Abstract
Changes in plant cellular metabolism require altered gene expression. Cellular adjustments and altered gene expression also occur in response to environmental stresses. Both of these situations involve changes in mitochondrial activities. Changes in the status of the mitochondria and resulting inputs for altered nuclear gene expression are communicated to the nucleus by interorganellar signaling called mitochondrial retrograde regulation (MRR). The study of plant MRR is a young field and the mechanisms and components are just beginning to be discovered. Evidence suggests that reactive oxygen species (ROS) can be involved in plant MRR, but this does not mean that they are involved in all cases. Calcium level changes, redox changes, and changes in metabolite levels are leading candidates for nonprotein signaling components. Protein signaling components like kinases, phosphatases, and transcription factors are likely to be involved, but only the recent discovery of the involvement of transcription factor Abscisic Acid Insensitive 4 in Arabidopsis provides a specific protein example. Growing evidence indicates overlaps of MRR with other signaling pathways, including those from chloroplasts. MRR could be linked to metabolic signaling and/or ROS production, but these would still originate in mitochondria and be components of MRR. The emerging view is that plant mitochondria are stress sensors that contribute to decisions regarding cell fate during stresses and that this is conveyed to the nucleus by MRR.
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- AOX:
-
Mitochondrial alternative oxidase
- CMS:
-
Cytoplasmic male sterility
- COX:
-
Cytochrome c oxidase
- CRR:
-
Chloroplastic retrograde regulation
- ETC:
-
Mitochondrial electron transport chain
- HR:
-
Hypersensitive response
- HSP:
-
Heat shock/stress protein
- MRR:
-
Mitochondrial retrograde regulation
- mt:
-
Mitochondrial
- NCS:
-
Non-chromosomal stripe
- OGE:
-
Organellar gene expression
- PCD:
-
Programmed cell death
- Redox:
-
Reduction/oxidation
- ROS:
-
Reactive oxygen species
- sHSP:
-
Small heat shock/stress protein
- TCA:
-
Tricarboxylic acid
References
Ahlfors, R., Macioszek, V., Rudd, J., Brosche, M., Schlichting, R., Scheel, D., Kangasjarvi, J. 2004. Stress hormone-independent activation and nuclear translocation of mitogen-activated protein kinases in Arabidopsis thaliana during ozone exposure. Plant J. 40:512–522.
Arnholdt-Schmitt, B., Costa, J. H., de Melo, D. 2006. AOX – a functional marker for efficient cell reprogramming under stress? Trends Plant Sci. 11:281–287.
Arpagaus, S., Rawyler, A., Braendle, R. 2002. Occurrence and characteristics of the mitochondrial permeability transition in plants. J. Biol. Chem. 277:1780–1787.
Bailey-Serres, J., Chang, R. 2005. Sensing and signalling in response to oxygen deprivation in plants and other organisms. Ann. Bot. 96:507–518.
Baker, C. J., Orlandi, E. W., Deahl, K. L. 2000. Oxygen metabolism in plant/bacteria interactions: characterization of the oxygen uptake response of plant suspension cells. Physiol. Mol. Plant Pathol. 57:159–167.
Balk, J., Leaver, C. J. 2001. The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release. Plant Cell 13:1803–1818.
Balk, J., Leaver, C. J., 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.
Basu, U., Good, A. G., Taylor, G. J. 2001. Transgenic Brassica napus plants overexpressing aluminum-induced mitochondrial manganese superoxide dismutase cDNA are resistant to aluminum. Plant Cell Environ. 24:1269–1278.
Bourque, S., Lemoine, R., Sequeira-Legrand, A., Fayolle, L., Delrot, S., Pugin, A. 2002. The elicitor cryptogein blocks glucose transport in tobacco cells. Plant Physiol.130:2177–2187.
Branco-Price, C., Kawaguchi, R., Ferreira, R. B., Bailey-Serres, J. 2005. Genome-wide analysis of transcript abundance and translation in Arabidopsis seedlings subjected to oxygen deprivation. Ann. Bot. 96:647–660.
Butow, R. A., Avadhani, N. G. 2004. Mitochondrial signaling, the retrograde response. Mol. Cell 14:1–15.
Castello, P. R., David, P. S., McClure, T., Crook, Z., Poyton, R. O. 2006. Mitochondrial cytochrome oxidase produces nitric oxide under hypoxic conditions: implications for oxygen sensing and hypoxic signaling in eukaryotes. Cell Metab. 3:277–287.
Chen, W., Singh, K. B. 1999. The auxin, hydrogen peroxide and salicylic acid induced expression of the Arabidopsis GST6 promoter is mediated in part by an ocs element. Plant J. 19:667–678.
Chen, W., Provart, N. J., Glazebrook, J., Katagiri, F., Chang, H. S., Eulgem, T., Mauch, F., Luan, S., Zou, G., Whitham, S. A., Budworth, P. R., Tao, Y., Xie, Z., Chen, X., Lam, S., Kreps, J. A., Harper, J. F., Si-Ammour, A., Mauch-Mani, B., Heinlein, M., Kobayashi, K., Hohn, T., Dangl, J. L., Wang, X., Zhu, T. 2002. Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14:559–574.
Cheng, S. H., Willmann, M. R., Chen, H. C., Sheen, J. 2002. Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol. 129:469–485.
Chung, H. J., Ferl, R. J. 1999. Arabidopsis alcohol dehydrogenase expression in both shoots and roots is conditioned by root growth environment. Plant Physiol. 121:429–436.
Coelho, S. M., Taylor, A. R., Ryan, K. P., Sousa-Pinto, I., Brown, M. T., Brownlee, C. 2002. Spatiotemporal patterning of reactive oxygen production and Ca2+ wave propagation in Fucus rhizoid cells. Plant Cell 14:2369–2381.
Curtis, M. J., Wolpert, T. J. 2002. The oat mitochondrial permeability transition and its implication in victorin binding and induced cell death. Plant J. 29:295–312.
Dat, J., Vandenabeele, S., Vranova, E., Van Montagu, M., Inzé, D., Van Breusegem, F. 2000. Dual action of the active oxygen species during plant stress responses. Cell Mol. Life Sci. 57:779–795.
de Pinto, M. C., Tommasi, F., De Gara, L. 2002. Changes in the antioxidant systems as part of the signaling pathway responsible for the programmed cell death activated by nitric oxide and reactive oxygen species in tobacco Bright-Yellow 2 cells. Plant Physiol. 130:698–708.
Desikan, R., Hancock, J., Neill, S. 2005. Reactive oxygen species as signalling molecules. In Antioxidants and reactive oxygen species in plants, ed. N. Smirnoff. pp. 169–196. Oxford: Blackwell.
Desikan, R., Reynolds, A., Hancock, J., Neill, S. J. 1998. Harpin and hydrogen peroxide both initiate programmed cell death but have differential effects on defence gene expression in Arabidopsis suspension cultures. Biochem. J. 330:115–120.
Devaux, F., Carvajal, E., Moye-Rowley, S., Jacq, C. 2002. Genome wide studies on the nuclear PDR3 controlled response to mitochondrial dysfunction in yeast. FEBS Lett. 515:25–28.
Djajanegara, I., Finnegan, P. M., Mathieu, C., McCabe, T., Whelan, J., Day, D.A. 2002. Regulation of alternative oxidase gene expression in soybean. Plant Mol. Biol. 50:735–742.
Dojcinovic, D. 2003. Analysis of cis-regions and trans-factors regulating the expression of the AtAOX1a gene. Master of Science thesis, Arizona State University.
Dojcinovic, D., Krosting, J., Harris, A. J., Wagner, D. J., Rhoads, D. M. 2005. Identification of regions of the Arabidopsis AtAOX1a promoter important for developmental and mitochondrial retrograde regulation of expression. Plant Mol. Biol. 58:159–175.
Dutilleul, C., Garmier, M., Noctor, G., Mathieu, C., Chetrit, P., Foyer, C. H., 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.
Evans, N. H., McAinsh, M. R., Hetherington, A. M., Knight, M. R. 2005. ROS perception in Arabidopsis thaliana, the ozone-induced calcium response. Plant J. 41:615–626.
Finnegan, P. M., Soole, K. L., Umbach, A. L. 2004. Alternative mitochondrial electron transport proteins in higher plants. In Advances in Photosynthesis and Respiration, Vol. 17, eds. D. A. Day, A. H. Millar, J. Whelan. pp. 163–230. Dordrecht: Kluwer.
Foyer, C. H., Noctor, G. 2003. Redox sensing and signaling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol. Plant. 119:355–364.
Foyer, C. H., Noctor, G. 2005. Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875.
Gadjev, I., Vanderauwera, S., Gechev, T. S., Laloi, C., Minkov, I. N., Shulaev, V., Apel, K., Inzé, D., Mittler, R., Van Breusegem, F. 2006. Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol.141:436–445.
Geigenberger, P. 2003. Response of plant metabolism to too little oxygen. Curr. Op. Plant Biol. 6:247–256.
Giraud, E., Van Aken, O., Ho L. H. M., Whelan, J. 2009. The transcription factor ABI4 is a regulator of mitochondrial retrograde expression of ALTERNATIVE OXIDASE1a. Plant Physiol. 150:1286–1296.
Gómez-Casati, D. F., Busi, M. V., Gonzalez Schain, N., Mouras, A., Zabaleta, E. J., Araya, A. 2002. A mitochondrial dysfunction induces the expression of nuclear encoded Complex I genes in engineered male sterile Arabidopsis thaliana. FEBS Lett. 532:70–74.
Gonzali, S., Loreti, E., Novi, G., Poggi, A., Alpi, A., Perata, P. 2005. The use of microarrays to study the anaerobic response in Arabidopsis. Ann. Bot. 96:661–668.
Gray, G. R., Maxwell, D. P., Villarimo, A. R., McIntosh, L. 2004. Mitochondria/nuclear signaling of alternative oxidase gene expression occurs through distinct pathways involving organic acids and reactive oxygen species. Plant Cell Rep. 23:497–503.
Gray, G. R., McIntosh, L. 1998. Respiratory carbon flux, NAD(P) + -dependent isocitrate dehydrogenases. In Plant Mitochondria, From Gene to Function, eds. I. M. Møller, P. Gardeström, K. Glimelius, E. Glaser, pp. 353–357. Leiden: Backhuys.
Guaragnella, N., Butow, R. A. 2003. ATO3 encoding a putative outward ammonium transporter is an RTG independent retrograde responsive gene regulated by GCN4 and the Ssy1 Ptr3 Ssy5 amino acid sensor system. J. Biol. Chem. 278:45882–45887.
Gutierres, S., Sabar, M., Lelandais, C., Chetrit, P., Diolez, P., Degand, H., Boutry, M., Vedel, F., de Kouchkovsky, Y., 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.
Hardingham, G. E., Chawla, S., Johnson, C. M., Bading, H. 1997. Distinct functions of nuclear and cytoplasmic calcium in the control of gene expression. Nature 385:260–265.
Hernould, M., Suharsono, Zabaleta, E., Carde, J. P., Litvak, S., Araya, A., Mouras, A. 1998. Impairment of tapetum and mitochondria in engineered male-sterile tobacco plants. Plant Mol. Biol. 36:499–508.
Ho, L. H. M., Giraud, E., Uggalla, V., Lister, R., Clifton, R., Glen, A., Thirkettle-Watts, D., Van Aken, O., Whelan, J. 2008. Identification of regulatory pathways controlling gene expression of stress- responsive mitochondrial proteins in Arabidopsis. Plant Physiol. 147:1858–1873.
Huang, S., Greenway, H., Colmer, T. D., Millar, A. H. 2005. Protein synthesis by rice coleoptiles during prolonged anoxia: implications for glycolysis, growth and energy utilization. Ann. Bot. 96:703–715.
Inzé, D., Van Montagu, M. 1995. Oxidative stress in plants. Curr. Op. Biotech. 6:153–158.
Jimenez, A., Hernandez, J. A., delRio, L. A., Sevilla, F. 1997. Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol. 114:275–284.
Jones, A., 2000. Does the plant mitochondrion integrate cellular stress and regulate programmed cell death? Trends Plant Sci. 5:225–230.
Karpova, O. V., Kuzmin, E. V., Elthon, T. E., Newton, K. J. 2002. Differential expression of alternative oxidase genes in maize mitochondrial mutants. Plant Cell 14:3271–3284.
Kim, J. H., Mahoney, N., Chan, K. L., Molyneux, R. J., Campbell, B. C. 2004. Secondary metabolites of the grapevine pathogen Eutypa lata inhibit mitochondrial respiration, based on a model bioassay using the yeast Saccharomyces cerevisiae. Curr. Microbiol. 49:282–287.
Kirchman, P. A., Kim, S., Lai, C. Y., Jazwinski, S. M. 1999. Interorganelle signaling is a determinant of longevity in Saccharomyces cerevisiae. Genetics 152:179–190.
Kocsy, G., Galiba, G., Brunold, C. 2001. Role of glutathione in adaptation and signalling during chilling and cold acclimation in plants. Physiol. Plant. 113:158–164.
Koiwa, H., Barb, A. W., Xiong, L. M., Li, F., McCully, M. G., Lee, B. H., Sokolchik, I., Zhu, J. H., Gong, Z. Z., Reddy, M., Sharkhuu, A., Manabe, Y., Yokoi, S., Zhu, J. K., Bressan R. A., Hasegawa, P. M. 2002. C-terminal domain phosphatase-like family members (AtCPLs) differentially regulate Arabidopsis thaliana abiotic stress signaling, growth, and development. Proc. Natl. Acad. Sci. USA 99:10893–10898.
Kovtun, Y., Chiu, W.-L., Guillaume, T., Sheen, J. 2000. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc. Natl. Acad. Sci. USA 97:2940–2945.
Krause, M., Durner J. 2004. Harpin inactivates mitochondria in Arabidopsis suspension cells. Mol. Plant Microbe Interact. 17:131–139.
Kreuzwieser, J., Hauberg, J., Howell, K. A., Carroll, A., Rennenberg, H., Millar, A. H., Whelan, J. 2009. Differential response of gray poplar leaves and roots underpins stress adaptation during hypoxia. Plant Physiol. 149:461–473.
Kubo, A., Aono, M., Nakajima, N., Saji, H., Tanaka, K., Kondo, N. 1999. Differential responses in activity of antioxidant enzymes to different environmental stresses in Arabidopsis thaliana. J. Plant Res. 112:279–290.
Kumagai, T., Kawamoto, Y., Nakamura, Y., Hatayama, I., Satoh, K., Osawa, T., Uchida, K. 2000. 4-hydroxy-2-nonenal, the end product of lipid peroxidation, is a specific inducer of cyclooxygenase-2 gene expression. Biochem. Biophys. Res. Commun. 273:437–441.
Kushnir, S., Babiychuk, E., Storozhenko, S., Davey, M. W., Papenbrock, J., De Rycke, R., Engler, G., Stephan, U. W., Lange, H., Kispal, G., Lill, R., Van Montagu, M. 2001. A mutation of the mitochondrial ABC transporter Sta1 leads to dwarfism and chlorosis in the Arabidopsis mutant starik. Plant Cell 13:89–100.
Kuzmin, E. V., Karpova, O. V., Elthon, T. E., Newton, K. J. 2004. Mitochondrial respiratory deficiencies signal up-regulation of genes for heat shock proteins. J. Biol. Chem. 279:20672–20677.
Kuzniak, E., Urbanek, H. 2000. The involvement of hydrogen peroxide in plant responses to stresses. ACTA Physiol. Plant 22:195–203.
Kwast, K. E., Burke, P. V., Poyton, R. O. 1998. Oxygen sensing and the transcriptional regulation of oxygen responsive genes in yeast. J. Exp. Biol. 201:1177–1195.
Logan, D. C., Knight, M. R. 2003. Mitochondrial and cytosolic calcium dynamics are differentially regulated in plants. Plant Physiol. 133:21–24.
Lu, G., Sehnke, P. C., Ferl, R. J. 1994. Phosphorylation and calcium binding properties of an Arabidopsis GF14 brain protein homolog. Plant Cell 6:501–510.
Mackenzie, S., McIntosh, L. 1999. Higher plant mitochondria. Plant Cell 11:571–586.
Mahalingam, R., Fedoroff, N. 2003. Stress response, cell death and signaling: the many faces of reactive oxygen species. Physiol. Plant. 119:56–68.
Martinez, I. M., Chrispeels, M. J. 2003. Genomic analysis of the unfolded protein response in Arabidopsis shown its connection to important cellular processes. Plant Cell 15:561–576.
Maxwell, D. P., Nickels, R., 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. 29:269–279.
Maxwell, D. P., Wang, Y., McIntosh, L.1999. The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc. Natl. Acad. Sci. USA 96:8271–8276.
McCammon, M. T., Epstein, C. B., Przybyla-Zawislak, B., McAlister-Henn, L., Butow, R. A. 2003. Global transcription analysis of Krebs tricarboxylic acid cycle mutants reveals an alternating pattern of gene expression and effects on hypoxic and oxidative genes. Mol. Biol. Cell 14:958–972.
Miles, G. P., Samuel, M. A., Zhang, Y., Ellis, B. E. 2005. RNA interference-based (RNAi) suppression of AtMPK6, an Arabidopsis mitogen-activated protein kinase, results in hypersensitivity to ozone and misregulation of AtMPK3. Environ. Pollut. 138:230–237.
Millar, A. H., Bergersen F. J., Day D. A. 1994. Oxygen affinity of terminal oxidases in soybean mitochondria. Plant Physiol. Biochem. 32:847–852.
Millar, A. H., Trend, A. E., Heazlewood, J. L. 2004. Changes in the mitochondrial proteome during the anoxia to air transition in rice focus around cytochrome-containing respiratory complexes. J. Biol. Chem. 279:39471–39478.
Minagawa, N., Koga, S., Nakano, M., Sakajo, S., Yoshimoto, A. 1992. Possible involvement of superoxide anion in the induction of cyanide-resistant respiration in Hansenula anomala. FEBS Lett. 302:217–219.
Mittova, V., Volokita, M., Guy, M., Tal, M. 2000. Activities of SOD and the ascorbate-glutathione cycle enzymes in subcellular compartments in leaves and roots of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii. Physiol. Plant 110:42–51.
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.
Newton, K. J., Gabay-Laughnan, S., DePaepe, R. 2004. Mitochondrial mutations in plants. In Advances in Photosynthesis and Respiration, Vol. 17, eds. D. A. Day, A. H. Millar, J. Whelan, pp. 121–142. Dordrecht: Kluwer.
Nie, X., Durnin, D. C., Igamberdiev, A. U., Hill, R. D. 2006. Cytosolic calcium is involved in the regulation of barley hemoglobin gene expression. Planta 223:542–549.
Nie, X., Hill, R. D. 1997. Mitochondrial respiration and hemoglobin gene expression in barley aleurone tissue. Plant Physiol. 114:835–840.
Norman, C., Howell, K. A., Millar, A. H., Whelan, J., Day, D.A. 2004. Salicylic acid is an uncoupler and inhibitor of mitochondrial electron transport. Plant Physiol. 134:492–501.
Ordog, S. H., Higgins, V. J., Vanlerberghe, G. C. 2002. Mitochondrial alternative oxidase is not a critical component of plant viral resistance but may play a role in the hypersensitive response. Plant Physiol. 129:1858–1865.
Patil, C., Walter, P. 2001. Intracellular signaling from the endoplasmic reticulum to the nucleus, the unfolded protein response in yeast and mammals. Curr. Opin. Cell Biol. 13:349–355.
Pesaresi, P., Masiero, S., Eubel, H., Braun, H.P., Bhushan, S., Glaser, E., Salamini, F., Leister, D. 2006. Nuclear photosynthetic gene expression is synergistically modulated by rates of protein synthesis in chloroplasts and mitochondria. Plant Cell 18:970–991.
Pitzschke, A., Hirt, H. 2006. Mitogen-activated protein kinases and reactive oxygen species signaling in plants. Plant Physiol. 141:351–356.
Popov, V. N., Simonian, R. A., Skulachev, V. P., Starkov, A. A. 1997. Inhibition of the alternative oxidase stimulates H2O2 production in plant mitochondria. FEBS Lett. 415:87–90.
Poyton, R. O., McEwen, J. E. 1996. Crosstalk between nuclear and mitochondrial genomes. Ann. Rev. Biochem. 65:563–607.
Price, A. H., Taylor, A., Ripley, S. J., Griffiths, A., Trewavas, A. J., Knight, M. R. 1994. Oxidative signals in tobacco increase cytosolic calcium. Plant Cell 6:1301–1310.
Pusl, T., Wu, J. J., Zimmerman, T. L., Zhang, L., Ehrlich, B. E., Berchtold, M. W., Hoek, J. B., Karpen, S. J., Nathanson, M. H., Bennett, A. M. 2002. Epidermal growth factor-mediated activation of the ETS-domain transcription factor Elk-1 requires nuclear calcium. J. Biol. Chem. 277:27517–27527.
Raghavendra, A. S., Padmasree, K. 2003. Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Trends Plant Sci. 8:546–553.
Rasmusson, A. G., Soole, K. L., Elthon, T. E. 2004. Alternative NAD(P)H dehydrogenases of plant mitochondria. Annu. Rev. Plant Biol. 55:23–39.
Rentel, M. C., Knight, M. R. 2004. Oxidative stress-induced calcium signaling in Arabidopsis. Plant Physiol. 135:1471–1479.
Rhoads, D.M., McIntosh, L. 1993. Cytochrome and alternative pathway respiration in tobacco: effects of salicylic acid. Plant Physiol. 103:877–883.
Rhoads, D. M., Subbaiah, C. C. 2007. Mitochondrial retrograde regulation in plants. Mitochondrion. 7:177–194.
Rhoads, D. M., Umbach, A. L., Subbaiah, C. C., Siedow, J. N. 2006. Mitochondrial ROS, contribution to oxidative stress and inter-organellar signaling. Plant Physiol. 141:357–366.
Rhoads, D. M., Vanlerberghe, G. C. 2004. Mitochondria-nucleus interactions, Evidence for mitochondrial retrograde communication in plant cells. In Advances in Photosynthesis and Respiration, Vol. 17, eds. D. A. Day, A. H. Millar, J. Whelan, pp. 83–106. Dordrecht: Kluwer.
Rhoads, D. M., White, S. J., Zhou, Y., Muralidharan, M., Elthon, T. E. 2005. Altered gene expression in plants with constitutive expression of a mitochondrial small heat shock protein suggests the involvement of retrograde regulation in the heat stress response. Physiol. Plant. 123:435–444.
Riechmann, J. L., Heard, J., Martin, G., Reuber, L., Jiang, C.-Z., Keddie, J., Adam, L., Pineda, O., Ratcliffe, O. J., Samaha, R. R., Creelman, R., Pilgrim, M., Broun, P., Zhang, J. Z., Ghandehari, D., Sherman, B. K., Yu, G.-L. 2000. Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110.
Robson, C. A., 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.
Rodermel, S. 2001. Pathways of plastid-to-nucleus signaling. Trends Plant Sci. 6:471–478.
Romeis, T., Ludwig, A. A., Martin, R., Jones, J. D. G. 2001. Calcium-dependent protein kinases play an essential role in a plant defence response. EMBO J. 20:5556–5567.
Rook, F., Hadingham, S. A., Li, Y., Bevan, M. W. 2006. Sugar and ABA response pathways and the control of gene expression. Plant Cell Environ. 29:426–434.
Saisho, D., Nakazono, M., Tsutsumi, N., Hirai, A. 2001. ATP synthesis inhibitors as well as respiratory inhibitors increase steady-state level of alternative oxidase mRNA in Arabidopsis thaliana. J. Plant Physiol. 158:241–245.
Samuel, M. A., Hall, H., Krzymowska, M., Drzewiecka, K., Hennig, J., Ellis, B. E. 2005. SIPK signaling controls multiple components of harpin-induced cell death in tobacco. Plant J. 42:406–416.
Sanders, D., Pelloux, J., Brownlee, C., Harper, J. F. 2002. Calcium at the crossroads of signaling. Plant Cell. 14(Suppl):S401–S417.
Sedbrook, J. C., Kronebusch, P. J., Borisy, G. G., Trewavas, A. J., Masson, P. H. 1996. Transgenic AEQUORIN reveals organ-specific cytosolic Ca2+ responses to anoxia in Arabidopsis thaliana seedlings. Plant Physiol. 111:243–257.
Sekito, T., Thornton, J., Butow, R. A. (2000) Mitochondria to nuclear signaling is regulated by the subcellular localization of the transcription factors Rtg1p and Rtg3p. Mol Biol Cell. 11: 2103–2115.
Siedow, J. N., Umbach, A. L. 1995. Plant mitochondrial electron transfer and molecular biology. Plant Cell. 7:821–831.
Subbaiah, C. C., Bush, D. S., Sachs, M. M. 1994. Elevation of cytosolic calcium precedes anoxic gene expression in maize suspension-cultured cells. Plant Cell. 6:1747–1762.
Subbaiah, C. C., Bush, D. S., Sachs, M. M. 1998. Mitochondrial contribution to the anoxic Ca2+ signal in maize suspension-cultured cells. Plant Physiol. 118:759–771.
Sun, Y. L., Zhao, Y., Hong, X., Zhai, Z. H. 1999. Cytochrome c release and caspase activation during menadione-induced apoptosis in plants. FEBS Lett. 462:317–321.
Sweetlove, L. J., Foyer, C. H. 2004. Roles for reactive oxygen species and antioxidants in plant mitochondria. In Advances in Photosynthesis and Respiration, Vol. 17, eds. D. A. Day, A. H. Millar, J. Whelan, pp. 307–320. Dordrecht: Kluwer.
Sweetlove, L. J., Heazlewood, J. L., Herald, V., Holtzapffel, R., Day, D. A., Leaver, C. J., Millar, A. H. 2002. The impact of oxidative stress on Arabidopsis mitochondria. Plant J. 32:891–904.
Takahashi, Y., Berberich, T., Miyazaki, A., Seo, S., Ohashi, Y., Kusano, T. 2003. Spermine signaling in tobacco: activation of mitogen-activated protein kinases by spermine is mediated through mitochondrial dysfunction. Plant J. 36:820–829.
Takahashi, Y., Berberich, T., Yamashita, K., Uehara, Y., Miyazaki, A., Kusano, T. 2004. Identification of tobacco HIN1 and two closely related genes as spermine-responsive genes and their differential expression during the Tobacco mosaic virus-induced hypersensitive response and during leaf- and flower-senescence. Plant Mol. Biol. 54:613–622.
Takahashi, Y., Uehara, Y., Berberich, T., Ito, A., Saitoh, H., Miyazaki, A., Terauchi, R., Kusano, T. 2004a. A subset of hypersensitive response marker genes, including HSR203J, is the downstream target of a spermine signal transduction pathway in tobacco. Plant J. 40:586–595.
Tang, D. G., La, E., Kern, J., Kehrer, J. P. 2002. Fatty acid oxidation and signaling in apoptosis. Biol. Chem. 383:425–442.
Taylor, N. L., Day, D. A., Millar, A. H. 2002. Environmental stress causes oxidative damage to plant mitochondria leading to inhibition of glycine decarboxylase. J. Biol. Chem. 277:42663–42668.
Tiwari, S. B., Belenghi, B., Levine, A. 2002. Oxidative stress increased respiration and generation of reactive oxygen species, resulting in ATP depletion, opening of mitochondrial permeability transition, and programmed cell death. Plant Physiol. 128:1271–1281.
Trewavas, A., 1999. Le calcium, c’est la vie, calcium makes waves. Plant Physiol. 120:1–6.
Tsuji, H., Nakazono, M., Saisho, D., Tsutsumi, N., Hirai, A., 2000. Transcript levels of the nuclear-encoded respiratory genes in rice decrease by oxygen deprivation: evidence for involvement of calcium in expression of the alternative oxidase 1a gene. FEBS Lett. 471:201–204.
Umbach, A. L., Fiorani, F., Siedow, J. N. 2005. Characterization of transformed Arabidopsis with altered alternative oxidase levels and analysis of effects on reactive oxygen species in tissue. Plant Physiol. 139:1806–1820.
Vacca, R. A., Valenti, D., Bobba, A., Merafina, R. S., Passarella, S., Marra, E. 2006. Cytochrome c is released in a reactive oxygen species-dependent manner and is degraded via caspase-like proteases in tobacco Bright-Yellow 2 cells en route to heat shock-induced cell death. Plant Physiol. 141:208–219.
Van Aken, O., Giraud, E., Clifton, R., Whelan, J. 2009. Alternative oxidase: a target and regulator of stress responses. Physiol. Plant. 137:354–361.
Vanlerberghe, G. C., Cvetkovska, M., Wang, J. 2009. Is the maintenance of homeostatic mitochondrial signaling during stress a physiological role for alternative oxidase? Physiol. Plant 137:392–406.
Vanlerberghe, G. C., Day, D. A., Wiskich, J. T., Vanlerberghe, A. E., McIntosh, L. 1995. Alternative oxidase activity in tobacco leaf mitochondria. Dependence on tricarboxylic acid cycle-mediated redox regulation and pyruvate activation. Plant Physiol. 109:353–361.
Vanlerberghe, G. C., McIntosh, L. 1996. Signals regulating the expression of the nuclear gene encoding alternative oxidase of plant mitochondria. Plant Physiol. 111:589–595.
Vanlerberghe, G. C., McIntosh, L. 1997. Alternative oxidase, from gene to function. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:703–734.
Vanlerberghe, G. C., Robson, C. A., Yip, J. Y. 2002. Induction of mitochondrial alternative oxidase in response to a cell signal pathway down-regulating the cytochrome pathway prevents programmed cell death. Plant Physiol. 129:1829–1842.
van Lis, R., Atteia, A. 2004. Control of mitochondrial function via photosynthetic redox signals. Photosynth. Res. 79:133–148.
Vranová, E., Inzé, D., Van Breusegem, F. 2002. Signal transduction during oxidative stress. J. Exp. Bot. 53:1227–1236.
Winger, A. M., Millar, A. H., Day, D. A. 2005. Sensitivity of plant mitochondrial terminal oxidases to the lipid peroxidation product 4-hydroxy-2-nonenal (HNE). Biochem. J. 387:865–870.
Woltering, E. J., van der Bent, A., Hoeberichts, F. A. 2002. Do plant caspases exist? Plant Physiol. 130:1764–1769.
Woo, D. K., Phang, T. L., Trawick, J. D., Poyton, R. O. 2009. Multiple pathways of mitochondrial-nuclear communication in yeast: intergenomic signaling involves ABF1 and affects a different set of genes than retrograde regulation. Biochim. Biophys. Acta Gene Reg. Mech. 1789:135–145.
Woo, D. K., Poyton, R. O. 2009. The absence of a mitochondrial genome in rho0 yeast cells extends lifespan independently of retrograde regulation. Exp. Geront. 44:390–397.
Woodson, J. D., Chory J. 2008. Coordination of gene expression between organellar and nuclear genomes. Nat. Rev. Genet. 9:383–395.
Xie, Z., Chen, Z. 1999. Salicylic acid induces rapid inhibition of mitochondrial electron transport and oxidative phosphorylation in tobacco cells. Plant Physiol. 120:217–225.
Xie, Z., Chen, Z. 2000. Harpin-induced hypersensitive cell death is associated with altered mitochondrial functions in tobacco cells. Mol. Plant Microbe Interact. 13:183–190.
Yamamoto, Y., Kobayashi, Y., Devi, S. R., Rikiishi, S., Matsumoto, H. 2002. Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells. Plant Physiol. 128:63–72.
Yao, N., Tada, Y., Sakamoto, M., Nakayashiki, H., Park, P., Tosa, Y., Mayama, S. 2002. Mitochondrial oxidative burst involved in apoptotic response in oats. Plant J. 30:567–579.
Yu, J., Nickels, R., McIntosh, L. 2001. A genome approach to mitochondrial-nuclear communication in Arabidopsis. Plant Physiol. Biochem. 39:345–353.
Yuasa, T., Ichimura, K., Mizoguchi, T., Shinozaki, K. 2001. Oxidative stress activates ATMPK6, an Arabidopsis homologue of MAP kinase. Plant Cell Physiol. 42:1012–1016.
Zaninotto, F., La Camera, S., Polverari, A., Delledonne, M. 2006. Cross talk between reactive nitrogen and oxygen species during the hypersensitive disease resistance response. Plant Physiol. 141:379–383.
Zarkovic, J., Anderson, S. L., 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.
Zhang, S. Q., Klessig, D. F. 2001. MAPK cascades in plant defense signaling. Trends Plant Sci. 6:520–527.
Zhang, B., Singh, K. 1994. Ocs element promoter sequences are activated by auxin and salicylic acid in Arabidopsis. Proc. Natl. Acad. Sci. USA 91:2507–2511.
Zhao, Q., Wang, J., Levichkin, I. V., Stasinopoulos, S., Ryan, M. T., Hoogenraad, N. J. 2002. A mitochondrial specific stress response in mammalian cells. EMBO J. 21:4411–4419.
Zhu, J. K. 2002. Salt and drought stress signal transduction in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 53:247–273.
Acknowledgments
I thank Ann Umbach for many helpful discussions leading to the preparation of this chapter. This work was supported by grants from the National Science Foundation (IOS-0822521) and the US Department of Agriculture (2009-35100-05007).
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Glossary
- Adenylate restriction: When the cellular level of ADP becomes so low that the formation of ATP becomes restricted, which has effects on many cellular processes including mitochondrial respiration.
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Hypersensitive response: A plant defense response to infection that directs death of cells adjacent to the infected cells so as to prevent spreading of the infection by depriving the pathogen of resources; a type of programmed cell death in plants.
- Programmed cell death: The well-orchestrated cellular death program that involves, in most cases, defined morphological changes and biochemical shifts aimed at controlled organism recovery of cellular components.
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Retrograde regulation: Communication pathways initiated by organelles that result in altered nuclear gene expression.
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Rhoads, D.M. (2011). Plant Mitochondrial Retrograde Regulation. In: Kempken, F. (eds) Plant Mitochondria. Advances in Plant Biology, vol 1. Springer, New York, NY. https://doi.org/10.1007/978-0-387-89781-3_16
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