Abstract
Acid soils with elevated aluminum (Al) saturations are worldwide distributed and harm the crop production in most of the tropical and subtropical regions. The initial and most dramatic symptoms of Al toxicity are changes on the external morphology and inhibition of elongation of roots. These changes have served as a marker for level of Al toxicity and the ability of plants tolerate this metal. Therefore, the goal of this study was to evaluate the Al effects on the growth root and the external morphology of root tips in two rice genotypes: Fernandes (CNA-1158) and Maravilha (CNA-6843-1), tolerant and sensitive to Al, respectively. The genotypes were treated with 0 and 1 mM of Al in Clark’s solution for different times (3, 6 and 9 days). The contents and the distribution of Al in root tips, as well as its morphology, were analyzed. After Al exposure, the content of this metal was higher in Al-sensitive genotype leading to inhibition of root length and decrease in root dry matter production, after the sixth day of treatment. Additionally, Al accumulation in the root tips (0–3 mm) of both genotypes was detected mainly in root cap cells. We also observed damage in the external micromorphology of the root tips, especially in the Al-sensitive Maravilha genotype. Al accumulation in root tips of this genotype induced cellular disorganization in the root cap cells, resulting in the peeling of the superficial layers. Overall, our findings evidenced the higher tolerance of one of genotypes (genotype Fernandes) to Al.
References
Čiamporová M (2002) Morphological and structural responses of plant roots to aluminium at organ, tissue, and cellular levels. Biol Plant 45:161–171
Clark RB (1975) Characterization of phosphatase of intact maize roots. J Agric Food Chem 23:458–460. https://doi.org/10.1021/jf60199a002
de Souza LT, Cambraia J, Ribeiro C et al (2015) Effects of aluminum on the elongation and external morphology of root tips in two maize genotypes. Bragantia 75:19–25. https://doi.org/10.1590/1678-4499.142
dos Reis AR, Lisboa LAM, Reis HPG et al (2018) Depicting the physiological and ultrastructural responses of soybean plants to Al stress conditions. Plant Physiol Biochem 130:377–390. https://doi.org/10.1016/j.plaphy.2018.07.028
Famoso AN, Clark RT, Shaff JE et al (2010) Development of a novel aluminum tolerance phenotyping platform used for comparisons of cereal aluminum tolerance and investigations into rice aluminum tolerance mechanisms. Plant Physiol 153:1678–1691. https://doi.org/10.1104/pp.110.156794
He HY, He LF, Gu MH, Li XF (2012) Nitric oxide improves aluminum tolerance by regulating hormonal equilibrium in the root apices of rye and wheat. Plant Sci 183:123–130. https://doi.org/10.1016/j.plantsci.2011.07.012
Jaskowiak J, Kwasniewska J, Milewska-Hendel A et al (2019) Aluminum alters the histology and pectin cell wall composition of barley roots. Int J Mol Sci 20:1–18. https://doi.org/10.3390/ijms20123039
Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol Plant Mol Biol 46:237–260. https://doi.org/10.1146/annurev.pp.46.060195.001321
Kochian LV, Piñeros MA, Liu J, Magalhaes JV (2015) Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Annu Rev Plant Biol 66:571–598. https://doi.org/10.1146/annurev-arplant-043014-114822
Kopittke PM, Moore KL, Lombi E et al (2015) Identification of the primary lesion of toxic aluminum in plant roots. Plant Physiol 167:1402–1411. https://doi.org/10.1104/pp.114.253229
Kusunoki K, Kobayashi Y, Kobayashi Y, Koyama H (2018) Comparative characterization of aluminum responsive transcriptome in Arabidopsis roots: comparison with other rhizotoxic ions at different stress intensities. Soil Sci Plant Nutr 64:469–481. https://doi.org/10.1080/00380768.2018.1454253
Liu MY, Lou HQ, Chen WW et al (2018) Two citrate transporters coordinately regulate citrate secretion from rice bean root tip under aluminum stress. Plant, Cell Environ 41:809–822. https://doi.org/10.1111/pce.13150
Nagayama T, Nakamura A, Yamaji N et al (2019) Changes in the distribution of pectin in root border cells under aluminum stress. Front Plant Sci 10:1216. https://doi.org/10.3389/fpls.2019.01216
Okamoto K, Yano K (2017) Al resistance and mechanical impedance to roots in Zea mays: reduced Al toxicity via enhanced mucilage production. Rhizosphere 3:60–66. https://doi.org/10.1016/j.rhisph.2016.12.005
Pirzadah TB, Malik B, Tahir I et al (2019) Aluminium stress modulates the osmolytes and enzyme defense system in Fagopyrum species. Plant Physiol Biochem 144:178–186. https://doi.org/10.1016/j.plaphy.2019.09.033
Ribeiro C, Cambraia J, Peixoto PHP, da Fonseca Júnior ÉM (2012) Antioxidant system response induced by aluminum in two rice cultivars. Braz J Plant Physiol 24:107–116. https://doi.org/10.1590/S1677-04202012000200004
Singh S, Tripathi DK, Singh S et al (2017) Toxicity of aluminium on various levels of plant cells and organism: a review. Environ Exp Bot 137:177–193. https://doi.org/10.1016/j.envexpbot.2017.01.005
Tahara K, Yamanoshita T, Norisada M et al (2008) Aluminum distribution and reactive oxygen species accumulation in root tips of two Melaleuca trees differing in aluminum resistance. Plant Soil 307:167–178. https://doi.org/10.1007/s11104-008-9593-5
Wang YS, Yang ZM (2005) Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L. Plant Cell Physiol 46:1915–1923. https://doi.org/10.1093/pcp/pci202
Yang JL, Ying YL, Zhang YJ et al (2008) Cell wall polysaccharides are specifically involved in the exclusion of aluminum from the rice root apex. Plant Physiol 146:602–611. https://doi.org/10.1104/pp.107.111989
Yang Z-B, He C, Ma Y et al (2017a) Jasmonic acid enhances Al-induced root growth inhibition. Plant Physiol 173:1420–1433. https://doi.org/10.1104/pp.16.01756
Yang Z, Liu G, Liu J et al (2017b) Synergistic action of auxin and cytokinin mediates aluminum-induced root growth inhibition in Arabidopsis. EMBO Rep 18:1213–1230. https://doi.org/10.15252/embr.201643806
Zhang M, Lu X, Li C et al (2018) Auxin efflux carrier ZmPGP1 mediates root growth inhibition under aluminum stress. Plant Physiol 177:819–832. https://doi.org/10.1104/pp.17.01379
Acknowledgements
The authors would like to thank the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) for financial support and the Conselho Nacional de Desenvolvimento Científico Tecnológico (CNPq) for fellowships. Also, we thank the Nucleus of Microscopy and Microanalysis at the Federal University of Viçosa for providing the equipment for experiments.
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C.R. and D.S.B. designed the study. D.S.B., R.N-S. and P.H.P.P performed the experiments and analyzed the data. K.V.G.R. and C.R. participated in the analyses involving micromorphology and microanalyses of root tips. C.R., K.V.G.R and D.S.B wrote the manuscript. All authors read and approved the final manuscript.
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Brito, D.S., Neri-Silva, R., Ribeiro, K.V.G. et al. Effects of aluminum on the external morphology of root tips in rice. Braz. J. Bot 43, 413–418 (2020). https://doi.org/10.1007/s40415-020-00620-9
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DOI: https://doi.org/10.1007/s40415-020-00620-9