Abstract
Mechanisms underlying differential tolerance to Manganese (Mn) toxicity in perennial ryegrass (Lolium perenne L.) cultivars are poorly understood. We evaluated activity of antioxidative enzymes and root exudation of carboxylates in four ryegrass cultivars subjected to increasing Mn supply under nutrient solution conditions. A growth reduction caused by Mn toxicity was smaller in Jumbo and Kingston than Nui and Aries cultivars. Shoot Mn accumulation varied in the order Nui > Aries > Kingston > Jumbo. Ascorbate peroxidase and guaiacol peroxidase activities increased with Mn excess. Mn-tolerant Jumbo and Kingston had high activity of these enzymes and relatively low lipid peroxidation. Kingston was most tolerant to high tissue Mn concentrations and had the highest superoxide dismutase activity. Increased activity of antioxidative enzymes in Mn-tolerant cultivars could protect their tissues against oxidative stress triggered by Mn excess. Mn toxicity induced root exudation of carboxylates; oxalate and citrate may decrease Mn availability in the rhizosphere, thus enhancing Mn tolerance in ryegrass.
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References
Bansal RL, Nayyar VK, Takkar PN (1991) Field screening of wheat cultivars for manganese efficiency. Field Crops Res 29:107–112 doi:10.1016/0378-4290(92)90081-J
Barceló J, Poschenrieder C (2002) Fast root growth responses, root exudates, and internal detoxification as clues to the mechanisms of aluminium toxicity and resistance: a review. Environ Exp Bot 48:75–92 doi:10.1016/S0098-8472(02)00013-8
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
Carver BF, Ownby JD (1995) Acid soil tolerance in wheat. Adv Agron 54:117–173 doi:10.1016/S0065-2113(08)60899-8
Darkó É, Ambrus H, Stefanovits-Bányai É, Fodor J, Bakos F, Barnabás B (2004) Aluminium 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
Del Río LA, Sandalio LM, Yanez J, Gomez M (1985) Induction of a manganese-containing superoxide dismutase in leaves of Pisum sativum L. by high nutrient levels of zinc and manganese. J Inorg Biochem 24:25–34 doi:10.1016/0162-0134(85)85011-X
Delhaize E, Ryan PR, Randall PJ (1993) Aluminum tolerance in wheat (Triticum aestivum L.). II Aluminum stimulated excretion of malic acid from root apices. Plant Physiol 103:695–702
Delhaize E, Ryan PR (1995) Aluminium toxicity and tolerance in plants. Plant Physiol 107:315–321
Demirevska-Kepova K, Simova-Stoilova L, Stoyanova Z, Hölzer R, Feller U (2004) Biochemical changes in barley plants after excessive supply of copper and manganese. Environ Exp Bot 52:253–266 doi:10.1016/j.envexpbot.2004.02.004
Du Z, Bramlage WJ (1992) Modified thiobarbaturic acid assay for measuring lipid peroxidation in sugar rich plant tissue extracts. J Agric Food Chem 40:1566–1570 doi:10.1021/jf00021a018
Fang Z, Zhang YG, Zhang FS (2000) Mechanisms of difference in Mn efficiency between wheat and oilseed rape. Pedosphere 10:213–220
Foy CD (1984) Physiological effects of hydrogen, aluminum, and manganese toxicity in acid soils, In Soil Acidity and Liming. Agron Monograph 12:57–97
Gallego SM, Benavides MP, Tomaro ML (1996) Effect of heavy metal ion excess on sunflower leaves: evidence for involvement of oxidative stress. Plant Sci 121:151–159 doi:10.1016/S0168-9452(96)04528-1
Giannopolitis CN, Ries SK (1977) Superoxide dismutases-occurrence in higher plants. Plant Physiol 59:309–314
González A, Steffen KL, Lynch JP (1998) Light and excess manganese implications for oxidative stress in common bean. Plant Physiol 118:493–504 doi:10.1104/pp.118.2.493
González A, Lynch JP (1999) Subcellular and tissue Mn concentration in bean leaves under Mn toxicity stress. Aust J Plant Physiol 26:811–822
Halliwell B, Gutteridge JMC (1998) Mechanisms of damage to cellular targets by oxidative stress: lipid peroxidation. In: Barry H, Gutteridge JMC (eds) Free Radicals in Biology and Medicine. Oxford Science Publication, pp. 284–306
Hegedus A, Erdei S, Horvath 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
Hoffland E, Kuyper TW, Wallander H, Plassard C, Gorbushina A (2004) The role of fungi in weathering. Front Ecol Environ 2:258–264
Horst WJ, Fecht M, Neumann A, Wissemeier AH, Maier P (1999) Physiology of manganese toxicity and tolerance in Vigna unguiculata (L.) Walp. J Plant Nutr Soil Sci 162:263–274 doi:10.1002/(SICI)1522-2624(199906)162:3<263::AID-JPLN263>3.0.CO;2-A
Jones DL, Darrah P (1994) Role of root derived organic acids in the mobilization of nutrients from the rhizosphere. Plant Soil 166:247–257 doi:10.1007/BF00008338
Krotz RM, Evangelou BP, Wagner GJ (1989) Relationships between cadmium, zinc, Cd-binding peptide and organic acid in tobacco suspension cells. Plant Physiol 91:780–787
Lidon FC, Teixeira MG (2000) Rice tolerance to excess Mn: implications in the chloroplast lamellae. Plant Physiol Biochem 38:969–978 doi:10.1016/S0981-9428(00)01207-9
Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278 doi:10.1016/S1360-1385(01)01961-6
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 52:91–100 doi:10.1007/s10725-007-9183-1
Memon AR, Yatazawa M (1984) Nature of manganese complexes in manganese accumulator plant—Acanthopanax sciadophylloides. J Plant Nutr 7:961–974 doi:10.1080/01904168409363257
Mittler R (2002) Oxidative stress, antioxidants, and stress tolerance. Trends Plant Sci 7:405–410 doi:10.1016/S1360-1385(02)02312-9
Mora ML, Baeza G, Pizarro C, Demanet R (1999) Effect of calcitic and dolomitic lime on physicochemical properties of a Chilean Andisol. Commun Soil Sci Plant Anal 30:427–439 doi:10.1080/00103629909370214
Mora ML, Cartes P, Demanet R, Cornforth IS (2002) The effects of lime and gypsum on pasture growth and composition on an acid Andisol in Chile. Commun Soil Sci Plant Anal 33:2069–2081 doi:10.1081/CSS-120005749
Mora ML, Alfaro MA, Jarvis SC, Demanet R, Cartes P (2006) Soil aluminum availability in Andisols of Southern Chile and its effect on forage production and animal metabolism. Soil Use Manage 22:95–101 doi:10.1111/j.1475-2743.2006.00011.x
Neumann G, Römheld V (1999) Root excretion of carboxylic acids and protons in phosphorus-deficient plants. Plant Soil 211:121–130 doi:10.1023/A:1004380832118
Ogawa K, Iwabuchi M (2001) A mechanism for promoting the germination of Zinnia elegans seeds by hydrogen peroxide. Plant Cell Physiol 42:286–291 doi:10.1093/pcp/pce032
Panchuk II, Zentgraf U, Volkov RA (2005) Expression of the Apx gene family during senescence of Arabidopsis thaliana. Planta 222:926–932 doi:10.1007/s00425-005-0028-8
Paul A, Hauck M, Fritz E (2003) Effects of manganese on element distribution and structure in thalli of the epiphytic lichens Hypogymnia physodes and Lecanora conizaeoides. Environ Exp Bot 50:113–124 doi:10.1016/S0098-8472(03)00017-0
Pinhero RG, Rao MV, Paliyath G, Murr DP, Fletcher RA (1997) Changes in activities of antioxidant enzymes and their relationship to genetic and paclobutrazol-induced chilling tolerance of maize seedlings. Plant Physiol 114:695–704
Rengel Z (2000) Uptake and transport of manganese in plants. In: Sigel A, Sigel H (eds) Metal Ions in Biological Systems. Marcel Dekker, New York, pp 57–87
Rosas A, Rengel Z, Mora ML (2007) Manganese supply and pH influence growth, carboxylate exudation and peroxidase activity of ryegrass and white clover. J Plant Nutr 30:253–270 doi:10.1080/01904160601118034
Ryan PR, Jones DL, Delhaize E (2001) Function and mechanism of organic acid exudation from plant roots. Annu Rev Plant Physiol Plant Mol Biol 52:527–560 doi:10.1146/annurev.arplant.52.1.527
Sadzawka A, Grez R, Carrasco A, Mora ML (2004) Métodos de análisis de tejidos vegetales. Comisión de Normalización y Acreditación (CNA) de la Sociedad Chilena de la Ciencia del Suelo. 53 p. http://alerce.inia.cl/docs/presentaciones/Doc001ASR.pdf.
Schützendubel A, Polle A (2002) Plant responses to abiotic stresses: Heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365 doi:10.1093/jexbot/53.372.1351
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
Shi QH, Zhu ZJ, He Y, Qian QQ, Yu JQ (2005) Silicon-mediated alleviation of Mn toxicity in Cucumis sativus L. in relation to activities of superoxide dismutase and ascorbate peroxidase. Phytochemistry 66:1551–1559 doi:10.1016/j.phytochem.2005.05.006
Shi QH, Zhu ZJ, Xu M, Qian QQ, Yu JQ (2006) Effects of excess manganese on the antioxidant system in Cucumis sativus L. under two light intensities. Environ Exp Bot 58:197–205 doi:10.1016/j.envexpbot.2005.08.005
Taylor GJ, Foy CD (1985) Mechanisms of aluminum tolerance in Triticum aestivum L. II. Differential pH induced by winter cultivars in nutrients solution. Am J Bot 22:695–701 doi:10.2307/2443681
Vose PB, Randall PJ (1962) Resistance to aluminum and manganese toxicities in plants related to variety and cation exchange capacity. Nature 196:85–86 doi:10.1038/196085a0
Wilson MJ, Jones D (1984) The occurrence and significance of manganese oxalate in Pertusaria corallina. Pedobiologia (Jena) 26:373–3
Yang XE, Baligar VC, Foster JC, Martens DC (1997) Accumulation and transport of nickel in relation to organic acids in ryegrass and maize grown with different nickel levels. Plant Soil 196:271–276 doi:10.1023/A:1004270528532
Yu Q, Rengel Z (1999) Micronutrient deficiency influences plant growth and activities of superoxide dismutase and ascorbate peroxidase in narrow leaf lupins. Ann Bot (Lond) 183:175–182 doi:10.1006/anbo.1998.0811
Zhao SY, Blumwald E (1998) Changes in oxidation-reduction state and antioxidant enzymes in the roots of jack pine seedlings during cold acclimation. Physiol Plant 104:134–142 doi:10.1034/j.1399-3054.1998.1040117.x
Acknowledgements
This work was supported by the International Cooperation FONDECYT project 7060093 and by the FONDECYT project 1061262 Grants. We thank to Dr. Cristián Wulff Zottele who supervised the idiomatic revision and the figure edition of the manuscript.
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Mora, M.L., Rosas, A., Ribera, A. et al. Differential tolerance to Mn toxicity in perennial ryegrass genotypes: involvement of antioxidative enzymes and root exudation of carboxylates. Plant Soil 320, 79–89 (2009). https://doi.org/10.1007/s11104-008-9872-1
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DOI: https://doi.org/10.1007/s11104-008-9872-1