Co-inoculation of Azospirillum brasilense and AMF in the development and copper content in maize and sorghum grown in contaminated soil
DOI:
https://doi.org/10.5433/1679-0359.2024v45n6p1957Keywords:
Contamination, Microorganisms, Sorghum bicolor, Zea mays.Abstract
Copper contamination has increased in soils subjected to the application of fungicides and organic fertilizers, including areas under maize and sorghum cultivation. Arbuscular mycorrhizal fungi (AMF) and Azospirillum brasilense bacteria have shown promise in promoting plant growth and could be an alternative for plant development in copper-contaminated soils. This study aimed to determine the influence of co-inoculation with AMF and Azospirillum brasilense on the development and copper levels in sorghum and maize plants cultivated in contaminated soil. The experimental design was completely randomized with a factorial arrangement (6x2), involving six inoculum sources (Acaulospora scrobiculata; Rhizoglomus clarum; Azospirillum brasilense; Acaulospora scrobiculata + Azospirillum brasilense; Rhizoglomus clarum + Azospirillum brasilense; and a control without inoculation) in soil with and without the addition of 400 mg kg-1 of Cu, with seven replications. The following parameters were evaluated: Plant height, culm diameter, number of tillers, root volume, chlorophyll a and b, leaf area, shoot dry mass, root dry mass, copper content in grains, shoot, and roots, mycorrhizal colonization, and the most probable number of A. brasilense in the roots. According to the results, the inoculum sources exhibited different significant interactions in the evaluations, depending on the crop and the Cu dose applied to the soil. Inoculation with A. scrobiculata in Cu-contaminated soils favored root growth, dry mass, and mycorrhizal colonization in sorghum. In contrast, the use of R. clarum resulted in better development of maize shoots. Regarding isolated inoculation and co-inoculations between A. brasilense and AMF, we found that these reduced the Cu content in the sorghum shoots to levels below Brazilian legislation, thus representing a potential for cultivation in soils with excess copper.
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References
Agência Nacional de Vigilância Sanitária (1998). Ministério da saúde. Portaria nº 30, de 13 de janeiro de 1998. ANVISA.
Agência Nacional de Vigilância Sanitária (2019). Ministério da saúde. Resolução da Diretoria Colegiada - RDC Nº 329, de 19 de dezembro de 2019. ANVISA.
Alemneh, A. A., Zhou, Y., Ryder, M. H., & Denton, M. D. (2022). Soil environment influences plant growth-promotion traits of isolated rhizobacteria. Pedobiologia, 90 (150785), 150785. doi: 10.1016/j.pedobi.2021.150785 DOI: https://doi.org/10.1016/j.pedobi.2021.150785
Alghamdi, A. G., & Alasmary, Z. (2022). Fate and transport of lead and copper in calcareous soil. Sustainability, 15(1), 775. doi: 10.3390/su15010775 DOI: https://doi.org/10.3390/su15010775
Andreazza, R., Camargo, F. A. O., Antoniolli, Z. I., Quadro, M. S., & Barcelos, A. (2013). A biorremediação de áreas contaminadas com cobre. Revista de Ciências Agrárias, 36(2), 127-136. doi: 10.19084/rca.16290
Benimeli, C. S., Medina, A., Navarro, C. M., Medina, R. B, Amoroso, M. J., & Gómez, M. I. (2010). Bioaccumulation of copper by Zea mays: impact on root, shoot and leaf growth. Water Air Soil Pollut, 210, 365-370. doi: 10.1007/s11270-009-0259-6 DOI: https://doi.org/10.1007/s11270-009-0259-6
Bisca, H. H., Machado, M. J., Costa, I. da, & Souza, D. S. (2023). Fungos micorrízicos arbusculares associados a dose de fósforo no crescimento da cultura do milho. Revista em Agronegócio e Meio Ambiente, 16(3), 1-13. doi: 10.17765/2176-9168.2023v16n3e11059 DOI: https://doi.org/10.17765/2176-9168.2023v16n3e11059
Blandino, M., Scapino, M., Rollè, L., Dinuccio, E., & Reyneri, A. (2023). Biomass and methane production in double cereal cropping systems with different winter cereal and maize plant densities. Agronomy, 13(2), 536. doi: 10.3390/agronomy13020536 DOI: https://doi.org/10.3390/agronomy13020536
Bourles, A., Guentas, L., Charvis, C., Gensous, S., Majorel, C., Crossay, T., Cvaloc, Y., Burtet-Sarramegna, V., Jourand, P., & Amir, H. (2020). Co-inoculation with a bacterium and arbuscular mycorrhizal fungi improves root colonization, plant mineral nutrition, and plant growth of a Cyperaceae plant in an ultramafic soil. Mycorrhiza, 30(1), 121-131. doi: 10.1007/s00572-019-00929-8 DOI: https://doi.org/10.1007/s00572-019-00929-8
Brasil, C., Matsumoto, L. S., Nogueira, M. A., Spago, F. R., Rampazo, L. G., Cruz, M. F., & Andrade, G. (2006). Effect of Bacillus thuringiensis on microbial functional groups in sorghum rhizosphere. Pesquisa Agropecuária Brasileira, 41(5), 873-877. doi: 10.1590/S0100-204X2006000500022 DOI: https://doi.org/10.1590/S0100-204X2006000500022
Cahyaningtyas, A., & Ezawa, T. (2023). Disturbance tolerance of arbuscular mycorrhizal fungi: characterization of life-history strategies along a disturbance gradient in a coastal dune ecosystem. Plant and Soil, 495, 1-15. doi: 10.1007/s11104-023-06337-4 DOI: https://doi.org/10.1007/s11104-023-06337-4
Cipoleta, N. S., Silva, L. F. S., & Lopes-Assad, M. L. R. C. (2019). Uso de resíduos orgânicos na atenuação de contaminação por cobre de Calda Bordalesa. Ambiência, 15(2), 289-307. doi: 10.5935/ambiencia.2019.02.01 DOI: https://doi.org/10.5935/ambiencia.2019.02.01
Damin, S., Carrenho, R., & Martins, S. (2020). The influence of mycorrhization on the growth of Zea mays L. and the sclerifcation of foliar tissues susceptible to chewing insect attacks. Brazilian Journal of Botany, 43(3), 493-502. doi: 10.1007/s40415-020-00621-8 DOI: https://doi.org/10.1007/s40415-020-00621-8
Dhalaria, R., Kumar, D., Kumar, H., Nepovimova, E., Kuča, K., Torequl Islam, M., & Verma, R. (2020). Arbuscular mycorrhizal fungi as potential agents in ameliorating heavy metal stress in plants. Agronomy, 10(6), 815. doi: 10.3390/agronomy10060815 DOI: https://doi.org/10.3390/agronomy10060815
Dhawi, F., Datta, R., & Ramakrishna, W. (2015). Mycorrhiza and PGPB modulate maize biomass, nutrient uptake and metabolic pathways in maize grown in mining-impacted soil. Plant Physiology and Biochemistry, 97(1), 390-399. doi: 10.1016/j.plaphy.2015.10.028 DOI: https://doi.org/10.1016/j.plaphy.2015.10.028
Dobereiner, J., Baldani, V. L. D., & Baldani, J. I. (1995). Como isolar e identificar bactérias diazotróficas de plantas não leguminosas. Empresa Brasileira de Pesquisa Agropecuária, CNPAB.
Eid, E. M., Shaltout, K. H., & Alamri, S. A. M. (2021). Monitored sewage sludge application improves soil quality, enhances plant growth, and provides evidence for metal remediation by Sorghum bicolor L. Journal Soil Science and Plant Nutrition, 21(3), 2325-2338. doi: 10.1007/s42729-021-00524 DOI: https://doi.org/10.1007/s42729-021-00524-x
Ferreira, D. F. (2011). S–SVAR - Sistema de análise de variância. Versão 5.3. UFLA.
Fukami, J., Cerezini, P., & Hungria, M. (2018). Azospirillum: benefits that go far beyond biological nitrogen fixation. AMB Express, 8(73), 1-12. doi: 10.1186/s13568-018-0608-1 DOI: https://doi.org/10.1186/s13568-018-0608-1
Giatti, A. B. P., & Piza, M. L. S. T. (2022). Avaliação do uso de Azospirillum brasilense na produtividade do Capim Mavuno (Urochloa brizantha cv. Marandu x Urochloa ruziziensis). Revista AgroFIB, 2, 105-116. doi: 10.59237/agrofib.v2i.576 DOI: https://doi.org/10.59237/agrofib.v2i.576
Giovanetti, M., & Mosse, B. (1980). An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytologist, 84(3), 489-500. doi: 10.1111/j.1469-8137.1980.tb04556.x DOI: https://doi.org/10.1111/j.1469-8137.1980.tb04556.x
Krämer, U. (2010). Metal hyperaccumulation in plants. Annual Review of Plant Biology, 61, 517-534. doi: 10.1146/annurev-arplant-042809-112156 DOI: https://doi.org/10.1146/annurev-arplant-042809-112156
Li, X. Y., Lin, M. L., Lu, F., Zhou, X., Xiong, X., Chen, L. S., & Huang, Z. R. (2023). Physiological and ultrastructural responses to excessive-copper-induced toxicity in two differentially copper tolerant citrus species. Plants, 12(2), 351. doi: 10.3390/plants12020351 DOI: https://doi.org/10.3390/plants12020351
Longhini, V. Z., Souza, W. C. R., Andreotti, M., Soares, N. A., & Costa, N. R. (2016). Inoculation of diazotrophic bacteria and nitrogen fertilization in topdressing in irrigated corn. Revista Caatinga, 29(2), 338-347. doi: 10.1590/1983-21252016v29n210rc. DOI: https://doi.org/10.1590/1983-21252016v29n210rc
Manual de Calagem e Adubação para os Estados do Rio Grande do Sul e de Santa Catarina (2016). Sociedade brasileira de ciência do solo. Núcleo Regional Sul.
Menezes, C. B., Fernandes, E. A., Parrella, R. A. C., Schaffert, R. E., & Rodrigues, J. A. S. (2021). Importância do sorgo para o abastecimento de grãos, forragem e bioenergia no Brasil. In C. B. Menezes, de (Ed.), Melhoramento Genético de Sorgo (Cap.1, pp. 14-58). Brasília, DF. http://www.alice.cnptia.embrapa.br/alice/handle/doc/1138157
Mir, A. R., Pichtel, J., & Hayat, S. (2021). Copper: uptake, toxicity and tolerance in plants and management of Cu-contaminated soil. Biometals, 34(4), 737-759. doi: 10.1007/s10534-021-00306-z DOI: https://doi.org/10.1007/s10534-021-00306-z
Mishra, D., Kumar, S., & Mishra, B. N. (2020). An overview of Morpho-physiological, biochemical, and molecular responses of sorghum towards heavy metal stress. Reviews of Environmental Contamination and Toxicology, 256, 155-177. doi: 10.1007/398_2020_61 DOI: https://doi.org/10.1007/398_2020_61
Miyazawa, M., Pavan, M. A., Muraoka, T., Carmo, C. D., & Melo, W. D. (2009). Análise química de tecido vegetal. In F. C. Silva (Org.). Manual de análises químicas de solos, plantas e fertilizantes (Cap. 2, pp. 59-85). Brasília.
Paiva, A. B., Taniguch, C. A. K., Romero, R. E., Pagano, M. C., & Weber, O. B. (2022). Chemical and microbiological attributes of sandy soil fertilized with crushed green coconut shell. Revista Ciência Agronômica, 53(e20207778), 20207778. doi: 10.5935/1806-6690.20220007 DOI: https://doi.org/10.5935/1806-6690.20220007
Peternella, W. S., Silva, F. F., & Costa, A. C. S. (2021). Evaluation of the phytoavailability of Cu (II) and Cr (III) for the growing of corn (Zea mays L.), cultivated in four soils of a toposequence derived from basalt. Open Access Library Journal, 8(8), 1-21. doi: 10.4236/oalib.1107707 DOI: https://doi.org/10.4236/oalib.1107707
Primieri, S., Santos, J. C. P., & Antunes, P. M. (2021). Nodule-associated bactéria alter the mutualism between arbuscular mycorrhizal fungi and N2 fixing bacteria. Soil Biology and Biochemistry, 154(108149), 1-7. doi: 10.1016/j.soilbio.2021.108149 DOI: https://doi.org/10.1016/j.soilbio.2021.108149
Ribeiro, V. P., Gomes, E. A., Sousa, S. M., Lana, U. G. P., Coelho, A. M., Marriel, I. E., & Oliveira-Paiva, C. A. (2022). Co-inoculation with tropical strains of Azospirillum and Bacillus is more efficient than single inoculation for improving plant growth and nutrient uptake in maize. Archives of Microbiology, 204(143), 1-13. doi: 10.1007/s00203-022-02759-3 DOI: https://doi.org/10.1007/s00203-022-02759-3
Rodrigues, A. C. D., Santos, A. M., Santos, F. S., Pereira, A. C. C., & Amaral Sobrinho, N. M. B. (2016). Mecanismos de respostas das plantas à poluição por metais pesados: possibilidade de uso de macrófitas para remediação de ambientes aquáticos contaminados. Revista Virtual de Química, 8(1), 262-276. doi: 10.5935/1984-6835.20160017 DOI: https://doi.org/10.5935/1984-6835.20160017
Santos, H. G., Jacomine, P. K. T., Anjos, L. H. C., Oliveira, V. A., Lumbreras, J. F., Coelho, M. R., Almeida, J. A., Araujo, J. C., Fº., Oliveira, J. B., & Cunha, T. J. F. (2018). Sistema brasileiro de classificação de solos (Cap. 5). EMBRAPA.
Sheng, M., Tang, M., Chen, H., Yang, B., Zhang, F., & Huang, Y. (2008). Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza, 18, 287-296. doi: 10.1007/S00572-008-0180-7 DOI: https://doi.org/10.1007/s00572-008-0180-7
Silva, I. R., & Mendonça, E. S. (2007). Matéria orgânica do solo (Cap. 1). Sociedade Brasileira de Ciência do Solo.
Silva, J. C. (2019). Desenvolvimento e capacidade fitoextratora de plantas agrícolas cultivadas em solo com diferentes texturas e teores de cobre. Dissertação de mestrado, Universidade de Santa Maria, Frederico Westphalen, RS, Brasil.
Sousa, L. F., Santos, J. G. D., Alexadrino, E., Mauricio, R. M., Martins, A. D., & Sousa, J. T. L. (2015). Método prático e eficiente para estimar a área foliar de gramíneas forrageiras tropicais. Archivos de Zootecnia, 64(245), 83-85. doi: 10.17765/2176-9168.2023v16n3e11059 DOI: https://doi.org/10.21071/az.v64i245.380
Tristão, F. S. M., Andrade, S. A. L., & Silveira, A. P. D. (2006). Fungos micorrízicos arbusculares na formação de mudas de cafeeiro, em substratos orgânicos comerciais. Bragantia, 65(4), 649-658. doi: 10.1590/S0006-87052006000400016 DOI: https://doi.org/10.1590/S0006-87052006000400016
Zhang, L., Yuxue, P., Wei, N., & Xiong, Z. T. (2014). Physiological responses of biomass allocation, root architecture, and invertase activity to copper stress in young seedlings from two populations of Kummerowia stipulacea (maxim.) Makino. Ecotoxicology and Environmental Safety, 104, 278-284. doi: 10.1016/j.ecoenv.2014.03.013 DOI: https://doi.org/10.1016/j.ecoenv.2014.03.013
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Copyright (c) 2024 Sinara Barros, Karuany Dorneles da Rosa, Victorino Menegat dos Santos, Eduardo Canepelle, Juliano Borela Magalhães, Ricardo Turchetto, Rodrigo Ferreira da Silva, Danni Maisa da Silva, Antônio Luis Santi
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