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Oxidative Stress Components Explored in Anoxic and Hypoxic Global Gene Expression Data

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Book cover Low-Oxygen Stress in Plants

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 21))

Abstract

Global gene expression data were analyzed to search for the genes related to oxidative stress response, to examine the differences between hypoxia and anoxia, and to reveal new components of oxygen deprivation response escaped from the previous analyses. Gene Set Z-score (GSZ) was used to report gene ontology (GO) classes that showed significant regulation and also partial up- and downregulation in Arabidopsis anoxic and hypoxic microarray data sets. Under both anoxia and hypoxia significant upregulation was reported for anaerobic respiration, response to low oxygen levels, and response to hypoxia. Comparable high GSZ scores were shown for several oxidative stress-related GO classes and for functional groups of biological processes known to involve oxygen radical formation such as: cellular respiration, wounding, and response to high light and UV-B. Availability of oxygen in hypoxic experimental sets was marked by upregulation of several oxygenases, including ACC-oxidase responsible for ethylene synthesis. Consistent strong induction of several Fe-dependent ketoglutarate oxygenases (FeKGO) in the majority of hypoxic conditions analyzed suggests an important and yet unidentified function for these enzymes. Based on metabolic and gene expression studies we suggest that FeKGO may function in a bypass route for part of the TCA cycle (citrate-isocitrate) inhibited under hypoxia. This would incorporate 2-ketoglutarate supplied by activated GABA shunt and form succinate, a TCA cycle and mitochondrial electron transport chain substrate. FeKGO turnover is sustained by the putative route coupled to ascorbate–monodehydroascorbate cycling and hemoglobin-dependent NO elimination. The analysis strongly supports earlier findings that formation of activated oxygen and oxidative stress is an integral part of the response to oxygen deprivation. Several novel functional gene groups were highlighted by the analysis: upregulation of cysteamine dioxygenase activity and FeKGO and downregulation of circadian rhythm-related genes.

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References

  • Asif M, Trivedi P, Misra P, Nath P (2009) Prolyl-4-hydroxylase (AtP4H1) mediates and mimics low oxygen response in Arabidopsis thaliana. Funct Integr Genomics 9:525–535

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Bailey-Serres J, Voesenek LACJ (2008) Flooding stress: acclimations and genetic diversity. Annu Rev Plant Biol 59:313–339

    CAS  PubMed  Google Scholar 

  • Banti V, Mafessoni F, Loreti E, Alpi A, Perata P (2010) The heat-inducible transcription factor HsfA2 enhances anoxia tolerance in Arabidopsis. Plant Physiol 152:1471–1483

    CAS  PubMed Central  PubMed  Google Scholar 

  • Baxter CJ, Redestig H, Schauer N, Repsilber D, Patil KR, Nielsen J, Selbig J, Liu J, Fernie AR, Sweetlove LJ (2007) The metabolic response of heterotrophic Arabidopsis cells to oxidative stress. Plant Physiol 143:312–325

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Benamar A, Rolletschek H, Borisjuk L, Avelange-Macherel M, Curien G, Mostefai HA, Andriantsitohaina R, Macherel D (2008) Nitrite–nitric oxide control of mitochondrial respiration at the frontier of anoxia. Biochim Biophys Acta—Bioenergetics 1777:1268–1275

    CAS  Google Scholar 

  • Berra E, Ginouves A, Pouyssegur J (2006) The hypoxia-inducible-factor hydroxylases bring fresh air into hypoxia signalling. EMBO Rep 7:41–45

    CAS  PubMed Central  PubMed  Google Scholar 

  • Biemelt S, Keetman U, Albrecht G (1998) Re-aeration following hypoxia or anoxia leads to activation of the antioxidative defense system in roots of wheat seedlings. Plant Physiol 116:651–658

    CAS  PubMed Central  PubMed  Google Scholar 

  • Biemelt S, Keetman U, Mock H, Grimm B (2000) Expression and activity of isoenzymes of superoxide dismutase in wheat roots in response to hypoxia and anoxia. Plant Cell Environ 23:135–144

    CAS  Google Scholar 

  • Blokhina O, Fagerstedt KV (2010a) Oxidative metabolism, ROS and NO under oxygen deprivation. Plant Physiol Biochem 48:359–373

    CAS  PubMed  Google Scholar 

  • Blokhina O, Fagerstedt KV (2010b) Reactive oxygen species and nitric oxide in plant mitochondria: origin and redundant regulatory systems. Physiol Plant 138:447–462

    CAS  PubMed  Google Scholar 

  • Blokhina OB, Virolainen E, Fagerstedt KV, Hoikkala A, Wähälä K, Chirkova TV (2000) Antioxidant status of anoxia-tolerant and -intolerant plant species under anoxia and reaeration. Physiol Plant 109:396–403

    CAS  Google Scholar 

  • Blokhina OB, Chirkova TV, Fagerstedt KV (2001) Anoxic stress leads to hydrogen peroxide formation in plant cells. J Exp Bot 52:1179–1190

    CAS  PubMed  Google Scholar 

  • Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot (Lond) 91:179–194

    CAS  Google Scholar 

  • Blomster T, Salojärvi J, Sipari N, Brosché M, Ahlfors R, Keinänen M, Overmyer K, Kangasjärvi J (2011) Apoplastic reactive oxygen species transiently decrease auxin signaling and cause stress-induced morphogenic response in Arabidopsis. Plant Physiol 157:1866–1883

    CAS  PubMed Central  PubMed  Google Scholar 

  • Borisjuk L, Macherel D, Benamar A, Wobus U, Rolletschek H (2007) Low oxygen sensing and balancing in plant seeds: a role for nitric oxide. New Phytol 176:813–823

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bouché N, Fait A, Bouchez D, Møller SG, Fromm H (2003) Mitochondrial succinic-semialdehyde dehydrogenase of the γ-aminobutyrate shunt is required to restrict levels of reactive oxygen intermediates in plants. Proc Natl Acad Sci U S A 100:6843–6848

    PubMed Central  PubMed  Google Scholar 

  • 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 (Lond) 96:647–660

    CAS  Google Scholar 

  • Branco-Price C, Kaiser KA, Jang CJH, Larive CK, Bailey-Serres J (2008) Selective mRNA translation coordinates energetic and metabolic adjustments to cellular oxygen deprivation and reoxygenation in Arabidopsis thaliana. Plant J 56:743–755

    CAS  PubMed  Google Scholar 

  • Brosnan JT, Brosnan ME (2006) The sulfur-containing amino acids: an overview. J Nutr 136:1636S–1640S

    CAS  PubMed  Google Scholar 

  • Cela J, Falk J, Munné-Bosch S (2009) Ethylene signaling may be involved in the regulation of tocopherol biosynthesis in Arabidopsis thaliana. FEBS Lett 583:992–996

    CAS  PubMed  Google Scholar 

  • Chang R, Jang C, Branco-Price C, Nghiem P, Bailey-Serres J (2012) Transient MPK6 activation in response to oxygen deprivation and reoxygenation is mediated by mitochondria and aids seedling survival in Arabidopsis. Plant Mol Biol 78:109–122

    CAS  PubMed  Google Scholar 

  • Dasgupta K, Ganesan S, Manivasagam S, Ayre B (2011) A cytochrome P450 monooxygenase commonly used for negative selection in transgenic plants causes growth anomalies by disrupting brassinosteroid signaling. BMC Plant Biol 11:67

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dordas C (2009) Nonsymbiotic hemoglobins and stress tolerance in plants. Plant Sci 176:433–440

    CAS  Google Scholar 

  • Dordas C, Rivoal J, Hill RD (2003) Plant haemoglobins, nitric oxide and hypoxic stress. Ann Bot (Lond) 91:173–178

    CAS  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Efron B, Tibshirani R (2007) On testing the significance of sets of genes. Ann Appl Stat 1:107–129

    Google Scholar 

  • Fait A, Yellin A, Fromm H (2005) GABA shunt deficiencies and accumulation of reactive oxygen intermediates: insight from Arabidopsis mutants. FEBS Lett 579:415–420

    CAS  PubMed  Google Scholar 

  • Fait A, Fromm H, Walter D, Galili G, Fernie AR (2008) Highway or byway: the metabolic role of the GABA shunt in plants. Trends Plant Sci 13:14–19

    CAS  PubMed  Google Scholar 

  • Fukao T, Bailey-Serres J (2004) Plant responses to hypoxia—is survival a balancing act? Trends Plant Sci 9:449–456

    CAS  PubMed  Google Scholar 

  • Fukao T, Bailey-Serres J (2008) Ethylene—a key regulator of submergence responses in rice. Plant Sci 175:43–51

    CAS  Google Scholar 

  • Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5:R80

    PubMed Central  PubMed  Google Scholar 

  • 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 (Lond) 96:661–668

    CAS  Google Scholar 

  • Greenway H, Gibbs J (2003) Review: mechanisms of anoxia tolerance in plants. II. Energy requirements for maintenance and energy distribution to essential processes. Funct Plant Biol 30:999–1036

    CAS  Google Scholar 

  • Gupta KJ, Zabalza A, van Dongen JT (2009) Regulation of respiration when the oxygen availability changes. Physiol Plant 137:383–391

    CAS  PubMed  Google Scholar 

  • Gupta KJ, Igamberdiev AU, Manjunatha G, Segu S, Moran JF, Neelawarne B, Bauwe H, Kaiser WM (2011a) The emerging roles of nitric oxide (NO) in plant mitochondria. Plant Sci 181:520–526

    CAS  PubMed  Google Scholar 

  • Gupta KJ, Hebelstrup KH, Mur LAJ, Igamberdiev AU (2011b) Plant hemoglobins: important players at the crossroads between oxygen and nitric oxide. FEBS Lett 585:3843–3849

    CAS  PubMed  Google Scholar 

  • Gupta KJ, Shah JK, Brotman Y, Jahnke K, Willmitzer L, Kaiser WM, Bauwe H, Igamberdiev AU (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

    CAS  PubMed  Google Scholar 

  • Hebelstrup KH, Igamberdiev AU, Hill RD (2007) Metabolic effects of hemoglobin gene expression in plants. Gene 398:86–93

    CAS  PubMed  Google Scholar 

  • Hebelstrup KH, van Zanten M, Mandon J, Voesenek LACJ, Harren FJM, Cristescu SM, Møller IM, Mur LAJ (2012) Haemoglobin modulates NO emission and hyponasty under hypoxia-related stress in Arabidopsis thaliana. J Exp Bot 63:5581–5591

    CAS  PubMed  Google Scholar 

  • Hill RD (2012) Non-symbiotic haemoglobins—what’s happening beyond nitric oxide scavenging? AoB Plants 2012:pls004

    PubMed Central  PubMed  Google Scholar 

  • Hoffman DL, Salter JD, Brookes PS (2007) Response of mitochondrial reactive oxygen species generation to steady-state oxygen tension: implications for hypoxic cell signaling. Am J Physiol Heart Circ Physiol 292:H101–H108

    CAS  PubMed  Google Scholar 

  • Huang S, Colmer TD, Millar AH (2008) Does anoxia tolerance involve altering the energy currency towards PPi? Trends Plant Sci 13:221–227

    CAS  PubMed  Google Scholar 

  • Hughes RK, De Domenico S, Santino A (2009) Plant cytochrome CYP74 family: biochemical features, endocellular localisation, activation mechanism in plant defence and improvements for industrial applications. ChemBioChem 10:1122–1133

    CAS  PubMed  Google Scholar 

  • Huxtable RJ (1992) Physiological actions of taurine. Physiol Rev 72:101–163

    CAS  PubMed  Google Scholar 

  • Igamberdiev AU, Hill RD (2009) Plant mitochondrial function during anaerobiosis. Ann Bot (Lond) 103:259–268

    CAS  Google Scholar 

  • Igamberdiev AU, Baron K, Manac’h-Little N, Stoimenova M, Hill RD (2005) The haemoglobin/nitric oxide cycle: involvement in flooding stress and effects on hormone signalling [Review]. Ann Bot (Lond) 96:557–564

    CAS  Google Scholar 

  • Igamberdiev AU, Bykova NV, Hill RD (2006) Nitric oxide scavenging by barley hemoglobin is facilitated by a monodehydroascorbate reductase-mediated ascorbate reduction of methemoglobin. Planta 223:1033–1040

    CAS  PubMed  Google Scholar 

  • Igamberdiev AU, Bykova NV, Shah JK, Hill RD (2010) Anoxic nitric oxide cycling in plants: participating reactions and possible mechanisms. Physiol Plant 138:393–404

    CAS  PubMed  Google Scholar 

  • Inzé A, Vanderauwera S, Hoeberichts FA, vanDorpe M, van Gaever T, van Breusegem F (2012) A subcellular localization compendium of hydrogen peroxide-induced proteins. Plant Cell Environ 35:308–320

    PubMed  Google Scholar 

  • Jaspers P, Kangasjärvi J (2010) Reactive oxygen species in abiotic stress signaling. Physiol Plant 138(4):405–413

    CAS  PubMed  Google Scholar 

  • Johnson WE, Li C, Rabinovic A (2007) Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics 8:118–127

    PubMed  Google Scholar 

  • Kataoka H, Ohnishi N (1986) Occurrence of taurine in plants. Agric Biol Chem 50(7):1887–1888

    CAS  Google Scholar 

  • Lasanthi-Kudahettige R, Magneschi L, Loreti E, Gonzali S, Licausi F, Novi G, Beretta O, Vitulli F, Alpi A, Perata P (2007) Transcript profiling of the anoxic rice coleoptile. Plant Physiol 144:218–231

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lee SC, Mustroph A, Sasidharan R, Vashisht D, Pedersen O, Oosumi T, Voesenek LACJ, Bailey-Serres J (2011) Molecular characterization of the submergence response of the Arabidopsis thaliana ecotype Columbia. New Phytol 190:457–471

    CAS  PubMed  Google Scholar 

  • Lewis DFV (2002) Oxidative stress: the role of cytochromes P450 in oxygen activation. J Chem Technol Biotechnol 77:1095–1100

    CAS  Google Scholar 

  • Li C, Chen Q, Gao X, Qi B, Chen N, Xu S, Chen J, Wang X (2005) AtHsfA2 modulates expression of stress responsive genes and enhances tolerance to heat and oxidative stress in Arabidopsis. Sci China C Life Sci 48:540–550

    CAS  PubMed  Google Scholar 

  • Licausi F (2011) Regulation of the molecular response to oxygen limitations in plants. New Phytol 190:550–555

    CAS  PubMed  Google Scholar 

  • Licausi F, Van Dongen JT, Giuntoli B, Novi G, Santaniello A, Geigenberger P, Perata P (2010) HRE1 and HRE2, two hypoxia-inducible ethylene response factors, affect anaerobic responses in Arabidopsis thaliana. Plant J 62:302–315

    CAS  PubMed  Google Scholar 

  • Lindermayr C, Saalbach G, Bahnweg G, Durner J (2006) Differential inhibition of Arabidopsis methionine adenosyltransferases by protein S-nitrosylation. J Biol Chem 281:4285–4291

    CAS  PubMed  Google Scholar 

  • Loenarz C, Schofield CJ (2008) Expanding chemical biology of 2-oxoglutarate oxygenases. Nat Chem Biol 4:152–156

    CAS  PubMed  Google Scholar 

  • Loreti E, Poggi A, Novi G, Alpi A, Perata P (2005) A genome-wide analysis of the effects of sucrose on gene expression in Arabidopsis seedlings under anoxia. Plant Physiol 137:1130–1138

    CAS  PubMed Central  PubMed  Google Scholar 

  • Luhua S, Ciftci-Yilmaz S, Harper J, Cushman J, Mittler R (2008) Enhanced tolerance to oxidative stress in transgenic Arabidopsis plants expressing proteins of unknown function. Plant Physiol 148:280–292

    PubMed Central  PubMed  Google Scholar 

  • Manac’h-Little N, Igamberdiev AU, Hill RD (2005) Hemoglobin expression affects ethylene production in maize cell cultures. Plant Physiol Biochem 43:485–489

    PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    CAS  PubMed  Google Scholar 

  • Mustroph A, Lee SC, Oosumi T, Zanetti ME, Yang H, Ma K, Yaghoubi-Masihi A, Fukao T, Bailey-Serres J (2010) Cross-kingdom comparison of transcriptomic adjustments to low-oxygen stress highlights conserved and plant-specific responses. Plant Physiol 152:1484–1500

    CAS  PubMed Central  PubMed  Google Scholar 

  • Narsai R, Rocha M, Geigenberger P, Whelan J, van Dongen JT (2011) Comparative analysis between plant species of transcriptional and metabolic responses to hypoxia. New Phytol 190(2):472–487

    CAS  PubMed  Google Scholar 

  • Navarre DA, Wendehenne D, Durner J, Noad R, Klessig DF (2000) Nitric oxide modulates the activity of tobacco aconitase. Plant Physiol 122:573–582

    CAS  PubMed Central  PubMed  Google Scholar 

  • Navrot N, Rouhier N, Gelhaye E, Jacquot J (2007) Reactive oxygen species generation and antioxidant systems in plant mitochondria. Physiol Plant 129:185–195

    CAS  Google Scholar 

  • Nelson D, Werck-Reichhart D (2011) A P450-centric view of plant evolution. Plant J 66:194–211

    CAS  PubMed  Google Scholar 

  • Newton MA, Quintana FA, den Boon JA, Sengupta S, Ahlquist P (2007) Random-set methods identify distinct aspects of the enrichment signal in gene-set analysis. Ann Appl Stat 1:85–106

    Google Scholar 

  • Obata T, Matthes A, Koszior S, Lehmann M, Araújo WL, Bock R, Sweetlove LJ, Fernie AR (2011) Alteration of mitochondrial protein complexes in relation to metabolic regulation under short-term oxidative stress in Arabidopsis seedlings. Phytochemistry 72:1081–1091

    CAS  PubMed  Google Scholar 

  • Petrov VD, Van Breusegem F (2012) Hydrogen peroxide—a central hub for information flow in plant cells. AoB Plants 2012:pls014

    PubMed Central  PubMed  Google Scholar 

  • Planchet E, Jagadis Gupta K, Sonoda M, Kaiser WM (2005) Nitric oxide emission from tobacco leaves and cell suspensions: rate limiting factors and evidence for the involvement of mitochondrial electron transport. Plant J 41:732–743

    CAS  PubMed  Google Scholar 

  • Potters G, Pasternak TP, Guisez Y, Jansen MAK (2009) Different stresses, similar morphogenic responses: integrating a plethora of pathways. Plant Cell Environ 32:158–169

    PubMed  Google Scholar 

  • Pucciariello C, Parlanti S, Banti V, Novi G, Perata P (2012) Reactive oxygen species-driven transcription in Arabidopsis under oxygen deprivation. Plant Physiol 159:184–196

    CAS  PubMed Central  PubMed  Google Scholar 

  • Qiao W, Fan L (2008) Nitric oxide signaling in plant responses to abiotic stresses. J Integr Plant Biol 50:1238–1246

    CAS  PubMed  Google Scholar 

  • Qu Z, Zhong N, Wang H, Chen A, Jian G, Xia G (2006) Ectopic expression of the cotton non-symbiotic hemoglobin gene GhHbd1 triggers defense responses and increases disease tolerance in Arabidopsis. Plant Cell Physiol 47:1058–1068

    CAS  PubMed  Google Scholar 

  • Rhoads DM, Umbach AL, Subbaiah CC, Siedow JN (2006) Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling. Plant Physiol 141:357–366

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ritchie ME, Silver J, Oshlack A, Holmes M, Diyagama D, Holloway A, Smyth GK (2007) A comparison of background correction methods for two-colour microarrays. Bioinformatics 23:2700–2707

    CAS  PubMed  Google Scholar 

  • Rocha M, Licausi F, Araujo WL, Nunes-Nesi A, Sodek L, Fernie AR, van Dongen JT (2010) Glycolysis and the tricarboxylic acid cycle are linked by alanine aminotransferase during hypoxia induced by waterlogging of Lotus japonicus. Plant Physiol 152:1501–1513

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sairam R, Kumutha D, Ezhilmathi K, Deshmukh P, Srivastava G (2008) Physiology and biochemistry of waterlogging tolerance in plants. Biol Plant 52:401–412

    CAS  Google Scholar 

  • Sakamoto A, Sakurao S, Fukunaga K, Matsubara T, Ueda-Hashimoto M, Tsukamoto S, Takahashi M, Morikawa H (2004) Three distinct Arabidopsis hemoglobins exhibit peroxidase-like activity and differentially mediate nitrite-dependent protein nitration. FEBS Lett 572:27–32

    CAS  PubMed  Google Scholar 

  • Santosa I, Ram P, Boamfa E, Laarhoven L, Reuss J, Jackson M, Harren F (2007) Patterns of peroxidative ethane emission from submerged rice seedlings indicate that damage from reactive oxygen species takes place during submergence and is not necessarily a post-anoxic phenomenon. Planta 226:193–202

    CAS  PubMed  Google Scholar 

  • Shimoda Y, Nagata M, Suzuki A, Abe M, Sato S, Kato T, Tabata S, Higashi S, Uchiumi T (2005) Symbiotic rhizobium and nitric oxide induce gene expression of non-symbiotic hemoglobin in Lotus japonicus. Plant Cell Physiol 46:99–107

    CAS  PubMed  Google Scholar 

  • Smyth GK (2005) LIMMA: linear models for microarray data. In: Bioinformatics and Computational Biology Solutions Using R and Bioconductor; Gentleman R, Carey V, Huber W, Irizarry R, Dudoit S (eds) Springer, New York, pp 397–420

    Google Scholar 

  • Stoimenova M, Igamberdiev AU, Gupta K, Hill RD (2007) Nitrite-driven anaerobic ATP synthesis in barley and rice root mitochondria. Planta 226:465–474

    CAS  PubMed  Google Scholar 

  • St-Pierre J, Brand MD, Boutilier RG (2000) Mitochondria as ATP consumers: cellular treason in anoxia. Proc Natl Acad Sci U S A 97:8670–8674

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sweetlove LJ, Beard KFM, Nunes-Nesi A, Fernie AR, Ratcliffe RG (2010) Not just a circle: flux modes in the plant TCA cycle. Trends Plant Sci 15:462–470

    CAS  PubMed  Google Scholar 

  • Törönen P, Ojala P, Marttinen P, Holm L (2009) Robust extraction of functional signals from gene set analysis using a generalized threshold free scoring function. BMC Bioinformatics 10:307

    PubMed Central  PubMed  Google Scholar 

  • Trevaskis B, Watts RA, Andersson CR, Llewellyn DJ, Hargrove MS, Olson JS, Dennis ES, Peacock WJ (1997) Two hemoglobin genes in Arabidopsis thaliana: the evolutionary origins of leghemoglobins. Proc Natl Acad Sci U S A 94:12230–12234

    CAS  PubMed Central  PubMed  Google Scholar 

  • Van Breusegem F, Bailey-Serres J, Mittler R (2008) Unraveling the tapestry of networks involving reactive oxygen species in plants. Plant Physiol 147:978–984

    PubMed Central  PubMed  Google Scholar 

  • van Dongen JT, Frohlich A, Ramirez-Aguilar SJ, Schauer N, Fernie AR, Erban A, Kopka J, Clark J, Langer A, Geigenberger P (2009) Transcript and metabolite profiling of the adaptive response to mild decreases in oxygen concentration in the roots of Arabidopsis plants. Ann Bot (Lond) 103:269–280

    Google Scholar 

  • Wang R, Guegler K, LaBrie ST, Crawford NM (2000) Genomic analysis of a nutrient response in Arabidopsis reveals diverse expression patterns and novel metabolic and potential regulatory genes induced by nitrate. Plant Cell Online 12:1491–1509

    CAS  Google Scholar 

  • Wulff A, Oliveira HC, Saviani EE, Salgado I (2009) Nitrite reduction and superoxide-dependent nitric oxide degradation by Arabidopsis mitochondria: influence of external NAD(P)H dehydrogenases and alternative oxidase in the control of nitric oxide levels. Nitric Oxide 21:132–139

    CAS  PubMed  Google Scholar 

  • Yan B, Dai Q, Liu X, Huang S, Wang Z (1996) Flooding-induced membrane damage, lipid oxidation and activated oxygen generation in corn leaves. Plant Soil 179:261–268

    CAS  Google Scholar 

  • Yoo S, Sheen J (2008) MAPK signaling in plant hormone ethylene signal transduction. Plant Signal Behav 3:848–849

    PubMed Central  PubMed  Google Scholar 

  • Yun B, Feechan A, Yin M, Saidi NBB, Le Bihan T, Yu M, Moore JW, Kang J, Kwon E, Spoel SH, Pallas JA, Loake GJ (2011) S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478:264–268

    CAS  PubMed  Google Scholar 

  • Zabalza A, van Dongen JT, Froehlich A, Oliver SN, Faix B, Gupta KJ, Schmalzlin E, Igal M, Orcaray L, Royuela M, Geigenberger P (2009) Regulation of respiration and fermentation to control the plant internal oxygen concentration. Plant Physiol 149:1087–1098

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhao L, Gu R, Gao P, Wang G (2008) A nonsymbiotic hemoglobin gene from maize, ZmHb, is involved in response to submergence, high-salt and osmotic stresses. Plant Cell Tissue Organ Cult 95:227–237

    CAS  Google Scholar 

  • Zhao M, Chen L, Zhang L, Zhang W (2009) Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis. Plant Physiol 151:755–767

    CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We wish to thank Julia Bailey-Serres, Joost van Dongen, Pierdomenico Perata, and Chiara Pucciariello for supplying the microarray datasets for our analysis. This work was supported by the Academy of Finland grant no. 123826.

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Correspondence to Olga B. Blokhina .

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Blokhina, O.B., Törönen, P., Fagerstedt, K.V. (2014). Oxidative Stress Components Explored in Anoxic and Hypoxic Global Gene Expression Data. In: van Dongen, J., Licausi, F. (eds) Low-Oxygen Stress in Plants. Plant Cell Monographs, vol 21. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1254-0_2

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