Aluminium, Iron and Silicon Subcellular Redistribution in Wheat Induced by Manganese Toxicity
Abstract
:1. Introduction
2. Materials and Methods
2.1. Characterisation of the Soil and Soil Solution
2.2. Experimental Setup
2.3. Wheat Subcellular Element Distribution
2.4. Manganese, Aluminium, Iron, and Silicon Analysis
2.4.1. Acid Digestion of Wheat Tissues
2.4.2. Quantitative Element Analysis
2.5. Data Analysis
3. Results
3.1. Manganese
3.2. Aluminium
3.3. Iron
3.4. Silicon
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Kochian, L.V.; Hoekenga, O.A.; Piñeros, M.A. How do crop plants tolerate acid soils? mechanisms of aluminum tolerance and phosphorous efficiency. Annu. Rev. Plant Biol. 2004, 55, 459–493. [Google Scholar] [CrossRef]
- Kochian, L.V.; Piñeros, M.A.; Liu, J.; Magalhaes, J.V. Plant Adaptation to Acid Soils: The Molecular Basis for Crop Aluminum Resistance. Annu. Rev. Plant Biol. 2015, 66, 571–598. [Google Scholar] [CrossRef]
- George, E.; Horst, W.J.; Neumann, E. Chapter 17—Adaptation of Plants to Adverse Chemical Soil Conditions. In Marschner’s Mineral Nutrition of Higher Plants, 3rd ed.; Marschner, P., Ed.; Academic Press: San Diego, CA, USA, 2012; pp. 409–472. ISBN 978-0-12-384905-2. [Google Scholar]
- Paterson, E.; Goodman, B.A.; Farmer, V.C. The Chemistry of Aluminium, Iron and Manganese Oxides in Acid Soils. In Soil Acidity; Springer Science and Business Media LLC: Berlin/Heidelberg, Germany, 1991; pp. 97–124. [Google Scholar]
- Marschner, H. Mechanisms of adaptation of plants to acid soils. Plant Soil 1991, 134, 1–20. [Google Scholar] [CrossRef]
- Mou, D.; Yao, Y.; Yang, Y.; Zhang, Y.; Tian, C.; Achal, V. Plant high tolerance to excess manganese related with root growth, manganese distribution and antioxidative enzyme activity in three grape cultivars. Ecotoxicol. Environ. Saf. 2011, 74, 776–786. [Google Scholar] [CrossRef] [PubMed]
- Goulding, K.W.T. Soil acidification and the importance of liming agricultural soils with particular reference to the United Kingdom. Soil Use Manag. 2016, 32, 390–399. [Google Scholar] [CrossRef]
- Khabaz-Saberi, H.; Setter, T.L.; Waters, I. Waterlogging Induces High to Toxic Concentrations of Iron, Aluminum, and Manganese in Wheat Varieties on Acidic Soil. J. Plant Nutr. 2006, 29, 899–911. [Google Scholar] [CrossRef]
- Khabaz-Saberi, H.; Barker, S.J.; Rengel, Z. Tolerance to ion toxicities enhances wheat grain yield in acid soils prone to drought and transient waterlogging. Crop. Pasture Sci. 2014, 65, 862–867. [Google Scholar] [CrossRef]
- Singh, S.; Tripathi, D.K.; Singh, S.; Sharma, S.; Dubey, N.; Chauhan, D.; Vaculik, M. Toxicity of aluminium on various levels of plant cells and organism: A review. Environ. Exp. Bot. 2017, 137, 177–193. [Google Scholar] [CrossRef]
- Zheng, S.J.; Yang, J.L. Target sites of aluminum phytotoxicity. Biol. Plant 2005, 49, 321–331. [Google Scholar] [CrossRef]
- Kochian, L.V. Cellular Mechanisms of Aluminum Toxicity and Resistance in Plants. Annu. Rev. Plant Biol. 1995, 46, 237–260. [Google Scholar] [CrossRef]
- Schroeder, J.I.; Delhaize, E.; Frommer, W.; Guerinot, M.L.; Harrison, M.J.; Herrera-Estrella, L.; Horie, T.; Kochian, L.; Munns, R.; Nishizawa, N.K.; et al. Using membrane transporters to improve crops for sustainable food production. Nat. Cell Biol. 2013, 497, 60–66. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sasaki, T.; Yamamoto, Y.; Ezaki, B.; Katsuhara, M.; Ahn, S.J.; Ryan, P.R.; Delhaize, E.; Matsumoto, H. A wheat gene encoding an aluminum-activated malate transporter. Plant J. 2004, 37, 645–653. [Google Scholar] [CrossRef] [PubMed]
- Becker, M.; Asch, F. Iron toxicity in rice—Conditions and management concepts. J. Plant Nutr. Soil Sci. 2005, 168, 558–573. [Google Scholar] [CrossRef]
- Camargo, C.E.D.O.; Felicio, J.C.; Filho, A.W.P.F.; De Freitas, J.G.; Ramos, V.J.; Kanthack, R.A.D.; De Castro, J.L. Melhoramento do trigo: XXX. Avaliação de linhagens com tolerância a toxicidade de alumínio, manganês e ferro em condições de campo. Bragantia 1995, 54, 81–93. [Google Scholar] [CrossRef] [Green Version]
- Camargo, C.E.D.O.; Felício, J.C.; De Freitas, J.G.; Filho, A.W.P.F. Tolerância de trigo, triticale e centeio a diferentes níveis de ferro em solução nutritiva. Bragantia 1988, 47, 295–304. [Google Scholar] [CrossRef] [Green Version]
- Keisling, T.C.; Thompson, L.F.; Slabaugh, W.R. Visual symptoms and tissue manganese concentrations associated with manganese toxicity in wheat. Commun. Soil Sci. Plant Anal. 1984, 15, 537–540. [Google Scholar] [CrossRef]
- Fernando, D.R.; Lynch, J.P. Manganese phytotoxicity: New light on an old problem. Ann. Bot. 2015, 116, 313–319. [Google Scholar] [CrossRef] [PubMed]
- Huang, H.; Zhao, Y.; Xu, Z.; Zhang, W.; Jiang, K. Physiological responses of Broussonetia papyrifera to manganese stress, a candidate plant for phytoremediation. Ecotoxicol. Environ. Saf. 2019, 181, 18–25. [Google Scholar] [CrossRef]
- Sparrow, L.; Uren, N. The role of manganese toxicity in crop yellowing on seasonally waterlogged and strongly acidic soils in north-eastern Victoria. Aust. J. Exp. Agric. 1987, 27, 303–307. [Google Scholar] [CrossRef]
- El-Jaoual, T.; Cox, D.A. Manganese toxicity in plants. J. Plant Nutr. 1998, 21, 353–386. [Google Scholar] [CrossRef]
- Doncheva, S.; Poschenrieder, C.; Stoyanova, Z.; Georgieva, K.; Velichkova, M.; Barceló, J. Silicon amelioration of manganese toxicity in Mn-sensitive and Mn-tolerant maize varieties. Environ. Exp. Bot. 2009, 65, 189–197. [Google Scholar] [CrossRef]
- de Vargas, J.P.; dos Santos, D.R.; Bastos, M.C.; Schaefer, G.; Parisi, P.B. Application forms and types of soil acidity corrective: Changes in depth chemical attributes in long term period experiment. Soil Tillage Res. 2019, 185, 47–60. [Google Scholar] [CrossRef]
- De Jesus, L.R.; Batista, B.L.; Lobato, A.K.D.S. Silicon reduces aluminum accumulation and mitigates toxic effects in cowpea plants. Acta Physiol. Plant. 2017, 39, 138. [Google Scholar] [CrossRef]
- Millaleo, R.; Diaz, M.R.-; Ivanov, A.G.; Mora, M.L.; Alberdi, M. Manganese as essential and toxic element for plants: Transport, accumulation and resistance mechanisms. J. Soil Sci. Plant Nutr. 2010, 10, 470–481. [Google Scholar] [CrossRef] [Green Version]
- Che, J.; Yamaji, N.; Shao, J.F.; Ma, J.F.; Shen, R.F. Silicon decreases both uptake and root-to-shoot translocation of manganese in rice. J. Exp. Bot. 2016, 67, 1535–1544. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Faria, J.M.; Teixeira, D.M.; Pinto, A.P.; Brito, I.; Barrulas, P.; Alho, L.; Carvalho, M. Toxic levels of manganese in an acidic Cambisol alters antioxidant enzymes activity, element uptake and subcellular distribution in Triticum aestivum. Ecotoxicol. Environ. Saf. 2020, 193, 110355. [Google Scholar] [CrossRef]
- Faria, J.; Teixeira, D.; Pinto, A.; Brito, I.; Barrulas, P.; Carvalho, M. The Protective Biochemical Properties of Arbuscular Mycorrhiza Extraradical Mycelium in Acidic Soils Are Maintained throughout the Mediterranean Summer Conditions. Agronomy 2021, 11, 748. [Google Scholar] [CrossRef]
- Faria, J.; Teixeira, D.; Pinto, A.P.; Brito, I.; Barrulas, P.; Carvalho, M. Arbuscular Mycorrhiza Inoculum Type Influences Phosphorus Subcellular Distribution in Shoots of Wheat Grown in Acidic Soil under Sustainble Agricultural Practices. In Proceedings of the 1st International Electronic Conference on Plant Science, Basel, Switzerland, 1–15 December 2020; p. 8596. [Google Scholar]
- Faria, J.M.S.; Pinto, A.P.; Teixeira, D.; Brito, I.; Carvalho, M. Diversity of Native Arbuscular Mycorrhiza Extraradical Mycelium Influences Antioxidant Enzyme Activity in Wheat Grown Under Mn Toxicity. Bull. Environ. Contam. Toxicol. 2021, 1–6. [Google Scholar] [CrossRef]
- Goss, M.J.; Carvalho, M.J.G.P.R. Manganese toxicity: The significance of magnesium for the sensitivity of wheat plants. Plant Soil 1992, 139, 91–98. [Google Scholar] [CrossRef]
- Goss, M.J.; Carvalho, M.J.G.P.R.; Cosimini, V.; Fearnhead, M.L. An approach to the identification of potentially toxic concentrations of manganese in soils. Soil Use Manag. 1992, 8, 40–43. [Google Scholar] [CrossRef]
- Le Bot, J.; Goss, M.; Carvalho, M.J.G.P.R.; Van Beusichem, M.L.; Kirkby, E.A. The significance of the magnesium to manganese ratio in plant tissues for growth and alleviation of manganese toxicity in tomato (Lycopersicon esculentum) and wheat (Triticum aestivum) plants. Plant Soil 1990, 124, 205–210. [Google Scholar] [CrossRef]
- Carvalho, M.; Goss, M.J.; Teixeira, D.M. Manganese toxicity in Portuguese Cambisols derived from granitic rocks: Causes, limitations of soil analyses and possible solutions. Rev. Cienc. Agrar. 2015, 38, 518–527. [Google Scholar] [CrossRef]
- Brito, I.; Carvalho, M.; Alho, L.; Goss, M. Managing arbuscular mycorrhizal fungi for bioprotection: Mn toxicity. Soil Biol. Biochem. 2014, 68, 78–84. [Google Scholar] [CrossRef] [Green Version]
- Zhang, H.; Guo, Q.; Yang, J.; Shen, J.; Chen, T.; Zhu, G.; Chen, H.; Shao, C. Subcellular cadmium distribution and antioxidant enzymatic activities in the leaves of two castor (Ricinus communis L.) cultivars exhibit differences in Cd accumulation. Ecotoxicol. Environ. Saf. 2015, 120, 184–192. [Google Scholar] [CrossRef]
- Khabaz-Saberi, H.; Rengel, Z. Aluminum, manganese, and iron tolerance improves performance of wheat genotypes in waterlogged acidic soils. J. Plant Nutr. Soil Sci. 2010, 173, 461–468. [Google Scholar] [CrossRef]
- Setter, T.; Waters, I.; Sharma, S.K.; Singh, K.N.; Kulshreshtha, N.; Yaduvanshi, N.P.S.; Ram, P.C.; Rane, J.; McDonald, G.; Khabaz-Saberi, H.; et al. Review of wheat improvement for waterlogging tolerance in Australia and India: The importance of anaerobiosis and element toxicities associated with different soils. Ann. Bot. 2008, 103, 221–235. [Google Scholar] [CrossRef] [Green Version]
- Wheeler, D.M.; Power, I.L. Comparison of plant uptake and plant toxicity of various ions in wheat. Plant Soil 1995, 172, 167–173. [Google Scholar] [CrossRef]
- Darkó, É.; Ambrus, H.; Stefanovits-Bányai, É.; Fodor, J.; Bakos, F.; Barnabás, B. 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. 2004, 166, 583–591. [Google Scholar] [CrossRef]
- Broadley, M.; Brown, P.; Cakmak, I.; Rengel, Z.; Zhao, F. Function of Nutrients: Micronutrients. Marschner’s Miner. Nutr. High. Plants 2012, 191–248. [Google Scholar] [CrossRef]
- Pinto, E.; Aguiar, A.; Ferreira, I. Influence of Soil Chemistry and Plant Physiology in the Phytoremediation of Cu, Mn, and Zn. Crit. Rev. Plant Sci. 2014, 33, 351–373. [Google Scholar] [CrossRef] [Green Version]
- Delhaize, E.; Gruber, B.; Ryan, P.R. The roles of organic anion permeases in aluminium resistance and mineral nutrition. FEBS Lett. 2007, 581, 2255–2262. [Google Scholar] [CrossRef] [Green Version]
- Pineros, M.; Cançado, G.M.; Kochian, L. Novel Properties of the Wheat Aluminum Tolerance Organic Acid Transporter (TaALMT1) Revealed by Electrophysiological Characterization in Xenopus Oocytes: Functional and Structural Implications. Plant Physiol. 2008, 147, 2131–2146. [Google Scholar] [CrossRef] [Green Version]
- Lambers, H.; Hayes, P.; Laliberté, E.; Oliveira, R.; Turner, B. Leaf manganese accumulation and phosphorus-acquisition efficiency. Trends Plant Sci. 2015, 20, 83–90. [Google Scholar] [CrossRef] [Green Version]
- Ghasemi-Fasaei, R.; Ronaghi, A. Interaction of Iron with Copper, Zinc, and Manganese in Wheat as Affected by Iron and Manganese in a Calcareous Soil. J. Plant Nutr. 2008, 31, 839–848. [Google Scholar] [CrossRef]
- Khabaz-Saberi, H.; Rengel, Z.; Wilson, R.; Setter, T.L. Variation for tolerance to high concentration of ferrous iron (Fe2+) in Australian hexaploid wheat. Euphytica 2009, 172, 275–283. [Google Scholar] [CrossRef]
- Castaings, L.; Caquot, A.; Loubet, S.; Curie, C. The high-affinity metal Transporters NRAMP1 and IRT1 Team up to Take up Iron under Sufficient Metal Provision. Sci. Rep. 2016, 6, 37222. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ishimaru, Y.; Bashir, K.; Nakanishi, H.; Nishizawa, N.K. OsNRAMP5, a major player for constitutive iron and manganese uptake in rice. Plant Signal. Behav. 2012, 7, 763–766. [Google Scholar] [CrossRef] [Green Version]
- Ishimaru, Y.; Masuda, H.; Bashir, K.; Inoue, H.; Tsukamoto, T.; Takahashi, M.; Nakanishi, H.; Aoki, N.; Hirose, T.; Ohsugi, R.; et al. Rice metal-nicotianamine transporter, OsYSL2, is required for the long-distance transport of iron and manganese. Plant J. 2010, 62, 379–390. [Google Scholar] [CrossRef] [PubMed]
- Barberon, M.; Dubeaux, G.; Kolb, C.; Isono, E.; Zelazny, E.; Vert, G. Polarization of IRON-REGULATED TRANSPORTER 1 (IRT1) to the plant-soil interface plays crucial role in metal homeostasis. Proc. Natl. Acad. Sci. USA 2014, 111, 8293–8298. [Google Scholar] [CrossRef] [Green Version]
- Cointry, V.; Vert, G. The bifunctional transporter-receptor IRT 1 at the heart of metal sensing and signalling. New Phytol. 2019, 223, 1173–1178. [Google Scholar] [CrossRef] [Green Version]
- Bhat, J.A.; Shivaraj, S.M.; Singh, P.; Navadagi, D.B.; Tripathi, D.K.; Dash, P.K.; Solanke, A.U.; Sonah, H.; Deshmukh, R. Role of Silicon in Mitigation of Heavy Metal Stresses in Crop Plants. Plants 2019, 8, 71. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rogalla, H.; Römheld, V. Role of leaf apoplast in silicon-mediated manganese tolerance of Cucumis sativus L. Plant Cell Environ. 2002, 25, 549–555. [Google Scholar] [CrossRef]
- Horst, W.J.; Fecht, M.; Naumann, A.; Wissemeier, A.H.; Maier, P. Physiology of manganese toxicity and tolerance in Vigna unguiculata (L.) Walp. J. Plant Nutr. Soil Sci. 1999, 162, 263–274. [Google Scholar] [CrossRef]
- Iwasaki, K.; Maier, P.; Fecht, M.; Horst, W.J. Leaf apoplastic silicon enhances manganese tolerance of cowpea (Vigna unguiculata). J. Plant Physiol. 2002, 159, 167–173. [Google Scholar] [CrossRef]
- Greger, M.; Landberg, T.; Vaculík, M. Silicon Influences Soil Availability and Accumulation of Mineral Nutrients in Various Plant Species. Plants 2018, 7, 41. [Google Scholar] [CrossRef] [Green Version]
- Sun, D.; Hussain, H.I.; Yi, Z.; Rookes, J.E.; Kong, L.; Cahill, D.M. Mesoporous silica nanoparticles enhance seedling growth and photosynthesis in wheat and lupin. Chemosphere 2016, 152, 81–91. [Google Scholar] [CrossRef]
- Alzahrani, Y.; Kuşvuran, A.; Alharby, H.F.; Kuşvuran, S.; Rady, M.M. The defensive role of silicon in wheat against stress conditions induced by drought, salinity or cadmium. Ecotoxicol. Environ. Saf. 2018, 154, 187–196. [Google Scholar] [CrossRef]
Element | mg MnCl2/kg Soil DW | ||
---|---|---|---|
µg/kg | 0.0 | 45.2 | 90.4 |
Mn | 642.0 ± 5.6 | 2247.4 ± 13.8 | 4152.8 ± 46.9 |
Al | 233.0 ± 3.4 | 264.8 ± 2.4 | 280.7 ± 4.1 |
Fe | 8.4 ± 0.0 | 8.7 ± 0.1 | 9.4 ± 0.0 |
Si | 768.7 ± 9.1 | 879.1 ± 13.9 | 996.8 ± 13.6 |
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Faria, J.M.S.; Teixeira, D.M.; Pinto, A.P.; Brito, I.; Barrulas, P.; Carvalho, M. Aluminium, Iron and Silicon Subcellular Redistribution in Wheat Induced by Manganese Toxicity. Appl. Sci. 2021, 11, 8745. https://doi.org/10.3390/app11188745
Faria JMS, Teixeira DM, Pinto AP, Brito I, Barrulas P, Carvalho M. Aluminium, Iron and Silicon Subcellular Redistribution in Wheat Induced by Manganese Toxicity. Applied Sciences. 2021; 11(18):8745. https://doi.org/10.3390/app11188745
Chicago/Turabian StyleFaria, Jorge M. S., Dora Martins Teixeira, Ana Paula Pinto, Isabel Brito, Pedro Barrulas, and Mário Carvalho. 2021. "Aluminium, Iron and Silicon Subcellular Redistribution in Wheat Induced by Manganese Toxicity" Applied Sciences 11, no. 18: 8745. https://doi.org/10.3390/app11188745
APA StyleFaria, J. M. S., Teixeira, D. M., Pinto, A. P., Brito, I., Barrulas, P., & Carvalho, M. (2021). Aluminium, Iron and Silicon Subcellular Redistribution in Wheat Induced by Manganese Toxicity. Applied Sciences, 11(18), 8745. https://doi.org/10.3390/app11188745