Plant and Soil

, Volume 363, Issue 1–2, pp 399–410 | Cite as

Oxidative stress is associated with aluminum toxicity recovery in apex of pea root

  • Hideaki Matsumoto
  • Hirotoshi Motoda
Regular Article



Although many studies on the mechanism of Al toxicity and tolerance have been conducted independently, events occurring during the recovery process from Al injury is limited. This study was to investigate Al toxicity recovery mechanism focusing in morphological and physiological aspect.


We investigated the mechanisms underlying Al toxicity recovery in terms of oxidative stress using the pea root apex as a model system.


The accumulation of reactive oxygen species was remarkably high in the root under continued Al treatment but decreased in the recovering root. The superoxide anion exuded in the presence of nicotinamide adenine dinucleotide phosphate (NADPH) showed a similar tendency with respect to the accumulation of reactive oxygen species. A similar pattern of lignin content and superoxide dismutase activity was observed among the treatments, while the increased peroxidation in the root under continued Al treatment did not decline with recovery treatment. A longitudinal section of the root under continued Al treatment showed the accumulation of superoxide anion, lignin and peroxide (H2O2) at the epidermal and outer cortex region where the Al induced injuries, including ruptures, are detected.


Oxidative stress is associated with the mechanism of Al toxicity recovery. The recovery process might include the elongation of the central cylinder as a consequence of the oxidative stress-induced formation of the zonal region (ZR). The results further suggest a plausible role for the ZR in the programmed cell death-like function involved in Al toxicity recovery.


Aluminum Oxidative stress Pea root Programmed cell death Recovery Toxicity 



This research was financially supported through a grant from the Japanese Ministry of Education, Sports, Science and Technology to H.M [Grand-in-Aid for Scientific Research C (2258007)].


  1. Achary VMM, Jena S, Panda KK, Panda BB (2008) Aluminium induced oxidative stress and DNA damage in root cells of Allium cepa L. Ecotoxicol Environ Saf 70:300–310PubMedCrossRefGoogle Scholar
  2. Amenós M, Corrale I, Poschnerieder C, Illés P, Baluška F, Barceló J (2009) Different effects of aluminum on the actin cytoskeleton and brefeldin A-sensitive vesicle recycling in root apex cells of two maize varities differeing in root elongation rate and aluminum tolerance. Plant Cell Physiol 50:528–540PubMedCrossRefGoogle Scholar
  3. Babourina O, Levent O, Cakmak I, Rengel Z (2006) Reactive oxygen species production in wheat roots is not linked with changes in H+ fluxes during acidic and aluminum stresses. Plant Sig Behav 1:70–75CrossRefGoogle Scholar
  4. Barcelö AR (1998) Hydrogen peroxide production is a general property of the lignifying xylem from vascular plants. Ann Bot 82:97–103CrossRefGoogle Scholar
  5. Basu U, Good A, Taylor GJ (2001) Transgenic Brassica napus plants overexpressing aluminium-induced mitochondrial manganese superoxide dismutase cDNA are resistant to aluminium. Plant Cell Envir 24:1269–1278Google Scholar
  6. Boscolo PRS, Menossi M, Jorge R (2003) Aluminum induced oxidative stress in maize. Phytochem 62:181–189CrossRefGoogle Scholar
  7. Buchanan BB, Gruissem W, Jones RL (2000) Biochemistry and molecular biology of plants. American Society of Plant Physiologist, RockvilleGoogle Scholar
  8. Budíkóvá S, Čiamporová M (1998) Growth and structural responses of maize roots to aluminium stress. In: Tsekos I, Moustakao M (eds) Progress in Botanical Research. Kluwer Academic Publishers, Dordrecht, pp 419–422CrossRefGoogle Scholar
  9. Cakmak I, Horst WJ (1991) Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468CrossRefGoogle Scholar
  10. Cakmak I, Marschner H (1988) Enhanced superoxide radical production in roots of zinc-deficient plants. J Exp Bot 39:1449–1460CrossRefGoogle Scholar
  11. Chaffai R, Tekitek A, Ferjani E (2005) Aluminum toxicity in maize seedlings (Zea mays L.): effect on growth and lipid content. J Agron 4:67–74CrossRefGoogle Scholar
  12. Čiamporová M (2000) Diverse responses of root cell structure to aluminum stress. Plant Soil 226:113–116CrossRefGoogle Scholar
  13. Čiamporová M (2002) Morphological and structural response of plant roots to aluminum at organ, tissue and cellular levels. Biologia Plantarum 45:161–171CrossRefGoogle Scholar
  14. Delhaize E, Ryan PR (1995) Aluminum toxicity and tolerance in plants. Plant Physiol 107:315–321PubMedGoogle Scholar
  15. Delisle G, Champoux M, Houde M (2001) Characterization of oxalate oxidase and cell death in Al-sensitive and tolerant wheat roots. Plant Cell Physiol 42:324–333PubMedCrossRefGoogle Scholar
  16. Devi SR, Yamamoto Y, Matsumoto H (2003) An intracellular mechanism of aluminum tolerance associated with high antioxidant status in cultured tobacco cells. J Inorg Biochem 97:59–68PubMedCrossRefGoogle Scholar
  17. Ezaki B, Kiyohara H, Matsumoto H, Nakashima S (2007) Overexpression of an auxilin-like gene (F9E10.5) can suppress Al uptake in roots of Arabidopsis. J Exp Bot 58:442–446Google Scholar
  18. Foreman J, Demidchlk V, Boyhwell JHF, Mylona P, Mledeman H, Torres MA, Linsteas P, Costa S, Brownlee C, Jones JDG, Davles JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446PubMedCrossRefGoogle Scholar
  19. Frahry G, Scopfer P (2001) NADH-stimulated cyanide-resistant superoxide production in maize coleoptiles analyzed with a tetrazolium-based assay. Planta 212:175–183PubMedCrossRefGoogle Scholar
  20. Giannopolitis CN, Ries SK (1977) Superoxide dismutases 1. Occurrence in higher plants. Plant Physiol 59:309–314PubMedCrossRefGoogle Scholar
  21. Huang JW, Pellet DW, Papernick LA, Kochian LV (1996) Aluminum interactions with voltage-dependent calcium transport in plasma membrane vesicles isolated from roots of aluminum-sensitive and tolerant wheat cultivars. Plant Physiol 110:561–569PubMedCrossRefGoogle Scholar
  22. Jones DL, Blancaflor EB, Kochian LV, Gilroy S (2006) Spatial coordination of aluminium uptake, production of reactive oxygen species, callose production and wall rigidification in maize roots. Plant Cell Environ 29:309–1318CrossRefGoogle Scholar
  23. Kawano T, Kadono T, Furuichi T, Muto S, Lapeyrie F (2003) Aluminum-induced distortion in calcium signaling involving oxidative burst and channel regulation in tobacco BT-2 cells. Biochem Biophys Res Commun 308:35–42PubMedCrossRefGoogle Scholar
  24. Kikui S, Sasaki T, Osawa H, Matsumoto H, Yamamot Y (2007) Malate enhances recovery from aluminum-caused inhibition of root elongation in wheat. Plant Soil 290:1–15CrossRefGoogle Scholar
  25. Kochian LV, Pineros MA, Hoekenga OA (2005) The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274:175–195CrossRefGoogle Scholar
  26. Kopittke PM, Blamey FPC, Menzies NW (2008) Toxicities of soluble Al, Cu. and La include rupture on rhizodermal and root critical cells of cowpea. Plant Soil 303:217–227CrossRefGoogle Scholar
  27. Li-Juan Q, Bo Z, Shi W-W, Li H-Y (2008) Hydrogen peroxide in planst: a versatile molecule of the reactive oxygen species nrtwork. J Integr Plant Biol 50:2–18CrossRefGoogle Scholar
  28. Liszkay A, Kenk B, Schopfer P (2003) Evidence for the involvement of cell wall peroxidase in the generation of hydroxyl radicals mediating extention growth. Planta 217:658–667Google Scholar
  29. Ma B, Wan J, Shen Z (2007) H2O2 production and antioxidant responses in seeds and early seedlings of two different rice varieties exposed to aluminum. Plant Growth Regul 52:91–100CrossRefGoogle Scholar
  30. Matsumoto H (2000) Cell biology of aluminum toxicity and tolerance in higher plant. Int Rev Cytol 200:1–46PubMedCrossRefGoogle Scholar
  31. Matsumoto H, Motoda H (2012) Review Aluminum toxicity recovery processes in root apexes. Possible association with oxidative stress. Plant Sci 185-186:1–8. doi: 10.1016/j.plantsci.2011.07.019 PubMedCrossRefGoogle Scholar
  32. Matsumoto H, Yamamoto Y (in press) Plant roots under aluminum stress: Toxicity and tolerance. In Plant Roots: The Hidden Half 4th Edition, Amran E and Beeckman T (ed) Taylor and Francis Books, ISBN: 978-1-4398-4648-3Google Scholar
  33. Mäder M, Amberg-Fisher V (1982) Role of peroxidase in lignifications of tobacco cells 1. Oxidation of nicotinamide adenine dinucleotide and formation of hydrogen peroxide by cell wall peroxidases. Plant Physiol 70:1128–1131PubMedCrossRefGoogle Scholar
  34. Motoda H, Kano Y, Hiragami F, Kawamura K, Matsumoto H (2010) Morphological changes in the apex of pea roots during and after recovery from aluminum treatment. Plant Soil 33:49–58CrossRefGoogle Scholar
  35. Motoda H, Kano Y, Hiragami F, Kawamura K, Matsumoto H (2011) Changes in rupture formation and zonary region stained with Evans blue during the recovery process from aluminum toxicity in the pea root apex. Plant Sig Behav 6:98–100CrossRefGoogle Scholar
  36. Navascuis J, P-Rontomé C, Sánchez DH, Staudinger C, Wiankoop S, R-Áivarez R, Becana M (2011) Oxidative stress is a consequence, not a cause, of aluminum toxicity in the forage legume Lotus comiculatus. New Phytol. doi: 10.1111/j.1469-8137.2011.03978.X
  37. Ogawa K, Kanematsu S, Asada K (1997) Generation of superoxide anion and localization of Cu Zn-superoxide dismutase in the vascular tissue of spinach hypocotyls: their association with lignifications. Plant Cell Physiol 38:1118–1126PubMedCrossRefGoogle Scholar
  38. Pan JW, Zhu MY, Chen H (2001) Aluminum-induced cell death in root-tip cells of barley. Envir Exp Bot 46:71–79CrossRefGoogle Scholar
  39. Panda SK, Matsumoto H (2010) Changes in antioxidant gene expression and induction of oxidative stress in pea (Pisum sativum L.) under Al stress. Biometals 23:753–762PubMedCrossRefGoogle Scholar
  40. Rincón-Zachary M, Teacter ND, Sparks JA, Valster AH, Motes CM, Blancaflor B (2010) Fluorescence reasonance energy transfer-sensitized emission of yellow camereon 3.60 reveals root zone-specific calcium signatures in Arabidopsis in response to aluminum and other trivalent cations. Plant Physiol 152:1442–1458PubMedCrossRefGoogle Scholar
  41. Rodríguez AA, Lascano HR, Bustos D, Taleisnik E (2007) Salinity-induced decrease in NADPH oxidase activity in the maize leaf blade elongation zone. J Plant Physiol 164:223–230PubMedCrossRefGoogle Scholar
  42. Sagi M, Fluh R (2001) Superoxide production by plant homologues of the gp91phox NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol 126:1281–1290PubMedCrossRefGoogle Scholar
  43. Sakihama Y, Yamasaki H (2002) Lipid peroxidation induced by phenolics in conjunction with aluminum ions. Biologia Plantarum 45:249–254CrossRefGoogle Scholar
  44. Sasaki M, Yamamoto Y, Matsumoto H (1996) Lignin deposition induced by aluminum in wheat (Triticum aestivum) roots. Physiol Plant 96:193–198CrossRefGoogle Scholar
  45. Schofield RMS, Pallon J, Fiskesjö G, Karlsson G, Malmqvist KG (1998) Aluminum and calcium distribution patterns in aluminum-intoxicated roots of Allium cepa do not support the calcium-displacement hypothesis and indicate signal-mediater inhibition of root growth. Planta 205:175–180CrossRefGoogle Scholar
  46. Tabuchi A, Matsumoto H (2001) Changes in cell-wall properties of wheat (Triticum aesivum) roots during aluminum-induced growth inhibition. Physiol Plant 112:353–358PubMedCrossRefGoogle Scholar
  47. Tabuchi A, Kikui S, Matsumoto H (2004) Differential effects of aluminum on osmotic potential and sugar accumulation in the root of Al-resistant and Al-sensitive wheat. Physiol Plant 12:106–112CrossRefGoogle Scholar
  48. Tahara K, Yamanoshita T, Norisada M, Hasegawa I, Kashima H, Sasaki S, Kojima K (2008) Aluminum distribution and reactive oxygen species accumulation in root tips of two Melaleuca trees differing in aluminum resistance. Plant Soil 307:167–178CrossRefGoogle Scholar
  49. Tamas L, Simonovicova M, Huttova J, Mistrik I (2003) Aluminium stimulated hydrogen peroxide production of germinating barley seeds. Envir Exp Bot 51:281–288CrossRefGoogle Scholar
  50. Tamas L, Huttova J, Mistrik I (2004) Inhibition of Al-induced root elongation and enhancement of Al-induced peroxidase in Al-sensitive and Al-resistant barley cultivars are positively correlated. Plant Soil 250:193–200CrossRefGoogle Scholar
  51. Yamamoto Y, Hachiya O, Matsumoto H (1997) Oxidative damage to membrane by a combination of aluminum and iron in suspension-cultured tobacco cells. Plant Cell Physiol 38:1333–1339CrossRefGoogle Scholar
  52. Yamamoto Y, Kobayashi Y, Matsumoto H (2001) Lipid peroxidation is an early symptom triggered by aluminum, but not the primary cause of elongation inhibition in pea roots. Plant Physiol 125:199–208PubMedCrossRefGoogle Scholar
  53. Yamamoto Y, Kobayashi Y, Devi SR, Rikiishi S, Matsumoto H (2002) Aluminum toxicity and its production of reactive oxygen species in plant cells. Plant Physiol 128:63–72PubMedCrossRefGoogle Scholar
  54. Yang S (2006) Possible involvement of NADPH oxidase in lanthanide cation-induced superoxide anion generation in BY-2 cells suspension culture. J Rare Earths 24:243–247CrossRefGoogle Scholar
  55. Yin L, Mano J, Wang S, Tsuji W, Tanaka K (2010a) The involvement of lipid peroxide-derived aldehydes in aluminum toxicity of tobacco roots. Plant Physiol 152:1406–1417PubMedCrossRefGoogle Scholar
  56. Yin L, Wang SS, Eltayeb AE, Uddin MI, Yamamoto Y, Tsuji W, Takeuchi Y, Tanaka K (2010b) Overexpression of dehydroascorbate reductase, but not monodehydroascorbate reductase, confers tolerance to aluminum stress in transgenic tobacco. Planta 231:609–621PubMedCrossRefGoogle Scholar
  57. Zhang W-H, Rengel Z (1999) Aluminium induces an increase in cytoplasmic calcium in intact wheat root apical cells. Aust J Plant Physiol 26:401–409CrossRefGoogle Scholar
  58. Zhang B, Wang X, Li X, Ni Y, Li H (2009) Aluminum uptake and disease resistance in Nicotiana rustica leaves. Ecotoxicol Environ Saf 73:655–663CrossRefGoogle Scholar
  59. Zheng SJ, Yang J (2005) Target sites of aluminum phytotoxicity. Biologia Plantarum 49:321–331CrossRefGoogle Scholar
  60. Zheng K, Pan JW, Ye L, Fu Y, Peng HZ, Kang B, Pan JH, Sha HH, Wang WZ, Zhu MY (2006) Prograrmmed cell death-involved aluminum toxicity in yeast alleviated by antibiotic members with decreased calcium signals. Plant Physiol 143:1–12CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Research Institute of Health and WelfareKIBI International UniversityTakahashi-cityJapan

Personalised recommendations