Differential expression of alternative oxidase genes in maize mitochondrial mutants

Plant Cell

Volumn 14, Issue 12, 2002, Pages 3271-3284

  Karpova, Olga V ^a   Kuzmin, Evgeny V ^a   Elthon, Thomas E ^b   Newton, Kathleen J ^a  

^a UNIVERSITY OF MISSOURI   (United States)

^b UNIVERSITY OF NEBRASKA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOMES; DNA; ENZYME INHIBITION; GENES; MUTAGENS;

CYTOPLASMA; MAIZE MITOCHONDRIA;

PLANT CELL CULTURE;

EMBRYOPHYTA; EUKARYOTA; ZEA MAYS;

EID: 0036918322     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.005603     Document Type: Article

References (77)

1. Alvarez, M.E., Pennell, R.I., Meijer, P.-J., Ishikawa, A., Dixon, R.A., and Lamb, C. (1998). Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92, 773-784.
2. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., and Struhl, K. (1992). Short Protocols in Molecular Biology. (New York: John Wiley & Sons).
3. Balk, J., Leaver, C.J., and McCabe, P.F. (1999). Translocation of cytochrome c from the mitochondria to the cytosol occurs during heat-induced programmed cell death in cucumber plants. FEBS Lett. 463, 151-154.
4. Baum, J.A., and Scandalios, J.G. (1981). Isolation and characterization of the cytosolic and mitochondrial superoxide dismutases of maize. Arch. Biochem. Biophys. 206, 249-264.
5. Berlett, B.S., and Stadtman, E.R. (1997). Protein oxidation in aging, disease, and oxidative stress. J. Biol. Chem. 272, 20313-20316.
6. Bhattramakki, D., and Elthon, T.E. (1997). Exogenous NAD(P)H dehydrogenases of plant mitochondria. Recent Res. Dev. Plant Physiol. 1, 93-104.
7. Chomczynski, P., and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 161, 156-159.
8. Coe, E. (1983). Maternally inherited abnormal plant types in maize. Maydica 28, 151-167.
9. Conley, C.S., and Hanson, M.R. (1995). How do alterations in plant mitochondrial genomes disrupt pollen development? J. Bioenerg. Biomembr. 27, 447-457.
10. Considine, M.J., Daley, D.O., and Whelan, J. (2001). The expression of alternative oxidase and uncoupling protein during fruit ripening in mango. Plant Physiol. 126, 1619-1629.
11. Considine, M.J., Holtzapffel, R.C., Day, D.A., Whelan, J., and Millar, A.H. (2002). Molecular distinction between alternative oxidase from monocots and dicots. Plant Physiol. 129, 949-953.
12. Cooper, P., and Newton, K.J. (1989). Maize nuclear background regulates the synthesis of a 22-kDa polypeptide in Zea luxurians mitochondria. Proc. Natl. Acad. Sci. USA 86, 7423-7426.
13. Dinant, M., Baurain, D., Coosemans, N., Joris, B., and Matagne, R.F. (2001). Characterization of two genes encoding the mitochondrial alternative oxidase in Chlamydomonas reinhardtii. Curr. Genet. 39, 101-108.
14. Djajanegara, I., Holtzapffel, R., Finnegan, P.M., Hoefnagel, M.H., Berthold, D.A., Wiskich, J.T., and Day, D.A. (1999). A single amino acid change in the plant alternative oxidase alters the specificity of organic acid activation. FEBS Lett. 454, 220-224.
15. Elthon, T.E., and McIntosh, L. (1987). Identification of the alternative terminal oxidase of higher plant mitochondria. Proc. Natl. Acad. Sci. USA 84, 8399-8403.
16. Elthon, T.E., Nickels, R.L., and McIntosh, L. (1989). Monoclonal antibodies to the alternative oxidase of higher plant mitochondria. Plant Physiol. 89, 1311-1317.
17. Finnegan, P.M., Whelan, J., Millar, A.H., Zhang, Q., Smith, M.K., Wiskich, J.T., and Day, D.A. (1997). Differential expression of the multigene family encoding the soybean mitochondrial alternative oxidase. Plant Physiol. 114, 455-466.
18. Finnegan, P.M., Wooding, A.R., and Day, D.A. (1999). An alternative oxidase monoclonal antibody recognises a highly conserved sequence among alternative oxidase subunits. FEBS Lett. 447, 21-24.
19. Garlid, K.D., Orosz, D.E., Modriansky, M., Vassanelli, S., and Jezek, P. (1996). On the mechanism of fatty acid-induced proton transport by mitochondrial uncoupling protein. J. Biol. Chem. 269, 2615-2620.
20. Gu, J., Miles, D., and Newton, K.J. (1993). Analysis of leaf sectors in the NCS6 mitochondrial mutant of maize. Plant Cell 5, 963-971.
21. Gutierres, S., Sabar, M., Lelandais, C., Chetrit, P., Diolez, P., Degand, H., Boutry, M., Vedel, F., de Kouchkovsky, Y., and De Paepe, R. (1997). Lack of mitochondrial and nuclear-encoded subunits of complex I and alteration of the respiratory chain in Nicotiana sylvestris mitochondrial deletion mutants. Proc. Natl. Acad. Sci. USA 94, 3436-3441.
22. Hiser, C., Kapranov, P., and McIntosh, L. (1996). Genetic modification of respiratory capacity in potato. Plant Physiol. 110, 277-286.
23. Hunt, M.D., and Newton, K.J. (1991). The NCS3 mutation: Genetic evidence for the expression of ribosomal protein genes in Zea mays mitochondria. EMBO J. 10, 1045-1052.
24. Ito, Y., Saisho, D., Nakazono, M., Tsutsumi, N., and Hirai, A. (1997). Transcript levels of tandem-arranged alternative oxidase genes in rice are increased by low temperature. Gene 203, 121-129.
25. Joseph-Horne, T., Babij, J., Wood, P.M., Hollomon, D., and Sessions, R.B. (2000). New sequence data enable modelling of the fungal alternative oxidase and explain an absence of regulation by pyruvate. FEBS Lett. 481, 141-146.
26. Karpova, O.V., and Newton, K.J. (1999). A partially assembled complex I in NAD4-deficient mitochondna of maize. Plant J. 17, 511-521.
27. Kliebenstein, D.J., Monde, R.A., and Last, R.L. (1998). Superoxide dismutase in Arabidopsis: An eclectic enzyme family with disparate regulation and protein localization. Plant Physiol. 118, 637-650.
28. Kowaltowski, A.J., Costa, A.D.T., and Verseci, A.E. (1998). Activation of the potato plant uncoupling mitochondrial protein inhibits reactive oxygen species generation by the respiratory chain. FEBS Lett. 425, 213-216.
29. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
30. Laloi, M., Klein, M., Riesmeier, J.W., Muller-Rober, B., Fleury, C., Bouillaud, F., and Ricquier, D. (1997). A plant cold-induced uncoupling protein. Nature 389, 135-136.
31. Lauer, M., Knudsen, C., Newton, K.J., Gabay-Laughnan, S., and Laughnan, J.R. (1990). A partially deleted mitochondrial cytochrome oxidase gene in the NCS6 abnormal growth mutant of maize. New Biol. 2, 179-186.
32. Marienfeld, J.R., and Newton, K.J. (1994). The maize NCS2 abnormal growth mutant has a chimeric nad4-nad7 mitochondrial gene and is associated with reduced complex I function. Genetics 138, 855-863.
33. Maxwell, D., Nickels, R.L., and McIntosh, L. (2002). Evidence of mitochondrial involvement in the transduction of signals required for the induction of genes associated with pathogen attack and senescence. Plant J. 29, 263-279.
34. Maxwell, D.P., Wang, Y., and McIntosh, L. (1999). The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc. Natl. Acad. Sci. USA 96, 8271-8276.
35. McCabe, T.C., Finnegan, P.M., Millar, A.H., Day, D.A., and Whelan, J. (1998). Differential expression of alternative oxidase genes in soybean cotyledons during postgerminative development. Plant Physiol. 118, 675-682.
36. McGonigle, B., Keeler, S.J., Lau, S.-M.C., Koeppe, M.K., and O'Keefe, D.P. (2000). A genomics approach to the comprehensive analysis of the glutathione S-transferase gene family in soybean and maize. Plant Physiol. 124, 1105-1120.
37. McIntosh, L., Eichler, T., Gray, G., Maxwell, D., Nickels, R.N., and Wong, Y. (1998). Biochemical and genetic controls exerted by plant mitochondria. Biochim. Biophys. Acta 1365, 278-284.
38. Meeuse, B.J.D. (1975). Thermogenic respiration in aroids. Annu. Rev. Plant Physiol. 26, 117-126.
39. Millar, A.H., Wiskich, J.T., Whelan, J., and Day, D.A. (1993). Organic acid activation of the alternative oxidase of plant mitochondria. FEBS Lett. 329, 259-262.
40. Millenaar, F.F., Benschop, J.J., Wagner, A.M., and Lambers, H. (1998). The role of the alternative oxidase in stabilizing the in vivo reduction state of the ubiquinone pool and the activation state of the alternative oxidase. Plant Physiol. 118, 599-607.
41. Millenaar, F.F., Gonzalez-Meler, M.A., Fiorani, F., Welschen, R., Ribas-Carbo, M., Siedow, J.N., Wagner, A.M., and Lambers, H. (2001). Regulation of alternative oxidase activity in six wild monocotyledonous species: An in vivo study at the whole root level. Plant Physiol. 126, 376-387.
42. Mittler, R., Lam, E., Shulaev, V., and Cohen, M. (1999). Signals controlling the expression of cytosolic ascorbate peroxidase during pathogen-induced programmed cell death in tobacco. Plant Mol. Biol. 39, 1025-1035.
43. Møller, I.M. (2001). Plant mitochondria and oxidative stress: Electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 561-591.
44. Moore, A.L., and Siedow, J.N. (1991). The regulation and nature of the cyanide-resistant alternative oxidase of plant mitochondria. Biochim. Biophys. Acta 1059, 121-140.
45. Murayama, S., and Handa, H. (2000). Isolation and characterization of cDNAs encoding mitochondrial uncoupling proteins in wheat: Wheat UCP genes are not regulated by low temperature. Mol. Gen. Genet. 264, 112-118.
46. Nantes, I.L., Fagian, M.M., Catisti, R., Arruda, P., Maia, I.G., and Vercesi, A.E. (1999). Low temperature and aging-promoted expression of PUMP in potato tuber mitochondria. FEBS Lett. 457, 103-106.
47. Newton, K., and Coe, E.J. (1986). Mitochondrial DNA changes in abnormal growth mutants of maize. Proc. Natl. Acad. Sci. USA 83, 7363-7366.
48. Newton, K.J. (1980). Studies of the Malate Dehydrogenase Isozymes in Zea mays. PhD dissertation (Bloomington, IN: Indiana University).
49. Newton, K.J., and Gabay-Laughnan, S. (1998). Abnormal growth and male sterility associated with mitochondrial DNA rearrangements in plants. In Mitochondrial DNA Mutations in Aging, Disease and Cancer, K.K. Singh, ed (Berlin: Springer-Verlag), pp. 365-381.
50. Newton, K.J., Knudsen, C., Gabay-Laughnan, S., and Laughnan, J.R. (1990). An abnormal growth mutant in maize has a defective mitochondrial cytochrome oxidase gene. Plant Cell 2, 107-113.
51. Newton, K.J., Mariano, J.M., Gibson, C.M., Kuzmin, E., and Gabay-Laughnan, S. (1996). Involvement of S2 episomal sequences in the generation of NCS4 deletion mutation in maize mitochondria. Dev. Genet. 19, 277-286.
52. Parsons, H.L., Yip, J.Y.H., and Vanlerberghe, G.C. (1999). Increased respiratory restriction during phosphate-limited growth in transgenic tobacco cells lacking alternative oxidase. Plant Physiol. 121, 1309-1320.
53. 2 production in plant mitochondria. FEBS Lett. 415, 87-90.
54. Purvis, A.C., and Shewfelt, R.L. (1993). Does the alternative pathway ameliorate chilling injury in sensitive plant tissues? Physiol. Plant. 88, 712-718.
55. Rhoads, D.M., Levings, C.S., III, and Siedow, J.N. (1995). URF13, a ligand-gated, pore-forming receptor for T-toxin in the inner membrane of cms-T mitochondria. J. Bioenerg. Biomembr. 27, 437-445.
56. Rhoads, D.M., and McIntosh, L. (1991). Isolation and characterization of a cDNA clone encoding an alternative oxidase protein of Sauromatum guttatum (Schott). Proc. Natl. Acad. Sci. USA 88, 2122-2126.
57. Rhoads, D.M., Umbach, A.L., Sweet, C.R., Lennon, A.M., Rauch, G.S., and Siedow, J.N. (1998). Regulation of the cyanide-resistant alternative oxidase of plant mitochondria: Identification of the cysteine residue involved in alpha-keto acid stimulation and inter-subunit disulfide bond formation. J. Biol. Chem. 273, 30750-30756.
58. Sabar, M., De Paepe, R., and de Kouchkovsky, Y. (2000). Complex I impairment, respiratory compensations, and photosynthetic decrease in nuclear and mitochondrial male sterile mutants of Nicotiana sylvestris. Plant Physiol. 124, 1239-1250.
59. Saika, H., Ohtsu, K., Hamanaka, S., Nakazono, M., Tsutsumi, N., and Hirai, A. (2002). AOX1c, a novel rice gene for alternative oxidase: Comparison with rice AOX1a and AOX1b. Genes Genet. Syst. 77, 31-38.
60. Saisho, D., Nambara, E., Naito, S., Tsutsumi, N., Hirai, A., and Nakazono, M. (1997). Characterization of the gene family for alternative oxidase from Arabidopsis thaliana. Plant Mol. Biol. 35, 585-596.
61. Sakajo, S., Minagawa, N., Komiyama, T., and Yoshimoto, A. (1991). Molecular cloning of cDNA for antimycin A-inducible mRNA and its role in cyanide-resistant respiration in Hansenula anomala. Biochim. Biophys. Acta 1090, 102-108.
62. Schnable, P.S., and Wise, R.P. (1998). The molecular basis of cytoplasmic male sterility and fertility restoration. Trends Plant Sci. 3, 175-180.
63. Shigeoka, S., Ishikawa, T., Tamoi, M., Miyagawa, Y., Takeda, T., Yabuta, Y., and Yoshimura, K. (2002). Regulation and function of ascorbate peroxidase isoenzymes. J. Exp. Bot. 53, 1305-1319.
64. Sluse, F.E., and Jarmuszkiewicz, W. (2000). Activity and functional interaction of alternative oxidase and uncoupling protein in mitochondria from tomato fruit. Braz. J. Med. Biol. Res. 33, 259-268.
65. Soole, K.L., and Menz, R.I. (1995). Functional molecular aspects of the NADH dehydrogenases of plant mitochondria. J. Bioenerg. Biomembr. 27, 397-406.
66. Sun, Y.-L., Zhao, Y., Hong, X., and Zhai, Z.-H. (1999). Cytochrome c release and caspase activation during menadione-induced apoptosis in plants. FEBS Lett. 462, 317-321.
67. Surpin, M., Larkin, R.M., and Chory, J. (2002). Signal transduction between the chloroplast and the nucleus. Plant Cell 14 (suppl.), S327-S338.
68. Umbach, A.L., Gonzalez-Meler, M.A., Sweet, C.R., and Siedow, J.N. (2002). Activation of the plant mitochondrial alternative oxidase: Insights from site-directed mutagenesis. Biochim. Biophys. Acta 1554, 118-128.
69. Umbach, A.L., and Siedow, J.N. (1993). Covalent and non-covalent dimers of the cyanide-resistant alternative oxidase protein in higher plant mitochondria and their relationship to enzyme activity. Plant Physiol. 103, 845-854.
70. Umbach, A.L., and Siedow, J.N. (1996). The reaction of the soybean cotyledon mitochondrial cyanide-resistant oxidase with sulfhydryl reagents suggests that alpha-keto acid activation involves the formation of a thioacetal. J. Biol. Chem. 271, 25019-25026.
71. Vanlerberghe, G. C., and McIntosh, L. (1994). Mitochondrial electron transport regulation of nuclear gene expression: Studies with the alternative oxidase gene of tobacco. Plant Physiol. 105, 867-874.
72. Vanlerberghe, G.C., and McIntosh, L. (1997). Alternative oxidase: From gene to function. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 703-734.
73. Wagner, A.M. (1995). A role for active oxygen species as second messengers in the induction of alternative oxidase gene expression in Petunia hybrida cells. FEBS Lett. 368, 339-342.
74. Wagner, A.M., and Moore, A.L. (1997). Structure and function of the plant alternative oxidase: Its putative role in the oxygen defence mechanism. Biosci. Rep. 17, 319-333.
75. Whelan, J., Millar, A.H., and Day, D.A. (1996). The alternative oxidase is encoded in a multigene family in soybean. Planta 198, 197-201.
76. Yamato, K.T., and Newton, K.J. (1999). Heteroplasmy and homoplasmy for maize mitochondrial mutants: A rare homoplasmic nad4 deletion mutant plant. J. Hered. 90, 369-373.
77. Yip, J.Y., and Vanlerberghe, G.C. (2001). Mitochondrial alternative oxidase acts to dampen the generation of active oxygen species during a period of rapid respiration induced to support a high rate of nutrient uptake. Physiol. Plant 112, 327-333.