSFERASE; ARABIDOPSIS PROTEIN; BACTERIAL DNA; T DNA; T-DNA;

ARABIDOPSIS; ARTICLE; ESSENTIAL GENE; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; RNA INTERFERENCE;

ACETYL-COA C-ACETYLTRANSFERASE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; DNA, BACTERIAL; GENE EXPRESSION REGULATION, PLANT; GENES, ESSENTIAL; GENETIC COMPLEMENTATION TEST; MUTAGENESIS, INSERTIONAL; RNA INTERFERENCE;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84862171951     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2012.04942.x     Document Type: Article

References (71)

1. Alexander, M.P., (1969) Differential staining of aborted and nonaborted pollen. Stain Technol. 44, 117-122.
2. Anderson, A.J., and, Dawes, E.A., (1990) Occurrence, metabolism, metabolic role, and industrial uses of bacterial polyhydroxyalkanoates. Microbiol. Rev. 54, 450-472. (Pubitemid 120004382)
3. Arigoni, D., Sagner, S., Latzel, C., Eisenreich, W., Bacher, A., and, Zenk, M.H., (1997) Terpenoid biosynthesis from 1-deoxy-d-xylulose in higher plants by intramolecular skeletal rearrangement. Proc. Natl Acad. Sci. USA, 94, 10600-10605. (Pubitemid 27430780)
4. Bais, P., Moon, S.M., He, K., et al. (2010) PlantMetabolomics.org: a web portal for plant metabolomics experiments. Plant Physiol. 152, 1807-1816.
5. Bonaventure, G., Beisson, F., Ohlrogge, J., and, Pollard, M., (2004) Analysis of the aliphatic monomer composition of polyesters associated with Arabidopsis epidermis: occurrence of octadeca-cis-6,cis-9-diene-1,18-dioate as the major component. Plant J. 40, 920-930. (Pubitemid 40047631)
6. Bouvier, F., Rahier, A., and, Camara, B., (2005) Biogenesis, molecular regulation and function of plant isoprenoids. Prog. Lipid Res. 44, 357-429. (Pubitemid 41608703)
7. Carland, F., Fujioka, S., and, Nelson, T., (2010) The sterol methyltransferases SMT1, SMT2, and SMT3 influence Arabidopsis development through nonbrassinosteroid products. Plant Physiol. 153, 741-756.
8. Carrie, C., Murcha, M.W., Millar, A.H., Smith, S.M., and, Whelan, J., (2007) Nine 3-ketoacyl-CoA thiolases (KATs) and acetoacetyl-CoA thiolases (ACATs) encoded by five genes in Arabidopsis thaliana are targeted either to peroxisomes or cytosol but not to mitochondria. Plant Mol. Biol. 63, 97-108. (Pubitemid 44950235)
9. Che, P., Wurtele, E.S., and, Nikolau, B.J., (2002) Metabolic and environmental regulation of 3-methylcrotonyl-coenzyme A carboxylase expression in Arabidopsis. Plant Physiol. 129, 625-637. (Pubitemid 34689151)
10. 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.
11. Cunillera, N., Arro, M., Delourme, D., Karst, F., Boronat, A., and, Ferrer, A., (1996) Arabidopsis thaliana contains two differentially expressed farnesyl-diphosphate synthase genes. J. Biol. Chem. 271, 7774-7780.
12. Cunillera, N., Boronat, A., and, Ferrer, A., (1997) The Arabidopsis thaliana FPS1 gene generates a novel mRNA that encodes a mitochondrial farnesyl-diphosphate synthase isoform. J. Biol. Chem. 272, 15381-15388. (Pubitemid 27255562)
13. Cunillera, N., Boronat, A., and, Ferrer, A., (2000) Spatial and temporal patterns of GUS expression directed by 5' regions of the Arabidopsis thaliana farnesyl diphosphate synthase genes FPS1 and FPS2. Plant Mol. Biol. 44, 747-758. (Pubitemid 32100057)
14. De-Eknamkul, W., and, Potduang, B., (2003) Biosynthesis of β-sitosterol and stigmasterol in Croton sublyratus proceeds via a mixed origin of isoprene units. Phytochemistry, 62, 389-398. (Pubitemid 36168941)
15. 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. (Pubitemid 30458033)
16. Dyer, J.H., Maina, A., Gomez, I.D., Cadet, M., Oeljeklaus, S., and, Schiedel, A.C., (2009) Cloning, expression and purification of an acetoacetyl CoA thiolase from sunflower cotyledon. Int. J. Biol. Sci. 5, 736-744.
17. Enjuto, M., Balcells, L., Campos, N., Caelles, C., Arro, 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.
18. 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.
19. Fatland, B.L., Ke, J., Anderson, M.D., Mentzen, W.I., Cui, L.W., Allred, C.C., Johnston, J.L., Nikolau, B.J., and, Wurtele, E.S., (2002) Molecular characterization of a heteromeric ATP-citrate lyase that generates cytosolic acetyl-coenzyme A in Arabidopsis. Plant Physiol. 130, 740-756. (Pubitemid 35235286)
20. Fatland, B.L., Nikolau, B.J., and, Wurtele, E.S., (2005) Reverse genetic characterization of cytosolic acetyl-CoA generation by ATP-citrate lyase in Arabidopsis. Plant Cell, 17, 182-203. (Pubitemid 41672996)
21. 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. (Pubitemid 28174068)
22. Germain, V., Rylott, E.L., Larson, T.R., Sherson, S.M., Bechtold, N., Carde, J.P., Bryce, J.H., Graham, I.A., and, Smith, S.M., (2001) Requirement for 3-ketoacyl-CoA thiolase-2 in peroxisome development, fatty acid β-oxidation and breakdown of triacylglycerol in lipid bodies of Arabidopsis seedlings. Plant J. 28, 1-12. (Pubitemid 33011505)
23. Hernandez-Pinzon, I., Ross, J.H., 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.
24. Hilson, P., Allemeersch, J., Altmann, T., et al. (2004) Versatile gene-specific sequence tags for Arabidopsis functional genomics: transcript profiling and reverse genetics applications. Genome Res. 14, 2176-2189. (Pubitemid 39440201)
25. Hiser, L., Basson, M.E., and, Rine, J., (1994) ERG10 from Saccharomyces cerevisiae encodes acetoacetyl-CoA thiolase. J. Biol. Chem. 269, 31383-31389. (Pubitemid 24379490)
26. Hsieh, M.H., and, Goodman, H.M., (2005) The Arabidopsis IspH homolog is involved in the plastid nonmevalonate pathway of isoprenoid biosynthesis. Plant Physiol. 138, 641-653. (Pubitemid 43793147)
27. Igual, J.C., Gonzalez-Bosch, C., Dopazo, J., and, Perez-Ortin, J.E., (1992) Phylogenetic analysis of the thiolase family. Implications for the evolutionary origin of peroxisomes. J. Mol. Evol. 35, 147-155.
28. Ishiguro, S., Nishimori, Y., Yamada, M., Saito, H., Suzuki, T., Nakagawa, T., Miyake, H., Okada, K., and, Nakamura, K., (2010) The Arabidopsis FLAKY POLLEN1 gene encodes a 3-hydroxy-3-methylglutaryl-coenzyme A synthase required for development of tapetum-specific organelles and fertility of pollen grains. Plant Cell Physiol. 51, 896-911.
29. 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. (Pubitemid 30421841)
30. Jefferson, R.A., (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol. Biol. Rep. 5, 387-405.
31. Karimi, M., De Meyer, B., and, Hilson, P., (2005) Modular cloning in plant cells. Trends Plant Sci. 10, 103-105. (Pubitemid 40323292)
32. 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. (Pubitemid 36159122)
33. Kasahara, H., Takei, K., Ueda, N., Hishiyama, S., Yamaya, T., Kamiya, Y., Yamaguchi, S., and, Sakakibara, H., (2004) Distinct isoprenoid origins of cis- and trans-zeatin biosyntheses in Arabidopsis. J. Biol. Chem. 279, 14049-14054. (Pubitemid 38468940)
34. Kolattukudy, P.E., (2001) Polyesters in higher plants. Adv. Biochem. Eng. Biotechnol. 71, 1-49.
35. Lalanne, E., Honys, D., Johnson, A., Borner, G.H., Lilley, K.S., Dupree, P., Grossniklaus, U., and, Twell, D., (2004) SETH1 and SETH2, two components of the glycosylphosphatidylinositol anchor biosynthetic pathway, are required for pollen germination and tube growth in Arabidopsis. Plant Cell, 16, 229-240. (Pubitemid 38162365)
36. Lange, B.M., and, Ghassemian, M., (2003) Genome organization in Arabidopsis thaliana: a survey for genes involved in isoprenoid and chlorophyll metabolism. Plant Mol. Biol. 51, 925-948. (Pubitemid 36579709)
37. Lange, B.M., Rujan, T., Martin, W., and, Croteau, R., (2000) Isoprenoid biosynthesis: the evolution of two ancient and distinct pathways across genomes. Proc. Natl Acad. Sci. USA, 97, 13172-13177.
38. Laule, O., Furholz, A., Chang, H.S., Zhu, T., Wang, X., Heifetz, P.B., Gruissem, W., and, Lange, M., (2003) Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 100, 6866-6871. (Pubitemid 36666671)
39. Li, X., Ilarslan, H., Brachova, L., Qian, H.R., Li, L., Che, P., Wurtele, E.S., and, Nikolau, B.J., (2011) Reverse-genetic analysis of the two biotin-containing subunit genes of the heteromeric acetyl-coenzyme A carboxylase in Arabidopsis indicates a unidirectional functional redundancy. Plant Physiol. 155, 293-314.
40. Lluch, M.A., Masferrer, A., Arro, M., Boronat, A., and, Ferrer, A., (2000) Molecular cloning and expression analysis of the mevalonate kinase gene from Arabidopsis thaliana. Plant Mol. Biol. 42, 365-376. (Pubitemid 30213414)
41. 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.
42. Meinke, D.W., (1982) Embryo-lethal mutants of Arabidopsis thaliana: evidence for gametophytic expression of the mutant genes. Theor. Appl. Genet. 63, 381-386.
43. Middleton, B., (1974) The kinetic mechanism and properties of the cytoplasmic acetoacetyl-coenzyme A thiolase from rat liver. Biochem J. 139, 109-121.
44. 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. (Pubitemid 29226500)
45. Noguchi, T., Fujioka, S., Takatsuto, S., Sakurai, A., Yoshida, S., Li, J., and, Chory, J., (1999) Arabidopsis det2 is defective in the conversion of (24R)-24-methylcholest-4-en-3-one to (24R)-24-methyl-5α-cholestan-3-one in brassinosteroid biosynthesis. Plant Physiol. 120, 833-840.
46. Oliver, D.J., Nikolau, B.J., and, Wurtele, E.S., (2009) Acetyl-CoA-life at the metabolic nexus. Plant Sci. 176, 597-601.
47. Pereto, J., Lopez-Garcia, P., and, Moreira, D., (2005) Phylogenetic analysis of eukaryotic thiolases suggests multiple proteobacterial origins. J. Mol. Evol. 61, 65-74. (Pubitemid 41188510)
48. Phillips, M.A., D'Auria, J.C., Gershenzon, J., and, Pichersky, E., (2008) The Arabidopsis thaliana type I isopentenyl diphosphate isomerases are targeted to multiple subcellular compartments and have overlapping functions in isoprenoid biosynthesis. Plant Cell, 20, 677-696. (Pubitemid 352844001)
49. Piffanelli, P., and, Murphy, D.J., (1998) Novel organelles and targeting mechanisms in the anther tapetum. Trends Plant Sci. 3, 250-253. (Pubitemid 28338425)
50. Piffanelli, P., Ross, J., and, Murphy, D.J., (1998) Biogenesis and function of the lipidic structures of pollen grains. Sex. Plant Reprod. 11, 65-80. (Pubitemid 28278548)
51. Reumann, S., Babujee, L., Ma, C., Wienkoop, S., Siemsen, T., Antonicelli, G.E., Rasche, N., Luder, F., Weckwerth, W., and, Jahn, O., (2007) Proteome analysis of Arabidopsis leaf peroxisomes reveals novel targeting peptides, metabolic pathways, and defense mechanisms. Plant Cell, 19, 3170-3193. (Pubitemid 350276719)
52. Riefler, M., Novak, O., Strnad, M., and, Schmulling, T., (2006) Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell, 18, 40-54. (Pubitemid 43951314)
53. Rodriguez-Concepcion, M., and, Boronat, A., (2002) Elucidation of the methylerythritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastids. A metabolic milestone achieved through genomics. Plant Physiol. 130, 1079-1089. (Pubitemid 35352936)
54. Sando, T., Takaoka, C., Mukai, Y., Yamashita, A., Hattori, M., Ogasawara, N., Fukusaki, E., and, Kobayashi, A., (2008) Cloning and characterization of mevalonate pathway genes in a natural rubber producing plant, Hevea brasiliensis. Biosci. Biotechnol. Biochem. 72, 2049-2060.
55. Sapir-Mir, M., Mett, A., Belausov, E., Tal-Meshulam, S., Frydman, A., Gidoni, D., and, Eyal, Y., (2008) Peroxisomal localization of Arabidopsis isopentenyl diphosphate isomerases suggests that part of the plant isoprenoid mevalonic acid pathway is compartmentalized to peroxisomes. Plant Physiol. 148, 1219-1228. (Pubitemid 352847484)
56. 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. (Pubitemid 32406376)
57. Schrick, K., Mayer, U., Horrichs, A., Kuhnt, C., Bellini, C., Dangl, J., Schmidt, J., and, Jurgens, G., (2000) FACKEL is a sterol C-14 reductase required for organized cell division and expansion in Arabidopsis embryogenesis. Genes Dev. 14, 1471-1484. (Pubitemid 30421840)
58. Smyth, D.R., Bowman, J.L., and, Meyerowitz, E.M., (1990) Early flower development in Arabidopsis. Plant Cell, 2, 755-767. (Pubitemid 120015483)
59. 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. (Pubitemid 34609214)
60. Sperling, P., and, Heinz, E., (2003) Plant sphingolipids: structural diversity, biosynthesis, first genes and functions. Biochim. Biophys. Acta, 1632, 1-15. (Pubitemid 36628111)
61. Suzuki, M., Kamide, Y., Nagata, N., et al. (2004) 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 J. 37, 750-761. (Pubitemid 38300519)
62. Suzuki, M., Nakagawa, S., Kamide, Y., Kobayashi, K., Ohyama, K., Hashinokuchi, H., Kiuchi, R., Saito, K., Muranaka, T., and, Nagata, N., (2009) Complete blockage of the mevalonate pathway results in male gametophyte lethality. J. Exp. Bot. 60, 2055-2064.
63. Thompson, S.L., and, Krisans, S.K., (1990) Rat liver peroxisomes catalyze the initial step in cholesterol synthesis. The condensation of acetyl-CoA units into acetoacetyl-CoA. J. Biol. Chem. 265, 5731-5735.
64. Tzafrir, I., Pena-Muralla, R., Dickerman, A., et al. (2004) Identification of genes required for embryo development in Arabidopsis. Plant Physiol. 135, 1206-1220. (Pubitemid 39009371)
65. Werner, T., Motyka, V., Strnad, M., and, Schmulling, T., (2001) Regulation of plant growth by cytokinin. Proc. Natl Acad. Sci. USA, 98, 10487-10492. (Pubitemid 32803046)
66. Wilson, Z.A., Morroll, S.M., Dawson, J., Swarup, R., and, Tighe, P.J., (2001) The Arabidopsis MALE STERILITY1 (MS1) gene is a transcriptional regulator of male gametogenesis, with homology to the PHD-finger family of transcription factors. Plant J. 28, 27-39. (Pubitemid 33011507)
67. Winzeler, E.A., Shoemaker, D.D., Astromoff, A., et al. (1999) Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science, 285, 901-906. (Pubitemid 29381993)
68. Withers, S.T., and, Keasling, J.D., (2007) Biosynthesis and engineering of isoprenoid small molecules. Appl. Microbiol. Biotechnol. 73, 980-990. (Pubitemid 44974305)
69. Wu, S.S., Moreau, R.A., Whitaker, B.D., and, Huang, A.H., (1999) Steryl esters in the elaioplasts of the tapetum in developing Brassica anthers and their recovery on the pollen surface. Lipids, 34, 517-523. (Pubitemid 29262597)
70. Zhang, H., Ohyama, K., Boudet, J., Chen, Z., Yang, J., Zhang, M., Muranaka, T., Maurel, C., Zhu, J.K., and, Gong, Z., (2008) Dolichol biosynthesis and its effects on the unfolded protein response and abiotic stress resistance in Arabidopsis. Plant Cell, 20, 1879-1898. (Pubitemid 352844539)
71. Ziegelhoffer, E.C., Medrano, L.J., and, Meyerowitz, E.M., (2000) Cloning of the Arabidopsis WIGGUM gene identifies a role for farnesylation in meristem development. Proc. Natl Acad. Sci. USA, 97, 7633-7638. (Pubitemid 30431515)