Coordination of plant mitochondrial biogenesis: Keeping pace with cellular requirements

Frontiers in Plant Science

Volumn 4, Issue JAN, 2014, Pages

  Welchen, Elina ^a   García, Lucila ^a   Mansilla, Natanael ^a   Gonzalez, Daniel H ^a  

^a UNIVERSIDAD NACIONAL DEL LITORAL   (Argentina)

Author keywords

Coordination; Mitochondrial biogenesis; Mitochondrial dynamics; Post transcriptional gene regulation; Retrograde signal; Site II

Indexed keywords

EID: 84900838657     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00551     Document Type: Review

References (122)

1. Attallah, C. V., Welchen, E., Pujol, C., Bonnard, G., and Gonzalez, D. H. (2007). Characterization of Arabidopsis thaliana genes encoding functional homologues of the yeast metal chaperone Cox19p, involved in cytochrome c oxidase biogenesis. Plant Mol. Biol. 65, 343-355. doi: 10.1007/s11103-007-9224-1
2. Baudisch, B., Langner, U., Garz, I., and Klösgen, R. B. (2014). The exception proves the rule? Dual targeting of nuclear-encoded proteins into endosymbiotic organelles. New Phytol. 201, 80-90. doi: 10.1111/nph.12482
3. Bian, Z., Li, L. M., Tang, R., Hou, D. X., Chen, X., Zhang, C. Y., et al. (2010). Identification of mouse liver mitochondria-associated miRNAs and their potential biological functions. Cell Res. 20, 1076-1078. doi: 10.1038/cr.2010.119
4. Binder, S., and Brennicke, A. (2003). Gene expression in plant mitochondria: transcriptional and post-transcriptional control. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 181-189. doi: 10.1098/rstb.2002.1179
5. Brumme, S., Kruft, V., Schmitz, U. K., and Braun, H. P. (1998). New insights into the co-evolution of cytochrome c reductase and the mitochondrial processing peptidase. J. Biol. Chem. 273, 13143-13149. doi: 10.1074/jbc.273.21.13143
6. Busi, M. V., Gomez-Lobato, M. E., Rius, S. P., Turowski, V. R., Casati, P., Zabaleta, E. J., et al. (2011). Effect of mitochondrial dysfunction on carbon metabolism and gene expression in flower tissues of Arabidopsis thaliana. Mol. Plant 4, 127-143. doi: 10.1093/mp/ssq065
7. Carrie, C., and Small, I. (2013). A reevaluation of dual-targeting of proteins to mitochondria and chloroplasts. Biochim. Biophys. Acta 1833, 253-259. doi: 10.1016/j.bbamcr.2012.05.029
8. Carrie, C., Giraud, E., Duncan, O., Xu, L., Wang, Y., Huang, S., 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. doi: 10.1074/jbc.M110.121202
9. Carrie, C., Kühn, K., Murcha, M. W., Duncan, O., Small, I. D., O'Toole, N., et al. (2009). Approaches to defining dual-targeted proteins in Arabidopsis. Plant J. 57, 1128-1139. doi: 10.1111/j.1365-313X.2008.03745.x
10. Clifton, R., Lister, R., Parker, K. L., Sappl, P. G., Elhafez, D., Millar, A. H., et al. (2005). Stress-induced co-expression of alternative respiratory chain components in Arabidopsis thaliana. Plant Mol. Biol. 58, 193-212. doi: 10.1007/s11103-005-5514-7
11. Collins, Y., Chouchani, E. T., James, A. M., Menger, K. E., Cochemé, H. M., and Murphy, M. P. (2012). Mitochondrial redox signalling at a glance. J. Cell Sci. 125, 801-806. doi: 10.1242/jcs.098475
12. Comelli, R. N., and Gonzalez, D. H. (2009). Divergent regulatory mechanisms in the response of respiratory chain component genes to carbohydrates suggests a model for gene evolution after duplication. Plant Signal. Behav. 4, 1179-1181. doi: 10.4161/psb.4.12.10045
13. Comelli, R. N., Viola, I. L., and Gonzalez, D. H. (2009). Characterization of promoter elements required for expression and induction by sucrose of the Arabidopsis COX5b-1 nuclear gene, encoding the zinc-binding subunit of cytochrome c oxidase. Plant Mol. Biol. 69, 729-743. doi: 10.1007/s11103-008-9451-0
14. Comelli, R. N., Welchen, E., Kim H. J., Hong, J. C., and Gonzalez, D. H. (2012). Delta subclass HD-Zip proteins and a B-3 AP2/ERF transcription factor interact with promoter elements required for expression of the Arabidopsis cytochrome c oxidase 5b-1 gene. Plant Mol. Biol. 80, 157-167. doi: 10.1007/s11103-012-9935-9
15. Cvetkovska, M., and Vanlerberghe, G. C. (2013). Alternative oxidase impacts the plant response to biotic stress by influencing the mitochondrial generation of reactive oxygen species. Plant Cell Environ. 36, 721-732. doi: 10.1111/pce.12009
16. Das, S., Ferlito, M., Kent, O. A., Fox-Talbot, A., Wang, R., Liu, D., et al. (2012). Nuclear miRNA regulates the mitochondrial genome in the heart. Circ. Res. 110, 1596-1603. doi: 10.1161/CIRCRESAHA.112.267732
17. De Clercq, I., Vermeirssen, V., Van Aken, O., Vandepoelie, K., Murcha, M. W., Law, S. R., et al. (2013). The membrane-bound NAC transcription factor ANAC013 functions in mitochondrial retrograde regulation of the oxidative stress response in Arabidopsis. Plant Cell 25, 3472-3490. doi: 10.1105/tpc.113.117168
18. Dojcinovic, D., Krosting, J., Harris, A. J., Wagner, D. J., and Rhoads, D. M. (2005). Identification of a region of the Arabidopsis AtAOX1apromoter necessary for mitochondrial retrograde regulation of expression. Plant Mol. Biol.58, 159-175. doi: 10.1007/s11103-005-5390-1
19. Dröse, S., and Brandt, U. (2012). Molecular mechanisms of superoxide production by the mitochondrial respiratory chain. Adv. Exp. Med. Biol. 748, 145-169. doi: 10.1007/978-1-4614-3573-0_6
20. Duchêne, A. M., and Giegé, P. (2012). Dual localized mitochondrial and nuclear proteins as gene expression regulators in plants? Front. Plant Sci. 3:221. doi: 10.3389/fpls.2012.00221
21. Duncan, O., Murcha, M. W., and Whelan, J. (2013). Unique components of the plant mitochondrial protein import apparatus. Biochim. Biophys. Acta 1833, 304-313. doi: 10.1016/j.bbamcr.2012.02.015
22. Elorza, A., León, G., Gómez, I., Mouras, A., Holuigue, L., Araya, A., et al. (2004). Nuclear SDH2-1 and SDH2-2 genes, encoding the iron-sulfur subunit of mitochondrial complex II in Arabidopsis, have distinct cell-specific expression patterns and promoter activities. Plant Physiol. 136, 4072-4087. doi: 10.1104/pp.104.049528
23. Finkemeier, I., Goodman, M., Lamkemeyer, P., Kandlbinder, A., Sweetlove, L. J., and Dietz, K. J. (2005). The mitochondrial type II peroxiredoxin F is essential for redox homeostasis and root growth of Arabidopsis thaliana under stress. J. Biol. Chem. 280, 12168-12180. doi: 10.1074/jbc.M413189200
24. Finkemeier, I., König, A. C., Heard, W., Nunes-Nesi, A., Pham, P. A., Leister, D., et al. (2013). Transcriptomic analysis of the role of carboxylic acids in metabolite signaling in Arabidopsis leaves. Plant Physiol. 162, 239-253. doi: 10.1104/pp.113.214114
25. Foyer, C. H., and Noctor, G. (2011). Ascorbate and glutathione: the heart of the redox hub. Plant Physiol. 155, 2-18. doi: 10.1104/pp.110.167569
26. Friedman, J. R., Lackner, L. L., West, M., DiBenedetto, J. R., Nunnari, J., and Voeltz, G. K. (2011). ER tubules mark sites of mitochondrial division. Science 334, 358-362. doi: 10.1126/science.1207385
27. Gagliardi, D., and Binder, S. (2007). "Expression of the plant mitochondrial genome, " in Annual Plant Reviews, Vol. 31, Plant Mitochondria, ed. D. C. Logan (Hoboken, NJ: John Wiley & Sons, Inc.), 50-96.
28. Gibala, M., Kicia, M., Sakamoto, W., Gola, E. M., Kubrakiewicz, J., Smakowska, E., et al. (2009). The lack of mitochondrial AtFtsH4 protease alters Arabidopsis leaf morphology at the late stage of rosette development under short-day photoperiod. Plant J. 59, 685-699. doi: 10.1111/j.1365-313X.2009.03907.x
29. Giegé, P., Sweetlove, L. J., and Leaver, C. (2005). Coordination of nuclear and mitochondrial genome expression during mitochondrial biogenesis in Arabidopsis. Plant Cell 17, 1497-1512. doi: 10.1105/tpc.104.030254
30. Giraud, E., Ng, S., Carrie, C., Duncan, O., Low, J., Lee, C. P., et al. (2010). TCP transcription factors link the regulation of genes encoding mitochondrial proteins with the circadian clock in Arabidopsis thaliana. Plant Cell 22, 3921-3934. doi: 10.1105/tpc.110.074518
31. Giraud, E., Van Aken, O., Ho, L. H. M., and Whelan, J. (2009). The transcription factor ABI4 is a regulator of mitochondrial retrograde expression of alternative oxidase1a. Plant Physiol. 150, 1286-1296. doi: 10.1104/pp.109.139782
32. Giraud, E., Van Aken, O., Uggalla, V., and Whelan, J. (2012). REDOX regulation of mitochondrial function in plants. Plant Cell Environ. 35, 271-280. doi: 10.1111/j.1365-3040.2011.02293.x
33. Gonzalez, D. H., Welchen, E., Attallah, C. V., Comelli, R. N., and Mufarrege, E. F. (2007). Transcriptional coordination of the biogenesis of the oxidative phosphorylation machinery in plants. Plant J. 5, 105-116. doi: 10.1111/j.1365-313X.2007.03121.x
34. Green, M. A., and Fry, S. C. (2005). Vitamin C degradation in plant cells via enzymatic hydrolysis of 4-O-oxalyl-L-threonate. Nature 433, 83-87. doi: 10.1038/nature03172
35. Gupta, K. J., Shah, J. K., Brotman, Y., Jahnke, K., Willmitzer, L., Kaiser, W. M., et al. (2012). Inhibition of aconitase by nitric oxide leads to induction of the alternative oxidase and to a shift of metabolism towards biosynthesis of amino acids. J. Exp. Bot. 63, 1773-1784. doi: 10.1093/jxb/ers053
36. Hamasaki, H., Yoshizumi, T., Takahashi, N., Higuchi, M., Kuromori, T., Imura, Y., et al. (2012). SD3, an Arabidopsis thaliana homolog of TIM21, affects intra-cellular ATP levels and seedling development. Mol. Plant 5, 461-471. doi: 10.1093/mp/ssr088
37. Hammani, K., Gobert, A., Hleibieh, K., Choulier, L., Small, I., and Giegé, P. (2011a). An Arabidopsis dual-localized pentatricopeptide repeat protein interacts with nuclear proteins involved in gene expression regulation. Plant Cell 23, 730-740. doi: 10.1105/tpc.110.081638
38. Hammani, K., Gobert, A., Small, I., and Giegé, P. (2011b). A PPR protein involved in regulating nuclear genes encoding mitochondrial proteins? Plant Signal. Behav. 6, 748-750. doi: 10.4161/psb.6.5.15148
39. Hicks, L. M., Cahoon, R. E., Bonner, E. R., Rivard, R. S., Sheffield, J., and Jez, J. M. (2007). Thiol-based regulation of redox-active glutamate-cysteine ligase from Arabidopsis thaliana. Plant Cell 19, 2653-2661. doi: 10.1105/tpc.107.052597
40. Ho, L. H. M., Giraud, E., Uggalla, V., Lister, R., Clifton, R., Glen, A., et al. (2008). Identification of regulatory pathways controlling gene expression of stress-responsive mitochondrial proteins in Arabidopsis. Plant Physiol. 147, 1858-1873. doi: 10.1104/pp.108.121384
41. Howell, K. A., Millar, A. H., and Whelan, J. (2006). Ordered assembly of mitochondria during rice germination begins with pro-mitochondrial structures rich in components of the protein import apparatus. Plant Mol. Biol. 60, 201-223. doi: 10.1007/s11103-005-3688-7
42. Howell, K. A., Millar, A. H., and Whelan, J. (2007). Building the powerhouse: what are the signals involved in plant mitochondrial biogenesis? Plant Signal. Behav. 2, 428-430. doi: 10.4161/psb.2.5.4464
43. Howell, K. A., Narsai, R., Carroll, A., Ivanova, A., Lohse, M., Usadel, B., et al. (2009). Mapping metabolic and transcript temporal switches during germination in rice highlights specific transcription factors and the role of RNA instability in the germination process. Plant Physiol. 149, 961-998. doi: 10.1104/pp.108.129874
44. Hyde, B. B., Twig, G., and Shirihai, O. S. (2010). Organellar vs cellular control of mitochondrial dynamics. Semin. Cell Dev. Biol. 21, 575-581. doi: 10.1016/j.semcdb.2010.01.003
45. Islam, S., and Takagi, S. (2010). Co-localization of mitochondria with chloroplasts is a light-dependent reversible response. Plant Signal. Behav. 5, 146-152. doi: 10.4161/psb.5.2.10410
46. Jones-Rhoades, M. W., and Bartel, D. P. (2004). Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol. Cell. 14, 787-799. doi: 10.1016/j.molcel.2004.05.027
47. Kamarajan, B. P., Sridhar, J., and Subramanian, S. (2012). In silico prediction of MicroRNAs in plant mitochondria. Int. J. Bioautomat. 12, 251-262.
48. Kerchev, P. I., Pellny, T. K., Vivancos, P. D., Kiddle, G., Hedden, P., Driscoll, S., et al. (2011). The transcription factor ABI4 Is required for the ascorbic acid-dependent regulation of growth and regulation of jasmonate-dependent defense signaling pathways in Arabidopsis. Plant Cell 23, 3319-3334. doi: 10.1105/tpc.111.090100
49. Kiddle, G., Pastori, G. M., Bernard, S., Pignocchi, C., Antoniw, J., Verrier, P. J., et al. (2003). Effects of leaf ascorbate content on defense and photosynthesis gene expression in Arabidopsis thaliana. Antioxid. Redox Signal. 5, 23-32. doi: 10.1089/152308603321223513
50. Kleine, T., and Leister, D. (2013). Retrograde signals galore. Front. Plant Sci. 12:45. doi: 10.3389/fpls.2013.00045
51. Kornmann, B. (2013). The molecular hug between the ER and the mitochondria. Curr. Opin. Cell Biol. 25, 443-448. doi: 10.1016/j.ceb.2013.02.010
52. Koussevitzky, S., Nott, A., Mockler, T. C., Hong, F., Sachetto-Martins, G., Surpin, M., et al. (2007). Signals from chloroplasts converge to regulate nuclear gene expression. Science 316, 715-719. doi: 10.1126/science. 1140516
53. Kwasniak, M., Majewski, P., Skibior, R., Adamowicz, A., Czarna, M., Sliwinska, E., et al. (2013). Silencing of the nuclear RPS10 gene encoding mitochondrial ribosomal protein alters translation in Arabidopsis mitochondria. Plant Cell 25, 1855-1867. doi: 10.1105/tpc.113.111294
54. Law, S. R., Narsai, R., Taylor, N. L., Delannoy, E., Carrie, C., Giraud, E., et al. (2012). Nucleotide and RNA metabolism prime translational initiation in the earliest events of mitochondrial biogenesis during Arabidopsis germination. Plant Physiol. 158, 1610-1627. doi: 10.1104/pp.111.192351
55. Lee C. P., Eubel H., and Millar A. H. (2010). Diurnal changes in mitochondrial function reveal daily optimization of light and dark respiratory metabolism in Arabidopsis. Mol. Cell Proteomics 9, 2125-2139. doi: 10.1074/mcp.M110.001214
56. Lee, C. P., Eubel, H., O'Toole, N., and Millar, A. H. (2008). Heterogeneity of the mitochondrial proteome for photosynthetic and non-photosynthetic Arabidopsis metabolism. Mol. Cell Proteomics 7, 1297-1316. doi: 10.1074/mcp.M700535-MCP200
57. Lee, C. P., Eubel, H., O'Toole, N., and Millar, A. H. (2011). Combining proteomics of root and shoot mitochondria and transcript analysis to define constitutive and variable components in plant mitochondria. Phytochemistry 72, 1092-1108. doi: 10.1016/j.phytochem.2010.12.004
58. 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. doi: 10.3389/fpls.2013.00004
59. Leister, D., Wang, X., Haberer, G., Mayer, C. F. X., and Kleine, T. (2011). Intracompartmental and intercompartmental transcriptional networks coordinate the expression of genes for organellar functions. Plant Physiol. 157, 386-404. doi: 10.1104/pp.111.177691
60. Liere, K., Weihe, A., and Börner, T. (2011). The transcription machineries of plant mitochondria and chloroplasts: composition, function, and regulation. J. Plant Physiol. 168, 1345-1360. doi: 10.1016/j.jplph.2011.01.005
61. Lindermayr, C., Sell, S., Müller, B., Leister, D., and Durner, J. (2010). Redox regulation of the NPR1-TGA1 system of Arabidopsis thaliana by nitric oxide. Plant Cell 22, 2894-2907. doi: 10.1105/tpc.109.066464
62. Li, P., Jiao, J., Gao, G., and Prabhakar, B. S. (2012). Control of mitochondrial activity by miRNAs. J. Cell Biochem. 113, 1104-1110. doi: 10.1002/jcb.24004
63. Livaja, M., Palmieri, M. C., von Rad, U., and Durner, J. (2008). The effect of the bacterial effector protein harpin on transcriptional profile and mitochondrial proteins of Arabidopsis thaliana. J. Proteomics 71, 148-159. doi: 10.1016/j.jprot.2008.04.002
64. Logan, D. C. (2006). Plant mitochondrial dynamics. Biochim. Biophys. Acta 1763, 430-441. doi: 10.1016/j.bbamcr.2006.01.003
65. Logan, D. C. (2010). The dynamic plant chondriome. Semin. Cell Dev. Biol. 21, 550-557. doi: 10.1016/j.semcdb.2009.12.010
66. Logan, D. C., and Leaver, C. J. (2000). Mitochondria-targeted GFP highlights the heterogeneity of mitochondrial shape, size and movement within living plant cells. J. Exp. Bot. 51, 865-871. doi: 10.1093/jexbot/51.346.865
67. Martín-Trillo, M., and Cubas, P. (2010). TCP genes: a family snapshot ten years later. Trends Plant Sci. 15, 31-39. doi: 10.1016/j.tplants.2009.11.003
68. Meyer, E. H., Tomaz, T., Carroll, A. J., Estavillo, G., Delannoy, E., Tanz, S. K., et al. (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. doi: 10.1104/pp.109.141770
69. Millar, A. H., Mittova, V., Kiddle, G., Heazlewood, J. L., Bartoli, C. G., Theodoulou, F. L., et al. (2003). Control of ascorbate synthesis by respiration and its implications for stress responses. Plant Physiol. 133, 443-447. doi: 10.1104/pp.103.028399
70. Mochizuki, N., Tanaka, R., Tanaka, A., Masuda, T., and Nagatani, A. (2008). The steady-state level of Mg-protoporphyrin IX is not a determinant of plastid-to-nucleus signaling in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 39, 15184-15189. doi: 10.1073/pnas.0803245105
71. Møller, I. M., and Sweetlove, L. J. (2010). ROS signalling-specificity is required. Trends Plant Sci. 15, 370-374. doi: 10.1016/j.tplants.2010.04.008
72. Morgan, M. J., Lehmann, M., Schwarzländer, M., Baxter, C. J., Sienkiewicz-Porzucek, A., Williams, T. C., et al. (2008). Decrease in manganese superoxide dismutase leads to reduced root growth and affects tricarboxylic acid cycle flux and mitochondrial redox homeostasis. Plant Physiol. 147, 101-114. doi: 10.1104/pp.107.113613
73. Mufarrege, E. F., Curi, G. C., and Gonzalez, D. H. (2009). Common sets of promoter elements determine the expression characteristics of three Arabidopsis genes encoding isoforms of mitochondrial cytochrome c oxidase subunit 6b. Plant Cell Physiol. 50, 1393-1399. doi: 10.1093/pcp/pcp080
74. Murcha, M. W., Wang, Y., Narsai, R., and Whelan, J. (2013). The plant mitochondrial protein import apparatus-the differences make it interesting. Biochim. Biophys. Acta doi: 10.1016/j.bbagen.2013.09.026
75. Murcha, M. W., Wang, Y., and Whelan, J. (2012). A molecular link between mitochondrial preprotein transporters and respiratory chain complexes. Plant Signal. Behav. 7, 1594-1597. doi: 10.4161/psb.22250
76. Ng, S., Ivanova, A., Duncan, O., Law, S. R., Van Aken, O., De Clercq, I., et al. (2013). A membrane-bound NAC transcription factor, ANAC017, mediates mitochondrial retrograde signaling in Arabidopsis. Plant Cell 25, 3450-3471. doi: 10.1105/tpc.113.113985
77. Obata, T., Matthes, A., Koszior, S., Lehmann, M., Araújo, W. L., Bock, R., et al. (2011). Alteration of mitochondrial protein complexes in relation to metabolic regulation under short-term oxidative stress in Arabidopsis seedlings. Phytochemistry 72, 1081-1091. doi: 10.1016/j.phytochem.2010.11.003
78. Pastori, G. M., Kiddle, G., Antoniw, J., Bernard, S., Veljovic-Jovanovic, S., Verrier, P. J., et al. (2003). Leaf vitamin C contents modulate plant defense transcripts and regulate genes that control development through hormone signaling. Plant Cell 15, 939-951. doi: 10.1105/tpc.010538
79. Peeters, N., and Small, I. (2001). Dual targeting to mitochondria and chloroplasts. Biochim. Biophys. Acta 1541, 54-63. doi: 10.1016/S0167-4889(01)00146-X
80. Peters, K., Nießen, M., Peterhänsel, C., Späth, B., Hölzle, A., Binder, S., et al. (2012). Complex I-complex II ratio strongly differs in various organs of Arabidopsis thaliana. Plant Mol. Biol. 79, 273-284. doi: 10.1007/s11103-012-9911-4
81. Polidoros, A. N., Mylona, P. V., Pasentsis, K., Scandalios, J. G., and Tsaftaris, A. S. (2005). The maize alternative oxidase 1a (Aox1a) gene is regulated by signals related to oxidative stress. Redox Rep. 10, 71-78. doi: 10.1179/135100005X21688
82. Preuten, T., Cincu, E., Fuchs, J., Zoschke, R., Liere, K., and Börner, T. (2010). Fewer genes than organelles: extremely low and variable gene copy numbers in mitochondria of somatic plant cells. Plant J. 64, 948-959. doi: 10.1111/j.1365-313X.2010.04389.x
83. Ribichich, K. F., Tioni, M. F., Chan, R. L., and Gonzalez, D. H. (2001). Cell-type-specific expression of plant cytochrome c mRNA in developing flowers and roots. Plant Physiol. 4, 1603-1610. doi: 10.1104/pp.125.4.1603
84. Rogers, K., and Chen, X. (2013). Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell 25, 2383-2399. doi: 10.1105/tpc.113.113159
85. Roschzttardtz, H., Fuentes, I., Vásquez, M., Corvalán, C., León, G., Gómez, I., et al. (2009). A nuclear gene encoding the iron-sulfur subunit of mitochondrial complex II is regulated by B3 domain transcription factors during seed development in Arabidopsis. Plant Physiol. 150, 84-95. doi: 10.1104/pp.109.136531
86. Schwarzländer, M., and Finkemeier, I. (2013). Mitochondrial energy and redox signaling in plants. Antioxid. Redox Signal. 18, 2122-2144. doi: 10.1089/ars.2012.5104
87. Schwarzländer, M., Logan, D. C., Johnston, I. G., Jones, N. S., Meyer, A. J., Fricker, M. D., et al. (2012). Pulsing of membrane potential in individual mitochondria: a stress-induced mechanism to regulate respiratory bioenergetics in Arabidopsis. Plant Cell 24, 1188-1201. doi: 10.1105/tpc.112.096438
88. Scott, I., and Logan, D. C. (2010). "Mitochondrial dynamics, " in Plant mitochondria, Advances of Plant Biology Series, ed. F. Kempken (New York: Springer), 31-63.
89. Seguí-Simarro, J. M., Coronado, M. J., and Staehelin, L. A. (2008). The mitochondrial cycle of Arabidopsis shoot apical meristem and leaf primordium meristematic cells is defined by a perinuclear tentaculate/cage-like mitochondrion. Plant Physiol. 148, 1380-1393. doi: 10.1104/pp.108.126953
90. Seguí-Simarro, J. M., and Staehelin, L. A. (2009). Mitochondrial reticulation in shoot apical meristem cells of Arabidopsis provides a mechanism for homogenization of mtDNA prior to gamete formation. Plant Signal. Behav. 4, 168-171. doi: 10.4161/psb.4.3.7755
91. Shaikhali, J., and Baier, M. (2010). Ascorbate regulation of 2-Cys peroxiredoxin-A promoter activity is light-dependent. J. Plant Physiol. 167, 461-467. doi: 10.1016/j.jplph.2009.10.021
92. Shaikhali, J., Heiber, I., Seidel, T., Ströher, E., Hiltscher, H., Birkmann, S., et al. (2008). The redox-sensitive transcription factor Rap2.4a controls nuclear expression of 2-Cys peroxiredoxin A and other chloroplast antioxidant enzymes. BMC Plant Biol. 8:48. doi: 10.1186/1471-2229-8-48
93. Shaikhali, J., Norén, L., Barajas-López, J. D., Srivastava, V., König, J., Sauer, U. H., et al. (2012). Redox mediated mechanisms regulate DNA-binding activity of the G-group of bZIP transcription factors in Arabidopsis. J. Biol. Chem. 287, 27510-27525. doi: 10.1074/jbc.M112.361394
94. Shedge, V., Davila, Y., Arrieta-Montiel, M. P., Mohammed, S., and MacKenzie, S. A. (2010). Extensive rearrangement of the Arabidopsis mitochondrial genome elicits cellular conditions for thermotolerance. Plant Physiol. 152, 1960-1970. doi: 10.1104/pp.109.152827
95. Stuart, R. A. (2008). Supercomplex organization of the oxidative phosphorylation enzymes in yeast mitochondria. J. Bioenerg. Biomembr. 40, 411-417. doi: 10.1007/s10863-008-9168-4
96. Tan, Y. F., Millar, A. H., and Taylor, N. L. (2012). Components of mitochondrial oxidative phosphorylation vary in abundance following exposure to cold and chemical stresses. J. Proteome Res. 11, 3860-3879. doi: 10.1021/pr3003535
97. Taylor, N. L., Howell, K. A., Heazlewood, J. L., Tan, T. Y., Narsai, R., Huang, S., et al. (2010). Analysis of the rice mitochondrial carrier family reveals anaerobic accumulation of a basic amino acid carrier involved in arginine metabolism during seed germination. Plant Physiol. 154, 691-704. doi: 10.1104/pp.110.162214
98. Tomasetti, M., Neuzil, J., and Dong, L. (2013). MicroRNAs as regulators of mitochondrial function: role in cancer suppression. Biochim. Biophys. Acta doi:10.1016/j.bbagen.2013.09.002 [Epub ahead of print].
99. Trémousaygue, D., Garnier, L., Bardet, C., Dabos, P., Hervé, C., and Lescure, B. (2003). Internal telomeric repeats and 'TCP domain' protein-binding sites co-operate to regulate gene expression in Arabidopsis thaliana cycling cells. Plant J. 33, 957-966. doi: 10.1046/j.1365-313X.2003.01682.x
100. Turrenes, J. F. (2003). Mitochondrial formation of reactive oxygen species. J. Physiol. 15, 335-344. doi: 10.1113/jphysiol.2003.049478
101. Uberti Manassero, N. G., Viola, I. L., Welchen, E., and Gonzalez, D. H. (2013). TCP transcription factors: architectures of plant form. Biomol. Concepts 4, 111-127. doi: 10.1515/bmc-2012-0051
102. Van Aken, O., and Whelan, J. (2012). Comparison of transcriptional changes to chloroplast and mitochondrial perturbations reveals common and specific responses in Arabidopsis. Front. Plant Sci. 3:281. doi: 10.3389/fpls.2012.00281
103. Van Aken, O., Zhang, B., Law, S., Narsai, R., and Whelan, J. (2013). AtWRKY40 and AtWRKY63 modulate the expression of stress-responsive nuclear genes encoding mitochondrial and chloroplast proteins. Plant Physiol. 162, 254-271. doi: 10.1104/pp.113.215996
104. Vanderauwera, S., Vandenbroucke, K., Inzé, A., van de Cotte, B., Mühlenbock, P., De Rycke, R., et al. (2012). AtWRKY15 perturbation abolishes the mitochondrial stress response that steers osmotic stress tolerance in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 109, 20113-20118. doi: 10.1073/pnas.1217516109
105. Vanlerberghe, G. C. (2013). Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants. Int. J. Mol. Sci. 14, 6805-6847. doi: 10.3390/ijms14046805
106. Vestergaard, C. L., Flyvbjerg, H., and Møller, I. M. (2012). Intracellular signaling by diffusion: can waves of hydrogen peroxide transmit intracellular information in plant cells? Front. Plant Sci. 3:295. doi: 10.3389/fpls.2012.00295
107. Viola, I. L., Güttlein, L. N., and Gonzalez, D. H. (2013). Redox modulation of plant developmental regulators from the class I TCP transcription factor family. Plant Physiol. 162, 1434-1447. doi: 10.1104/pp.113.216416
108. Wang, H., Wang, S., Lu, Y., Alvarez, S., Hicks, L. M., Ge, X., et al. (2012). Proteomic analysis of early-responsive redox-sensitive proteins in Arabidopsis. J. Proteome Res. 11, 412-424. doi: 10.1021/pr200918f
109. Watanabe, C. K., Hachiya, T., Takahara, K., Kawai-Yamada, M., Uchimiya, H., Uesono, Y., et al. (2010). Effects of AOX1a deficiency on plant growth, gene expression of respiratory components and metabolic profile under low-nitrogen stress in Arabidopsis thaliana. Plant Cell Physiol. 51, 810-822. doi: 10.1093/pcp/pcq033
110. Welchen, E., Chan, R. L., and González, D. H. (2002). Metabolic regulation of genes encoding cytochrome c and cytochrome c oxidase subunit Vb in Arabidopsis. Plant Cell Environ. 25, 1605-1615. doi: 10.1046/j.1365-3040.2002.00940.x
111. Welchen, E., Chan, R. L., and Gonzalez, D. H. (2004). The promoter of the Arabidopsis nuclear gene COX5b-1, encoding subunit 5b of the mitochondrial cytochrome c oxidase, directs tissue-specific expression by a combination of positive and negative regulatory elements. J. Exp. Bot. 55, 1997-2004. doi: 10.1093/jxb/erh223
112. Welchen, E., and Gonzalez, D. H. (2006). Overrepresentation of elements recognized by TCP-domain transcription factors in the upstream regions of nuclear genes encoding components of the mitochondrial oxidative phosphorylation Machinery. Plant Physiol. 141, 540-545. doi: 10.1104/pp.105.075366
113. Welchen, E., Viola, I. L., Kim, H. J., Prendes, L. P., Comelli, R. N., Hong, J. C., et al. (2009). A segment containing a G-box and an ACGT motif confers differential expression characteristics and responses to the Arabidopsis Cytc-2 gene, encoding an isoform of cytochrome c. J. Exp. Bot. 60, 829-845. doi: 10.1093/jxb/ern331
114. Westermann, B. (2012). Mitochondrial fusion and fission in cell life and death. Nat. Rev. Mol. Cell Biol. 11, 872-884. doi: 10.1038/nrm3013
115. Xu, L., Carrie, C., Law, S. R., Murcha, M. W., and Whelan, J. (2013a). Acquisition, conservation, and loss of dual-targeted proteins in land plants. Plant Physiol. 161, 644-662. doi: 10.1104/pp.112.210997
116. Xu, L., Law, S. R., Murcha, M. W., Whelan, J., and Carrie, C. (2013b). The dual targeting ability of type II NAD(P)H dehydrogenases arose early in land plant evolution. BMC Plant Biol. 13:100. doi: 10.1186/1471-2229-13-100
117. Yamamoto, H., Morino, K., Nishio, Y., Ugi, S., Yoshizaki, T., Kashiwagi, A., et al. (2012). MicroRNA-494 regulates mitochondrial biogenesis in skeletal muscle through mitochondrial transcription factor A and Forkhead box j3. Am. J. Physiol. Endocrinol. Metab. 303, 1419-1427. doi: 10.1152/ajpendo.00097.2012
118. Yogev, O., and Pines, O. (2011). Dual targeting of mitochondrial proteins: mechanism, regulation and function. Biochim. Biophys. Acta 1808, 1012-1020. doi: 10.1016/j.bbamem.2010.07.004
119. Yoshinaga, K., Arimura, S., Niwa, Y., Tsutsumi, N., Uchimiya, H., and Kawai-Yamada, M. (2005). Mitochondrial behaviour in the early stages of ROS stress leading to cell death in Arabidopsis thaliana. Ann. Bot. 96, 337-342. doi: 10.1093/aob/mci181
120. Zarepour, M., Simon, K., Wilch, M., Nieländer, U., Koshiba, T., Seo, M., et al. (2012). Identification of superoxide production by Arabidopsis thaliana aldehyde oxidases AAO1 and AAO3. Plant Mol. Biol. 80, 659-671. doi: 10.1007/s11103-012-9975-1
121. Zarkovic, J., Anderson, S. L., and Rhoads, D. M. (2005). A reporter gene system used to study developmental expression of alternative oxidase and isolate mitochondrial retrograde regulation mutants in Arabidopsis. Plant Mol. Biol. 57, 871-888. doi: 10.1007/s11103-005-3249-0
122. Zottini, M., Barizza, E., Bastianelli, F., Carimi, F., and Lo Schiavo, F. (2006). Growth and senescence of Medicago truncatula cultured cells are associated with characteristic mitochondrial morphology. New Phytol. 172, 239-247. doi: 10.1111/j.1469-8137.2006.01830.x