Abstract
Aluminum (Al) contamination in acidic soil is a major problem in paddy field, causing grain yield loss, especially in central plains of Thailand. The objective of this study was to assess Al content in the root tissues, its translocation to the leaves, and Al toxicity in three genotypes of rice, RD35 (local acidic-tolerant), Azucena (positive-check Al-tolerant), and IR64 (high yielding) under 0 (control) or 1 mM AlCl3 (Al toxicity) at pH 4.5. Al content in the root tissues of rice cv. RD35 under 1 mM AlCl3 was peaked at 4.18 mg g‒1 DW and significantly translocated to leaf tissues (0.35 mg g‒1 DW), leading to reduced leaf greenness (SPAD) (by 44.9% over the control) and declined net photosynthetic rate (Pn) (by 54.5% over the control). In contrast, Al level in cvs. Azucena and IR64 was restricted in the roots (2.12 mg g‒1 DW) with low amount of translocation in the leaf tissues (0.26 mg g‒1 DW), resulting in maintained values of SPAD and Pn. In cv. RD35, root and shoot traits including root length, root fresh weight, shoot height, shoot fresh weight, and shoot dry weight in 1 mM Al treatment were significantly dropped by > 35% over the control, whereas these parameters in cvs. Azucena and IR64 were retained. Based on the results, RD35 rice genotype was identified as Al sensitive as it demonstrated Al toxicity in both aboveground and belowground parts, whereas Azucena and IR64 were found tolerant to 1 mM Al as they demonstrated storage of Al in the root tissues to reduce toxicity in the leaf tissues. The study suggests that root traits, shoot attributes, chlorophyll degradation, and photosynthetic reduction can be successfully employed for the screening of Al-tolerant genotypes in rice breeding programs.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data are available from the authors if needed for review.
Code availability
(software application or custom code): Not applicable.
References
Ali, S., Zeng, F., Qiu, L., & Zhang, G. (2011). The effect of chromium and aluminum on growth, root morphology, photosynthetic parameters and transpiration of the two barley cultivars. Biologia Plantarum, 55, 291–296. https://doi.org/10.1007/s10535-011-0041-7
Alia, F. J., Shanshuddin, J., Fauziah, C. I., Ahmad Husni, M. H., & Panhwar, Q. A. (2015). Effects of aluminum, iron and/or low pH on rice seedlings grown in solution culture. International Journal of Agriculture and Biology, 17, 4. https://doi.org/10.17957/IJAB/14.0019
Alvarez, I., Sam, O., Reynaldo, I., Testillano, P. S., Risueño, M. C., & Aria, M. (2012). Morphological and cellular changes in rice roots (Oryza sativa L.) caused by Al stress. Botanical Studies, 53, 67–73.
Alvim, M. N., Ramos, F. T., Oliveira, D. C., Isaias, R. M. S., & Franca, M. G. C. (2012). Aluminum localization and toxicity symptoms related to root growth inhibition in rice (Oryza sativa L.) seedlings. Journal of Bioscience, 37, 1079–1088. https://doi.org/10.1007/s12038-012-9275-6
Arunakumara, K. K. I. U., Walpola, B. C., & Yoon, M. H. (2013). Aluminum toxicity and tolerance mechanism in cereals and legumes—a review. Journal of the Korean Society for Applied Biological Chemistry, 56, 1–9. https://doi.org/10.1007/s13765-012-2314-z
Awasthi, J. P., Saha, B., Regon, P., Sahoo, S., Chowra, U., Pradhan, A., Roy, A., & Panda, S. K. (2017). Morpho-physiological analysis of tolerance to aluminum toxicity in rice varieties of Northeast India. PLoS ONE, 12, e0176357. https://doi.org/10.1371/journal.pone.0176357
Awasthi, J. P., Saha, B., Panigrahi, J., Yanase, E., Koyama, H., & Panda, S. K. (2019). Redox balance, metabolic fingerprint and physiological characterization in contrasting Northeast Indian rice for aluminum stress tolerance. Scientific Reports, 9, 1–21. https://doi.org/10.1038/s41598-019-451583-3
Barker, A.V., & Pilbeam, D.J. (2007). Handbook of Plant Nutrition, 1st edition 613. CRC/Taylor and Francis.
Bhoomika, K., Pyngrope, S., & Dubey, R. S. (2013). Differential responses of antioxidant enzymes to aluminum toxicity in two rice (Oryza sativa L.) cultivars with marked presence and elevated activity of Fe-SOD and enhanced activities of Mn-SOD and catalase in aluminum tolerant cultivar. Plant Growth Regulation, 71, 235–252. https://doi.org/10.1007/s10725-013-9824-5
Bian, M., Zhou, M., Sun, D., & Li, C. (2013). Molecular approaches unravel the mechanism of acid soil tolerance in plants. The Crop Journal, 1, 91–104. https://doi.org/10.1016/j.cj.2013.08.002
Bidhan, R. O. Y., & Bhadra, S. (2014). Effects of toxic levels of aluminium on seedling parameters of rice under hydroponic culture. Rice Science, 21, 217–223. https://doi.org/10.1016/S1672-6308(13)60182-1
Chang, S., Jing-hao, W., Gao-ling, S., Lai-qing, L., Jun-xia, D., Jian-lin, W., & Qing-sheng, C. (2015). Different aluminum tolerance among indica, japonica and hybrid rice varieties. Rice Science, 22, 123–131. https://doi.org/10.1016/j.rsci.2015.05.016
Cha-um, S., Supaibulwatana, K., & Kirdmanee, C. (2006). Water relation, photosynthetic ability and growth of Thai jasmine rice (Oryza sativaL.ssp.indica cv. KDML 105) to salt stress by application of exogenous glycinebetaine and choline. Journal of Agronomy and Crop Science, 192, 25–36. https://doi.org/10.1111/j.1439-037X.2006.00186.x
de Freitas, L. B., Fernandes, D. M., Maia, S., Moniz, A., Mazziero, B. G., & Steiner, F. (2019). Sources and doses of aluminum in experiments with rice in nutrient solution. Revista Brasileira de Engenharia Agrícola e Ambiental, 23, 511–517. https://doi.org/10.1590/1807-1929/agriambi.v23n7p511-517
Elisa, A. A., Ninomiya, S., Shamshuddin, J., & Roslan, I. (2016). Alleviating aluminum toxicity in an acid sulfate soil from Peninsular Malaysia by calcium silicate application. Solid Earth, 7, 367–374. https://doi.org/10.5194/se-7-367-2016
Frankowski, M. (2016). Aluminum uptake and migration from the soil compartment into Betula pendula for two different environments: A polluted and environmentally protected area of Poland. Environmental Science and Pollution Research, 23, 1398–1407. https://doi.org/10.1007/s11356-015-5367-9
Guo, T. R., Yao, P. C., Zhang, Z. D., Wang, J. J., & Mei, W. (2012). Involvement of antioxidative defense system in rice seedlings exposed to aluminum toxicity and phosphorus deficiency. Rice Science, 19, 207–212. https://doi.org/10.1016/S1672-6308(12)60042-0
Huang, C. F., Yamaji, N., Nishimura, M., Tajima, S., & Ma, J. F. (2009). A rice mutant sensitive to Al toxicity is defective in the specification of root outer cell layers. Plant and Cell Physiology, 50, 976–985. https://doi.org/10.1093/pcp/pcp050
Hussain, F., Bronson, K. F., & Peng, S. (2000). Use of chlorophyll meter sufficiency indices for nitrogen management of irrigated rice in Asia. Agronomy Journal, 92, 875–879. https://doi.org/10.2134/agronj2000.925875x
IRRI (2002). Standard evaluation system for rice. International Rice Research Institute. The Philippines.
Jahan, N., Abd Manan, F., Mansoor, A., Zaidi, M. A., Shahwani, M. N., & Javed, M. A. (2018). Development of novel protocol to Al3+ stress tolerance at germination stage in indica rice through statistical approaches. The Scientific World Journal, 2018, 8180174. https://doi.org/10.1155/2018/8180174
Jahan, N., Javed, M. A., Khan, A., Manan, F. A., & Tabassum, B. (2021). Genetic architecture of Al3+ toxicity tolerance in rice F2:3 populations determined through QTL mapping. Ecotoxicology, 30, 794–805. https://doi.org/10.1007/s10646-021-02413-6
Kang, D. J., Futakuchi, K., Seo, Y. J., Vijarnsorn, P., & Ishii, R. (2012). Evaluation of Al-tolerance on upland and lowland types of NERICA lines under hydroponic conditions. Journal of Crop Science and Biotechnology, 15, 25–31. https://doi.org/10.1007/s12892-011-0083-6
Khush, G. S. (2005). What it will take to feed 5.0 billion rice consumers in 2030? Plant Molecular Biology, 59, 1–6. https://doi.org/10.1007/s11103-005-2159-5
Klug, B., Specht, A., & Horst, W. J. (2011). Aluminum localization in root tips of the aluminium-accumulating plant species buckwheat (Fagopyrum esculentum Moench). Journal of Experimental Botany, 62, 5453–5462. https://doi.org/10.1093/jxb/err222
Kochian, L. V., Hoekenga, O. A., & Pineros, M. A. (2004). How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annual Review of Plant Biology, 55, 459–493. https://doi.org/10.1146/annurev.arplant.55.031903.141655
Kumar, A., Pandey, A., & Pattanayak, A. (2013). Evaluation of rice germplasm under jhum cultivation in Northeast India and breeding for aluminium tolerance. Indian Journal of Genetics, 73, 153–161. https://doi.org/10.5958/j.0975-6906.73.2.022
Kuo, M. C., & Kao, C. H. (2003). Aluminum effects on lipid peroxidation and antioxidative enzyme activities in rice leaves. Biologia Plantarum, 46, 149–152. https://doi.org/10.1023/A:1022356322373
Li, W., Du, J., Feng, H., Wu, Q., Xu, G., Shabala, S., & Yu, L. (2020). Function of NHX-type transporters in improving rice tolerance to aluminum stress and soil acidity. Planta, 251, 1–13. https://doi.org/10.1007/s00425-020-03361-x
Loggini, B., Scartazza, A., Brugnoli, E., & Navari-Izzo, F. (1999). Antioxidant defense system, pigment composition, and photosynthetic efficiency in two wheat cultivars subjected to drought. Plant Physiology, 119, 1091–1099. https://doi.org/10.1104/pp.119.3.1091
Lu, H. L., Dong, G., Hua, H., Zhao, W. R., Li, J. Y., & Xu, R. K. (2020). Method for initially selecting Al-tolerant rice varieties based on the charge characteristics of their roots. Ecotoxicology and Environmental Safety, 187, 109813. https://doi.org/10.1016/j.ecoenv.2019.109813
Ma, J. F. (2000). Role of organic acids in detoxification of aluminum in higher plants. Plant and Cell Physiology, 41, 383–390. https://doi.org/10.1093/pcp/41.4.383
Ma, J. F. (2007). Syndrome of aluminum toxicity and diversity of aluminum resistance in higher plants. International Review of Cytology, 264, 225–252. https://doi.org/10.1016/S0074-7696(07)64005-4
Ma, J. F., Shen, R., Zhao, Z., Wissuwa, M., Takeuchi, Y., Ebitani, T., & Yano, M. (2002). Response of rice to Al stress and identification of quantitative trait loci for Al tolerance. Plant and Cell Physiology, 43, 652–659. https://doi.org/10.1093/pcp/pcf081
Maxwell, K., & Johnson, G. N. (2000). Chlorophyll fluorescence—A practical guide. Journal of Experimental Botany, 51, 659–668. https://doi.org/10.1093/jexbot/51.345.659
Meriga, B., Reddy, B. K., Rao, K. R., Reddy, L. A., & Kishor, P. K. (2004). Aluminium-induced production of oxygen radicals, lipid peroxidation and DNA damage in seedlings of rice (Oryza sativa). Journal of Plant Physiology, 161, 63–68. https://doi.org/10.1078/0176-1617-01156
Mishra, P., & Dubey, R. S. (2008). Effect of aluminium on metabolism of starch and sugars in growing rice seedlings. Acta Physiologiae Plantarum, 30, 265–275. https://doi.org/10.1007/s11738-007-0115-5
Munde, N. A., Jadhao, K. R., Samal, K. C., Pradhan, S. K., & Rout, G. R. (2016). Allele mining in Indica rice (Oryza sativa L.) for ATP binding cassette (ABC) transporter gene family for aluminum tolerance. Indian Journal of Plant Physiology, 21, 161–170. https://doi.org/10.1007/s40502-016-0217-4
Nagasaka, S., Teraoka, T., Matsumoto, S., Mori, S., & Yoshimura, E. (2003). Difference in Al sensitivity between seminal and crown roots of rice nursery seedlings. Soil Science and Plant Nutrition, 49, 897–902. https://doi.org/10.1080/00380768.2003.10410353
Nguyen, V. T., Burow, M. D., Nguyen, H. T., Le, B. T., Le, T. D., & Paterson, A. H. (2001). Molecular mapping of genes conferring aluminum tolerance in rice (Oryza sativa L.). Theoretical and Applied Genetics, 102, 1002–1010. https://doi.org/10.1007/s001220000472
Pan, W., Shou, J., Zhou, X., Zha, X., Guo, T., Zhu, M., & Pan, J. (2011). Al-induced cell wall hydroxyproline-rich glycoprotein accumulation is involved in alleviating Al toxicity in rice. Acta Physiologiae Plantarum, 33, 601–608. https://doi.org/10.1007/s11738-010-0684-6
Pandey, P., Srivastava, R. K., Rajpoot, R., Rani, A., Pandey, A. K., & Dubey, R. S. (2016). Water deficit and aluminum interactive effects on generation of reactive oxygen species and responses of antioxidative enzymes in the seedlings of two rice cultivars differing in stress tolerance. Environmental Science and Pollution Research, 23, 1516–1528. https://doi.org/10.1007/s11356-015-5392-8
Peixoto, H. P., da Matta, F. M., & da Matta, J. C. (2002). Responses of the photosynthetic apparatus to aluminum stress in two sorghum cultivars. Journal of Plant Nutrition, 25, 821–832. https://doi.org/10.1081/PLN-120002962
Phukunkamkaew, S., Tisarum, R., Pipatsitee, P., Samphumphuang, T., Maksup, S., & Cha-um, S. (2021). Morpho-physiological responses of indica rice (Oryza sativa sub. indica) to aluminum toxicity at seedling stage. Environmental Science and Pollution Research, 28, 29321–29331. https://doi.org/10.1007/s11356-021-12804-1
Shen, R., & Ma, J. F. (2001). Distribution and mobility of aluminum in an Al-accumulating plant, Fagopyrum esculentum Moench. Journal of Experimental Botany, 52, 1683–1687. https://doi.org/10.1093/jexbot/52.361.1683
Shetty, R., & Prakash, N. B. (2020). Effect of different biochars on acid soil and growth parameters of rice plants under aluminium toxicity. Scientific Reports, 10, 1–10. https://doi.org/10.1038/s41598-020-69262-x
Shetty, R., Vidya, C. S. N., Prakash, N. B., Lux, A., & Vaculík, M. (2020). Aluminum toxicity in plants and its possible mitigation in acid soils by biochar: A review. Science of the Total Environment, 765, 142744. https://doi.org/10.1016/j.scitotenv.2020.142744
Soomro, A. A., Abro, M. A., Leghari, N., Leghari, G. M., & Soomro, A. A. (2015). Evaluation of aluminum toxicity tolerance in rice (Oryza sativa L.). Science International, 27, 2251–2255.
Tarantino, T. B., Barbosa, I. S., Lima, D. D. C., Pereira, M. D. G., Teixeira, L. S., & Korn, M. G. A. (2017). Microwave-assisted digestion using diluted nitric acid for multi-element determination in rice by ICP OES and ICP-MS. Food Analytical Methods, 10, 1007–1015. https://doi.org/10.1007/s12161-016-0658-4
Tisarum, R., Pongprayoon, W., Sithtisarn, S., Sampumphuang, T., Sotesaritkul, T., Datta, A., Singh H. P., & Cha-um, S. (2021). Expression levels of genes involved in metal homeostasis, physiological adaptation, and growth characteristics of rice (Oryza sativa L.) genotypes under Fe and/or Al toxicity. Protoplasma, 1–16. https://doi.org/10.1007/s00709-021-01719-w
Tsutsui, T., Yamaji, N., Huang, C. F., Motoyama, R., Nagamura, Y., & Ma, J. F. (2012). Comparative genome-wide transcriptional analysis of Al-responsive genes reveals novel Al tolerance mechanisms in rice. PLoS ONE, 7, e48197. https://doi.org/10.1371/journal.pone.0048197
Wang, J. W., & Kao, C. H. (2004). Reduction of aluminum-inhibited root growth of rice seedlings with supplemental calcium, magnesium and organic acids. Crop, Environment and Bioinformatics, 1, 191–198. https://doi.org/10.30061/CEB.200409.0004
Wang, J. W., & Kao, C. H. (2005). Effect of aluminium on endosperm reserve mobilization in germinating rice grains. Biologia Plantarum, 49, 405–409. https://doi.org/10.1007/s10535-005-0015-8
Wang, J. W., & Kao, C. H. (2006). Aluminum-inhibited root growth of rice seedlings is mediated through putrescine accumulation. Plant and Soil, 288, 373–381. https://doi.org/10.1007/s11104-006-9127-y
Wang, J. W., & Kao, C. H. (2007). Protective effect of ascorbic acid and glutathione on AlCl3-inhibited growth of rice roots. Biologia Plantarum, 51, 493–500. https://doi.org/10.1007/s10535-007-0104-y
Xue, Y., Wan, J., Jiang, L., Wang, C., Liu, L., Zhang, Y. M., & Zhai, H. (2006a). Identification of quantitative trait loci associated with aluminum tolerance in rice (Oryza sativa L.). Euphytica, 150, 37–45. https://doi.org/10.1007/s10681-006-9089-4
Xue, Y., Wan, J. M., Jiang, L., Liu, L. L., Su, N., Zhai, H. Q., & Ma, J. F. (2006b). QTL analysis of aluminum resistance in rice (Oryza sativa L.). Plant and Soil, 287, 375–383. https://doi.org/10.1007/s11104-006-9086-3
Yan, L., Riaz, M., Liu, J., Yu, M., & Cuncang, J. (2021). The aluminum tolerance and detoxification mechanisms in plants; recent advances and prospects. Critical Reviews in Environmental Science and Technology, 1–37,. https://doi.org/10.1080/10643389.2020.1859306
Yang, J. L., Li, Y. Y., Zhang, Y. J., Zhang, S. S., Wu, Y. R., Wu, P., & Zheng, S. J. (2008). Cell wall polysaccharides are specifically involved in the exclusion of aluminum from the rice root apex. Plant Physiology, 146, 602–611. https://doi.org/10.1104/pp.107.111989
Zhang, C., Wu, P., Tang, C., Tao, X., Han, Z., Sun, J., & Liu, H. (2013). The study of soil acidification of paddy field influenced by acid mine drainage. Environmental Earth Sciences, 70, 2931–2940. https://doi.org/10.1007/s12665-013-2351-x
Zhang, F., Yan, X., Han, X., Tang, R., Chu, M., Yang, Y., Yang, Y. H., Zhao, F., Fu, A., Luan, S., & Lan, W. (2019). A defective vacuolar proton pump enhances aluminum tolerance by reducing vacuole sequestration of organic acids. Plant Physiology, 181, 743–761. https://doi.org/10.1104/pp.19.00626
Zhu, C. Q., Hu, W. J., Cao, X. C., Zhu, L. F., Bai, Z. G., Huang, J., Liang, Q. D., Jin, Q. Y., & Zhang, J. H. (2020). Role of salicylic acid in alleviating the inhibition of root elongation by suppressing ethylene emission in rice under Al toxicity conditions. Plant Growth Regulation, 90, 475–487. https://doi.org/10.1007/s10725-019-00554-7
Funding
This work was supported by The National Science and Technology Development Agency (NSTDA) (Grant Number P-18-51456) and partially supported post-graduated scholarship for Suwanna Phukunkamkaew by the Thailand Graduate Institute of Science and Technology (TGIST).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by SP, RT, and TS. The first draft of the manuscript was written by SM and SC, as well as grammatical proofreading with context editing by HPS, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare they have no financial interests.
Consent to participate
All the authors consent to participate.
Consent to publish
All the authors consent to publish the manuscript.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Phukunkamkaew, S., Tisarum, R., Sotesaritkul, T. et al. Aluminum uptake, translocation, physiological changes, and overall growth inhibition in rice genotypes (Oryza sativa) at vegetative stage. Environ Geochem Health 45, 187–197 (2023). https://doi.org/10.1007/s10653-022-01291-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10653-022-01291-z