Engineering cytoplasmic male sterility via the chloroplast genome by expression of β-ketothiolase

Plant Physiology

Volumn 138, Issue 3, 2005, Pages 1232-1246

  Ruiz, Oscar N ^a,b   Daniell, Henry ^a  

^a UNIVERSITY OF CENTRAL FLORIDA   (United States)

^b MIDWEST RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYMES; GENES; MORPHOLOGY; SCANNING ELECTRON MICROSCOPY; SEED; TISSUE;

ANTHERS; CHLOROPLAST GENOME; LIGHT REGULATION; PHAA GENE;

PLANTS (BOTANY);

CHLOROPHYLLS; ENZYMES; GENES; PLANT TISSUES; PLANTS; PLASTIDS;

ENDOTHECIUM;

ACETYL COENZYME A ACYLTRANSFERASE;

ACINETOBACTER; ARTICLE; CHLOROPLAST; CYTOPLASM; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GENOME; MOLECULAR CLONING; PHYSIOLOGY; REPRODUCTION; TRANSGENIC PLANT;

ACETYL-COA C-ACYLTRANSFERASE; ACINETOBACTER; CHLOROPLASTS; CLONING, MOLECULAR; CYTOPLASM; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; GENOME, PLANT; PLANTS, GENETICALLY MODIFIED; REPRODUCTION; TRANSCRIPTION, GENETIC;

EID: 27244443586     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.104.057729     Document Type: Article

References (76)

1. Ariizumi T, Hatakeyama K, Hinata K, Inatsugi R, Nishida I, Sato S, Kato T, Tabata S, Toriyama K (2004) Disruption of the novel plant protein NEF1 affects lipid accumulation in the plastids of the tapetum and exine formation of pollen, resulting in male sterility in Arabidopsis thaliana. Plant J 39: 170-181
2. Bateson W, Gairdner AE (1921) Male sterility in flax subject to two types of segregation. J Genet 11: 269-275
3. Bentolila S, Alfonso AA, Hanson MR (2002) A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proc Natl Acad Sci USA 99: 10887-10892
4. Bohmert K, Balbo I, Kopka J, Mittendorf V, Nawrath C, Poirier Y, Tischendorf G, Trethewey RN, Willmitzer L (2000) Transgenic Arabidopsis plants can accumulate polyhydroxybutyrate to up to 4% of their fresh weight. Planta 211: 841-845
5. Bohmert K, Balbo I, Steinbuchel A, Tischendorf G, Willmitzer L (2002) Constitutive expression of the beta-ketothiolase gene in transgenic plants. A major obstacle for obtaining polyhydroxybutyrate-producing plants. Plant Physiol 128: 1282-1290
6. Chebolu S, Daniell H (2005) Chloroplast derived vaccine antigens and biopharmaceuticals: expression, folding, assembly and functionality. Curr Trends Microbiol Immunol (in press)
7. Chittenden RJ, Pellow CA (1927) A suggested interpretation of certain cases of anisogeny. Nature 119: 10-12
8. Cui X, Wise RP, Schnable PS (1996) The rf2 nuclear restorer gene of male-sterile T-cytoplasm maize. Science 272: 1334-1336
9. Daniell H (1997) Transformation and foreign gene expression in plants mediated by microprojectile bombardment. Methods Mol Biol 62: 453-488
10. Daniell H (2002) Molecular strategies for gene containment in transgenic crops. Nat Biotechnol 20: 581-586
11. Daniell H (2004) Medical molecular pharming: therapeutic recombinant antibodies, biopharmaceuticals, and edible vaccines in transgenic plants engineered via the chloroplast genome. In RM Goodman, ed, Encyclopedia of Plant and Crop Science. Marcel Decker, New York, pp 704-710
12. Daniell H, Carmona-Sanchez O, Burns B (2004b) Chloroplast derived antibodies, biopharmaceuticals and edible vaccines. In S Schillberg, ed, Molecular Farming. Wiley-VCH Verlag, Weinheim, Germany, Chapter 8, pp 113-133
13. Daniell H, Chebolu S, Kumar S, Singleton M, Falconer R (2005a) Chloroplast-derived vaccine antigens and other therapeutic proteins. Vaccine 23: 1779-1783
14. Daniell H, Cohill PR, Kumar S, Dufourmantel N, Dubald M (2004c) Chloroplast genetic engineering. In H Daniell, C Chase, eds, Molecular Biology and Biotechnology of Plant Organelles. Springer Publishers, Dordrecht, The Netherlands, pp 443-490
15. Daniell H, Datta R, Varma S, Gray S, Lee SB (1998) Containment of herbicide resistance through genetic engineering of the chloroplast genome. Nat Biotechnol 16: 345-348
16. Daniell H, Dhingra A (2002) Multigene engineering: dawn of an exciting new era in biotechnology. Curr Opin Biotechnol 13: 136-141
17. Daniell H, Khan MS, Allison L (2002) Milestones in chloroplast genetic engineering: an environmentally friendly era in biotechnology. Trends Plant Sci 7: 84-91
18. Daniell H, Kumar S, Dufourmantel N (2005b) Breakthrough in chloroplast genetic engineering of agronomically important crops. Trends Biotechnol 23: 238-245
19. Daniell H, Lee SB, Panchal T, Weibe PO (2001a) Expression of the native cholera toxin B subunit gene and assembly as functional oligomers in transgenic chloroplasts. J Mol Biol 311: 1001-1009
20. Daniell H, Muthukumar B, Lee SB (2001b) Marker free transgenic plants: engineering the chloroplast genome without the use of antibiotic selection. Curr Genet 39: 109-116
21. Daniell H, Ruiz ON, Dhingra A (2004a) Chloroplast genetic engineering to improve agronomic traits. Methods Mol Biol 286: 111-137
22. Davis JT, Moore RN, Imperiali B, Pratt AJ, Kobayashi K, Masamune S, Sinskey AJ, Walsh CT (1987) Biosynthetic thiolase from Zoogloea ramigera. J Biol Chem 262: 82-89
23. De Cosa B, Moar W, Lee SB, Miller M, Daniell H (2001) Overexpression of the Bt cry2Aa2 operon in chloroplasts leads to formation of insecticidal crystals. Nat Biotechnol 19: 71-74
24. DeGray G, Rajasekaran K, Smith F, Sanford J, Daniell H (2001) Expression of an antimicrobial peptide via the chloroplast genome to control phytopathogenic bacteria and fungi. Plant Physiol 127: 852-862
25. Delourme R, Foisset N, Horvais R, Barret P, Champagne G, Cheung WY, Landry BS, Renard M (1998) Characterisation of the radish introgression carrying the Rfo restorer gene for Ogu-INRA cytoplasmic male sterility in rapeseed (Brassica napus L.). Theor Appl Genet 97: 129-134
26. Dhingra A, Daniell H (2005) Chloroplast genetic engineering via organogenesis or somatic embryogenesis. In J Sanchez-Serano, ed, Arabidopsis Protocols II. Humana Press, Totowa, NJ (in press)
27. Dhingra A, Portis AR Jr, Daniell H (2004) Enhanced translation of a chloroplast-expressed RbcS gene restores small subunit levels and photosynthesis in nuclear RbcS antisense plants. Proc Natl Acad Sci USA 101: 6315-6320
28. Dufourmantel N, Pelissier B, Garçon F, Peltier JM, Tissot G (2004) Generation of fertile transplastomic soybean. Plant Mol Biol 55: 479-489
29. Eibl C, Zou Z, Beck A, Kim M, Mullet J, Koop HU (1999) In vivo analysis of plastid psbA, rbcL and rp132 UTR elements by chloroplast transformation: tobacco plastid gene expression is controlled by modulation of transcript levels and translation efficiency. Plant J 19: 333-345
30. Fatland BL, Ke J, Anderson MD, Mentzen WI, Cui LW, Allred CC, Johnston JL, Nikolau BJ, Wurtele ES (2002) Molecular characterization of a heteromeric ATP-citrate lyase that generates cytosolic acetyl-coenzyme A in Arabidopsis. Plant Physiol 130: 740-756
31. Fernandez-San Millan A, Mingo-Castel A, Miller M, Daniell H (2003) A chloroplast transgenic approach to hyper-express and purify human serum albumin, a protein highly susceptible to proteolytic degradation. Plant Biotechnol J 1: 71-79
32. Goetz M, Godt DE, Guivarc'h A, Kahmann U, Chriqui D, Roitsch T (2001) Induction of male sterility in plants by metabolic engineering of the carbohydrate supply. Proc Natl Acad Sci USA 98: 6522-6527
33. Guda C, Lee SB, Daniell H (2000) Stable expression of biodegradable protein based polymer in tobacco chloroplasts. Plant Cell Rep 19: 257-262
34. Hagemann R (1992) Plastid genetics in higher plants. In RG Herrmann, ed, Cell Organelles. Springer-Verlag, New York, pp 65-96
35. Hagemann R (2004) The sexual inheritance of plant organelles. In H Daniell, C Chase, eds, Molecular Biology and Biotechnology of Plant Organelles. Springer Publisher, Dordrecht, The Netherlands, pp 87-108
36. Havey MJ (2004) The use of cytoplasmic male sterility for hybrid seed production. In H Daniell, C Chase, eds, Molecular Biology and Biotechnology of Plant Organelles. Springer Publisher, Dordrecht, The Netherlands, pp 617-628
37. Hernould M, Suharsono S, Litvak S, Araya A, Mouras A (1993) Male-sterility induction in transgenic tobacco plants with an unedited atp9 mitochondrial gene from wheat. Proc Natl Acad Sci USA 90: 2370-2374
38. Hernould M, Suharsono S, Zabaleta E, Carde JP, Litvak S, Araya A, Mouras A (1998) Impairment of tapetum and mitochondria in engineered male-sterile tobacco plants. Plant Mol Biol 36: 499-508
39. Jones H, Clarke A (1943) Inheritance of male sterility in the onion and the production of hybrid seed. Proc Am Soc Hortic Sci 43: 189-194
40. Koizuka N, Imai R, Fujimoto H, Hayakawa T, Kimura Y, Kohno-Murase J, Sakai T, Kawasaki S, Imamura J (2003) Genetic characterization of a pentatricopeptide repeat protein gene, orf687, that restores fertility in the cytoplasmic male-sterile Kosena radish. Plant J 34: 407-415
41. Koltunow AM, Truettner J, Cox KH, Wallroth M, Goldberg RB (1990) Different temporal and spatial gene expression patterns occur during anther development. Plant Cell 2: 1201-1224
42. Kota M, Daniell H, Varma S, Garczynski SF, Gould F, William MJ (1999) Overexpression of the Bacillus thuringiensis (Bt) Cry2Aa2 protein in chloroplasts confers resistance to plants against susceptible and Bt-resistant insects. Proc Natl Acad Sci USA 96: 1840-1845
43. Kozaki A, Kamada K, Nagano Y, Iguchi H, Sasaki Y (2000) Recombinant carboxyltransferase responsive to redox of pea plastidic acetyl-CoA carboxylase. J Biol Chem 275: 10702-10708
44. Kriete G, Niehaus K, Perlick AM, Puhler A, Broer I (1996) Male sterility in transgenic tobacco plants induced by tapetum-specific deacetylation of the externally applied non-toxic compound N-acetyl-L-phosphinothricin. Plant J 9: 809-818
45. Kumar S, Daniell H (2004) Engineering the chloroplast genome for hyperexpression of human therapeutic proteins and vaccine antigens. Methods Mol Biol 267: 365-383
46. Kumar S, Dhingra A, Daniell H (2004a) Plastid-expressed betaine aldehyde dehydrogenase gene in carrot cultured cells, roots, and leaves confers enhanced salt tolerance. Plant Physiol 136: 2843-2854
47. Kumar S, Dhingra A, Daniell H (2004b) Manipulation of gene expression facilitates cotton plastid transformation by somatic embryogenesis and maternal inheritance of transgenes. Plant Mol Biol 56: 203-216
48. Lee SB, Kwon HB, Kwon SJ, Park SC, Jeong MJ, Han SE, Byun MO, Daniell H (2003) Accumulation of trehalose within transgenic chloroplasts confers drought tolerance. Mol Breed 11: 1-13
49. Leelavathi S, Gupta N, Maiti S, Ghosh A, Reddy VS (2003) Overproduction of an alkali and thermostable xylanase in tobacco chloroplasts and efficient recovery of the enzyme. Mol Breed 11: 59-67
50. Leelavathi S, Reddy VS (2003) Chloroplast expression of His-tagged GUS-fusions: a general strategy to overproduce and purify foreign proteins using transplastomic plants as bioreactors. Mol Breed 11: 49-58
51. Liu F, Cui X, Horner HT, Weiner H, Schable PS (2001) Mitochondrial aldehyde dehydrogenase activity is required for male fertility in maize. Plant Cell 13: 1063-1078
52. Lossl A, Eibl C, Harlotf HJ, Jung C, Koop HU (2003) Polyester synthesis in transplastomic tobacco (Nicotiana tabacum L.): significant contents of polyhydroxybutyrate are associated with growth reduction. Plant Cell Rep 21: 891-899
53. Mariani C, De Beuckeleer M, Truettner J, Leemans J, Goldberg RB (1990) Induction of male-sterility in plants by a chimeric ribonuclease gene. Nature 347: 737-741
54. McBride KE, Svab Z, Schaaf DJ, Hogan PS, Stalker DM, Maliga P (1995) Amplification of a chimeric Bacillus gene in chloroplasts leads to an extraordinary level of an insecticidal protein in tobacco. Biotechnology (N Y) 13: 362-365
55. Molina A, Herva-Stubbs S, Daniell H, Mingo-Castel AM, Veramendi J (2004) High yield expression of a viral peptide animal vaccine in transgenic tobacco chloroplasts. Plant Biotechnol 2: 141-153
56. Monde RA, Greene JC, Stern DB (2000) The sequence and secondary structure of the 3′-UTR affect 3′-end maturation, RNA accumulation, and translation in tobacco chloroplasts. Plant Mol Biol 44: 529-542
57. Napoli CA, Fahy D, Wang HY, Taylor LP (1999) White anther: a petunia mutant that abolishes pollen flavonol accumulation, induces male sterility, and is complemented by a chalcone synthase transgene. Plant Physiol 120: 615-622
58. Nawrath C, Porier Y, Somerville C (1994) Targeting of the polyhydroxybutyrate biosynthetic pathway to the plastids of Arabidopsis thaliana result in high levels of polymer accumulation. Proc Natl Acad Sci USA 91: 12760-12764
59. Nikolau BJ, Oliver DJ, Schnable PS, Wurtele ES (2000) Molecular biology of acetyl-CoA metabolism. Biochem Soc Trans 28: 591-593
60. Page RA, Okada S, Harwood JL (1994) Acetyl-CoA carboxylase exerts strong flux control over lipid synthesis in plants. Biochim Biophys Acta 1210: 369-372
61. Perez-Prat E, van Lookeren Campagne MM (2002) Hybrid seed production and the challenge of propagating male sterile plants. Trends Plant Sci 7: 199-203
62. Poirier Y, Dennis DE, Klomparens K, Somerville C (1992) Polyhydroxybutyrate, a biodegradable thermoplastic in transgenic plants. Science 256: 520-523
63. Post-Beittenmiller D, Jaworski JG, Ohlrogge JB (1991) In vivo pools of free and acylated acyl carrier proteins in spinach. Evidence for sites of regulation of fatty acid biosynthesis. J Biol Chem 266: 1858-1865
64. Rawsthorne S (2002) Carbon flux and fatty acid synthesis in plants. Prog Lipid Res 41: 182-196
65. Ruiz ON, Hussein H, Terry N, Daniell H (2003) Phytoremediation of organomercurial compounds via chloroplast genetic engineering. Plant Physiol 132: 1344-1352
66. Schnurr JA, Shockey JM, de Boer GJ, Browse JA (2002) Fatty acid export from the chloroplast. Molecular characterization of a major plastidial acyl-coenzyme A synthetase from Arabidopsis. Plant Physiol 129: 1700-1709
67. Schuster G, Gruissem W (1991) Chloroplast mRNA 3′ end processing requires a nuclear-encoded RNA-binding protein. EMBO J 10: 1493-1502
68. Senior PJ, Dawes EA (1973) The regulation of poly-beta-hydroxybutyrate metabolism in Azotobacter beijerinckii. Biochem J 134: 225-238
69. Smith B, Crowther T (1995) Inbreeding depression and single cross hybrids in leeks (Allium ampeloprasum ssp. porrum). Euphytica 86: 87-94
70. Staub JM, Garcia B, Graves J, Hajdukiewicz PTJ, Hunter P, Nehra N, Paradkar V, Schlittler M, Carroll JA, Spatola L, et al (2000) High-yield production of a human therapeutic protein in tobacco chloroplasts. Nat Biotechnol 18: 333-338
71. Sugita M, Sugiura M (1996) Regulation of gene expression in chloroplasts of higher plants. Plant Mol Biol 32: 315-326
72. Vitanen PV, Devine AL, Kahn S, Deuel DL, Van Dyk DE, Daniell H (2004) Metabolic engineering of the chloroplast genome using the Escherichia coli ubiC gene reveals that chorismate is a readily abundant precursor for p-hydroxybenzoic acid synthesis. Plant Physiol 136: 4048-4060
73. Wang A, Xia Q, Xie W, Dumonceaux T, Zou J, Datla R, Selvaraj G (2002) Male gametophyte development in bread wheat (Triticum aestivum L.): molecular, cellular, and biochemical analyses of a sporophytic contribution to pollen wall ontogeny. Plant J 30: 613-623
74. Watson J, Koya V, Leppla SH, Daniell H (2004) Expression of Bacillus anthracis protective antigen in transgenic tobacco chloroplasts: development of an improved anthrax vaccine in a non-food/feed crop. Vaccine 22: 4374-4384
75. Yui R, Iketani S, Mikami T, Kubo T (2003) Antisense inhibition of mitochondrial pyruvate dehydrogenase E1alpha subunit in anther tapetum causes male sterility. Plant J 34: 57-66
76. Zheng Z, Xia Q, Dauk M, Shen W, Selvaraj G, Zou J (2003) Arabidopsis AtGPAT1, a member of the membrane-bound glycerol-3-phosphate acyltransferase gene family, is essential for tapetum differentiation and male fertility. Plant Cell 15: 1872-1887