Abstract
Aluminum stress usually reduces plant root growth due to the accumulation of Al in specific zones of the root apex. The objectives of this study were to determine the localization of Al in the root apex of Sorghum bicolor (L.) Moech. and its effects on membrane integrity, callose accumulation, and root growth in selected cultivars. Seedlings were grown in a nutrient solution containing 0, 27, or 39 μM Al3+ for 24, 48, and 120 h. The Al stress significantly reduced root growth, especially after 48 and 120 h of exposure. A higher Al accumulation, determined by fluorescence microscopy after staining with a Morin dye, occurred in the root extension zone of the sensitive cultivar than in the tolerant cultivar. The membrane damage and callose accumulation were also higher in the sensitive than resistant cultivar. It was concluded that the Al stress significantly reduced root growth through the accumulation of Al in the root extension zone, callose accumulation, and impairment of plasma membrane integrity.
Abbreviations
- BIO-EARN:
-
Eastern African Regional Programme and Research Network for Biotechnology, Biosafety and Biotechnology Policy Development
- ICRISAT:
-
International Crops Research Institute for the Semi-Arid Tropics
- SIDA:
-
Swedish International Development Agency
References
Ahn, S.J., Matsumoto, H.: The role of the plasma membrane in the response of plant roots to aluminum toxicity. — Plant Signal. Behav. 1: 37–45, 2006.
Alvim, M.N., Ramos, F.T., Oliveira, D.C., Isaias, R.M.S., Franca, M.G.C.: Aluminium localization and toxicity symptoms related to root growth inhibition in rice (Oryza sativa L.) seedlings. — J. Biosci. 37: 1079–1088, 2012.
Baker, J.C., Mock, N.M.: An improved method for monitoring cell death in cell suspension and leaf disc assays using Evans blue. — Plant Cell Tissue Organ Cult. 39: 7–12, 1994.
Bhuja, P., McLachlan, K., Stephens, J., Taylor, G.: Accumulation of 1,3-beta-D-glucans, in response to aluminum and cytosolic calcium in Triticum aestivum. — Plant Cell Physiol. 45: 543–549, 2004.
Cartes, P., McManus, M., Wulff-Zottele, C., Leung, S., Gutiérrez-Moraga, A., Mora, M.D.L.: Differential superoxide dismutase expression in ryegrass cultivars in response to short term aluminium stress. — Plant Soil 350: 353–363, 2012.
Cheprot, R.K., Matonyei, T.K., Maritim, K.K., Were, B.A., Dangasuk, O.G., Onkware, A.O. Gudu, S.: Physiological characterization of Kenyan sorghum lines for tolerance to aluminium. — Int. J. nat. Sci. Res. 2: 59–71, 2014.
Garzón, T., Gunsé, B., Moreno, A.R., Tomos, A.D., Barceló, J., Poschenrieder, C.: Aluminium-induced alteration of ion homeostasis in root tip vacuoles of two maize varieties differing in Al tolerance. — Plant Sci. 180: 709–715, 2011.
Goncalves, J.F.D., Cambraia, J., Mosquim, P.R., Araujo, E.F.: Aluminum effect on organic acid production and accumulation in sorghum. — J. Plant Nutr. 28: 507–520, 2005.
Gunse, B., Poschenrieder, C., Barcelo, J.: Water transport properties of roots and root cortical cells in proton- and Alstressed maize varieties. — Plant Physiol. 113: 595–602, 1997.
Illéš, P., Schlicht, M., Pavlovkin, J., Lichtscheidl, I., Baluška, F., Ovečka, M.: Aluminium toxicity in plants: internalization of aluminium into cells of the transition zone in Arabidopsis root apices related to changes in plasma membrane potential, endosomal behaviour, and nitric oxide production. — J. exp. Bot. 57: 4201–4213, 2006.
Kaneko, M., Yoshimura, E., Nishizawa, N.K., Mori, S.: Time course study of aluminum-induced callose formation in barley roots as observed by digital microscopy and low-vacuum scanning electron microscopy. — Soil Sci. Plant Nutr. 45: 701–712, 1999.
Kochian, L., Piñeros, M., Hoekenga, O.: The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. — Plant Soil 274: 175–195, 2005.
Koehle, H., Jeblick, W., Poten, F., Blaschek, W., Kauss, H.: Chitosan-elicited callose synthesis in soybean (Glycine max) cultivar Harosoy-63 cells as a calcium-dependent process. — Plant Physiol. 77: 544–551, 1985.
Magalhaes, J.V., Garvin, D.F., Wang, Y., Sorrells, M.E., Klein, P.E., Schaffert, R.E., Li, L., Kochian, L.V.: Comparative mapping of a major aluminum tolerance gene in sorghum and other species in the Poaceae. — Genetics 167: 1905–1914, 2004.
Magalhaes, J.V., Liu, J., Guimaraes, C.T., Lana, U.G., Alves, V.M., Wang, Y.H., Schaffert, R.E., Hoekenga, O.A., Pineros, M.A., Shaff, J.E., Klein, P.E., Carneiro, N.P., Coelho, C.M., Trick, H.N., Kochian, L.V.: A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. — Nat. Genet. 39: 1156–1161, 2007.
Martins, N., Goncales, S., Romano, A.: Metabolism and aluminium accumulation in Plantago almogravensis and P. Algarbiensis in response to low pH and aluminium stress. — Biol. Plant. 57: 325–331, 2013.
Massot, N., Llugany, M., Poschenrieder, C., Barcelo, J.: Callose production as indicator of aluminum toxicity in bean cultivars. — J. Plant Nutr. 22: 1–10, 1999.
Narro, L.A., Arcos, A.L.: Genetics of aluminum-induced callose formation in maize roots, a selection trait for aluminum resistance. — Crop Sci. 50: 1848–1853, 2010.
Panda, S.K., Matsumoto, H.: Molecular physiology of aluminium toxicity and tolerance in plants. — Bot. Rev. 74: 326–347, 2007.
Peixoto, P.H.P., Cambraia, J., Sant’Anna, R., Mosquim, P.R., Moreira, M.A.: Aluminum effects on fatty acid composition and lipid peroxidation of a purified plasma membrane fraction of root apices of two sorghum cultivars. — J. Plant Nutr. 24: 1061–1070, 2001.
Pirselova, B., Matusikova, I.: Callose: the plant cell wall polysaccharide with multiple biological functions. — Acta Physiol. Plant. 35: 635–644, 2013.
Ringo, J.H., Mneney, E.E., Onkware, A.O., Were, B.A., Too, E.J., Owuoche, J.O., Gudu, S.O.: Tolerance to aluminium toxicity in Tanzanian sorghum genotypes. — Afr. Crop Sci. J. 18: 155–164, 2010.
Silva, S., Rodriguez, E., Pinto-Carnide, O., Martins-Lopes, P., Matos, M., Guedes-Pinto, H., Santos, C.: Zonal responses of sensitive vs. tolerant wheat roots during Al exposure and recovery. — J. Plant Physiol. 169: 760–769, 2012.
Sivaguru, M., Horst, W.J.: The distal part of the transition zone is the most aluminum-sensitive apical root zone of maize. — Plant Physiol. 116: 155–163, 1998.
Sivaguru, M., Fujiwara, T., Samaj J., Baluska, F., Yang, Z., Osawa, H., Maeda, T., Mori, T., Volkmann, D., Matsumoto, H.: Aluminium-induced 1-3-β-glucan inhibits cell-to-cell trafficking of molecules through plasmodesmata. A new mechanism of aluminium toxicity in plants. — Plant Physiol. 124: 991–1005, 2000.
Smith, E., Naik, D., Cumming, J.R.: Genotypic variation in aluminum resistance, cellular aluminum fractions, callose and pectin formation and organic acid accumulation in roots of Populus hybrids. — Environ. exp. Bot. 72: 182–193, 2011.
Tamás, L., Budíková, S., Šimonovičová, M., Huttová, J., Široká, B., Mistrík, I.: Rapid and simple method for Al-toxicity analysis in emerging barley roots during germination. — Biol. Plant. 50: 87–93, 2006.
Too, E.J.: Physiological and Molecular Characterization of Resistance to Aluminium Stress in Selected Grain Sorghums. — Thesis. Biological Sciences, Moi University, Eldoret 2011.
Von Uexküll, H.R., Mutert, E.: Global extent, development and economic impact of acid soils. — Plant Soil 171: 1–15, 1995.
Xu, F.J., Li, G., Jin, C.W., Liu, W.J., Zhang, S.S., Zhang, Y.S., Lin, X.Y.: Aluminum-induced changes in reactive oxygen species accumulation, lipid peroxidation and antioxidant capacity in wheat root tips. — Biol. Plant. 56: 89–96, 2012.
Yamamoto, Y., Kobayashi, Y., Devi, S.R., Rikiishi, S., Matsumoto, H.: Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells. — Plant Physiol. 128: 63–72, 2002.
Yang, Z., Eticha, D., Albacete, A., Rao, I.M., Roitsch, T., Horst, W.J.: Physiological and molecular analysis of the interaction between aluminium toxicity and drought stress in common bean (Phaseolus vulgaris). — J. exp. Bot. 63: 3109–3125, 2012.
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Acknowledgements: This work was supported by SIDA under the BIO-EARN programme given to the Moi University and the Swedish University of Agricultural Sciences through funding from the Swedish Ministry of Foreign Affairs as part of its special allocation on global food security (UD40). The authors are grateful to ICRISAT for sorghum seed.
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Too, E.J., Carlsson, A.S., Onkware, A.O. et al. Cell membrane integrity, callose accumulation, and root growth in aluminum-stressed sorghum seedlings. Biol Plant 58, 768–772 (2014). https://doi.org/10.1007/s10535-014-0455-0
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DOI: https://doi.org/10.1007/s10535-014-0455-0