NMAT4, A maturase factor required for nad1 pre-mRNA processing and maturation, is essential for holocomplex i biogenesis in Arabidopsis mitochondria

Plant Journal

Volumn 78, Issue 2, 2014, Pages 253-268

  Cohen, Sigal ^a   Zmudjak, Michal ^a   Colas Des Francs Small, Catherine ^b   Malik, Sunita ^c   Shaya, Felix ^d   Keren, Ido ^a,e   Belausov, Eduard ^d   Many, Yair ^d   Brown, Gregory G ^c   Small, Ian ^b   Ostersetzer Biran, Oren ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c MCGILL UNIVERSITY   (Canada)

^d VOLCANI CENTER   (Israel)

^e STONY BROOK UNIVERSITY   (United States)

Author keywords

Arabidopsis; group II intron; maturase; mitochondria; respiration; splicing

Indexed keywords

CABLE JOINTING; GENES; NUCLEIC ACIDS; PLANTS (BOTANY); PROTEINS; SEED;

ARABIDOPSIS; GROUP II INTRON; MATURASE; OPEN READING FRAME; PROTEIN COFACTORS; RESPIRATION; RESPIRATORY FUNCTION; SEEDLING ESTABLISHMENT;

MITOCHONDRIA;

ARABIDOPSIS; BACTERIA (MICROORGANISMS); EUKARYOTA; MAGNOLIOPHYTA;

ARABIDOPSIS PROTEIN; MESSENGER RNA; MITOCHONDRIAL PROTEIN; NAD1 PROTEIN, ARABIDOPSIS; NMAT4 PROTEIN, ARABIDOPSIS; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; RNA PRECURSOR;

ARABIDOPSIS; GENETICS; GERMINATION; GROWTH, DEVELOPMENT AND AGING; INTRON; METABOLISM; MITOCHONDRION; PHENOTYPE; PHYSIOLOGY; RNA PROCESSING; RNA SPLICING; SEEDLING; ULTRASTRUCTURE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GERMINATION; INTRONS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; NADH DEHYDROGENASE; PHENOTYPE; RNA PRECURSORS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA SPLICING; RNA, MESSENGER; SEEDLING;

EID: 84898469256     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12466     Document Type: Article

References (95)

1. Adams, K.L., Qiu, Y.-L., Stoutemyer, M., and, Palmer, J.D., (2002) Punctuated evolution of mitochondrial gene content: high and variable rates of mitochondrial gene loss and transfer to the nucleus during angiosperm evolution. Proc. Natl Acad. Sci. USA, 99, 9905-9912.
2. Ahlert, D., Piepenburg, K., Kudla, J., and, Bock, R., (2006) Evolutionary origin of a plant mitochondrial group II intron from a reverse transcriptase/maturase-encoding ancestor. J. Plant. Res. 119, 363-371.
3. Antonicka, H., Ogilvie, I., Taivassalo, T., Anitori, R.P., Haller, R.G., Vissing, J., Kennaway, N.G., and, Shoubridge, E.A., (2003) Identification and characterization of a common set of complex I assembly intermediates in mitochondria from patients with complex I deficiency. J. Biol. Chem. 278, 43081-43088.
4. Baradaran, R., Berrisford, J.M., Minhas, G.S., and, Sazanov, L.A., (2013) Crystal structure of the entire respiratory complex I. Nature, 494, 443-448.
5. Barkan, A., (2004) Intron splicing in plant organelles. In Molecular Biology and Biotechnology of Plant Organelles (, Daniell, H., and, Chase, C., eds). Dordrecht, The Netherlands: Kluwer Academic Publishers, pp. 281-308.
6. Bonen, L., (2008) Cis- and trans-splicing of group II introns in plant mitochondria. Mitochondrion, 8, 26-34.
7. Brennicke, A., and, Leaver, C.J., (2007) Mitochondrial genome organisation and expression in plants. Encyclopedia of Life Sciences. Chichester, UK: Wiley.
8. Candales, M.A., Duong, A., Hood, K.S., Li, T., Neufeld, R.A.E., Sun, R., McNeil, B.A., Wu, L., Jarding, A.M., and, Zimmerly, S., (2011) Database for bacterial group II introns. Nucleic Acids Res. 40, 187-190.
9. Cardol, P., Matagne, R.F., and, Remacle, C., (2002) Impact of mutations affecting ND mitochondria-encoded subunits on the activity and assembly of complex I in Chlamydomonas. Implication for the structural organization of the enzyme. J. Mol. Biol. 319, 1211-1221.
10. Carrie, C., Murcha, M.W., Kuehn, K., et al. (2008) Type II NAD(P)H dehydrogenases are targeted to mitochondria and chloroplasts or peroxisomes in Arabidopsis thaliana. FEBS Lett. 582, 3073-3079.
11. Carrie, C., Giraud, E., Duncan, O., et al. (2010) Conserved and novel functions for Arabidopsis thaliana MIA40 in assembly of proteins in mitochondria and peroxisomes. J. Biol. Chem. 285, 36138-36148.
12. Cenik, C., Chua, H.N., Zhang, H., Tarnawsky, S.P., Akef, A., Derti, A., Tasan, M., Moore, M.J., Palazzo, A.F., and, Roth, F.P., (2011) Genome analysis reveals interplay between - UTR introns and nuclear mRNA export for secretory and mitochondrial genes. PLoS Genet. 7, e1001366.
13. Clifton, R., Lister, R., Parker, K., Sappl, P., Elhafez, D., Millar, A., Day, D., and, Whelan, J., (2005) Stress-induced co-expression of alternative respiratory chain components in Arabidopsis thaliana. Plant Mol. Biol. 58, 193-212.
14. 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.
15. Colas des Francs-Small, C., and, Small, I., (2013) Surrogate mutants for studying mitochondrially encoded functions. Biochimie, doi: 10.1016/j.biochi. 2013.1008.1019. (in press).
16. Colas des Francs-Small, C., Kroeger, T., Zmudjak, M., Ostersetzer-Biran, O., Rahimi, N., Small, I., and, Barkan, A., (2012) A PORR domain protein required for rpl2 and ccmFc intron splicing and for the biogenesis of c-type cytochromes in Arabidopsis mitochondria. Plant J. 69, 996-1005.
17. Cousineau, B., Smith, D., Lawrence-Cavanagh, S., Mueller, J.E., Yang, J., Mills, D., Manias, D., Dunny, G., Lambowitz, A.M., and, Belfort, M., (1998) Retrohoming of a bacterial group II intron: mobility via complete reverse splicing, independent of homologous DNA recombination. Cell, 94, 451-462.
18. Cousineau, B., Lawrence, S., Smith, D., and, Belfort, M., (2000) Retrotransposition of a bacterial group II intron. Nature, 404, 1018-1021.
19. Dlakic, M., and, Mushegian, A., (2011) Prp8, the pivotal protein of the spliceosomal catalytic center, evolved from a retroelement-encoded reverse transcriptase. RNA, 17, 799-808.
20. Dombrovska, O., and, Qiu, Y.-L., (2004) Distribution of introns in the mitochondrial gene nad1 in land plants: phylogenetic and molecular evolutionary implications. Mol. Phylogenet. Evol. 32, 246-263.
21. Dutilleul, C., Garmier, M., Noctor, G., Mathieu, C., Chetrit, P., Foyer, C.H., and, de Paepe, R., (2003) Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. Plant Cell, 15, 1212-1226.
22. Dutilleul, C., Lelarge, C., Prioul, J.L., De Paepe, R., Foyer, C.H., and, Noctor, G., (2005) Mitochondria-driven changes in leaf NAD status exert a crucial influence on the control of nitrate assimilation and the integration of carbon and nitrogen metabolism. Plant Physiol. 139, 64-78.
23. Ellis, M., Egelund, J., Schultz, C.J., and, Bacic, A., (2010) Arabinogalactan proteins: key regulators at the cell surface? Plant Physiol. 153, 403-419.
24. 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.
25. Emanuelsson, O., Nielsen, H., Brunak, S., and, von Heijne, G., (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300, 1005-1016.
26. Falcon de Longevialle, A., Meyer, E.H., Andres, C., Taylor, N.L., Lurin, C., Millar, A.H., and, Small, I.D., (2007) The pentatricopeptide repeat gene OTP43 is required for trans-splicing of the mitochondrial nad1 intron 1 in Arabidopsis thaliana. Plant Cell, 19, 3256-3265.
27. Focks, N., and, Benning, C., (1998) wrinkled1: a novel, low-seed-oil mutant of Arabidopsis with a deficiency in the seed-specific regulation of carbohydrate metabolism. Plant Physiol. 118, 91-101.
28. Forner, J., Weber, B., Thuss, S., Wildum, S., and, Binder, S., (2007) Mapping of mitochondrial mRNA termini in Arabidopsis thaliana: t-elements contribute to - and 3- end formation. Nucleic Acids Res. 35, 3676-3692.
29. Gagliardi, D., and, Binder, S., (2007) Expression of the plant mitochondrial genome. In Plant Mitochondria (, Logan, D., ed.). Ames, IA: Blackwell Publishing, pp. 50-95.
30. Gallie, D.R., (2013) l -Ascorbic acid: a multifunctional molecule supporting plant growth and development. Scientifica, 1, 1-24.
31. Garmier, M., Carroll, A.J., Delannoy, E., Vallet, C., Day, D.A., Small, I.D., and, Millar, A.H., (2008) Complex I dysfunction redirects cellular and mitochondrial metabolism in Arabidopsis. Plant Physiol. 148, 1324-1341.
32. Gleave, A.P., (1992) A versatile binary vector system with a T-DNA organizational-structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol. Biol. 20, 1203-1207.
33. Guo, W., and, Mower, J., (2013) Evolution of plant mitochondrial intron-encoded maturases: frequent lineage-specific loss and recurrent intracellular transfer to the nucleus. J. Mol. Evol. 77, 43-54.
34. 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.
35. Gutierres, S., Combettes, B., De Paepe, R., Mirande, M., Lelandais, C., Vedel, F., and, Chetrit, P., (1999) In the Nicotiana sylvestris CMSII mutant, a recombination-mediated change - to the first exon of the mitochondrial nad1 gene is associated with lack of the NADH:ubiquinone oxidoreductase (complex I) NAD1 subunit. Eur. J. Biochem. 261, 361-370.
36. Hruz, T., Laule, O., Szabo, G., Wessendorp, F., Bleuler, S., Oertle, L., Widmayer, P., Gruissem, W., and, Zimmermann, P., (2008) Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv. Bioinformatics, 2008, 420747.
37. Jadid, N., Mialoundama, A.S., Heintz, D., et al. (2011) DOLICHOL PHOSPHATE MANNOSE SYNTHASE1 mediates the biogenesis of isoprenyl-linked glycans and influences development, stress response, and ammonium hypersensitivity in Arabidopsis. Plant Cell, 23, 1985-2005.
38. Kabeya, Y., and, Sato, N., (2005) Unique translation initiation at the second AUG codon determines mitochondrial localization of the phage-type RNA polymerases in the moss Physcomitrella patens. Plant Physiol. 138, 369-382.
39. Karpova, O.V., and, Newton, K.J., (1999) A partially assembled complex I in NAD4-deficient mitochondria of maize. Plant J. 17, 511-521.
40. Karpova, O.V., Kuzmin, E.V., Elthon, T.E., and, Newton, K.J., (2002) Differential expression of alternative oxidase genes in maize mitochondrial mutants. Plant Cell, 14, 3271-3284.
41. Kazak, L., Reyes, A., Duncan, A.L., Rorbach, J., Wood, S.R., Brea-Calvo, G., Gammage, P.A., Robinson, A.J., Minczuk, M., and, Holt, I.J., (2013) Alternative translation initiation augments the human mitochondrial proteome. Nucleic Acids Res. 41, 2354-2369.
42. Keren, I., Klipcan, L., Bezawork-Geleta, A., Kolton, M., Shaya, F., and, Ostersetzer-Biran, O., (2008) Characterization of the molecular basis of group II intron RNA recognition by CRS1-CRM domains. J. Biol. Chem. 283, 23333-23342.
43. Keren, I., Bezawork-Geleta, A., Kolton, M., Maayan, I., Belausov, E., Levy, M., Mett, A., Gidoni, D., Shaya, F., and, Ostersetzer-Biran, O., (2009) AtnMat2, a nuclear-encoded maturase required for splicing of group-II introns in Arabidopsis mitochondria. RNA, 15, 2299-2311.
44. Keren, I., Tal, L., des Francs-Small, C.C., Araújo, W.L., Shevtsov, S., Shaya, F., Fernie, A.R., Small, I., and, Ostersetzer-Biran, O., (2012) nMAT1, a nuclear-encoded maturase involved in the trans-splicing of nad1 intron 1, is essential for mitochondrial complex I assembly and function. Plant J. 71, 413-426.
45. Klodmann, J., Sunderhaus, S., Nimtz, M., Jänsch, L., and, Braun, H.-P., (2010) Internal architecture of mitochondrial complex I from Arabidopsis thaliana. Plant Cell, 22, 797-810.
46. Knoop, V., (2012) Seed plant mitochondrial genomes: complexity evolving. In Genomics of Chloroplasts and Mitochondria (, Bock, R., and, Knoop, V., eds). East Lansing, MI: Michigan State University, pp. 175-195.
47. Köhler, D., Schmidt-Gattung, S., and, Binder, S., (2010) The DEAD-box protein PMH2 is required for efficient group II intron splicing in mitochondria of Arabidopsis thaliana. Plant Mol. Biol. 72, 459-467.
48. Koprivova, A., Colas des Francs-Small, C., Calder, G., Mugford, S.T., Tanz, S., Lee, B.-R., Zechmann, B., Small, I., and, Kopriva, S., (2010) Identification of a pentatricopeptide repeat protein implicated in splicing of intron 1 of mitochondrial nad7 transcripts. J. Biol. Chem. 285, 32192-32199.
49. Kühn, K., Carrie, C., Giraud, E., Wang, Y., Meyer, E.H., Narsai, R., Colas des Francs-Small, C., Zhang, B., Murcha, M.W., and, Whelan, J., (2011) The RCC1 family protein RUG3 is required for splicing of nad2 and complex I biogenesis in mitochondria of Arabidopsis thaliana. Plant J. 67, 1067-1080.
50. Laemmli, U.K., (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
51. Lamattina, L., Gonzalez, D., Gualberto, J., and, Grienenberger, J.-M., (1993) Higher plant mitochondria encode an homologue of the nuclear-encoded 30-kDa subunit of bovine mitochondrial complex I. Eur. J. Biochem. 217, 831-838.
52. Lambowitz, A.M., and, Zimmerly, S., (2011) Group II introns: mobile ribozymes that invade DNA. Cold Spring Harb. Perspect. Biol. 3, a003616.
53. Law, S.R., Narsai, R., Taylor, N.L., Delannoy, E., Carrie, C., Giraud, E., Millar, A.H., Small, I., and, Whelan, J., (2012) Nucleotide and RNA metabolism prime translational initiation in the earliest events of mitochondrial biogenesis during Arabidopsis germination. Plant Physiol. 158, 1610-1627.
54. Lee, B.H., Lee, H., Xiong, L., and, Zhu, J.K., (2002) A mitochondrial complex I defect impairs cold-regulated nuclear gene expression. Plant Cell, 14, 1235-1251.
55. Lee, C.P., Taylor, N.L., and, Millar, A.H., (2013) Recent advances in the composition and heterogeneity of the Arabidopsis mitochondrial proteome. Front. Plant Sci. 4, 4.
56. 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.
57. Matsuura, M., Noah, J.W., and, Lambowitz, A.M., (2001) Mechanism of maturase-promoted group II intron splicing. EMBO J. 20, 7259-7270.
58. Meyer, E.H., Tomaz, T., Carroll, A.J., Estavillo, G., Delannoy, E., Tanz, S.K., Small, I.D., Pogson, B.J., and, Millar, A.H., (2009) Remodeled respiration in ndufs4 with low phosphorylation efficiency suppresses Arabidopsis germination and growth and alters control of metabolism at night. Plant Physiol. 151, 603-619.
59. Meyer, E.H., Solheim, C., Tanz, S.K., Bonnard, G., and, Millar, A.H., (2011) Insights into the composition and assembly of the membrane arm of plant complex I through analysis of subcomplexes in Arabidopsis mutant lines. J. Biol. Chem. 286, 26081-26092.
60. Mireau, H., Lancelin, D., and, Small, I.D., (1996) The same Arabidopsis gene encodes both cytosolic and mitochondrial alanyl-tRNA synthetases. Plant Cell, 8, 1027-1039.
61. Mohr, G., and, Lambowitz, A.M., (2003) Putative proteins related to group II intron reverse transcriptase/maturases are encoded by nuclear genes in higher plants. Nucleic Acids Res. 31, 647-652.
62. Mohr, S., Matsuura, M., Perlman, P.S., and, Lambowitz, A.M., (2006) A DEAD-box protein alone promotes group II intron splicing and reverse splicing by acting as an RNA chaperone. Proc. Natl Acad. Sci. USA, 103, 3569-3574.
63. Nakagawa, N., and, Sakurai, N., (2006) A mutation in At-nMat1a, which encodes a nuclear gene having high similarity to group II intron maturase, causes impaired splicing of mitochondrial nad4 transcript and altered carbon metabolism in Arabidopsis thaliana. Plant Cell Physiol. 47, 772-783.
64. Narsai, R., Law, S.R., Carrie, C., Xu, L., and, Whelan, J., (2011) In depth temporal transcriptome profiling reveals a crucial developmental switch with roles for RNA processing and organelle metabolism that are essential for germination in Arabidopsis thaliana. Plant Physiol. 157, 1342-1362.
65. 2+ concentration on group II intron RNA folding investigated by UV cross-linking. Biochemistry, 42, 12466-12480.
66. Ossowski, S., Schwab, R., and, Weigel, D., (2008) Gene silencing in plants using artificial microRNAs and other small RNAs. Plant J. 53, 674-690.
67. Ostersetzer, O., Cooke, A.M., Watkins, K.P., and, Barkan, A., (2005) CRS1, a chloroplast group II intron splicing factor, promotes intron folding through specific interactions with two intron domains. Plant Cell, 17, 241-255.
68. Perales, M., Eubel, H., Heinemeyer, J., Colaneri, A., Zabaleta, E., and, Braun, H.-P., (2005) Disruption of a nuclear gene encoding a mitochondrial gamma carbonic anhydrase reduces complex I and supercomplex I + III2 levels and alters mitochondrial physiology in Arabidopsis. J. Mol. Biol. 350, 263-277.
69. Pineau, B., Layoune, O., Danon, A., and, De Paepe, R., (2008) l -galactono-1,4-lactone dehydrogenase is required for the accumulation of plant respiratory complex I. J. Biol. Chem. 283, 32500-32505.
70. Pyle, A.M., and, Lambowitz, A.M., (1999) Group II introns: ribozymes that splice RNA and invade DNA. In The RNA World, 3rd edn (, Gesteland, R., Cech, T.R., and, Atkins, J., eds). Cold Spring Harbor, NY: Cold Spring Harbor Press, pp. 469-505.
71. Rasmusson, A.G., Geisler, D.A., and, Møller, I.M., (2008) The multiplicity of dehydrogenases in the electron transport chain of plant mitochondria. Mitochondrion, 8, 47-60.
72. Remacle, C., Baurain, D., Cardol, P., and, Matagne, R.F., (2001) Mutants of Chlamydomonas reinhardtii deficient in mitochondrial complex I: characterization of two mutations affecting the nd1 coding sequence. Genetics, 158, 1051-1060.
73. Rigas, S., Daras, G., Laxa, M., Marathias, N., Fasseas, C., Sweetlove, L.J., and, Hatzopoulos, P., (2009) Role of Lon1 protease in post-germinative growth and maintenance of mitochondrial function in Arabidopsis thaliana. New Phytol. 181, 588-600.
74. 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.
75. Sato, S., Nakamura, Y., Kaneko, T., Asamizu, E., and, Tabata, S., (1999) Complete structure of the chloroplast genome of Arabidopsis thaliana. DNA Res. 6, 283-290.
76. Schertl, P., Sunderhaus, S., Klodmann, J., Gergoff Grozeff, G.E., Bartoli, C.G., and, Braun, H.-P., (2012) l -galactono-1,4-lactone dehydrogenase (GLDH) forms part of three subcomplexes of mitochondrial complex I in Arabidopsis thaliana. J. Biol. Chem. 283, 32500-32505.
77. Schmitz-Linneweber, C., and, Small, I., (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci. 13, 663-670.
78. Schwab, R., Ossowski, S., Riester, M., Warthmann, N., and, Weigel, D., (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell, 18, 1121-1133.
79. Small, I., Peeters, N., Legeai, F., and, Lurin, C., (2004) Predotar: a tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics, 4, 1581-1590.
80. Strubin, M., Long, E.O., and, Mach, B., (1986) Two forms of the la antigen-associated invariant chain result from alternative initiations at two in-phase AUGs. Cell, 47, 619-625.
81. Sunderhaus, S., Dudkina, N.V., Jansch, L., Klodmann, J., Heinemeyer, J., Perales, M., Zabaleta, E., Boekema, E.J., and, Braun, H.P., (2006) Carbonic anhydrase subunits form a matrix-exposed domain attached to the membrane arm of mitochondrial complex I in plants. J. Biol. Chem. 281, 6482-6488.
82. Sunderland, P.A., West, C.E., Waterworth, W.M., and, Bray, C.M., (2006) An evolutionarily conserved translation initiation mechanism regulates nuclear or mitochondrial targeting of DNA ligase 1 in Arabidopsis thaliana. Plant J. 47, 356-367.
83. Tabata, K., Ôba, K., Suzuki, K., and, Esaka, M., (2001) Generation and properties of ascorbic acid-deficient transgenic tobacco cells expressing antisense RNA for l -galactono-1,4-lactone dehydrogenase. Plant J. 27, 139-148.
84. Takenaka, M., Verbitskiy, D., van der Merwe, J.A., Zehrmann, A., and, Brennicke, A., (2008) The process of RNA editing in plant mitochondria. Mitochondrion, 8, 35-46.
85. Tanz, S.K., Castleden, I., Hooper, C.M., Vacher, M., Small, I., and, Millar, H.A., (2013) SUBA3: a database for integrating experimentation and prediction to define the SUBcellular location of proteins in Arabidopsis. Nucleic Acids Res. 41, D1185-D1191.
86. Tomaz, T., Bagard, M., Pracharoenwattana, I., Lindén, P., Lee, C.P., Carroll, A.J., Ströher, E., Smith, S.M., Gardeström, P., and, Millar, A.H., (2010) Mitochondrial malate dehydrogenase lowers leaf respiration and alters photorespiration and plant growth in Arabidopsis. Plant Physiol. 154, 1143-1157.
87. Ugalde, C., Vogel, R., Huijbens, R., van den Heuvel, B., Smeitink, J., and, Nijtmans, L., (2004) Human mitochondrial complex I assembles through the combination of evolutionary conserved modules: a framework to interpret complex I deficiencies. Hum. Mol. Genet. 13, 2461-2472.
88. Unseld, M., Marienfeld, J.R., Brandt, P., and, Brennicke, A., (1997) The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat. Genet. 15, 57-61.
89. Veljovic-Jovanovic, S.D., Pignocchi, C., Noctor, G., and, Foyer, C.H., (2001) Low ascorbic acid in the vtc-1 mutant of Arabidopsis is associated with decreased growth and intracellular redistribution of the antioxidant system. Plant Physiol. 127, 426-435.
90. Wamboldt, Y., Mohammed, S., Elowsky, C., Wittgren, C., de Paula, W.B.M., and, Mackenzie, S.A., (2009) Participation of leaky ribosome scanning in protein dual targeting by alternative translation initiation in higher plants. Plant Cell, 21, 157-167.
91. Wank, H., SanFilippo, J., Singh, R.N., Matsuura, M., and, Lambowitz, A.M., (1999) A reverse transcriptase/maturase promotes splicing by binding at its own coding segment in a group II intron RNA. Mol. Cell, 4, 239-250.
92. Xu, Y.-Z., Arrieta-Montiel, M.P., Virdi, K.S., et al. (2011) MutS HOMOLOG1 is a nucleoid protein that alters mitochondrial and plastid properties and plant response to high light. Plant Cell, 23, 3428-3441.
93. Yamaguchi, M., and, Hatefi, Y., (1993) Mitochondrial NADH:ubiquinone oxidoreductase (complex I): proximity of the subunits of the flavoprotein and the iron-sulfur protein subcomplexes. Biochemistry, 32, 1935-1939.
94. Yoshida, K., and, Noguchi, K., (2009) Differential gene expression profiles of the mitochondrial respiratory components in illuminated Arabidopsis leaves. Plant Cell Physiol. 50, 1449-1462.
95. Zmudjak, M., Colas des Francs-Small, C., Keren, I., Shaya, F., Belausov, E., Small, I., and, Ostersetzer-Biran, O., (2013) mCSF1, a nucleus-encoded CRM protein required for the processing of many mitochondrial introns, is involved in the biogenesis of respiratory complexes I and IV in Arabidopsis. New Phytol. 199, 379-394.