Manganese toxicity in rice plants mitigated by silicon effects on leaf tissues
DOI:
https://doi.org/10.5433/1679-0359.2019v40n6p2523Keywords:
Oryza sativa, Plant nutrition, Micronutrient, Foliar micromorphometry.Abstract
Anatomical modifications of leaves and other organs associated with mineral nutrition have been observed in many plants. However, little is known about the quantitative effects of Si and Mn on the anatomy of plant leaves, especially in rice. This study aimed to quantify the tissue thickness of rice leaves and the density of silica bodies in rice leaves grown in a nutrient solution supplemented with Si and Mn and evaluate the possible effects of Si on Mn toxicity. Treatments were arranged in a 2×3 factorial scheme = six combinations of treatments, two doses of Si (0 and 2 mmol L-1), and three doses of Mn (0.5, 2.5, and 10 µmol L-1) in randomized complete block design with four replications. After 39 days in the nutrient solution with the respective treatments, anatomical and micromorphometric measures of the leaf blade were carried out to determine the thickness and area of leaf tissues. The data were submitted to analysis of variance (ANOVA) and Tukey’s multiple comparisons test of means(p?0,05). The abaxial and adaxial epidermal thickness, as well as the density of silica bodies increased with the addition of Si to the nutrient solution. This study demonstrated that Si reduced the number of vascular bundles and Mn reduced the thickness of the chlorenchyma with increasing doses. Manganese doses of up to 10 ?mol L-1 do not inhibit the uptake and deposition of silicon in rice leaf tissues. Higher Si concentration in the solution caused anatomical changes in the leaf, which was associated with a possible alleviation of Mn toxicity due to the higher concentration of Si in plants since this effect was observed mainly when Si was present in the nutrient solution.References
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CURRIE, H. A., PERRY, C. C. Silica in plants: biological, biochemical and chemical studies. Annals of Botany, v. 100, n. 7, p. 1383-1389, 2007. DOI: 10.1093/aob/mcm247
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KRAUS, J. E.; ARDUIM, M. Manual básico de métodos em morfologia vegetal. Seropédica: Edurj, 1997. v. 1, 198 p.
KUMAR, S.; SOUKUP, M.; ELBAUM, R. Silicification in grasses: variation between different cell types. Plant Science, v. 8, p. 1-8, 2017. DOI: 10.3389/fpls.2017.00438
LI, P.; SONG, A.; LI, Z.; FAN, F.; LIANG, Y. Silicon ameliorates manganese toxicity by regulating manganese transport and antioxidant reactions in rice (Oryza sativa L.). Plant and Soil, v. 354, p. 407-419, 2012. DOI: 10.1007/s11104-011-1076-4
LIANG, Y.; SUN, W.; ZHU, Y.-G.; CHRISTIE, P. Mechanisms of silicon-mediated alleviation of abiotic stresses in higher plants: a review. Environmental Pollution, v. 147, p. 422-428, 2007. DOI: 10.1016/j.envpol.2006.06.008
LUX, A.; LUXOVÁ, M.; HATTORI, T.; INANAGA, S.; SUGIMOTO, Y. Silicification in sorghum (Sorghum bicolor) cultivars with different drought tolerance. Physiologia Plantarum, v. 115, n. 1, p. 87-92, 2002. DOI: 10.1034/j.1399-3054.2002.1150110.x
MA, J. F.; MIYAKE, Y.; TAKAHASHI, E. Silicon as a beneficial element for crop plants. In: DATNOFF, L. E.; SNYDER, G. H.; KORNDORFER, G.H. Silicon in agriculture. Amsterdam: Elsevier Science, 2001. p. 17-39.
MA, J. F.; TAKAHASHI, E. Soil, fertilizer, and plant silicon research in Japan. Amsterdam: Elsevier Science, 2002. 281 p.
MA, J. F.; YAMAJI, N. Silicon uptake and accumulation in higher plants. Trends Plant Science, v. 11, n. 8, p. 92-397, 2006. DOI: 10.1016/j.tplants.2006.06.007
MA, J. F. Role of silicon in enhancing the resistance of plants to biotic and abiotic stresses. Soil Science and Plant Nutrition, v. 50, n. 1, p. 11-18, 2004. DOI: 10.1080/00380768.2004.10408447
MAUAD, M.; CRUSCIOL, C. A. C.; GRASSI FILHO, H.; MACHADO, S. R. Deposição de sílica e teor de nitrogênio e silício em arroz. Semina:Ciências Agrárias, v. 34, n. 4, p. 1653-1662, 2013. DOI: 10.5433/1679-0359.2013v34n4p1653
MEENA, V.; DOTANIYA, M.; COUMAR, V.; RAJENDIRAN, S.; KUNDU, S.; RAO, A. S. A case for silicon fertilization to improve crop yields in tropical soils. Proceedings of the National Academy of Sciences, India Section B: Biolical Sciences, v. 84, n. 3, p. 505-518, 2014. DOI: 10.1007/s40011-013-0270-y
MELO, S. P. Silício e fósforo para estabelecimento do capim-Marandu num Latossolo Vermelho-Amarelo. 2005. Tese (Doutorado em Solos e Nutrição de Plantas) - Universidade Estadual Paulista "Júlio de Mesquita Filho", Piracicaba.
METCALFE, C. R. Anatomy of the Monocotyledons. Oxford: Clarendon Press, 1960. 731 p.
MOTOMURA, H.; FUJII, T.; SUZUKI, M. Distribution of silicified cells in the leaf blades of Pleioblastus chino (Franchet et Savatier) Makino (Bambusoideae). Annals of Botany, v. 85, n. 5, p. 751-757, 2000. DOI: 10.1006/anbo.2000.1124
NING, D. F.; SONG, A.; FAN, F. L.; LI, Z. J.; LIANG, Y. C. Effects of slag-based silicon fertilizer on rice growth and brown-spot resistance. PLoS One, v. 9, n. 7, e102681, 2014. DOI: 10.1371/journal.pone.0102681
O’BRIEN, T. P.; McCULLY, M. E. The study of plant structure: principles and selected methods. Melburne: Termarcarphy Pty, 1981. 357 p.
PAPADAKIS, I. E.; DIMASSI, K. N.; BOSABALIDIS, A. M.; THERIOS, I. N.; PATAKAS, A.; GIANNAKOULA, A. Effects of B excess on some physiological and anatomical parameters of ‘Navelina’ orange plants grafted on two rootstocks. Environmental and Experimental Botany, v. 51, p. 247-257, 2004. DOI: 10.1016/j.envexpbot.2003.11.004
REYNOLDS, O. L.; KEEPING, M. G.; MEYER, J. H. Silicon-augmented resistance of plants to herbivorous insects: a review. Annals of Applied Biology, v. 155, n. 2, p. 171-186, 2009. DOI: 10.1111/j.1744-7348.2009.00348.x
ROGALLA, H; RÖMHELD, V. Role of leaf apoplast in silicon mediated manganese tolerance of Cucumis sativus L. Plant Cell Environment, v. 25, n. 4, p. 549-555, 2002. DOI: 10.1046/j.1365-3040.2002.00835.x
SANTOS, E. F.; SANTINI, J. M. K.; PAIXAO, A. P.; JÚNIOR, E. F.; LAVRES, J.; CAMPOS, M.; REIS, A. R. D. Physiological highlights of manganese toxicity symptoms in soybean plants: Mn toxicity responses. Plant Physiology and Biochemistry, v. 113, n. 1, p. 6-19, 2017. DOI: 10.1016/j.plaphy.2017.01.022
SHANE, M. W.; MCCULLY, M. E.; LAMBERS, H. Tissue and cellular phosphorus storage during development of phosphorus toxicity in Hakea prostrata (Proteaceae), Journal of Experimental Botany, v. 55, n. 339, p. 1033-1044, 2004. DOI: 10.1093/jxb/erh111
SHI, Q. H.; BAO, Z. Y.; ZHU, Z. J.; HE Y.; QIAN, Q. Q.; YU, J. Q. Silicon-mediated alleviation of Mn toxicity in Cucumis sativus in relation to activities of superoxide dismutase and ascorbate peroxidase. Phytochemistry, v. 66, p. 1551-1559, 2005. DOI: 10.1016/j.phytochem.2005.05.006
WILLIAMS, D. E.; VLAMIS, J. The effect of silicon on yield and manganese-54 uptake and distribution in the leaves of barley plants grown in culture solutions. Plant Physiology, v. 32, n. 5, p. 404-409, 1957. DOI: 10.1104/pp.32.5.404
WILSON, J. R. Variation on leaf characteristics with level of insertion on a grass tiller. I. Development rate, chemical composition and dry matter digestibility. Australian Journal of Agricultural Research, v. 27, n. 2, p. 343-354, 1976. DOI: 10.1071/AR9760343
YOSHIDA, S. Fundamental of rice crop science. Los Baños: International Rice Research Institute, 1981. 269 p.
ZANÃO JÚNIOR, L. A.; ALVAREZ V., V. H.; CARVALHO-ZANÃO, M. P.; FONTES, R. L. F.; GROSSI, J. A. S. Produção de rosas influenciada pela aplicação de doses de silício no substrato. Revista Brasileira de Ciência do Solo, v. 37, n. 6, p. 1611-1619, 2013. DOI: 10.1590/S0100-06832013000600017
ZANÃO JÚNIOR, L. A.; FONTES, R. L. F.; AVILA, V. T. Aplicação do silício para aumentar a resistência do arroz à mancha-parda. Pesquisa agropecuária Brasileira, v. 44, n. 2, p. 203-206, 2009a. DOI: 10.1590/S0100-204X2009000200013
ZANÃO JÚNIOR, L. A.; FONTES, R. L. F.; NEVES, J. C. L.; KORNDÖRFER, G. H.; ÁVILA, V. T. Rice grown in nutrient solution with doses of manganese and silicon. Revista Brasileira de Ciência do Solo, v. 34, n. 5, p. 1629-1639, 2010. DOI: 10.1590/S0100-06832010000500016
ZANÃO JÚNIOR, L. A.; RODRIGUES, F. A.; FONTES, R. L. F.; KORNDÖRFER, G. H.; NEVES, J. C. L. Rice resistance to brow spot mediated by silicon and its interaction whit manganese. Journal of Phytopathology, v. 157, n. 2, p. 73-78, 2009b. DOI: 10.1111/j.1439-0434.2008.01447.x
ZHANG, C.; WANG, L.; ZHANG, W.; ZHANG, F. Do lignification and silicification of the cell wall precede silicon deposition in the silica cell of the rice (Oryza sativa L.) leaf epidermis? Plant Soil, v. 372, n. 1-2, p. 137-149, 2013. DOI: 10.1007/s11104-013-1723-z
AGRIOS, G. N. Plant pathology. San Diego: Academic Press, 1988. 803 p.
AGUIAR, T. V.; SANT’ANNA-SANTOS, B. F.; AZEVEDO, A. A.; FERREIRA, R. S. Anati quanti: software de análises quantitativas para estudos em anatomia vegetal. Planta Daninha, v. 25, n. 4, p. 649-659, 2007. DOI: 10.1590/S0100-83582007000400001.
ANDRADE, F. A.; ANDRADE, C. G. T. J.; MIGLIORANZA, E. Detecção de sílica em folha bandeira de trigo. Semina: Ciências Agrárias, v. 33, p. 2555-2562, 2012. Suplemento 1. DOI: 10.5433/1679-0359.2012v33Supl1p2555
CUNHA, K. P. V.; NASCIMENTO, C. W. A. Silicon effects on metal tolerance and structural changes in maize (Zea mays L.) grown on a cadmium and zinc enriched soil. Water Air Soil Pollution, v. 197, p. 323-330, 2008. DOI: 10.1007/s11270-008-9814-9
CURRIE, H. A., PERRY, C. C. Silica in plants: biological, biochemical and chemical studies. Annals of Botany, v. 100, n. 7, p. 1383-1389, 2007. DOI: 10.1093/aob/mcm247
DEBONA, D.; RODRIGUES, F. A.; DATNOFF, L. E. Silicon's role in abiotic and biotic plant stresses. Annual Review of Phytopathology, v. 55, n. 1, p. 85-107, 2017. DOI: 10.1146/annurev-phyto-080516-035312
DOMICIANO, G. P.; RODRIGUES, F. A.; MOREIRA, W. R.; OLIVEIRA, H. V.; VALE, F. X. R.; XAVIER FIHA, M. S. Silício no progresso da mancha marrom na folha bandeira do trigo. Tropical Plant Pathology, v. 35, n. 3, p. 86-189, 2010. DOI: 10.1590/S1982-56762010000300009
DONCHEVA, S. N.; POSCHENRIEDERB, C.; STOYANOVAA, Z. L.; GEORGIEVAA, K.; VELICHKOVAC, M.; BARCELÓ, J. Silicon amelioration of manganese toxicity in Mn-sensitive and Mn-tolerant maize varieties. Environment Experimental Botany, v. 65, p. 189-197, 2009. DOI: 10.1016/j.envexpbot.2008.11.006
EPSTEIN, E. Silicon: its manifold roles in plants. Annals of Applied Biology, v. 155, p. 155-160, 2009. DOI:10.1111/j.1744-7348.2009.00343.x
EPSTEIN, E.; BLOOM, A. J. Mineral nutrition of plants: principles and perspectives. 2. ed. Massachussets: Sinauer, 2005. 380 p.
FAUTEUX, F.; RÉMUS-BOREL, W.; MENZIES, J. G.; BÉLANGER, R. R. Silicon and plant disease resistance against pathogenic fungi. FEMS Microbiol. Letters, v. 249, p. 1-6, 2005. DOI: 10.1016/j.femsle.2005.06.034
FERNANDO, D. R.; BATIANOFF, G. N.; BAKER, A. J.; WOODROW, I. E. In vivo localisation of manganese in the hyperaccumulator Gossia bidwillii (Benth.) N. Snow & Guymer (Myrtaceae) by cryo-SEM/EDAX. Plant, Cell & Environment, v. 29, p. 1012-1020, 2006. DOI: 10.1111/j.1365-3040.2006.01498.x
FLECK, A. T.; NYE, T.; REPENNING, C.; STAHL, F.; ZAHN, M.; SCHENK, M. K. Silicon enhances suberization and lignification in roots of rice (Oryza sativa). Journal of Experimental Botany, v. 62, n. 6, p. 2001-2011, 2010. DOI: 10.1093/jxb/erq392
FREITAS, L. B.; FERNANDER, D. M.; MAIA, S. C. M. Silício na nutrição mineral e acúmulo de alumínio em plantas de arroz de terras altas. Pesquisa Agropecuária Tropical, v. 45, n. 4, p. 440-448, 2015. DOI: 10.1590/1983-40632015v4538085
GONG, H.; ZHU, X.; CHEN, K.; WANG, S.; ZHANG, C. Silicon alleviates oxidative damage of wheat plants in pots under drought. Plant Science, v. 169, n. 2, p. 313-321, 2005. DOI: 10.1016/j.plantsci.2005.02.023
KRAUS, J. E.; ARDUIM, M. Manual básico de métodos em morfologia vegetal. Seropédica: Edurj, 1997. v. 1, 198 p.
KUMAR, S.; SOUKUP, M.; ELBAUM, R. Silicification in grasses: variation between different cell types. Plant Science, v. 8, p. 1-8, 2017. DOI: 10.3389/fpls.2017.00438
LI, P.; SONG, A.; LI, Z.; FAN, F.; LIANG, Y. Silicon ameliorates manganese toxicity by regulating manganese transport and antioxidant reactions in rice (Oryza sativa L.). Plant and Soil, v. 354, p. 407-419, 2012. DOI: 10.1007/s11104-011-1076-4
LIANG, Y.; SUN, W.; ZHU, Y.-G.; CHRISTIE, P. Mechanisms of silicon-mediated alleviation of abiotic stresses in higher plants: a review. Environmental Pollution, v. 147, p. 422-428, 2007. DOI: 10.1016/j.envpol.2006.06.008
LUX, A.; LUXOVÁ, M.; HATTORI, T.; INANAGA, S.; SUGIMOTO, Y. Silicification in sorghum (Sorghum bicolor) cultivars with different drought tolerance. Physiologia Plantarum, v. 115, n. 1, p. 87-92, 2002. DOI: 10.1034/j.1399-3054.2002.1150110.x
MA, J. F.; MIYAKE, Y.; TAKAHASHI, E. Silicon as a beneficial element for crop plants. In: DATNOFF, L. E.; SNYDER, G. H.; KORNDORFER, G.H. Silicon in agriculture. Amsterdam: Elsevier Science, 2001. p. 17-39.
MA, J. F.; TAKAHASHI, E. Soil, fertilizer, and plant silicon research in Japan. Amsterdam: Elsevier Science, 2002. 281 p.
MA, J. F.; YAMAJI, N. Silicon uptake and accumulation in higher plants. Trends Plant Science, v. 11, n. 8, p. 92-397, 2006. DOI: 10.1016/j.tplants.2006.06.007
MA, J. F. Role of silicon in enhancing the resistance of plants to biotic and abiotic stresses. Soil Science and Plant Nutrition, v. 50, n. 1, p. 11-18, 2004. DOI: 10.1080/00380768.2004.10408447
MAUAD, M.; CRUSCIOL, C. A. C.; GRASSI FILHO, H.; MACHADO, S. R. Deposição de sílica e teor de nitrogênio e silício em arroz. Semina:Ciências Agrárias, v. 34, n. 4, p. 1653-1662, 2013. DOI: 10.5433/1679-0359.2013v34n4p1653
MEENA, V.; DOTANIYA, M.; COUMAR, V.; RAJENDIRAN, S.; KUNDU, S.; RAO, A. S. A case for silicon fertilization to improve crop yields in tropical soils. Proceedings of the National Academy of Sciences, India Section B: Biolical Sciences, v. 84, n. 3, p. 505-518, 2014. DOI: 10.1007/s40011-013-0270-y
MELO, S. P. Silício e fósforo para estabelecimento do capim-Marandu num Latossolo Vermelho-Amarelo. 2005. Tese (Doutorado em Solos e Nutrição de Plantas) - Universidade Estadual Paulista "Júlio de Mesquita Filho", Piracicaba.
METCALFE, C. R. Anatomy of the Monocotyledons. Oxford: Clarendon Press, 1960. 731 p.
MOTOMURA, H.; FUJII, T.; SUZUKI, M. Distribution of silicified cells in the leaf blades of Pleioblastus chino (Franchet et Savatier) Makino (Bambusoideae). Annals of Botany, v. 85, n. 5, p. 751-757, 2000. DOI: 10.1006/anbo.2000.1124
NING, D. F.; SONG, A.; FAN, F. L.; LI, Z. J.; LIANG, Y. C. Effects of slag-based silicon fertilizer on rice growth and brown-spot resistance. PLoS One, v. 9, n. 7, e102681, 2014. DOI: 10.1371/journal.pone.0102681
O’BRIEN, T. P.; McCULLY, M. E. The study of plant structure: principles and selected methods. Melburne: Termarcarphy Pty, 1981. 357 p.
PAPADAKIS, I. E.; DIMASSI, K. N.; BOSABALIDIS, A. M.; THERIOS, I. N.; PATAKAS, A.; GIANNAKOULA, A. Effects of B excess on some physiological and anatomical parameters of ‘Navelina’ orange plants grafted on two rootstocks. Environmental and Experimental Botany, v. 51, p. 247-257, 2004. DOI: 10.1016/j.envexpbot.2003.11.004
REYNOLDS, O. L.; KEEPING, M. G.; MEYER, J. H. Silicon-augmented resistance of plants to herbivorous insects: a review. Annals of Applied Biology, v. 155, n. 2, p. 171-186, 2009. DOI: 10.1111/j.1744-7348.2009.00348.x
ROGALLA, H; RÖMHELD, V. Role of leaf apoplast in silicon mediated manganese tolerance of Cucumis sativus L. Plant Cell Environment, v. 25, n. 4, p. 549-555, 2002. DOI: 10.1046/j.1365-3040.2002.00835.x
SANTOS, E. F.; SANTINI, J. M. K.; PAIXAO, A. P.; JÚNIOR, E. F.; LAVRES, J.; CAMPOS, M.; REIS, A. R. D. Physiological highlights of manganese toxicity symptoms in soybean plants: Mn toxicity responses. Plant Physiology and Biochemistry, v. 113, n. 1, p. 6-19, 2017. DOI: 10.1016/j.plaphy.2017.01.022
SHANE, M. W.; MCCULLY, M. E.; LAMBERS, H. Tissue and cellular phosphorus storage during development of phosphorus toxicity in Hakea prostrata (Proteaceae), Journal of Experimental Botany, v. 55, n. 339, p. 1033-1044, 2004. DOI: 10.1093/jxb/erh111
SHI, Q. H.; BAO, Z. Y.; ZHU, Z. J.; HE Y.; QIAN, Q. Q.; YU, J. Q. Silicon-mediated alleviation of Mn toxicity in Cucumis sativus in relation to activities of superoxide dismutase and ascorbate peroxidase. Phytochemistry, v. 66, p. 1551-1559, 2005. DOI: 10.1016/j.phytochem.2005.05.006
WILLIAMS, D. E.; VLAMIS, J. The effect of silicon on yield and manganese-54 uptake and distribution in the leaves of barley plants grown in culture solutions. Plant Physiology, v. 32, n. 5, p. 404-409, 1957. DOI: 10.1104/pp.32.5.404
WILSON, J. R. Variation on leaf characteristics with level of insertion on a grass tiller. I. Development rate, chemical composition and dry matter digestibility. Australian Journal of Agricultural Research, v. 27, n. 2, p. 343-354, 1976. DOI: 10.1071/AR9760343
YOSHIDA, S. Fundamental of rice crop science. Los Baños: International Rice Research Institute, 1981. 269 p.
ZANÃO JÚNIOR, L. A.; ALVAREZ V., V. H.; CARVALHO-ZANÃO, M. P.; FONTES, R. L. F.; GROSSI, J. A. S. Produção de rosas influenciada pela aplicação de doses de silício no substrato. Revista Brasileira de Ciência do Solo, v. 37, n. 6, p. 1611-1619, 2013. DOI: 10.1590/S0100-06832013000600017
ZANÃO JÚNIOR, L. A.; FONTES, R. L. F.; AVILA, V. T. Aplicação do silício para aumentar a resistência do arroz à mancha-parda. Pesquisa agropecuária Brasileira, v. 44, n. 2, p. 203-206, 2009a. DOI: 10.1590/S0100-204X2009000200013
ZANÃO JÚNIOR, L. A.; FONTES, R. L. F.; NEVES, J. C. L.; KORNDÖRFER, G. H.; ÁVILA, V. T. Rice grown in nutrient solution with doses of manganese and silicon. Revista Brasileira de Ciência do Solo, v. 34, n. 5, p. 1629-1639, 2010. DOI: 10.1590/S0100-06832010000500016
ZANÃO JÚNIOR, L. A.; RODRIGUES, F. A.; FONTES, R. L. F.; KORNDÖRFER, G. H.; NEVES, J. C. L. Rice resistance to brow spot mediated by silicon and its interaction whit manganese. Journal of Phytopathology, v. 157, n. 2, p. 73-78, 2009b. DOI: 10.1111/j.1439-0434.2008.01447.x
ZHANG, C.; WANG, L.; ZHANG, W.; ZHANG, F. Do lignification and silicification of the cell wall precede silicon deposition in the silica cell of the rice (Oryza sativa L.) leaf epidermis? Plant Soil, v. 372, n. 1-2, p. 137-149, 2013. DOI: 10.1007/s11104-013-1723-z
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2019-08-29
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Zanão Júnior, L. A., Fontes, R. L. F., Pereira, J. D., Carvalho-Zanão, M. P., & Pereira, N. (2019). Manganese toxicity in rice plants mitigated by silicon effects on leaf tissues. Semina: Ciências Agrárias, 40(6), 2523–2534. https://doi.org/10.5433/1679-0359.2019v40n6p2523
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