Defining the mitochondrial stress response in arabidopsis thaliana

Molecular Plant

Volumn 2, Issue 6, 2009, Pages 1310-1324

  Van Aken, Olivier ^a   Zhang, Botao ^a   Carrie, Chris ^a   Uggalla, Vindya ^a   Paynter, Ellen ^a   Giraud, Estelle ^a   Whelan, James ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; GREEN FLUORESCENT PROTEIN;

ARABIDOPSIS; ARTICLE; DNA MICROARRAY; GENETICS; HOMEOSTASIS; MITOCHONDRION; OXIDATION REDUCTION REACTION; PHYSIOLOGY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GREEN FLUORESCENT PROTEINS; HOMEOSTASIS; MITOCHONDRIA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDATION-REDUCTION;

EID: 71249116157     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/ssp053     Document Type: Article

References (71)

1. Achard, P., Baghour, M., Chapple, A., Hedden, P., Van Der Straeten, D., Genschik, P., Moritz, T., and Harberd, N.P. (2007). The plant stress hormone ethylene controls floral transition via DELLA-dependent regulation of floral meristem-identity genes. Proc. Natl. Acad. Sci. U.S.A. 104, 6484-6489.
2. Arnholdt-Schmitt, B., Costa, J.H., and de Melo, D. (2006). AOX-a functional marker for efficient cell reprogramming under stress? Trends Plant Sci. 11, 281-287.
3. Bartoli, C.G., Gó mez, F., Mart́nez, D.E., and Guiamet, J.J. (2004). Mitochondria are the main target for oxidative damage in leaves of wheat (Triticum aestivum L.). J. Exp. Bot. 55, 1663-1669
4. Bolliger, L., Deloche, O., Glick, B.S., Georgopoulos, C., Jenö, P., Kronidou, N., Horst, M., Morishima, N., and Schatz, G. (1994). A mitochondrial homolog of bacterial GrpE interacts with mitochondrial hsp70 and is essential for viability. EMBO J. 13, 1998-2006.
5. Borecky, J., Nogueira, F.T., de Oliveira, K.A., Maia, I.G., Vercesi, A.E., and Arruda, P. (2006). 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, 849-864.
6. Carrie, C., Kühn, K., Murcha, M.W., Duncan, O., Small, I.D., O'Toole, N., and Whelan, J. (2009). Approaches to defining dual-targeted proteins in Arabidopsis. Plant J. 57, 1128-1139.
7. Carrie, C., Murcha, M.W., Kuehn, K., Duncan, O., Barthet, M., Smith, P.M., Eubel, H., Meyer, E., Day, D.A., Millar, A.H., and Whelan, J. (2008). Type II NAD(P)H dehydrogenases are targeted to mitochondria and chloroplasts or peroxisomes in Arabidopsis thaliana. FEBS Lett. 582, 3073-3079.
8. Chew, O., Whelan, J., and Millar, A.H. (2003). Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J. Biol. Chem. 278, 46869-46877.
9. Choi, H., Hong, J., Ha, J., Kang, J., and Kim, S.Y. (2000). ABFs, a family of ABA-responsive element binding factors. J. Biol. Chem. 275, 1723-1730.
10. Clifton, R., Lister, R., Parker, K.L., Sappl, P.G., Elhafez, D., Millar, A.H., Day, D.A., and Whelan, J. (2005). Stress-induced co-expression of alternative respiratory chain components in Arabidopsis thaliana. Plant Mol. Biol. 58, 193-212.
11. Clifton, R., Millar, A.H., and Whelan, J. (2006). Alternative oxidases in Arabidopsis: a comparative analysis of differential expression in the gene family provides new insights into function of nonphosphorylating bypasses. Biochimica et Biophysica Acta. 1757, 730-741.
12. Dojcinovic, D., Krosting, J., Harris, A.J., Wagner, D.J., and Rhoads, D.M. (2005). Identification of a region of the Arabidopsis AtAOX1a promoter necessary for mitochondrial retrograde regulation of expression. Plant Mol. Biol. 58, 159-175.
13. Dutilleul, C., Garmier, M., Noctor, G., Mathieu, C., Ché trit, 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.
14. Eubel, H., Lee, C.P., Kuo, J., Meyer, E.H., Taylor, N.L., and Millar, A.H. (2007). Free-flow electrophoresis for purification of plant mitochondria by surface charge. Plant J. 52, 583-594.
15. Eulgem, T., and Somssich, I.E. (2007). Networks of WRKY transcription factors in defense signaling. Curr. Opin. Plant Biol. 10, 366-371.
16. Fujita, M., Fujita, Y., Noutoshi, Y., Takahashi, F., Narusaka, Y., Yamaguchi-Shinozaki, K., and Shinozaki, K. (2006). Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr. Opin. Plant Biol. 9, 436-442.
17. Gadjev, I., Vanderauwera, S., Gechev, T.S., Laloi, C., Minkov, I.N., Shulaev, V., Apel, K., Inzé , D., Mittler, R., and Van Breusegem, F. (2006). Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol. 141, 436-445.
18. Gechev, T.S., Van Breusegem, F., Stone, J.M., Denev, I., and Laloi, C. (2006). Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. Bioessays. 28, 1091-1101.
19. Giegé , P., Sweetlove, L.J., Cognat, V., and Leaver, C.J. (2005). Coordination of nuclear and mitochondrial genome expression during mitochondrial biogenesis in Arabidopsis. Plant Cell. 17, 1497-1512.
20. Giraud, E., et al. (2008). The absence of ALTERNATIVE OXIDASE1a in Arabidopsis results in acute sensitivity to combined light and drought stress. Plant Physiol. 147, 595-610.
21. Gygi, S.P., Rochon, Y., Franza, B.R., and Aebersold, R. (1999). Correlation between protein and mRNA abundance in yeast. Mol. Cell Biol. 19, 1720-1730.
22. Hamel, P., Saint-Georges, Y., de Pinto, B., Lachacinski, N., Altamura, N., and Dujardin, G. (2004). Redundancy in the function of mitochondrial phosphate transport in Saccharomyces cerevisiae and Arabidopsis thaliana. Mol. Microbiol. 51, 307-317.
23. Heazlewood, J.L., Verboom, R.E., Tonti-Filippini, J., Small, I., and Millar, A.H. (2007). SUBA: the Arabidopsis Subcellular Database. Nucleic Acids Res. 35, D213-D218.
24. Heazlewood, J.L., Tonti-Filippini, J.S., Gout, A.M., Day, D.A., Whelan, J., and Millar, A.H. (2004). Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components, provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins. Plant Cell. 16, 241-256.
25. Hernandez, J.A., Campillo,A., Jimenez,A., Alarcon, J.J., and Sevilla, F. (1999).Responseof antioxidant systems and leafwater relations to NaCl stress in pea plants. New Phytologist. 141, 241-251.
26. Ho, L.H., Giraud, E., Uggalla, V., Lister, R., Clifton, R., Glen, A., Thirkettle-Watts, D., Van Aken, O., and Whelan, J. (2008). Identification of regulatory pathways controlling gene expression of stress-responsive mitochondrial proteins in Arabidopsis. Plant Physiol. 147, 1858-1873.
27. Holec, S., et al. (2006). Relaxed transcription in Arabidopsis mitochondria is counterbalanced by RNA stability control mediated by polyadenylation and polynucleotide phosphorylase. Mol. Cell. Biol. 26, 2869-2876.
28. Hunte, C., Koepke, J., Lange, C., Rossmanith, T., and Michel, H. (2000). Structure at 2.3 A resolution of the cytochrome bc(1) complex from the yeast Saccharomyces cerevisiae co-crystallized with an antibody Fv fragment. Structure. 8, 669-684.
29. Irizarry, R.A., Hobbs, B., Collin, F., Beazer-Barclay, Y.D., Antonellis, K.J., Scherf, U., and Speed, T.P. (2003). Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 4, 249-264.
30. Iturbe-Ormaetxe, I., Escuredo Pedro, R., Arrese-Igor, C., and Becana, M. (1998). Oxidative damage in pea plants exposed to water deficit or paraquat. Plant Physiol. 116, 173-181.
31. Jiang, Y., Yang, B., Harris, N.S., and Deyholos, M.K. (2007). Comparative proteomic analysis of NaCl stress-responsive proteins in Arabidopsis roots. J. Exp. Bot. 58, 3591-3607.
32. Kagaya, Y., Ohmiya, K., and Hattori, T. (1999). RAV1, a novel DNAbinding protein, binds to bipartite recognition sequence through two distinct DNA-binding domains uniquely found in higher plants. Nucleic Acids Res. 27, 470-478.
33. Kleffmann, T., Russenberger, D., von Zychlinski, A., Christopher,W., Sjölander, K., Gruissem, W., and Baginsky, S. (2004). The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Curr. Biol. 14, 354-362.
34. Koroleva, O.A., Tomlinson, M.L., Leader, D., Shaw, P., and Doonan, J.H. (2005). High-throughput protein localization in Arabidopsis using Agrobacterium-mediated transient expression of GFP-ORF fusions. Plant J. 41, 162-174.
35. Levine, A., Tenhaken, R., Dixon, R., and Lamb, C. (1994). H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell. 79, 583-593.
36. Linka, N., Theodoulou, F.L., Haslam, R.P., Linka, M., Napier, J.A., Neuhaus, H.E., and Weber, A.P. (2008). Peroxisomal ATP import is essential for seedling development in Arabidopsis thaliana. Plant Cell. 20, 3241-3257.
37. Lister, R., Chew, O., Rudhe, C., Lee, M.N., and Whelan, J. (2001). Arabidopsis thaliana ferrochelatase-I and -II are not imported into Arabidopsis mitochondria. FEBS Lett. 506, 291-295.
38. Millar, A.H., and Leaver, C.J. (2000). The cytotoxic lipid peroxidation product, 4-hydroxy-2-nonenal, specifically inhibits decarboxylating dehydrogenases in the matrix of plant mitochondria. FEBS Lett. 481, 117-121.
39. Millar,A.H.,Carrie,C.,Pogson,B.,andWhelan, J. (2009). Exploringthe function:location nexus-usingmultiple linesof evidence indefining the subcellular location of plant proteins. Plant Cell. in press.
40. Molina, C., and Grotewold, E. (2005). Genome wide analysis of Arabidopsis core promoters BMC. Genomics. 6, 25.
41. Murcha, M.W., Elhafez, D., Lister, R., Tonti-Filippini, J., Baumgartner, M., Philippar, K., Carrie, C., Mokranjac, D., Soll, J., and Whelan, J. (2007). Characterization of the preprotein and amino acid transporter gene family in Arabidopsis. Plant Physiol. 143, 199-212.
42. Narsai, R., Howell, K.A., Millar, A.H., O'Toole, N., Small, I., and Whelan, J. (2007). Genome-wide analysis of mRNA decay rates and their determinants in Arabidopsis thaliana. Plant Cell. 19, 3418-3436.
43. Navrot, N., Collin, V., Gualberto, J., Gelhaye, E., Hirasawa, M., Rey, P., Knaff, D.B., Issakidis, E., Jacquot, J.P., and Rouhier, N. (2006). Plant glutathione peroxidases are functional peroxiredoxins distributed in several subcellular compartments and regulated during biotic and abiotic stresses. Plant Physiol. 142, 1364-1379.
44. Ndimba, B.K., Chivasa, S., Simon,W.J., and Slabas, A.R. (2005). Identification of Arabidopsis salt and osmotic stress responsive proteins using two-dimensional difference gel electrophoresis and mass spectrometry. Proteomics. 5, 4185-4196.
45. Norman, C., Howell, K.A., Millar, A.H., Whelan, J.M., and Day, D.A. (2004). Salicylic acid is an uncoupler and inhibitor of mitochondrial electron transport. Plant Physiol. 134, 492-501.
46. Palmblad, M., Mills, D.J., and Bindschedler, L.V. (2008). Heat-shock response in Arabidopsis thaliana explored by multiplexed quantitative proteomics using differential metabolic labeling. J. Proteom. Res. 7, 780-785.
47. Palmieri, L., Picault, N., Arrigoni, R., Besin, E., Palmieri, F., and Hodges, M. (2008). Molecular identification of three Arabidopsis thaliana mitochondrial dicarboxylate carrier isoforms: organ distribution, bacterial expression, reconstitution into liposomes and functional characterization. Biochem. J. 410, 621-629.
48. Pellny, T.K., et al. (2008). Mitochondrial respiratory pathways modulate nitrate sensing and nitrogen-dependent regulation of plant architecture in Nicotiana sylvestris. Plant J. 54, 976-992.
49. Phee, B.K., Cho, J.H., Park, S., Jung, J.H., Lee, Y.H., Jeon, J.S., Bhoo, S.H., and Hahn, T.R. (2004). Proteomic analysis of the response of Arabidopsis chloroplast proteins to high light stress. Proteomics. 4, 3560-3568.
50. Picault, N., Hodges, M., Palmieri, L., and Palmieri, F. (2004). The growing family of mitochondrial carriers in Arabidopsis. Trends Plant Sci. 9, 138-146.
51. Rizhsky, L., Liang, H., and Mittler, R. (2003). The water-water cycle is essential for chloroplast protection in the absence of stress. J. Biol. Chem. 278, 38921-43895
52. Robson, C.A., and Vanlerberghe, G.C. (2002). Transgenic plant cells lacking mitochondrial alternative oxidase have increased susceptibility to mitochondria-dependent and -independent pathways of programmed cell death. Plant Physiol. 129, 1908-1920.
53. Roberts, K., and McCann, M.C. (2000). Xylogenesis: the birth of a corpse. Curr. Opin. Plant Biol. 3, 517-522.
54. Rushton, P.J., Torres, J.T., Parniske, M., Wernert, P., Hahlbrock, K., and Somssich, I.E. (1996). Interaction of elicitor-induced DNAbinding proteins with elicitor response elements in the promoters of parsley PR1 genes. EMBO J. 15, 5690-5700.
55. Sarry, J.E., et al. (2006). The early responses of Arabidopsis thaliana cells to cadmium exposure explored by protein and metabolite profiling analyses. Proteomics. 6, 2180-2198.
56. Scharf, K.D., Siddique, M., and Vierling, E. (2001). The expanding family of Arabidopsis thaliana small heat stress proteins and a new family of proteins containing alpha-crystallin domains (Acd proteins). Cell Stress Chaperones. 6, 225-237.
57. Scott, I., and Logan, D.C. (2008). Mitochondrial morphology transition is an early indicator of subsequent cell death in Arabidopsis. New Phytol. 177, 90-101.
58. Sohn, K.H., Lee, S.C., Jung, H.W., Hong, J.K., and Hwang, B.K. (2006). Expression and functional roles of the pepper pathogen-induced transcription factor RAV1 in bacterial disease resistance, and drought and salt stress tolerance. Plant Mol. Biol. 61, 897-915.
59. Stamler, R., Kappé , G., Boelens, W., and Slingsby, C. (2005). Wrapping the alpha-crystallin domain fold in a chaperone assembly. J. Mol. Biol. 353, 68-79.
60. Su, Z., Chai, M.F., Lu, P.L., An, R., Chen, J., and Wang, X.C. (2007). AtMTM1, a novel mitochondrial protein, may be involved in activation of the manganese-containing superoxide dismutase in Arabidopsis. Planta. 226, 1031-1039.
61. Taylor, N.L., Tan, Y.F., Jacoby, R.P., and Millar, A.H. (2009). Abiotic environmental stress induced changes in the Arabidopsis thaliana chloroplast, mitochondria and peroxisome proteomes. J. Proteomics. 72, 367-378.
62. Van Aken, O., et al. (2007). Mitochondrial type-I prohibitins of Arabidopsis thaliana are required for supporting proficient meristem development. Plant J. 52, 850-864.
63. Van Aken, O., Giraud, E., Clifton, R., and Whelan, J. (2009). Alternative oxidase: a target and regulator of stress responses. Physiol. Plant. in press.
64. Vandenbroucke, K., Robbens, S., Vandepoele, K., Inzé , D., Van de Peer, Y., and Van Breusegem, F. (2008). Hydrogen peroxideinduced gene expression across kingdoms: a comparative analysis. Mol. Biol. Evol. 25, 507-516.
65. Vanderauwera, S., Zimmermann, P., Rombauts, S., Vandenabeele, S., Langebartels, C., Gruissem, W., Inzé , D., and Van Breusegem, F. (2005). Genome-wide analysis of hydrogen peroxide-regulated gene expression in Arabidopsis reveals a high light-induced transcriptional cluster involved in anthocyanin biosynthesis. Plant Physiol. 139, 806-821.
66. Verniquet, F., Gaillard, J., Neuburger, M., and Douce, R. (1991). Rapid inactivation of plant aconitase by hydrogen peroxide. Biochem J. 276, 643-648.
67. Vidi, P.A., Kanwischer, M., Baginsky, S., Austin, J.R., Csucs, G., Dörmann, P., Kessler, F., and Bréhé lin, C. (2006). Tocopherol cyclase (VTE1) localization and vitamin E accumulation in chloroplast plastoglobule lipoprotein particles. J. Biol. Chem. 281, 11225-11234.
68. Yao, N., Tada, Y., Sakamoto, M., Nakayashiki, H., Park, P., Tosa, Y., and Mayama, S. (2002). Mitochondrial oxidative burst involved in apoptotic response in oats. Plant J. 30, 567-579.
69. Zhang, Y.,Marcillat, O., Giulivi, C., Ernster, L., and Davies, K.J. (1990). The oxidative inactivation of mitochondrial electron transport chain components and ATPase. J. Biol. Chem. 265, 16330-16336.
70. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L., and Gruissem, W. (2004). GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621-2632.
71. Zybailov, B., Rutschow, H., Friso, G., Rudella, A., Emanuelsson, O., Sun, Q., and van Wijk, K.J. (2008). Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLoS ONE. 3, e1994.