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Volume 37 Issue 10
Oct.  2010
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Abstract
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Article Navigation >  Journal of Genetics and Genomics  > 2010  >  37(10): 667-683

A nuclear-encoded mitochondrial gene AtCIB22 is essential for plant development in Arabidopsis

doi: 10.1016/S1673-8527(09)60085-0
  • a 

    College of Agronomy and Biotechnology, China Agricultural University, Beijing 100094, China

  • b 

    National Laboratory of Protein Engineering and Plant Genetic Engineering, Peking University, Beijing 100871, China

  • c 

    The National Plant Gene Research Center (Beijing), Beijing 100101, China

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  • Corresponding author: E-mail address: qulj@pku.edu.cn (Li-Jia Qu)
  • Received Date: 2010-02-28
  • Accepted Date: 2010-07-22
  • Rev Recd Date: 2010-07-18
    • Available Online: 2010-10-27
  • Publish Date: 2010-10-20
    Abstract
  • Complex I (the NADH:ubiquinone oxidoreductase) of the mitochondrial respiratory chain is a complicated, multi-subunit, membrane-bound assembly and contains more than 40 different proteins in higher plants. In this paper, we characterize the Arabidopsis homologue (designated as AtCIB22) of the B22 subunit of eukaryotic mitochondrial Complex I. AtCIB22 is a single-copy gene and is highly conserved throughout eukaryotes. AtCIB22 protein is located in mitochondria and theAtCIB22 gene is widely expressed in different tissues. Mutant Arabidopsis plants with a disrupted AtCIB22 gene display pleiotropic phenotypes including shorter roots, smaller plants and delayed flowering. Stress analysis indicates that the AtCIB22 mutants' seed germination and early seedling growth are severely inhibited by sucrose deprivation stress but more tolerant to ethanol stress. Molecular analysis reveals that in moderate knockdown AtCIB22 mutants, genes including cell redox proteins and stress related proteins are significantly up-regulated, and that in severe knockdown AtCIB22 mutants, the alternative respiratory pathways including NDA1, NDB2, AOX1a and AtPUMP1 are remarkably elevated. These data demonstrate that AtCIB22 is essential for plant development and mitochondrial electron transport chains in Arabidopsis. Our findings also enhance our understanding about the physiological role of Complex I in plants.
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  • [1]
    Alonso, J.M., Stepanova, A.N., Leisse, T.J. et al. Science, 301 (2003),pp. 653-657
    [2]
    Bailey-Serres, J., Chang, R. Sensing and signalling in response to oxygen deprivation in plants and other organisms Ann. Bot., 96 (2005),pp. 507-518
    [3]
    Baranova, E.A., Holt, P.J., Sazanov, L.A. J. Mol. Biol., 366 (2007),pp. 140-154
    [4]
    Borecky, J., Nogueira, F.T., de Oliveira, K.A. et al. The plant energy-dissipating mitochondrial systems: depicting the genomic structure and the expression profiles of the gene families of uncoupling protein and alternative oxidase in monocots and dicots J. Exp. Bot., 57 (2006),pp. 849-864
    [5]
    Brangeon, J., Sabar, M., Gutierres, S. et al. Plant J., 21 (2000),pp. 269-280
    [6]
    Cadenas, E., Boveris, A., Ragan, C.I. et al. Production of superoxide radicals and hydrogen peroxide by NADH-ubiquinone reductase and ubiquinol-cytochrome c reductase from beef-heart mitochondria Arch. Biochem. Biophys., 180 (1977),pp. 248-257
    [7]
    Cardol, P., Vanrobaeys, F., Devreese, B. et al. Biochim. Biophys. Acta, 1658 (2004),pp. 212-224
    [8]
    Chinnery, P.F., Brown, D.T., Andrews, R.M. et al. Brain, 124 (2001),pp. 209-218
    [9]
    Clough, S.J., Bent, A.F. Plant J., 16 (1998),pp. 735-743
    [10]
    Cocheme, H.M., Murphy, M.P. Complex I is the major site of mitochondrial superoxide production by paraquat J. Biol. Chem., 283 (2008),pp. 1786-1798
    [11]
    Considine, M.J., Goodman, M., Echtay, K.S. et al. Superoxide stimulates a proton leak in potato mitochondria that is related to the activity of uncoupling protein J. Biol. Chem., 278 (2003),pp. 22298-22302
    [12]
    de Longevialle, A.F., Meyer, E.H., Andres, C. et al. Plant Cell, 19 (2007),pp. 3256-3265
    [13]
    Dong, J., Chen, C., Chen, Z. Plant Mol. Biol., 51 (2003),pp. 21-37
    [14]
    Dutilleul, C., Garmier, M., Noctor, G. et al. Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation Plant Cell, 15 (2003),pp. 1212-1226
    [15]
    Echtay, K.S. Mitochondrial uncoupling proteins–what is their physiological role? Free Radic Biol. Med., 43 (2007),pp. 1351-1371
    [16]
    Fauser, S., Leo-Kottler, B., Besch, D. et al. Ophthalmic Genet., 23 (2002),pp. 191-197
    [17]
    Fernie, A.R., Carrari, F., Sweetlove, L.J. Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport Curr. Opin. Plant Biol., 7 (2004),pp. 254-261
    [18]
    Garmier, M., Carroll, A.J., Delannoy, E. et al. Plant Physiol., 148 (2008),pp. 1324-1341
    [19]
    Giege, P., Heazlewood, J.L., Roessner-Tunali, U. et al. Plant Cell, 15 (2003),pp. 2140-2151
    [20]
    Greenamyre, J.T., Sherer, T.B., Betarbet, R. et al. Complex I and Parkinson's disease IUBMB Life, 52 (2001),pp. 135-141
    [21]
    Grivennikova, V.G., Vinogradov, A.D. Generation of superoxide by the mitochondrial Complex I Biochim. Biophys. Acta, 1757 (2006),pp. 553-561
    [22]
    Guan, H., Kang, D., Fan, M. et al. J. Integr. Plant Biol., 51 (2009),pp. 130-139
    [23]
    Guenebaut, V., Schlitt, A., Weiss, H. et al. Consistent structure between bacterial and mitochondrial NADH:ubiquinone oxidoreductase (complex I) J. Mol. Biol., 276 (1998),pp. 105-112
    [24]
    Gutierres, S., Sabar, M., Lelandais, C. et al. Proc. Natl. Acad. Sci. USA, 94 (1997),pp. 3436-3441
    [25]
    Heazlewood, J.L., Howell, K.A., Millar, A.H. Biochim. Biophys. Acta, 1604 (2003),pp. 159-169
    [26]
    Hirst, J., Carroll, J., Fearnley, I.M. et al. The nuclear encoded subunits of complex I from bovine heart mitochondria Biochim. Biophys. Acta, 1604 (2003),pp. 135-150
    [27]
    Hourton-Cabassa, C., Matos, A. Rita, Zachowski, A., Moreau, F. The plant uncoupling protein homologues: a new family of energy-dissipating proteins in plant mitochondria Plant Physiol. Biochem., 42 (2004),pp. 283-290
    [28]
    Ishizaki, K., Schauer, N., Larson, T.R. et al. Plant J., 47 (2006),pp. 751-760
    [29]
    Ismond, K.P., Dolferus, R., de Pauw, M. et al. Plant Physiol., 132 (2003),pp. 1292-1302
    [30]
    Jaquinod, M., Villiers, F., Kieffer-Jaquinod, S. et al. Mol. Cell Proteomics, 6 (2007),pp. 394-412
    [31]
    Kato-Noguchi, H., Morokuma, M. Ethanolic fermentation and anoxia tolerance in four rice cultivars J. Plant Physiol., 164 (2007),pp. 168-173
    [32]
    Khan, S.Z. Mitochondrial complex-1 in Parkinson's disease Neurol. India, 54 (2006),p. 351
    [33]
    Klodmann, J., Sunderhaus, S., Nimtz, M. et al. Plant Cell, 22 (2010),pp. 797-810
    [34]
    Lamattina, L., Gonzalez, D., Gualberto, J. et al. Higher plant mitochondria encode an homologue of the nuclear-encoded 30-kDa subunit of bovine mitochondrial complex I Eur. J. Biochem., 217 (1993),pp. 831-838
    [35]
    Lambert, A.J., Brand, M.D. Reactive oxygen species production by mitochondria Methods Mol. Biol., 554 (2009),pp. 165-181
    [36]
    Lee, B.H., Lee, H., Xiong, L. et al. A mitochondrial complex I defect impairs cold-regulated nuclear gene expression Plant Cell, 14 (2002),pp. 1235-1251
    [37]
    Li, L., Foster, C.M., Gan, Q. et al. Plant J., 58 (2009),pp. 485-498
    [38]
    Liu, Y.G., Mitsukawa, N., Oosumi, T. et al. Plant J., 8 (1995),pp. 457-463
    [39]
    Livak, K.J., Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method Methods, 25 (2001),pp. 402-408
    [40]
    MacDonald, R.C., Kimmerer, T.W. Plant Physiol., 102 (1993),pp. 173-179
    [41]
    Marienfeld, J.R., Newton, K.J. Genetics, 138 (1994),pp. 855-863
    [42]
    Maxwell, D.P., Wang, Y., McIntosh, L. The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells Proc. Natl. Acad. Sci. USA, 96 (1999),pp. 8271-8276
    [43]
    Meyer, E.H., Taylor, N.L., Millar, A.H. Resolving and identifying protein components of plant mitochondrial respiratory complexes using three dimensions of gel electrophoresis J. Proteome Res., 7 (2008),pp. 786-794
    [44]
    Meyer, E.H., Tomaz, T., Carroll, A.J. et al. Plant Physiol., 151 (2009),pp. 603-619
    [45]
    Mittler, R., Kim, Y., Song, L. et al. FEBS Lett., 580 (2006),pp. 6537-6542
    [46]
    Nakagawa, N., Sakurai, N. Plant Cell Physiol., 47 (2006),pp. 772-783
    [47]
    Newton, K.J., Coe, E.H. Mitochondrial DNA changes in abnormal growth (nonchromosomal stripe) mutants of maize Proc. Natl. Acad. Sci. USA, 83 (1986),pp. 7363-7366
    [48]
    Palmieri, L., Picault, N., Arrigoni, R. et al. Biochem. J., 410 (2008),pp. 621-629
    [49]
    Perales, M., Eubel, H., Heinemeyer, J. et al. J. Mol. Biol., 350 (2005),pp. 263-277
    [50]
    Qin, G., Gu, H., Zhao, Y. et al. Plant Cell, 17 (2005),pp. 2693-2704
    [51]
    Qin, G., Ma, Z., Zhang, L. et al. Cell Res., 17 (2007),pp. 249-263
    [52]
    Rasmusson, A.G., Heiser, V.V., Zabaleta, E. et al. Physiological, biochemical and molecular aspects of mitochondrial complex I in plants Biochim. Biophys. Acta, 1364 (1998),pp. 101-111
    [53]
    Rasmusson, A.G., Soole, K.L., Elthon, T.E. Alternative NAD(P)H dehydrogenases of plant mitochondria Annu. Rev. Plant Biol., 55 (2004),pp. 23-39
    [54]
    Sabar, M., De Paepe, R., de Kouchkovsky, Y. Complex I impairment, respiratory compensations, and photosynthetic decrease in nuclear and mitochondrial male sterile mutants of Nicotiana sylvestris Plant Physiol., 124 (2000),pp. 1239-1250
    [55]
    Sauerbrunn, N., Schlaich, N.L. Planta, 218 (2004),pp. 552-561
    [56]
    Schuelke, M., Smeitink, J., Mariman, E. et al. Mutant NDUFV1 subunit of mitochondrial complex I causes leukodystrophy and myoclonic epilepsy Nat. Genet., 21 (1999),pp. 260-261
    [57]
    Smith, A.M., Ratcliffe, R.G., Sweetlove, L.J. Activation and function of mitochondrial uncoupling protein in plants J. Biol. Chem., 279 (2004),pp. 51944-51952
    [58]
    Sun, F., Huo, X., Zhai, Y. et al. Crystal structure of mitochondrial respiratory membrane protein complex II Cell, 121 (2005),pp. 1043-1057
    [59]
    Sunderhaus, S., Dudkina, N.V., Jansch, L. et al. Carbonic anhydrase subunits form a matrix-exposed domain attached to the membrane arm of mitochondrial complex I in plants J. Biol. Chem., 281 (2006),pp. 6482-6488
    [60]
    Tamura, K., Dudley, J., Nei, M. et al. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0 Mol. Biol. Evol., 24 (2007),pp. 1596-1599
    [61]
    Umbach, A.L., Fiorani, F., Siedow, J.N. Plant Physiol., 139 (2005),pp. 1806-1820
    [62]
    Urano, K., Hobo, T., Shinozaki, K. FEBS Lett., 579 (2005),pp. 1557-1564
    [63]
    Vanlerberghe, G.C., McIntosh, L. ALTERNATIVE OXIDASE: from gene to function Annu. Rev. Plant Physiol. Plant Mol. Biol., 48 (1997),pp. 703-734
    [64]
    Vidal, G., Ribas-Carbo, M., Garmier, M. et al. Lack of respiratory chain complex I impairs alternative oxidase engagement and modulates redox signaling during elicitor-induced cell death in tobacco Plant Cell, 19 (2007),pp. 640-655
    [65]
    Walker, J.E. The NADH:ubiquinone oxidoreductase (complex I) of respiratory chains Q Rev. Biophys., 25 (1992),pp. 253-324
    [66]
    Wang, W., Fang, H., Groom, L. et al. Superoxide flashes in single mitochondria Cell, 134 (2008),pp. 279-290
    [67]
    Wang, Z., Cao, G., Wang, X. et al. Plant Cell Rep., 27 (2008),pp. 125-135
    [68]
    Weigel, D., Ahn, J.H., Blazquez, M.A. et al. Plant Physiol., 122 (2000),pp. 1003-1013
    [69]
    Wiedemann, N., Urzica, E., Guiard, B. et al. Essential role of Isd11 in mitochondrial iron-sulfur cluster synthesis on Isu scaffold proteins EMBO J., 25 (2006),pp. 184-195
    [70]
    Yang, H., Yang, S., Li, Y. et al. Plant Physiol., 145 (2007),pp. 135-146
    [71]
    Zhang, S., Wang, L., Hao, Y. et al. Mitochondrion, 8 (2008),pp. 205-210
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