biologia plantarum

International journal on Plant Life established by Bohumil Nìmec in 1959

Biologia plantarum 56:537-544, 2012 | DOI: 10.1007/s10535-012-0107-1

Oligogalacturonides stimulate antioxidant system in alfalfa roots

D. Camejo1, M. C. Martí1, E. Olmos1, W. Torres2, F. Sevilla1, A. Jiménez1,*
1 Department of Stress Biology and Plant Pathology, CEBAS-CSIC, Murcia, Spain
2 Department of Plant Physiology and Biochemistry, INCA, S. José de las Lajas, La Habana, Cuba

Alfalfa (Medicago sativa L.) roots were treated with 50 and 100 μg cm-3 of oligogalacturonide (OGA) solutions with a degree of polymerization between 7 and 15. Changes in the activities of superoxide dismutase (SOD), catalase (CAT), peroxidase (POX), ascorbate peroxidase (APX), monodehydroascorbate reductase (MDHAR) and dehydroascorbate reductase (DHAR) as well as ascorbate (ASC) content were determined in crude extract of alfalfa roots after 30, 60 and 120 min of treatment. An increase in the SOD activity was observed in roots treated with 50 and 100 μg cm-3 OGA, which could be related to its O2 .- scavenging function. As concern H2O2 scavenging, CAT activity was increased in the first 30 min by both OGA concentrations, while POX was a key enzyme at higher OGA concentration and treatment duration. ASC content firstly increased upon exposure to high OGA concentration, and then decreased after longer treatment while low OGA concentration had no effect on ASC content.

Keywords: ascorbate; ascorbate peroxidase; catalase; dehydroascorbate reductase; monodehydroascorbate reductase; reactive oxygen species; peroxidase; superoxide dismutase
Subjects: ascorbate; ascorbate peroxidase; catalase; dehydroascorbate reductase; monodehydroascorbate reductase; reactive oxygen species; peroxidase; superoxide dismutase; oligogalacturonide

Received: October 25, 2010; Accepted: March 16, 2011; Published: September 1, 2012  Show citation

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Camejo, D., Martí, M.C., Olmos, E., Torres, W., Sevilla, F., & Jiménez, A. (2012). Oligogalacturonides stimulate antioxidant system in alfalfa roots. Biologia plantarum56(3), 537-544. doi: 10.1007/s10535-012-0107-1
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References

  1. Aebi H.: Catalase in vitro. - Methods in Enzymol. 105: 121-126, 1984. Go to original source...
  2. Allan, A.C., Fluhr, R.: Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells. - Plant Cell 9: 1559-1572, 1997. Go to original source...
  3. Badawi, G.H., Kawano, N., Yamauchi, Y., Shimada, E., Sasaki, R., Kubo, A., Tanaka, K.: Over-expression of ascorbate peroxidase in tobacco chloroplasts enhances the tolerance to salt stress and water deficit. - Physiol. Plant. 121: 231-238, 2004. Go to original source...
  4. Bellincampi, D., Salvi, G., De Lorenzo, G., Cervone, F., Marfà, V., Eberhard, S., Darvill, A., Albersheim, P.: Oligogalacturonides inhibit the formation of roots on tobacco explants. - Plant J. 4: 207-213, 1993. Go to original source...
  5. Binet, M.N., Bourque, S., Lebrun-Garcia, A., Chiltz, A., Pugin, A.: Comparison of the effects of cryptogein and oligogalacturonides on tobacco cells and evidence of different forms of desensitization induced by these elicitors. - Plant Sci. 137: 33-41, 1998. Go to original source...
  6. Bishop, P.D., Pearce, G., Bryant, J.E., Ryan, C.A.: Isolation and characterization of the proteinase inhibitor-inducing factor from tomato leaves: identity and activity of poly-and oligogalacturonide fragments. - J. biol. Chem. 259: 13172-13177, 1984. Go to original source...
  7. Bolwell, G.P., Buti, V.S., Davies, D.R., Zimmerlin, A.: The origin of the oxidative burst in plants. - Free Rad. Res. 23: 517-532, 1995. Go to original source...
  8. Bradford, M.M.: Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. - Anal. Biochem. 72: 248-254, 1976. Go to original source...
  9. Branca, C., De Lorenzo, G., Cervone, F.: Competitive inhibition of the auxin-induced elongation by α-D-oligogalacturonides in pea stem segments. - Physiol. Plant. 72: 499-504, 1988. Go to original source...
  10. Bruce, R.J., West, C.A.: Elicitation of lignin biosynthesis and isoperoxidase activity by pectic fragments in suspension-cultures of castor bean. - Plant Physiol. 91: 889-897, 1989. Go to original source...
  11. Camejo, D., Martí, M.C., Jiménez, A., Cabrera, J.C., Olmos, E., Sevilla, F.: Effect of oligogalacturonides on root length, extracellular alkalinization and O2.-.-accumulation in alfalfa. - J. Plant Physiol. 168: 566-575, 2011. Go to original source...
  12. Camejo, D., Martí, M.C., Nicolás, E., Alarcón, J.J., Jiménez, A., Sevilla, F.: Response of superoxide dismutase isoenzymes in tomato plants (Lycopersicon esculentum) during thermoacclimation of the photosynthetic apparatus. - Physiol. Plant. 131: 367-377, 2007. Go to original source...
  13. Cheeseman J.M.: Hydrogen peroxide concentrations in leaves under natural conditions. - J. exp. Bot.. 57: 2435-2444, 2006. Go to original source...
  14. Chen, Z., Gallie, D.R.: Increasing tolerance to ozone by elevating foliar ascorbic acid confers greater protection against ozone than increasing avoidance. - Plant Physiol. 138: 1673-1689, 2005. Go to original source...
  15. Córdoba, F., González-Reyes, J.A.: Ascorbate and plant cell growth. - J. Bioenerg. Biomemb. 26: 399-405, 1994. Go to original source...
  16. Córdoba-Pedregosa, M.C., Villalba, J.M., Córdoba, F., González-Reyes, J.A.: Changes in intracellular and apoplastic peroxidase activity, ascorbate redox status, and root elongation induced by enhanced ascorbate content in Allium cepa L. - J. exp. Bot. 56: 685-694, 2003. Go to original source...
  17. Côté, F., Hahn, M.G.: Oligosaccharins: structures and signal transduction. - Plant mol. Biol. 26: 1379-1411, 1994. Go to original source...
  18. Dalton, D.A., Langeberg, L., Treneman, N.: Correlations between the ascorbate-glutathione pathway and effectiveness in legume root nodules. - Physiol. Plant. 87: 365-370, 1993. Go to original source...
  19. Díaz-Vivancos, P., Barba-Espín, G., Clemente-Moreno, M.J., Hernández, J.A.: Characterization of the antioxidant system during the vegetative development of pea plants. - Biol. Plant. 54: 76-82, 2010 Go to original source...
  20. Dumas, B., Cheviet, J.P., Sailland, A., Freyssinet, G.: Characterization of oxalate oxidase - a plant enzyme capable of degrading the major phytotoxin produced by Sclerotinia sclerotiorum. - In: Fritig, B., Legrand, M. (ed.): Mechanisms of Plant Defense Responses. Pp. 451-451, Kluver Academic Publishers, Dordrecht 1993. Go to original source...
  21. Dunand, C., Crèvecoeur, M., Penel, C.: Distribution of superoxide and hydrogen peroxide in Arabidopsis root and their influence on root development: possible interaction with peroxidases. - New Phytol. 174: 332-341, 2007. Go to original source...
  22. Eltayeb, A.E., Kawano, N., Badawi, G.H., Kaminaka, H., Sanekata, T., Shibahara, T., Inanaga, S., Tanaka, K.: Overexpression of monodehydroascorbate reductase in transgenic tobacco confers enhanced tolerance to ozone, salt and polyethylene glycol stresses. - Planta 225: 1255-1264, 2007. Go to original source...
  23. Farmer, E.E., Moloshok, T.D., Saxton, M.J., Ryan, C.A.: Oligosaccharide signaling in plants: specificity of oligouronide-enhanced plasma membrane protein phosphorylation. - J. biol. Chem. 266: 3140-3145, 1991. Go to original source...
  24. Ferrer, M.A., Barceló, A.R.: Differential effects of nitric oxide on peroxidase and H2O2 production by the xylem of Zinnia elegans. - Plant Cell Environ. 22: 891-897, 1999. Go to original source...
  25. Gómez, J.M., Jiménez, A., Olmos, E., Sevilla, F.: Location and effects of long-term NaCl stress on superoxide dismutase and ascorbate peroxidase isoenzymes of pea (Pisum sativum cv. Puget) chloroplasts. - J. exp. Bot. 55: 119-130, 2004. Go to original source...
  26. Hassan, H.M., Fridovich, I.: Regulation of synthesis of superoxide-dismutase in Escherichia-coli - induction by methyl viologen. - J. biol. Chem. 252: 7667-7672, 1977. Go to original source...
  27. Hernández, J.A., Ferrer, M.A., Jiménez, A., Ros Barceló, A., Sevilla, F.: Antioxidant system and O2.- /H2O2 production in the apoplast of pea leaves. Its relation with salt-induced necrotic lesions in minor veins. - Plant Physiol. 127: 817-831, 2001. Go to original source...
  28. Horemans, N., Foyer, C.H., Asard, H.: Transport and action of ascorbate at the plant plasma membrane. - Trends Plant Sci. 5: 263-267, 2000. Go to original source...
  29. Jiménez, A., Hernández, J.A., Del Río, L.A., Sevilla, F.: Evidence for presence of the ascorbate-glutation cycle in mitochondria, chloroplast and peroxisomes of pea (Pisum sativum L.) leaves. - Plant Physiol. 114: 275-284, 1997. Go to original source...
  30. Kato, N., Esaka, M.: Changes in ascorbate oxidase gene expression and ascorbate levels in cell division and cell elongation in tobacco cells. - Physiol. Plant. 105: 321-329, 1999. Go to original source...
  31. Klessig, D.F., Durner, J., Noad, R., Navarre, D.A., Wendehenne, D., Kumar, D., Zhou, J.M., Shah, J., Zhang, S.Q., Kachroo, P., Trifa, Y., Pontier, D., Lam, E., Silva, H.: Nitric oxide and salicylic acid signaling in plant defense. - PNAS 97: 8849-8855, 2000. Go to original source...
  32. Kwon, S.Y., Choi, S.M., Ahn, Y.O., Lee, H.S., Lee H.B., Park Y.M., Kwak, S.S.: Enhanced stress-tolerance of transgenic tobacco plants expressing a human dehydroascorbate reductase gene. - J. Plant Physiol. 160: 347-353, 2003. Go to original source...
  33. Lamb, C., Dixon, R.A.: The oxidative burst in plant disease resistance. - Annu. Rev. Plant Physiol. Plant mol. Biol. 48: 251-275, 1997. Go to original source...
  34. Legendre, L., Rueter, S., Heinstein, P.F., Low, P.S.: Characterization of the oligogalacturonide-induced oxidative burst in cultured soybean (Glycine-max) cells. - Plant Physiol. 102: 233-240, 1993. Go to original source...
  35. Locato, V., Balestrazzi, A., De Gara, L., Carbonera, D.: Reduced expression of top1beta gene induces programmed cell death and alters ascorbate metabolism in Daucus carota cultured cells. - J. exp. Bot. 57: 1667-1676, 2006. Go to original source...
  36. Low, P.S., Merida, J.R.: The oxidative burst in plant defense: function and signal transduction. - Physiol. Plant. 96: 533-542, 1996. Go to original source...
  37. Maia, J.M., Costa de Macedo, C.E., Voigt, E.L., Freitas, J.B.S., Silveira, J.A.G.: Antioxidative enzymatic protection in leaves of two contrasting cowpea cultivars under salinity. - Biol. Plant. 54: 159-163, 2010. Go to original source...
  38. Marfà, V., Gollin, D.J., Eberhard, S., Mohnen, D., Darvill, A.G., Albersheim, P.: Oligosaccharides are able to induce flowers to form on tobacco explants. - Plant J. 1: 217-225, 1991. Go to original source...
  39. Mathieu, Y., Kurkjian, A., Xia, H., Guern, J., Koller, A., Spiro, M.D., O'Neill, M., Albersheim, P., Darvill, A.: Membrane responses induced by oligogalacturonides in suspension-cultured tobacco cells. - Plant J. 1: 333-343, 1991.
  40. McCord, J.M., Fridovich, I.: Superoxide dismutase: an enzymic function for erythrocuprein. - J. Biol. Biochem. 244: 6049-6055, 1969. Go to original source...
  41. Messiaen, J., Van Custsen, P.: Defense gene transcription in carrot cells treated with oligogalacturonides. - Plant Cell Physiol. 34: 1117-23, 1993.
  42. Messiaen, J., Vancutsem, P.: Membrane, cytosolic, and nuclear responses induced by oligogalacturonides in suspension-cultured carrot cells. - J. Trace Microprop. Tech. 12: 231-238, 1994.
  43. Mittler, R., Herr, E.H., Orvar, B.L., Van Camp, W., Willekens, H., Inze, D., Ellis, B.E.: Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyperresponsive to pathogen infection. - PNAS 96: 14165-14170, 1999. Go to original source...
  44. Mittler, R., Vanderauwera, S., Gollery, M., Van Breugesem, F.: Reactive oxygen gene network of plant. - Trends Plant Sci. 9: 490-498, 2004. Go to original source...
  45. Mittova, V., Tal, M., Volokita, M., Guy, M. Up-regulation of the leaf mitochondrial and peroxisomal antioxidative systems in response to salt-induced oxidative stress in the wild salt-tolerant tomato species Lycopersicon pennellii. - Plant Cell Environ. 26: 845-856, 2003. Go to original source...
  46. Ogawa, K., Kanematsu, S., Asada, K.: Intra- and extra-cellular localization of "cytosolic" CuZn-superoxide dismutase in spinach leaf and hypocotyl. - Plant Cell Physiol. 37: 790-799, 1996. Go to original source...
  47. Pastori, G.M., Del Río, L.A.: An activated-oxygen-mediated role for peroxisomes in the mechanism of senescence of Pisum sativum L. leaves. - Planta 193: 385-391, 1994. Go to original source...
  48. Pastori, G.M., Kiddle, G., Antoniw, J., Bernard, S., Veljovic-Jovanovic, S., Verrier, P. J., Noctor, G., Foyer, C.H.: Leaf vitamin C contents modulate plant defense transcripts and regulate genes that control development through hormone signaling. - Plant Cell 15: 939-951, 2003. Go to original source...
  49. Pavet, V., Olmos, E., Kiddle, G., Mowla, S., Kumar, S., Antoniw, J., Alvarez, M.O., Foyer, C.H.: Ascorbic acid deficiency activates cell death and disease resistance responses in Arabidopsis. - Plant Physiol. 139: 1291-1303, 2005. Go to original source...
  50. Pellinen, R.I., Korhonen, M.S., Tauriainen, A.A., Palva, E.T., Kangasjarvi, J.: Hydrogen peroxide activates cell death and defense gene expression in birch. - Plant Physiol. 130: 549-560, 2002. Go to original source...
  51. Penel, C., Greppin, H.: Binding of plant isoperoxidases to pectin in the presence of calcium. - FEBS Letters. 343: 51-55, 1994. Go to original source...
  52. Penel, C., Van Cutsem, P., Greppin, H.: Interactions of a plant peroxidase with oligogalacturonides in the presence of calcium ions. - Phytochemistry 51: 193-198, 1999. Go to original source...
  53. Pignocchi, C., Foyer, C.H.: Apoplastic ascorbate metabolism and its role in the regulation of cell signalling. - Current Opin. Plant Biol. 6: 379-389, 2003. Go to original source...
  54. Puppo, A., Groten, K., Bastian, F., Carzaniga, R., Soussi, M., Lucas, M.M., de Felipe, M.R., Harrison, J., Vanacker, H., Foyer, C.H.: Legume nodule senescence: roles for redox and hormone signalling in the orchestration of the natural aging process. - New Phytol. 165: 683-701, 2005. Go to original source...
  55. Ros Barceló, A.: Lignification in plant cell walls. - Int. Rev. Cytol. Survey Cell Biol. 176: 87-132, 1997. Go to original source...
  56. Ros Barceló, A.: Peroxidase and H2O2 production by plant cells: truths and clues. - Curr. Topics Phytochem. 3: 197-202, 2000.
  57. Rose, J.K.C., O'Neill, M.A., Albersheim, P., Darvell, A.: The primary cell wall of higher plants. - In: Ernst, W., Hart, E.W. (ed.): Oligosaccharides in Chemistry and Biology. Pp. 783-803, Wiley, London 1999. Go to original source...
  58. Smirnoff, N.: Ascorbic acid: metabolism and functions of a multi-facetted molecule. - Curr. Opin. Plant Biol. 3: 229-235, 2000. Go to original source...
  59. Spiro, M.D., Bowers, J.F., Cosgrove, D.J.: A comparison of oligogalacturonide-and auxin-induced extracellular alkalinization and growth responses in roots of intact cucumber seedlings. - Plant Physiol. 130: 895-903, 2002. Go to original source...
  60. Spiro, M.D., Kates, K.A., Koller, A.L., O'Neill, M.A., Albersheim, P., Darvill, A.G.: Purification and characterization of biologically active (1→4)-linked α-D-oligogalacturonides after partial digestion of polygalacturonic acid with endopolygalacturonase. - Carbohydrate Res. 247: 9-20, 1993. Go to original source...
  61. Stennis, M.J., Chandra, S., Ryan, C.A., Low, P.S.: Systemin potentiates the oxidative burst in cultured tomato cells. - Plant Physiol. 117: 1031-1036, 1998. Go to original source...
  62. Stevens, R., Page, D., Gouble, B., Garchery, C., Zamir, D., Causse, M.: Tomato fruit ascorbic acid content is linked with monodehydroascorbate reductase activity and tolerance to chilling stress. - Plant Cell Environ. 31: 1086-1096, 2008. Go to original source...
  63. Torres, M.A., Dangl, J.L.: Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. - Curr. Opin. Plant Biol. 8: 397-403, 2005. Go to original source...
  64. Torres, M.A., Jones, J.D.G., Dangl, J.L.: Reactive oxygen species signaling in response to phatogens. - Plant Physiol. 141: 373-378, 2006. Go to original source...
  65. Ushimaru, T., Nakagawa, T., Fujioka, Y., Daicho, K., Naito, M., Yamauchi, Y., Nonaka, H., Amako, K., Yamawaki, K., Murata, N.: Transgenic Arabidopsis plants expressing the rice dehydroascorbate reductase gene are resistant to salt stress. - J. Plant Physiol. 163: 1179-1184, 2006. Go to original source...
  66. Vanacker, H., Sandalio, L.M., Jiménez, A., Palma, J.M., Corpas, F.J., Meseguer, V., Gómez, M., Sevilla, F., Leterrier, M., Foyer, C.H., Del Río, L.A.: Roles for redox regulation in leaf senescence of pea plants grown on different sources of nitrogen nutrition. - J. exp. Bot. 57: 1735-1745, 2006. Go to original source...
  67. Vandenabeele, S., Van der Kelen, V., Dat, J., Gadjev, I., Boonefaes, T., Morsa, S., Rottiers, P., Slooten, L., Van Montagu, M., Zabeau, M., Inze, D., Van Breusegem, F.: A comprehensive analysis of hydrogen peroxide-induced gene expression in tobacco. - PNAS 100: 16113-16118, 2003. Go to original source...
  68. Vuletiæ, M., Had¾i-Ta¹koviæ ©ukaloviæ, V., Vuèiniæ, ®.: Superoxide synthase and dismutase activity of membranes from maize roots. - Protoplasma. 221: 73-77, 2003. Go to original source...
  69. Walker-Simmons, M., Jin, D., West, C.A., Hakwiger, L., Ryan, C.A.: Comparison of proteinase inhibitor-inducing activities and phytoalexin elicitor activities of a pure fungal endopolygalacturonase, pectic fragments, and chitosan. - Plant Physiol. 76: 833-836, 1984. Go to original source...
  70. Yin, L., Wang, S., Eltayeb, A.E., Uddin, Md.I., Yamamoto, Y., Tsuji, W., Takeuchi, Y., Tanaka, K.: Overexpression of dehydroascorbate reductase, but not monodehydroascorbate reductase, confers tolerance to aluminium stress in transgenic tobacco. - Planta. 231: 609-621, 2010. Go to original source...