Mutations in the Arabidopsis gene IMMUTANS cause a variegated phenotype by inactivating a chloroplast terminal oxidase associated with phytoene desaturation

Plant Cell

Volumn 11, Issue 1, 1999, Pages 57-68

  Carol, Pierre ^a   Stevenson, David ^b,d   Bisanz, Cordelia ^a   Breitenbach, Jürgen ^c   Sandmann, Gerhard ^c   Mache, Regis ^a   Coupland, George ^b   Kuntz, Marcel ^a  

^a UNIV GRENOBLE ALPES   (France)

^b JOHN INNES CENTRE   (United Kingdom)

^c GOETHE UNIVERSITY   (Germany)

^d ROTHAMSTED RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CAROTENOID; CHLOROPLAST; GENE MUTATION; PHYTOENE; PLANT GENETICS; TERMINAL OXIDASE;

ARABIDOPSIS; EMBRYOPHYTA;

EID: 0032697005     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.11.1.57     Document Type: Article

References (61)

1. Al-Babili, S., Von Lintig, J., Haubruck, H., and Beyer, P. (1996). A novel, soluble form of phytoene desaturase from Narcissus pseudonarcissus chromoplasts is Hsp70-complexed and competent for flavinylation, membrane association and enzymatic activation. Plant J. 9, 601-612.
2. Albrecht, M., Klein, A., Hugueney, P., Sandmann, G., and Kuntz, M. (1995). Molecular cloning and functional expression in E. coli of a novel plant enzyme mediating ζ-carotene desaturation. FEBS Lett. 372, 199-202.
3. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
4. Bancroft, I., and Dean, C. (1993). Transposition pattern of the maize element Ds in Arabidopsis thaliana. Genetics 134, 1221-1229.
5. Bartley, G.E., Vitanen, P.V., Pecker, I., Chamovitz, D., Hirschberg, J., and Scolnik, P.A. (1991). Molecular cloning and expression in photosynthetic bacteria of a soybean cDNA coding for phytoene desaturase, an enzyme of the carotenoid biosynthetic pathway. Proc. Natl. Acad. Sci. USA 88, 6532-6536.
6. Bennoun, P. (1982). Evidence for a respiratory chain in the chloroplast. Proc. Natl. Acad. Sci. USA 79, 4352-4356.
7. Bevan, M., et al. (1998). Analysis of 1.9 Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana. Nature 391, 485-488.
8. Beyer, P., Mayer, M.P., and Kleinig, H. (1989). Molecular oxygen and the state of geometric isomerism of intermediates are essential in the carotene desaturation and cyclization reactions in daffodil chromoplasts. Eur. J. Biochem. 184, 141-150.
9. Bilang, R., and Bogorad, L. (1996). Light-dependent developmental control of rbcS gene expression in epidermal cells of maize leaves. Plant Mol. Biol. 31, 831-841.
10. Bramley, P.M. (1997). Isoprenoid metabolism. In Plant Biochemistry, P.M. Dey and J.B. Harborne, eds (San Diego, CA: Academic Press), pp. 417-437.
11. Burrows, P.A., Sazanov, L.A., Svab, Z., Maliga, P., and Nixon, P.J. (1998). Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disputed plastid ndh genes. EMBO J. 17, 868-876.
12. Chatterjee, M., Sparvoli, S., Edmunds, C., Garosi, P., Findlay, K., and Martin, C. (1996). DAG, a gene required for chloroplast differentiation and palisade development in Antirrhinum majus. EMBO J. 15, 4194-4207.
13. Chory, J., and Susek, R.E. (1994). Light signal transduction and the control of seedling development. In Arabidopsis, E.M. Meyerowitz and C.R. Somerville, eds (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press), pp. 579-614.
14. Corona, V., Aracri, B., Kosturkova, G., Bartley, G.E., Pitto, L., Giorgetti, L., Scolnik, P.A., and Giuliano, G. (1996). Regulation of a carotenoid biosynthesis gene promoter during plant development. Plant J. 9, 505-512.
15. Coupland, G. (1992). Transposon tagging in Arabidopsis. In Methods in Arabidopsis Research, C. Koncz, N.-H. Chua, and J. Schell, eds (Singapore: World Scientific), pp. 290-310.
16. Cowling, R.J., Kamiya, Y., Seto, H., and Harberd, N.P. (1998). Gibberellin dose-response regulation of GA4 gene transcript levels in Arabidopsis thaliana. Plant Physiol. 117, 1195-1203.
17. Creusot, F., Fouilloux, E., Dron, M., Lafleuriel, J., Picard, G., Billault, A., LePaslier, D., Cohen, D., Chaboute, M., Durr, A., Fleck, J., Gigot, C., Camilleri, C., Bellini, C., Caboche, M., and Bouchez, D. (1995). The CIC library: A large insert YAC library for genome mapping in Arabidopsis thaliana. Plant J. 8, 763-770.
18. Davis, B.H. (1976). Carotenoids. In Biochemistry of Plant Pigments, Vol. 2, T.W. Goodwin, ed (London: Academic Press), pp. 38-165.
19. Feild, T.S., Nedbal, L., and Ort, D.R. (1998). Nonphotochemical reduction of the plastoquinone pool in sunflower leaves originates from chlororespiration. Plant Physiol. 116, 1209-1218.
20. Fraser, P.D., Linden, H., and Sandmann, G. (1993). Purification and reactivation of recombinant Synechococcus phytoene desaturase from an overexpressing strain of Escherichia coli. Biochem. J. 291, 687-692.
21. Han, C.D., Coe, E.H., Jr., and Martienssen, R.A. (1992). Molecular cloning and characterisation of iojap (ij), a pattern striping gene of maize. EMBO J. 11, 4037-4046.
22. Hudson, A., Carpenter, R., Doyle, S., and Coen, E.S. (1993). Olive: A key gene required for chlorophyl biosynthesis in Antirrhinum majus. EMBO J. 12, 3711-3719.
23. Inada, H., Kusumi, K., Nishimura, M., and Iba, K. (1996). Specific expression of the chloroplast gene for RNA polymerase (rpoB) at an early stage of leaf development in rice. Plant Cell Physiol. 37, 229-232.
24. Keddie, J.S., Carroll, B., Jones, J.D., and Gruissem, W. (1996). The DCL gene of tomato is required for chloroplast development and palisade cell morphogenesis in leaves. EMBO J. 16, 4208-4217.
25. Linden, H., Lucas, M.M., de Felipe, M.R., and Sandmann, G. (1993). Immunogold localization of phytoene desaturase in higher plant chloroplasts. Physiol. Plant. 88, 229-236.
26. Lister, C., and Dean, C. (1993). Recombinant inbred lines for mapping RFLP and phenotypic markers in Arabidopsis thaliana. Plant J. 4, 745-750.
27. Long, D., Martin, M., Sundberg, E., Swinburne, J., Puangsomlee, P., and Coupland, G. (1993). The maize transposable element system Ac/Ds as a mutagen in Arabidopsis: Identification of an albino mutation induced by Ds insertion. Proc. Natl. Acad. Sci. USA 90, 10370-10374.
28. Long, D., Goodrich, J., Wilson, K., Sundberg, E., Martin, M., Puangsomlee, P., and Coupland, G. (1997). Ds elements on all five Arabidopsis chromosomes and assessment of their utility for transposon tagging. Plant J. 11, 145-148.
29. Machida, C., Onouchi, H., Koizumi, J., Hamada, S., Semiarti, E., Torikai, S., and Machida, Y. (1997). Characterization of the transposition pattern of the Ac element in Arabidopsis thaliana using endonuclease I-Scel. Proc. Natl. Acad. Sci. USA 94, 8675-8680.
30. 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.
31. Marin, E., Nussaume, L., Quesada, A., Gonneau, M., Sotta, B., Hugueney, P., Frey, A., and Marion-Poll, A. (1996). Molecular identification of zeaxanthin epoxidase of Nicotiana plumbaginifolia, a gene involved in abscisic acid biosynthesis and corresponding to the ABA locus of Arabidopsis thaliana. EMBO J. 15, 2331-2342.
32. Martínez-Zapater, J.M., Gil, P., Capel, J., and Somerville, C.R. (1992). Mutations at the Arabidopsis CHM locus promote rear-rangements of the mitochondrial genome. Plant Cell 4, 889-899.
33. Michl, D., Robinson, C., Shackleton, J.B., Herrman, R.G., and Klosgen, R.B. (1994). Targeting of proteins to the thylakoids by bipartite presequences: CF0II is imported by a novel, third pathway. EMBO J. 6, 1310-1317.
34. Moffatt, B.A., McWhinnie, E.A., Agarwal, S.K., and Schaff, D.A. (1994). The adenine phosphoribosyltransferase-encoding gene of Arabidopsis thaliana. Gene 143, 211-216.
35. Mullet, J.E. (1988). Chloroplast development and gene expression. Annu. Rev. Plant Physiol. Plant Mol. Biol. 39, 475-502.
36. Nakai, K., and Kanehisa, M. (1992). A knowledge base for predicting protein localization sites in eukaryotic cells. Genomics 14, 897-911.
37. Nievelstein, V., Vandekerckhove, J., Tadros, M.H., von Lintig, J., Nitschke, W., and Beyer, P. (1995). Carotene desturation is linked to a respiratory redox pathway in Narcissus pseudonarcissus chromoplast membranes: Involvement of a 23-kDa oxygene-evolving-complex-like protein. Eur. J. Biochem. 233, 864-872.
38. Norris, S.R., Barrette, T.R., and DellaPenna, D. (1995). Genetic dissection of carotenoid synthesis in Arabidopsis defines plasto-quinone as an essential component of phytoene desaturation. Plant Cell 7, 2139-2149.
39. Pascal, N., Block, M.A., Pallet, K.E., Joyard, J., and Douce, R. (1995). Inhibition of carotenoid biosynthesis in sycamore cells deprived of iron. Plant Physiol. Biochem. 33, 97-104.
40. Pogson, B., McDonald, K.A., Truong, M., Britton, G., and DellaPenna, D. (1996). Arabidopsis carotenoid mutants demonstrate that lutein is not essential for photosynthesis in higher plants. Plant Cell 8, 1627-1639.
41. Rédei, G.P. (1963). Somatic instability caused by a cysteine-sensitive gene in Arabidopsis. Science 139, 767-769.
42. Reiter, R.S., Coomber, S.A., Bourett, T.M., Bartley, G.E., and Scolnik, P.A. (1994). Control of leaf and chloroplast development by the Arabidopsis gene pale cress. Plant Cell 6, 1253-1264.
43. Röbbelen, G. (1968). Genbedingte Rotlicht-Empfindlichkeit der Chloroplastendifferenzierung bei Arabidopsis. Planta 80, 237-254.
44. Sakamoto, W., Kondo, H., Murata, M., and Motoyoshi, F. (1996). Altered mitochondrial gene expression in a maternal distorted leaf mutant of Arabidopsis induced by chloroplast mutator. Plant Cell 8, 1377-1390.
45. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
46. Sandmann, G., and Albrecht, M. (1990). Accumulation of colorless carotenes and derivatives during interaction of bleaching herbicides with phytoene desaturation. Z. Naturforsch. 45C, 487-491.
47. Schmidt, R., West, J., Love, K., Lenehan, Z., Lister, C., Thompson, H., Bouchez, D., and Dean, C. (1995). Physical map and organization of Arabidopsis thaliana chromosome 4. Science 270, 480-483.
48. Schultz, A., Ort, O., Beyer, P., and Kleinig, H. (1993). SC-0051, a 2-benzoyl-cyclohexane-1,3-dione bleaching herbicide, is a potent inhibitor of the enzyme p-hydroxyphenylpyruvate dioxygenase. FEBS Lett. 318, 162-166.
49. Siedow, J.N., and Umbach, A.L. (1995). Plant mitochondrial electron transfer and molecular biology. Plant Cell 7, 821-831.
50. Sundaresan, V., Springer, P., Volpe, T., Haward, S., Jones, J.D., Dean, C., Ma, H., and Martienssen, R. (1995). Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements. Genes Dev. 9, 1797-1810.
51. Sundberg, E., Slagter, J.G., Fridborg, I., Cleary, S.P., Robinson, C., and Coupland, G. (1997). ALBINO3, an Arabidopsis nuclear gene essential for chloroplast differentiation, encodes a chloroplast protein that shows homology to proteins present in bacterial membranes and yeast mitochondria. Plant Cell 9, 717-730.
52. Swinburne, J., Balcells, L., Scofield, S.R., Jones, J.D.G., and Coupland, G. (1992). Elevated levels of Activator transposase mRNA are associated with high frequencies of Dissociation excision in Arabidopsis. Plant Cell 4, 583-595.
53. Tan, B.C., Schwartz, S.H., Zeevaart, J.A.D., and McCarty, D.R. (1997). Genetic control of abscisic acid biosynthesis in maize. Proc. Natl. Acad. Sci. USA 94, 12235-12240.
54. Taylor, W.C. (1989). Regulatory interactions between nuclear and plastid genomes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 211-233.
55. Vanlerberghe, G.C., and McIntosh, L. (1997). Alternative oxidase: From gene to function. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 703-734.
56. von Heijne, G., Steppuhn, J., and Herrmann, R.G. (1989). Domain structure of mitochondrial and chloroplast targeting peptides. Eur. J. Biochem. 180, 535-545.
57. Waegemann, K., and Soil, J. (1995). Characterization and isolation of the chloroplast protein import machinery. In Methods in Cell Biology, Vol. 50, D.W. Galbraith, D.P. Bourque, and H.J. Bohnert, eds (New York: Academic Press), pp. 255-268.
58. Walbot, V. (1992). Strategies for mutagenesis and gene cloning using transposon tagging and T-DNA insertional mutagenesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43, 49-92.
59. Wetzel, C.M., Jiang, C.-Z., Meehan, L.J., Voytas, D.F., and Rodermel, S.R. (1994). Nuclear-organelle interactions: The immutans variegation mutant of Arabidopsis is plastid autonomous and impaired in carotenoid biosynthesis. Plant J. 6, 161-175.
60. Whitelam, G.C., Johnson, E., Peng, J., Carol, P., Anderson, M.L., Cowl, J.S., and Harberd, N.P. (1993). Phytochrome A null mutants of Arabidopsis display a wild-type phenotype in white light. Plant Cell 5, 757-768.
61. Wu, D., Wright, D.A., Wetzel, C., Voytas, D.F., and Rodermel, S. (1999). The IMMUTANS variegation locus of Arabidopsis defines a mitochondrial alternative oxidase homolog that functions during early chloroplast biogenesis. Plant Cell 11, 43-55.