Abstract
In flooded soils, oxygen is a serious limiting factor for plant growth and survival. However, as evident from their evolutionary diversification and ecological success, plants have acquired the ability to sense and adapt to oxygen deficits. Here, I attempt a synthesis of recent developments in oxygen-signaling research, in particular, the role of transient ionic (calcium) and redox (reactive oxygen species) changes in the perception of oxygen deprivation by plant cells. An emerging theme from this analysis is that the oxygen-signaling network comprises both positive and negative feedback loops that augment or moderate these cellular perturbations encoding the stress. Further, plant tolerance to oxygen deprivation seems to depend on the ability of cells to regulate these signaling circuits and rapidly attain homeostasis.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Abercrombie J, Halfhill M, Ranjan P, Rao M, Saxton A, Yuan J, Stewart C (2008) Transcriptional responses of Arabidopsis thaliana plants to As (V) stress. BMC Plant Biol 8:87
Ahsan N, Lee D-G, Lee S-H, Kang KY, Bahk JD, Choi MS, Lee I-J, Renaut J, Lee B-H (2007) A comparative proteomic analysis of tomato leaves in response to waterlogging stress. Physiol Planta 131:555–570
Arpagaus S, Rawyler AJ, Braendle RA (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 (Lond) 96:507–518
Bailey-Serres J, Voesenek LACJ (2008) Flooding stress: acclimations and genetic diversity. Annu Rev Plant Biol 59:313–39
Baxter-Burrell A, Yang Z, Springer PS, Bailey-Serres J (2002) RopGAP4-dependent rop GTPase rheostat control of Arabidopsis oxygen deprivation tolerance. Science 296:2026–2028
Berchner-Pfannschmidt U, Frede S, Wotzlaw C, Fandrey J (2008) Imaging of the hypoxia-inducible factor pathway: insights into oxygen sensing. Eur Respir J 32:210–217
Branco-Price C, Kawaguchi R, Ferreira RB, Bailey-Serres J (2005) Genome-wide analysis of transcript abundance and translation in Arabidopsis seedlings subjected to oxygen deprivation. Ann Bot 96:647–660
Branco-Price C, Chang R, Ferreira R, Bailey-Serres J (2006) Mitochondria-initiated signaling in Arabidopsis under low oxygen. Poster presented at Plant Biology 2006, American Society of Plant Biologists, Boston, 5–9 Aug 2006, abstract P36049
Bucher M, Brandle R, Kuhlemeier C (1994) Ethanolic fermentation in transgenic tobacco expressing Zymomonas mobilis pyruvate decarboxylase. EMBO J 13:2755–2763
Carystinos GD, Heather MR, Monroy AF, Rajinder DS, Poole RJ (1995) Vacuolar H+-translocating pyrophosphatase is induced by anoxia or chilling in seedlings of rice. Plant Physiol 108:641–649
Chang W, Small DA, Toghrol F, Bentley WE (2006) Global transcriptome analysis of Staphylococcus aureus response to hydrogen peroxide. J Bacteriol 188:1648–1659
Chang WWP, Huang L, Shen M, Webster C, Burlingame AL, Roberts JKM (2000) Patterns of protein synthesis and tolerance of anoxia in root tips of maize seedlings acclimated to a low-oxygen environment, and identification of proteins by mass spectrometry. Plant Physiol 122:295–317
Chung H-J, Ferl RJ (1999) Arabidopsis alcohol dehydrogenase expression in both shoots and roots is conditioned by root growth environment. Plant Physiol 121:429–436
Davletova S, Schlauch K, Coutu J, Mittler R (2005) The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol 139:847–856
Demidchik V, Maathuis FJM (2007) Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development. New Phytol 175:387–404
Desikan R, Mackerness SAH, Hancock JT, Neill SJ (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol 127:159–172
Dirmeier R, O'Brien KM, Engle M, Dodd A, Spears E, Poyton RO (2002) Exposure of yeast cells to anoxia induces transient oxidative stress. Implications for the induction of hypoxic genes. J Biol Chem 277:34773–34784
Ederli L, Morettini R, Borgogni A, Wasternack C, Miersch O, Reale L, Ferranti F, Tosti N, Pasqualini S (2006) Interaction between nitric oxide and ethylene in the induction of alternative oxidase in ozone-treated tobacco plants. Plant Physiol 142:595–608
Frade JM, Michaelidis TM (1997) Origin of eukaryotic programmed cell-death - a consequence of aerobic metabolism. BioEssays 19:827–832
Geigenberger P (2003) Response of plant metabolism to too little oxygen. Curr Opin Plant Biol 6:247–256
Gibbs J, Greenway H (2003) Review: mechanisms of anoxia tolerance in plants. I. Growth, survival and anaerobic catabolism. Funct Plant Biol 30:1–47
Gilles-Gonzalez MA, Gonzalez G (2005) Heme-based sensors: defining characteristics, recent developments, and regulatory hypotheses. J Inorg Biochem 99:1–22
Gong W, Hao B, Mansy SS, Gonzalez G, Gilles-Gonzalez MA, Chan MK (1998) Structure of a biological oxygen sensor: a new mechanism for heme-driven signal transduction. Proc Natl Acad Sci U S A 95:15177–15182
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
Gunawardena A, Pearce DM, Jackson MB, Hawes CR, Evans DE (2001) Characterisation of programmed cell death in aerenchyma formation. Planta 212:205–214
Guzy RD, Hoyos B, Robin E, Chen H, Liu L, Mansfield KD, Simon MC, Hammerling U, Schumacker PT (2005) Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab 1:401–408
Huang S, Greenway H, Colmer TD, Millar AH (2005) Protein Synthesis by rice coleoptiles during prolonged anoxia: implications for glycolysis, growth and energy utilization. Ann Bot 96:703–715
Kadota Y, Goh T, Tomatsu H, Tamauchi R, Higashi K, Muto S, Kuchitsu K (2004) Cryptogein-induced initial events in tobacco BY-2 cells: pharmacological characterization of molecular relationship among cytosolic Ca2+ transients, anion efflux and production of reactive oxygen species. Plant Cell Physiol 45:160–170
Klok EJ, Wilson IW, Wilson D, Chapman SC, Ewing RM, Somerville SC, Peacock WJ, Dolferus R, Dennis ES (2002) Expression profile analysis of the low-oxygen response in Arabidopsis root cultures. Plant Cell 14:2481–2494
Koonin EV, Aravind L (2002) Origin and evolution of eukaryotic apoptosis: the bacterial connection. Cell Death Differ 9:394–404
Kuzmin EV, Karpova OV, Elthon TE, Newton KJ (2004) Mitochondrial respiratory deficiencies signal up-regulation of genes for heat shock proteins. J Biol Chem 279:20672–20677
Kwast KE, Hand SC (1996) Oxygen and pH regulation of protein synthesis in mitochondria from Artemia franciscana embryos. Biochem J 313:207–213
Kwast KE, Burke PV, Staahl BT, Poyton RO (1999) Oxygen sensing in yeast: evidence for the involvement of the respiratory chain in regulating the transcription of a subset of hypoxic genes. Proc Natl Acad Sci U S A 96:5446–5451
Liu F, VanToai T, Moy LP, Bock G, Linford LD, Quackenbush J (2005) Global transcription profiling reveals comprehensive insights into hypoxic response in Arabidopsis. Plant Physiol 137:1115–1129
Maxwell DP, Wang Y, McIntosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci U S A 96:8271–8276
Millar AH, Bergersen FJ, Day DA (1994) Oxygen affinity of terminal oxidases in soybean mitochondria. Plant Physiol Biochem 32:847–852
Millar AH, Trend AE, Heazlewood JL (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
Moskvin OV, Kaplan S, Gilles-Gonzalez M-A, Gomelsky M (2007) Novel heme-based oxygen sensor with a revealing evolutionary history. J Biol Chem 282:28740–28748
Mühlenbock P, Plaszczyca M, Mellerowicz E, Karpinski S (2007) Lysigenous aerenchyma formation in Arabidopsis is controlled by LESION SIMULATING DISEASE1. Plant Cell 19:3819–3830
Nakazono M, Tsuji H, Li YH, Saisho D, Arimura S, Tsutsumi N, Hirai A (2000) Expression of a gene encoding mitochondrial aldehyde dehydrogenase in rice increases under submerged conditions. Plant Physiol 124:587–598
Nie X, Hill RD (1997) Mitochondrial respiration and hemoglobin gene expression in barley aleurone tissue. Plant Physiol 114:835–840
Nie X, Durnin DC, Igamberdiev AU, Hill RD (2006) Cytosolic calcium is involved in the regulation of barley hemoglobin gene expression. Planta 223:542–549
Ogasawara Y, Kaya H, Hiraoka G, Yumoto F, Kimura S, Kadota Y, Hishinuma H, Senzaki E, Yamagoe S, Nagata K, Nara M, Suzuki K, Tanokura M, Kuchitsu K (2008) Synergistic activation of the Arabidopsis NADPH oxidase AtrbohD by Ca2+ and phosphorylation. J Biol Chem 283:8885–8892
Okimoto R, Sachs MM, Porter EK, Freeling M (1980) Patterns of polypeptide synthesis in various maize organs under anaerobiosis. Planta 150:89–94
Pang JY, Newman I, Mendham N, Zhou M, Shabala S (2006) Microelectrode ion and O2 fluxes measurements reveal differential sensitivity of barley root tissues to hypoxia. Plant Cell Environ 29:1107–1121
Papagiannis MD (1984) Life-related aspects of stellar evolution. Orig Life 14:43–50
Paul A-L, Ferl RJ (1991) Adh1 and Adh2 regulation. Maydica 36:129–134
Popov VN (2003) Possible role of free oxidation processes in the regulation of reactive oxygen species production in plant mitochondria. Biochem Soc Trans 31:1316–1317
Porterfield DM, Kuang A, Smith PJS, Crispi ML, Musgrave ME (1999) Oxygen-depleted zones inside reproductive structures of Brassicaceae: implications for oxygen control of seed development. Can J of Bot 77:1439–1446
Pouysségur J, Mechta-Grigoriou F (2006) Redox regulation of the hypoxia-inducible factor. Biol Chem 387:1337–1346
Rhoads DM, Umbach AL, Subbaiah CC, Siedow JN (2006) Mitochondrial ROS: contribution to oxidative stress and inter-organellar signaling. Plant Physiol 141:357–366
Ribas-Carbo M, Berry JA, Azcon-Bieto J, Siedow JN (1994) The reaction of the plant mitochondrial cyanide-resistant alternative oxidase with oxygen. Biochim Biophys Acta 118:205–212
Rolletschek H, Borisjuk L, Koschorreck M, Wobus U, Weber H (2002) Legume embryos develop in a hypoxic environment. J Exp Bot 53:1099–1107
Sagi M, Fluhr R (2001) Superoxide production by plant homologues of the gp91(phox) NADPH oxidase: modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol 126:1281–1290
Sagi M, Fluhr R (2006) Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol 141:336–340
Sedbrook JC, Kronebusch PJ, Borisy GG, Trewavas AJ, Masson PH (1996) Transgenic AEQUORIN reveals organ-specific cytosolic Ca2+ responses to anoxia and Arabidopsis thaliana seedlings. Plant Physiol 111:243–257
Subbaiah CC, Sachs MM (2003) Molecular and cellular adaptations of maize to flooding stress. Ann Bot 91:119–127
Subbaiah CC, Sachs MM (2007) Responses to oxygen deprivation and potential for enhanced flooding tolerance in Maize. In: Bennitzen J, Hake S (eds) The maize handbook, 2nd edn, Springer-Verlag, Berlin Heidelberg
Subbaiah CC, Bush DS, Sachs MM (1994a) Elevation of cytosolic calcium precedes anoxic gene expression in maize suspension-cultured cells. Plant Cell 6:1747–1762
Subbaiah CC, Zhang J-K, Sachs MM (1994b) Involvement of intracellular calcium in anaerobic gene expression and survival of maize seedlings. Plant Physiol 105:369–376
Subbaiah CC, Bush DS, Sachs MM (1998) Mitochondrial contribution to the anoxic Ca2+ signal in maize suspension-cultured cells. Plant Physiol 118:759–771
Subbaiah CC, Kollipara KP, Sachs MM (2000) A Ca2+-dependent cysteine protease is associated with anoxia-induced root tip death in maize. J Exp Bot 51:721–730
Subbaiah CC, Shah N, Rhoads DM (2006) Role of reactive oxygen species and alternative oxidase in hypoxia signaling in Arabidopsis. Poster presented at Plant Biology 2006, American Society of Plant Biologists, Boston, 5–9 Aug 2006, abstract P36053
Szal B, Jolivet Y, Hasenfratz-Sauder MP, Dizengremel P, Rychter AM (2003) Oxygen concentration regulates alternative oxidase expression in barley roots during hypoxia and post-hypoxia. Physiol Plant 119:494–502
Takeda S, Gapper C, Kaya H, Bell E, Kuchitsu K, Dolan L (2008) Local positive feedback regulation determines cell shape in root hair cells. Science 319:1241–1244
Tamura S, Kuramochi H, Ishizawa K (2001) Involvement of calcium ion in the stimulated shoot elongation of arrowhead tubers under anaerobic conditions. Plant Cell Physiol 42:717–722
Taylor BL (2007) Aer on the inside looking out: paradigm for a PAS-HAMP role in sensing oxygen, redox and energy. Mol Microbiol 65:1415–1424
Taylor BL, Zhulin IB (1999) PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev 63:479–506
Taylor BL, Zhulin IB, Johnson MS (1999) Aerotaxis and other energy-sensing behavior in bacteria. Annu Rev Microbiol 53:103–128
Tiwari BS, 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
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
Virolainen E, Blokhina O, Fagerstedt K (2002) Ca2+-induced high amplitude swelling and cytochrome c release from wheat (Triticum aestivum L.) mitochondria under anoxic stress. Ann Bot 90:509–516
Waypa GB, Marks JD, Mack MM, Boriboun C, Mungai PT, Schumacker PT (2002) Mitochondrial reactive oxygen species trigger calcium increases during hypoxia in pulmonary arterial myocytes. Circ Res 91:719–726
Wong HL, Pinontoan R, Hayashi K, Tabata R, Yaeno T, Hasegawa K, Kojima C, Yoshioka H, Iba K, Kawasaki T, Shimamoto K (2007) Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. Plant Cell 19:4022–4034
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
Yang T, Poovaiah BW (2002) Hydrogen peroxide homeostasis: activation of plant catalase by calcium/calmodulin. Proc Natl Acad Sci U S A 99:4097–4102
Yu J, Nickels R, McIntosh L (2001) A genome approach to mitochondrial-nuclear communication in Arabidopsis. Plant Physiol Biochem 39:345–353
Acknowledgement
I thank Barry Taylor (Loma Linda University, CA, USA) for a critical reading of the manuscript.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2009 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Subbaiah *, C. (2009). Ionic Loops and Rebounds: Oxygen-Deprivation Signaling in Plants. In: Mancuso, S., Balu¿ka, F. (eds) Signaling in Plants. Signaling and Communication in Plants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-89228-1_10
Download citation
DOI: https://doi.org/10.1007/978-3-540-89228-1_10
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-540-89227-4
Online ISBN: 978-3-540-89228-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)