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Reactive oxygen species production and antioxidative defense in pea (Pisum sativum L.) root nodules after short-term aluminum treatment

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Abstract

Pea plants (Pisum sativum L.) were treated with 50 μM aluminum chloride at pH 4.5 for 2 or 24 h at room temperature. Following treatment, root nodule Al uptake, the generation of reactive oxygen species (ROS, O −·2 and H2O2), and the activities of the antioxidant enzymes catalase (CAT), superoxide dismutase (SOD) and peroxidase (POX) were investigated. Aluminum accumulation was found chiefly in the apoplast of the nodule cortex, endodermis and meristem, while the formation of peroxide was detected in the nodule cortex, infection threads and bacteroidal tissue. Further, there were increased levels of superoxide in the meristem and bacteroidal tissue. The activity of SOD (EC 1.15.1.1) and POX (EC 1.11.1.7) increased in the Al-treated nodules and the roots of pea plants, whereas CAT (EC 1.11.1.6) activity decreased. The Al absorbed by the nodules induced ROS production. The POX and SOD are important ROS-scavengers in Al-stressed nodules.

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References

  • Ahn SJ, Sivaguru M, Chung GC, Rengel Z, Matsumoto H (2002) Aluminium-induced growth inhibition is associated with impaired efflux and influx of H+ across the plasma membrane in root apices of squash (Cucurbita pepo). J Exp Bot 53:1959–1966

    Article  PubMed  CAS  Google Scholar 

  • Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341. doi:10.1093/jexbot/53.372.1331

    Article  PubMed  CAS  Google Scholar 

  • Alva AK, Assher CJ, Edwards DG (1990) Effect of solution pH, external calcium concentration and aluminum activity on nodulation and early growth of cowpea. Aust J Agric Res 41:359–365. doi:10.1071/AR9900359

    Article  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399. doi:10.1146/annurev.arplant.55.031903.141701

    Article  PubMed  CAS  Google Scholar 

  • Balestrasse KB, Gallego SM, Tomaro ML (2006) Aluminium stress affects nitrogen fixation and assimilation in soybean (Glycine max L.). Plant Growth Regul 48:271–281. doi:10.1007/s10725-006-0010-x

    CAS  Google Scholar 

  • Basu U, Good AG, Taylor GJ (2001) Transgenic Brassica napus plants overexpressing aluminum-induced mitochondrial manganese superoxide dismutase cDNA are resistant to aluminum. Plant Cell Environ 24:1269–1278. doi:10.1046/j.0016-8025.2001.00783.x

    Article  CAS  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and assay applicable to acrylamide gels. Anal Biochem 44:276–287. doi:10.1016/0003-2697(71)90370-8

    Article  PubMed  CAS  Google Scholar 

  • Becana M, Salin ML (1989) Superoxide dismutases in nodules of leguminous plants. Can J Bot 67:415–421. doi:10.1139/b89-057

    Article  CAS  Google Scholar 

  • Becana M, Paris FJ, Sandalio LM, del Río LA (1989) Isoenzymes of superoxide dismutase in nodules of Phaseolus vulgaris L., Pisum sativum L., and Vigna unguiculata (L.). Plant Physiol 90:1286–1292

    Article  PubMed  CAS  Google Scholar 

  • Becana M, Dalton DA, Morana JF, Iturbe-Ormaetxea I, Matamorosa MA, Rubioa MC (2000) Reactive oxygen species and antioxidants in legume nodules. Physiol Plant 109:372–381. doi:10.1034/j.1399-3054.2000.100402.x

    Article  CAS  Google Scholar 

  • Blancaflor EB, Jones DL, Gilroy S (1998) Alterations in the cytoskeleton accompany aluminum-induced growth inhibition and morphological changes in the primary roots of maize. Plant Physiol 118:159–172

    Article  PubMed  CAS  Google Scholar 

  • Bordeleau LM, Provost D (1994) Nodulation and nitrogen fixation in extreme environments. Plant Soil 161:115–125. doi:10.1034/j.1399-3054.2000.100402.x

    Article  CAS  Google Scholar 

  • Borucki W, Sujkowska M (2008) The effects of sodium chloride-salinity upon growth, nodulation, and root nodule structure of pea (Pisum sativum L.) plants. Acta Physiol Plant 30:293–301. doi:10.1007/s11738-007-0120-8

    Article  CAS  Google Scholar 

  • Boscolo PRS, Menossi M, Jorge RA (2003) Aluminum induced oxidative stress in maize. Phytochemistry 62:181–189. doi:10.1016/S0031-9422(02)00491-0

    Article  PubMed  CAS  Google Scholar 

  • Bowler C, Van Montagu M, Inze D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43:83–116

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. doi:10.1016/0003-2697(76)90527-3

    Article  PubMed  CAS  Google Scholar 

  • Browne BA, Driscoll CT, McColl JG (1990) Aluminum speciation using morin. II. Principles and procedures. J Environ Qual 19:73–82

    Article  CAS  Google Scholar 

  • Bueno P, Varela J, Gimenez GG, Del Rio LA (1995) Peroxisomal copper, zinc superoxide dismutase: characterization of the isoenzyme from watermelon cotyledons. Plant Physiol 108:1151–1160

    Article  PubMed  CAS  Google Scholar 

  • Cakmak I, Horst WJ (1991) Effect of aluminum on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468. doi:10.1111/j.1399-3054.1991.tb00121.x

    Article  CAS  Google Scholar 

  • Chandran D, Sharopova N, Ivashuta S, Gnatt JS, Vandenbosch KA, Samac DA (2008) Transcriptome profiling identified novel genes associated with aluminum toxicity, resistance and tolerance in Medicago truncatula. Planta 228:151–16683. doi:10.1007/s00425-008-0726-0

    Article  PubMed  CAS  Google Scholar 

  • Churin Y, Schilling S, Bőrner T (1999) A gene family encoding glutathione peroxidase homologues in Hordeum vulgare (barley). FEBS Lett 459:33–38. doi:10.1016/S0014-5793(99)01208-9

    Article  PubMed  CAS  Google Scholar 

  • Čiamporová M (2000) Diverse response of root cell structure to aluminum stress. Plant Soil 226:113–116. doi:10.10213/A:102646803157

    Article  Google Scholar 

  • Dalton DA, Baird LM, Langeberg L, Taugher CY, Anyan WR, Vance CP, Sarath G (1993) Subcellular localization of oxygen defense enzymes in soybean (Glycine max [L.] Merr.) root nodules. Plant Physiol 102:481–489. doi:10.1104/pp.102.2.481

    PubMed  CAS  Google Scholar 

  • Darko E, Ambrus H, Stefanovits-Banyai E, Fodor J, Bakos F (2004) Aluminum toxicity, Al tolerance and oxidative stress in an Al-sensitive wheat genotype and in Al-tolerant lines developed by in vitro microspore selection. Plant Sci 166:583–591. doi:10.1016/j.plantsci.2003.10.023

    Article  CAS  Google Scholar 

  • de Lima ML, Copeland L (1994) Changes in the ultrastructure of the root tip of wheat following exposure to aluminum. Aust J Plant Physiol 21:85–94

    Article  Google Scholar 

  • Delisle G, Champoux M, Houde M (2001) Characterization of oxalate oxidase and cell death in Al-sensitive and tolerant wheat roots. Plant Cell Physiol 42:324–333

    Article  PubMed  CAS  Google Scholar 

  • Doncheva S, Amenos M, Poschenrieder C, Barcelo J (2005) Root cell patterning: a primary target for aluminum toxicity in maize. J Exp Bot 56:1213–1220. doi:10.1093/jxb/eri115

    Article  PubMed  CAS  Google Scholar 

  • Ezaki B, Yamamoto Y, Matsumoto H (1996) Expression of a moderately anionic peroxidase is induced by aluminum treatment in tobacco cells: possible involvement of peroxidase isozymes in aluminum ion stress. Physiol Plant 96:21–28. doi:10.1111/j.1399-3054.1996.tb00178.x

    Article  CAS  Google Scholar 

  • Ezaki B, Gardner RC, Ezaki Y, Matsumoto H (2000) Expression of aluminum-induced genes in transgenic Arabidopsis plants can ameliorate aluminum stress and/or oxidative stress. Plant Physiol 122:657–665. doi:10.1104/pp.122.3.657

    Article  PubMed  CAS  Google Scholar 

  • Ezaki B, Katsuhara M, Kawamura M, Matsumoto H (2001) Different mechanisms of four aluminum (Al)-resistant transgenes for Al toxicity in Arabidopsis. Plant Physiol 127:918–927. doi:10.1104/pp.010399

    Article  PubMed  CAS  Google Scholar 

  • Fahraeus G (1957) The infection of clover root hairs by nodule bacteria studied by single glass slide technique. J Gen Microbiol 16:374–381

    PubMed  CAS  Google Scholar 

  • Ferreira RR, Fornazier RF, Vitoria AP, Lea PJ, Azevedo RA (2002) Changes in antioxidant enzyme activities in soybean under cadmium stress. J Plant Nutr 25:327–342. doi:10.1081/PLN-100108839

    Article  CAS  Google Scholar 

  • Flis SE, Glenn AR, Dilworth MJ (1993) The interaction between aluminium and root nodule bacteria. Soil Biol Biochem 25:403–417

    Article  CAS  Google Scholar 

  • Foyer CH, Descouvieres P, Kunert KJ (1994) Protection against oxygen radicals: an important defense mechanism studied in transgenic plants. Plant Cell Environ 17:507–523. doi:10.1111/j.1365-3040.1994.tb00146.x

    Article  CAS  Google Scholar 

  • Fryer MJ, Oxborough K, Mullineaux PM, Baker NR, Smirnoff N (2002) Imaging of photo-oxidative stress responses in leaves. J Exp Bot 53:1249–1254. doi:10.1093/jexbot/53.372.1249

    Article  PubMed  CAS  Google Scholar 

  • Hegedüs A, Erdei S, Horváth G (2001) Comparative studies of H2O2 detoxifying enzymes in green and greening barley seedlings under cadmium stress. Plant Sci 160:1085–1093. doi:10.1016/S0168-9452(01)00330-2

    Article  PubMed  Google Scholar 

  • Hérouart D, Baudouin E, Fredo P, Harrison J, Santos R, Jamet A, Van de Sype G, Touati D, Puppo A (2002) Reactive oxygen species, nitric oxide and glutathione: a key role in the establishment of the legume–Rhizobium symbiosis? Plant Physiol Biochem 40:619–624. doi:10.1016/S0981-9428(02)01415-8

    Article  Google Scholar 

  • Hiraga S, Sasaki K, Ito H, Ohashi Y, Matsui H (2001) A large family of class III plant peroxidases. Plant Cell Physiol 42:462–468. doi:10.1093/pcp/pce061

    Article  PubMed  CAS  Google Scholar 

  • Horst WJ, Schmohl N, Kollmeier M, Baluška F, Sivaguru M (1999) Does aluminum affect root growth of maize through interaction with the cell wall–plasma membrane–cytoskeleton continuum? Plant Soil 215:163–174

    Article  CAS  Google Scholar 

  • Hossain AKMZ, Koyama H, Hara T (2006) Growth and cell wall properties of two wheat cultivars differing in their sensitivity to aluminum stress. J Plant Physiol 163:39–47

    Article  CAS  Google Scholar 

  • Igual JM, Rodriguezbarrueco C, Cervantes E (1997) The effect of aluminum on nodulation and nitrogen fixation in Casuarina cunninghamiana Miq. Plant Soil 190:41–46. doi:10.1023/A:1004259123008

    Article  CAS  Google Scholar 

  • Iturbe-Ormaetxe I, Matamoros MA, Rubio MC, Dalton DA, Becana M (2001) The antioxidants of legume nodule mitochondria. Mol Plant-Microbe Interact 14:1189–1196. doi:10.1094/MPMI.2001.14.10.1189

    Article  PubMed  CAS  Google Scholar 

  • Jaleel CA, Riadh K, Gopi R, Manivannan P, Ine`s J, Al-Juburi HJ, Chang-Xing Z, Hong-Bo S, Panneerselvam R (2009) Antioxidant defense responses: physiological plasticity in higher plants under abiotic constraints. Acta Physiol Plant 31:427–436. doi:10.1007/s11738-009-0275-6

    Article  CAS  Google Scholar 

  • James A, Siguard S, Van de Sype G, Puppo A, Hèrouart D (2003) Expression of the bacterial catalase genes in Sinorhizobium melilotiMedicago sativa symbiosis and their crucial role during the infection process. Mol Plant-Microbe Interact 16:217–225

    Article  Google Scholar 

  • Jebara S, Jebara M, Limam F, Aouani ME (2005) Changes in ascorbate peroxidase, catalase, guaiacol peroxidase and superoxide dismutase activities under salt stress. J Plant Physiol 162:929–936. doi:10.1016/j.jplph.2004.10.005

    Article  PubMed  CAS  Google Scholar 

  • Jones DL, Blancaor EB, Kochian LV, Gilroy S (2006) Spatial coordination of aluminum uptake, production of reactive oxygen species, callose production and wall rigidification in maize roots. Plant Cell Environ 29:1309–1318. doi:10.1111/j.1365-3040.2006.01509.x

    Article  PubMed  CAS  Google Scholar 

  • Kaneko Y, Newcomb EH (1987) Cytochemical localization of uricase and catalase in developing root nodules of soybean. Protoplasma 140:1–12. doi:10.1007/BF01273250

    Article  Google Scholar 

  • Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 27:137A–138A

    Google Scholar 

  • Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol Plant Mol Biol 46:237–260. doi:10.1146/annurev.pp.46.060195.001321

    Article  CAS  Google Scholar 

  • Konarska A (2005) Changes in the development and structure of Raphanus sativus L. var. radicula Pers. root under aluminum stress conditions. Acta Sci Pol 4:85–97

    Google Scholar 

  • Konarska A (2008) Changes in the ultrastructure of Capsicum annuum L. seedlings roots under aluminum stress conditions. Acta Agrobot 61:27–32

    Google Scholar 

  • Kumari M, Taylor GJ, Deyholos MK (2008) Transcriptomic responses to aluminum stress in roots of Arabidopsis thaliana. Mol Genet Genomics 279:339–357. doi:10.1007/s00438-007-0316-z

    Article  PubMed  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 277:680–685

    Article  Google Scholar 

  • Lavid N, Schwartz A, Yarden O, Tel-Or E (2001) The involvement of polyphenols and peroxidase activities in heavy-metal accumulation by epidermal glands of the waterlily (Nymphaceae). Planta 212:323–331

    Article  PubMed  CAS  Google Scholar 

  • Lewis NG, Yamamoto E (1990) Lignin: occurrence, biogenesis, and degradation. Annu Rev Plant Physiol Plant Mol Biol 41:455–469. doi:10.1146/annurev.pp.41.060190.002323

    Article  PubMed  CAS  Google Scholar 

  • Liu Q, Yang JL, He LS, Li YY, Zheng SJ (2008) Effect of aluminum on cell wall, plasma membrane, antioxidants and root elongation in triticale. Biol Plant 52:87–92. doi:10.1007/s10535-008-0014-7

    Article  CAS  Google Scholar 

  • Ma JF, Shen RF, Nagao S, Tanimoto E (2004) Aluminum targets elongating cells by reducing cell wall extensibility in wheat roots. Plant Cell Physiol 45:583–589

    Article  PubMed  CAS  Google Scholar 

  • Matamoros MA, Dalton DA, Ramos J, Clemente MR, Rubio MC, Becana M (2003) Biochemistry and molecular biology of antioxidants in the rhizobia–legume symbiosis. Plant Physiol 133:499–509. doi:10.1104/pp.103.025619

    Article  PubMed  CAS  Google Scholar 

  • Matsumoto H (2000) Cell biology of aluminum toxicity and tolerance in higher plants. Int Rev Cytol 200:1–46

    Article  PubMed  CAS  Google Scholar 

  • Meriga B, Reddy BK, Rao KR, Reddy LA, Kavi Kishor PB (2004) Aluminum-induced production of oxygen radicals, lipid peroxidation and DNA damage in seedlings of rice (Oryza sativa). J Plant Physiol 161:63–68

    Article  PubMed  CAS  Google Scholar 

  • Milla MAR, Butler E, Huete AR, Wilson CF, Anderson O, Gustafson JP (2002) Expressed sequence tag-based gene expression analysis under aluminum stress in rye. Plant Physiol 130:1706–1716

    Article  PubMed  CAS  Google Scholar 

  • Mohammadi M, Karr AL (2001) Superoxide anion generation in effective and ineffective soybean root nodules. J Plant Physiol 158:1023–1029

    Article  CAS  Google Scholar 

  • Moran JF, James EK, Rubio MC, Sarath G, Klucas RV, Becana M (2003) Functional characterization and expression of a cytosolic iron-superoxide dismutase from cowpea root nodules. Plant Physiol 133:773–782. doi:10.1104/pp.103.023010

    Article  PubMed  CAS  Google Scholar 

  • Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot 53:1237–1247. doi:10.1093/jexbot/53.372.1237

    Article  PubMed  CAS  Google Scholar 

  • Pan S-M, Yau Y-Y (1992) Characterization of superoxide dismutase in Arabidopsis. Plant Cell Physiol 37:58–66

    Google Scholar 

  • Panda SK, Matsumoto H (2007) Molecular physiology of aluminum toxicity and tolerance in plants. Bot Rev 73(4):326–347

    Article  Google Scholar 

  • Panda SK, Singha LB, Khan MH (2003) Does aluminium phytotoxicity induce oxidative stress in greengram (Vigna radiata)? Bulg J Plant Physiol 29:77–86

    Google Scholar 

  • Panda SK, Baluska F, Matsumoto H (2009) Aluminium stress signaling in plants. Plant Signal Behav 4(7):592–597

    Article  PubMed  CAS  Google Scholar 

  • Passardi F, Longet D, Penel C, Dunand C (2004) The class III peroxidase multigenic family in rice and its evolution in land plants. Phytochemistry 65:1879–1893. doi:10.1016/j.phytochem.2004.06.023

    Article  PubMed  CAS  Google Scholar 

  • Passardi F, Cosio C, Penel C, Dunand C (2005) Peroxidases have more functions than a Swiss army knife. Plant Cell Rep 24:255–265. doi:10.1007/s00299-005-0972-6

    Article  PubMed  CAS  Google Scholar 

  • Peixoto PHP, Cambraia J, Sant’anna R, Mosquim PR, Moreira MA (1999) Aluminum effects on lipid peroxidation and on the activities of enzymes of oxidative metabolism in sorghum. Rev Bras Fisiol Veg 11:137–143

    CAS  Google Scholar 

  • Polidoros AN, Scandalios JG (1999) Role of hydrogen peroxide and different classes of antioxidants in the regulation of catalase and glutathione S-transferase gene expression in maize (Zea mays L.). Physiol Plant 106:112–120

    Article  CAS  Google Scholar 

  • Polle E, Konzak CF, Kittrick JA (1978) Visual detection of aluminum tolerance levels in wheat by hematoxylin staining of seedling roots. Crop Sci 18:823–827

    Article  CAS  Google Scholar 

  • Polle A, Otter T, Seifert F (1994) Apoplastic peroxidase and lignification in needles of Norway spruce (Picea abies L.). Plant Physiol 106:53–60. doi:10.1104/pp.106.1.53

    PubMed  CAS  Google Scholar 

  • Rengel Z, Zhang WH (2003) Role of dynamics of intracellular calcium in aluminum-toxicity syndrome. New Phytol 159:295–314

    Article  CAS  Google Scholar 

  • Richards KD, Schott EJ, Sharma YK, Davis KR, Gardner RC (1998) Aluminum induces oxidative stress genes in Arabidopsis thaliana. Plant Physiol 116:409–418

    Article  PubMed  CAS  Google Scholar 

  • Rubio MC, James EK, Clemente MR, Bucciarelli B, Fedorova M, Vance CP, Becana M (2004) Localization of superoxide dismutases and hydrogen peroxide in legume root nodules. Mol Plant-Microbe Interact 17:1294–1305. doi:10.1094/MPMI.2004.17.12.1294

    Article  PubMed  CAS  Google Scholar 

  • Ryan PR, Ditomaso JM, Kochian LV (1993) Aluminum toxicity in roots: an investigation of spatial sensitivity and the role of the root cap. J Exp Bot 44:437–446

    Article  CAS  Google Scholar 

  • Salzer P, Corbière H, Boller T (1998) Hydrogen peroxide accumulation in Medicago truncatula roots colonized by the arbuscular mycorrhiza-forming fungus Glomus intraradice. Planta 208:319–325. doi:10.1007/s004250050565

    Article  Google Scholar 

  • Santos R, Hérouart D, Puppo A, Touati D (2000) Critical protective role of bacterial superoxide dismutase in Rhizobium–legume symbiosis. Mol Microbiol 38:750–759

    Article  PubMed  CAS  Google Scholar 

  • Santos R, Hérouart D, Sigaud S, Touati D, Puppo A (2001) Oxidative burst in alfalfa–Sinorhizobium meliloti symbiotic interaction. Mol Plant-Microbe Interact 14:86–89. doi:10.1094/MPMI.2001.14.1.86

    Article  PubMed  CAS  Google Scholar 

  • Sasaki M, Yamamoto Y, Matsumoto H (1996) Lignin deposition induced by aluminum in wheat (Triticum aestivum) roots. Physiol Plant 96:193–198

    Article  CAS  Google Scholar 

  • Scandalios JG, Guan L, Polidoros AN (1997) Catalases in plants: gene structure, properties, regulation, and expression. In: Scandalios JG (ed) Oxidative stress and the molecular biology of antioxidant defenses. Cold Spring Harbor, New York, pp 343–406

    Google Scholar 

  • Shamssudin ZH, Kasran R, Edwards DG, Blamey FPC (1992) Effect of calcium and aluminum on nodulation, nitrogen fixation and growth of groundnut in solution culture. Plant Soil 144:273–2799. doi:10.1007/BF00012885

    Article  Google Scholar 

  • Sharma P, Dubey RS (2007) Involvement of oxidative stress and role of antioxidative defense system in growing rice seedlings exposed to toxic concentrations of aluminum. Plant Cell Rep 26:2027–2038. doi:10.1007/s00299-007-0416-6

    Article  PubMed  CAS  Google Scholar 

  • Shaw BP (1995) Effect of mercury and cadmium on the activities of antioxidative enzymes in the seedlings of Phaseolus aureus. Biol Plant 37:587–596

    Article  CAS  Google Scholar 

  • Silva IR, Smyth TJ, Raper CD, Carter TE, Rufty TW (2001) Differential aluminum tolerance in soybean: an evaluation of the role of organic acids. Physiol Plant 112:200–210

    Article  PubMed  CAS  Google Scholar 

  • Šimonovičová M, Tamás L, Huttová J, Mistrík I (2004) Effect of aluminum on oxidative stress related enzymes activities in barley roots. Biol Plant 48:261–266. doi:10.1023/B:BIOP.0000033454.95515.8a

    Article  Google Scholar 

  • Sivaguru M, Horst WJ (1998) The distal part of the transition zone is the most aluminum-sensitive apical root zone of Zea mays L. Plant Physiol 116:155–163. doi:10.1104/pp.116.1.155

    Article  CAS  Google Scholar 

  • Sivaguru M, Fujiwara T, Samaj J, Baluska F, Yang Z, Osawa H, Maeda T, Mori T, Volkmann D, Matsumoto H (2000) Aluminum-induced 1,3-β-d-glucan inhibits cell-to-cell trafficking of molecules through plasmodesmata. A new mechanism of aluminum toxicity in plants. Plant Physiol 124:991–1005. doi:10.1104/pp.124.3.991

    Article  PubMed  CAS  Google Scholar 

  • Sivaguru M, Pike S, Gassmann W, Baskin TI (2003) Aluminum rapidly depolymerized cortical microtubules and depolarizes the plasma membrane: evidence that these responses are mediated by a glutamate receptor. Plant Cell Physiol 44:667–675. doi:10.1093/pcp/pcg094

    Article  PubMed  CAS  Google Scholar 

  • Sobkowiak R, Rymer K, Rucińska R, Deckert J (2004) Cadmium-induced changes in antioxidant enzymes in suspension culture of soybean cells. Acta Biochim Polon 51:219–222

    PubMed  CAS  Google Scholar 

  • Streller S, Wingsle G (1994) Pinus sylvestris L. needles contain extracellular CuZn superoxide dismutase. Planta 192:195–201

    Article  PubMed  CAS  Google Scholar 

  • Tamás L, Huttová J, Mistrík I, Šimonovičová M, Široká B (2006) Aluminium-induced drought and oxidative stress in barley roots. J Plant Physiol 163:781–784. doi:10.1016/j.jplph.2005.08.012

    Article  PubMed  CAS  Google Scholar 

  • Tice KR, Parker DR, DeMason DA (1992) Operationally defined apoplastic and symplastic aluminum fractions in root tips of aluminum intoxicated wheat. Plant Physiol 100:309–318

    Article  PubMed  CAS  Google Scholar 

  • Vargas MC, Encarnacion S, Davalos A, Reyes-Perez A, Mora Y, Garcia-de los Santos A, Brom S, Mora J (2003) Only one catalase KatG, is detectable in Rhizobium etli, and is encoded along with the regulator OxyR on a plasmid replicon. Microbiology 149:1165–1176. doi:10.1099/mic.0.25909-0

    Google Scholar 

  • Vasse J, De Billy F, Camut S, Truchet G (1990) Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules. J Bacteriol 172:4295–4306

    PubMed  CAS  Google Scholar 

  • Verma S, Dubey RS (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164:645–655. doi:10.1016/S0168-9452(03)00022-0

    Article  CAS  Google Scholar 

  • Wayne LG, Diaz GA (1986) A double staining method for differentiating between two classes of mycobacterial catalase in polyacrylamide electrophoresis gels. Anal Biochem 157:89–92

    Article  PubMed  CAS  Google Scholar 

  • Wisniewski JP, Rathbun EA, Knox JP, Brewin NJ (2000) Involvement of diamine oxidase and peroxidase in insolubilization of the extracellular matrix: implications for pea nodule initiation by Rhizobium leguminosarum. Mol Plant-Microbe Interact 13:413–420

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto Y, Kobayashi Y, Rama Devi S, Rikiishi S, Matsumoto H (2003) Oxidative stress triggered by aluminum in plant roots. Plant Soil 255:239–243. doi:10.1023/A:1026127803156

    Article  CAS  Google Scholar 

  • Yamasaki H, Sakihama Y, Ikehara N (1997) Flavonoid-peroxidase reaction as a detoxification mechanism of plant cells against H2O2. Plant Physiol 115:1405–1412

    PubMed  CAS  Google Scholar 

  • Zheng SJ, Yang JL (2005) Target sites of aluminum phytotoxicity. Biol Plant 49:321–331

    Article  CAS  Google Scholar 

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The author thanks Dr. Adam Drzymała for expert technical assistance.

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Correspondence to Marzena Sujkowska-Rybkowska.

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Sujkowska-Rybkowska, M. Reactive oxygen species production and antioxidative defense in pea (Pisum sativum L.) root nodules after short-term aluminum treatment. Acta Physiol Plant 34, 1387–1400 (2012). https://doi.org/10.1007/s11738-012-0935-9

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