SOIL WATERLOGGING ASSOCIATED WITH IRON EXCESS POTENTIATES PHYSIOLOGICAL DAMAGE TO SOYBEAN LEAVES

Autores

DOI:

10.31413/nativa.v10i3.13332

Palavras-chave:

gas exchange, chlorophylls, Glycine max, ferrous ion

Resumo

Many plants are exposed to soil waterlogging, including soybean plants. Soil waterlogging exponentially increases the availability of iron (Fe) and causes O2 depletion, which may result in excessive uptake of Fe and shortage of O2 to the roots and also nodules in leguminous plants, resulting in overproduction of reactive oxygen species and lipid peroxidation. The present study aimed to evaluate physiological damage to soybean leaves at the second trifoliate (V2) stage when exposed to non-waterlogged and waterlogged soils and combined with one moderate and two toxic levels of Fe. Soybean plants were vulnerable to soil waterlogging at all Fe levels tested, presenting the highest values of malonaldehyde, hydrogen peroxide, and Fe accumulation in the shoot, which resulted in accentuated damage to gas exchange and chlorophyll content, consequently leading to lower shoot dry weight. In contrast, soybean plants cultivated under optimal water availability showed less damage caused by excess Fe, mainly at 125 mg dm-3 Fe, since the traits of net photosynthetic rate, water use efficiency, instantaneous carboxylation efficiency, malonaldehyde, and shoot dry weight were not affected.

Keywords: chlorophylls; gas exchange; Glycine max; ferrous ion.

 

Encharcamento do solo associado ao excesso de ferro potencializa os danos fisiológicos às folhas de soja

 

RESUMO: Muitas plantas estão expostas ao encharcamento do solo, incluindo plantas de soja. O encharcamento do solo aumenta exponencialmente a disponibilidade de ferro (Fe) no solo e causa depleção de O2, o que pode resultar na absorção excessiva de Fe e escassez de O2 para as raízes e também nódulos em plantas leguminosas, resultando em superprodução de espécies reativas de oxigênio e peroxidação lipídica. O presente estudo teve como objetivo avaliar os danos fisiológicos às folhas de soja no segundo estádio trifoliado (V2) quando exposta a solos não encharcados e encharcados combinado com um nível moderado e dois níveis tóxicos de Fe. As plantas de soja foram vulneráveis ​​ao encharcamento do solo em todos os níveis de Fe testados, apresentando os maiores valores de malonaldeído, peróxido de hidrogênio e acúmulo de Fe na parte aérea, o que resultou em danos acentuados nas trocas gasosas e no conteúdo de clorofila, consequentemente levando a menor peso seco de parte aérea. Em contrapartida, plantas de soja cultivadas sob disponibilidade hídrica ótima apresentaram menos danos causados ​​pelo excesso de Fe, principalmente a 125 mg dm-3 Fe, uma vez que as características de taxa fotossintética líquida, eficiência do uso da água, eficiência de carboxilação instantânea, malonaldeído e peso seca da parte aérea não foram afetados.

Palavras-chave: clorofilas; trocas gasosas; Glycine max; íon ferroso.

Referências

AGUILAR, J. V.; LAPAZ, A. DE M.; SANCHES, C. V.; YOSHIDA, C. H. P.; CAMARGOS, L. S. D.; FURLANI-JÚNIOR, E. Application of 2, 4-D hormetic dose associated with the supply of nitrogen and nickel on cotton plants. Journal of Environmental Science and Health, Part B, v. 56, n. 9, p. 852-859, 2021. https://doi.org/10.1080/03601234.2021.1966280

ALEXIEVA, V.; SERGIEV, I.; MAPELLI, S.; KARANOV, E. The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant, Cell & Environment, v. 24, n. 12, p. 1337-1344, 2001. https://doi.org/10.1046/j.1365-3040.2001.00778.x

ARAÚJO, T. O.; ISAURE, M. P.; CHOUBASSI, G.; BIERLA, K.; SZPUNAR, J.; TRCERA, N.; CHAY, S.; ALCON, C.; SILVA, L. C.; CURIE, C.; MARI, S. Paspalum urvillei and Setaria parviflora, two grasses naturally adapted to extreme iron-rich environments. Plant Physiology and Biochemistry, v. 151, n. 6, p. 144-156, 2020. https://doi.org/10.1016/j.plaphy.2020.03.014

BARBOSA, M. R.; SILVA, M. M. A.; WILLADINO, L.; ULISSES, C.; CAMARA, T. R. Geração e desintoxicação enzimática de espécies reativas de oxigênio em plantas. Ciência Rural, v. 44, n. 3, p. 453-460, 2014. https://doi.org/10.1590/S0103-84782014000300011

BATAGLIA, O. C.; MASCARENHAS, H. A. A. Toxicidade de ferro em soja. Bragantia, v. 40, n. 1, p. 199-203, 1981. https://doi.org/10.1590/S0006-87051981000100021

BECANA, M.; MORAN, J. F.; Iturbe-Ormaetxe, I. Iron-dependent oxygen free radical generation in plants subjected to environmental stress: toxicity and antioxidant protection Plant and soil, v. 201, n. 1, p. 137-147, 1998. https://doi.org/10.1023/A:1004375732137

CHATTERJEE, C.; GOPAL, R.; DUBE, B. K. Impact of iron stress on biomass, yield, metabolism and quality of potato (Solanum tuberosum L.). Scientia horticulturae, v. 108, n. 1, p. 1-6, 2006. https://doi.org/10.1016/j.scienta.2006.01.004

DUFEY, I.; HAKIZIMANA, P.; DRAYE, X.; LUTTS, S.; BERTIN, P. QTL mapping for biomass and physiological parameters linked to resistance mechanisms to ferrous iron toxicity in rice. Euphytica, v. 167, n. 2, p. 143-160, 2009. https://doi.org/10.1007/s10681-008-9870-7

FEHR, W. R.; CAVINESS, C. E.; BURMOOD, D. T.; PENNINGTON, J. S. Stage of development descriptions for soybeans, Glycine Max (L.) Merrill1. Crop science, v. 11, n. 6, p. 929-931, 1971. https://doi.org/10.2135/cropsci1971.0011183X001100060051x

FREI, M.; TETTEH, R. N.; RAZAFINDRAZAKA, A. L.; FUH, M. A.; WU, L. B.; BECKER, M. Responses of rice to chronic and acute iron toxicity: genotypic differences and biofortification aspects. Plant and Soil, v. 408, n. 1, p. 149-161, 2016. https://doi.org/10.1007/s11104-016-2918-x

GREENWAY, H.; ARMSTRONG, W.; COLMER, T. D. Conditions leading to high CO2 (> 5 kPa) in waterlogged–flooded soils and possible effects on root growth and metabolism. Annals of Botany, v. 98, n. 1, p. 9-32, 2006. https://doi.org/10.1093/aob/mcl076

HEATH, R. L.; PACKER, L. Photoperoxidation in isolated chloroplasts. Archives of biochemistry and biophysics, v. 125, n. 1, p. 189-198, 1968. https://doi.org/10.1016/0003-9861(68)90654-1

IBAÑEZ, T. B.; SANTOS, L. F.; LAPAZ, A. M.; RIBEIRO, I. V.; RIBEIRO, F. V.; REIS, A. R.; MOREIRA, A.; HEINRICHS, R. Sulfur modulates yield and storage proteins in soybean grains. Scientia Agricola, v. 78, n. 1, p. e20190020, 2020. https://doi.org/10.1590/1678-992X-2019-0020

KOKUBUN, M. Genetic and cultural improvement of soybean for waterlogged conditions in Asia. Field Crops Research, v. 152, n. 14, p. 3-7, 2013. https://doi.org/10.1016/j.fcr.2012.09.022

LAPAZ, A. M.; CAMARGOS, L. S.; YOSHIDA, C. H. P.; FIRMINO, A. C.; FIGUEIREDO, P. A. M.; AGUILAR, J. V.; NICOLAI, A. B.; PAIVA, W. S.; CRUZ, V. H.; TOMAZ, R. S. Response of soybean to soil waterlogging associated with iron excess in the reproductive stage. Physiology and Molecular Biology of Plants, v. 26, n. 8, p. 1635-1648, 2020. https://doi.org/10.1007/s12298-020-00845-8

LAPAZ, A. M.; SANTOS, L. F. M.; YOSHIDA, C. H. P.; HEINRICHS, R.; CAMPOS, M.; REIS, A. R. Physiological and toxic effects of selenium on seed germination of cowpea seedlings. Bragantia, v. 78, n. 4, p. 498-508, 2019. https://doi.org/10.1590/1678-4499.20190114

LAPAZ, A. M.; YOSHIDA, C. H. P.; GORNI, P. H.; FREITAS-SILVA, L.; ARAÚJO, T. O.; RIBEIRO, C. Iron toxicity: effects on the plants and detoxification strategies. Acta bot. bras, v. 36, p. e2021abb0131, 2022. https://doi.org/10.1590/0102-33062021abb0131

LICHTENTHALER, H. K.; WELLBURN, A. R. Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochemical Society Transactions, v. 11, p. 591-592, 1983.

LORETI, E.; VAN VEEN, H.; PERATA, P. Plant responses to flooding stress Current Opinion in Plant Biology, v. 33, p. 64-71, 2016. https://doi.org/10.1016/j.pbi.2016.06.005

MALAVOLTA, E.; VITTI, G. C.; OLIVEIRA, A. S. Avaliação do estado nutricional de plantas: princípios e aplicações. 2. ed. Piracicaba: Potafos, 1997. 319p

MARANGUIT, D.; GUILLAUME, T.; KUZYAKOV, Y. Effects of flooding on phosphorus and iron mobilization in highly weathered soils under different land-use types: Short-term effects and mechanisms. Catena, v. 158, n. 14, p. 161-170, 2017. https://doi.org/10.1016/j.catena.2017.06.023

MARTÍNEZ-ALCÁNTARA, B.; JOVER, S.; QUIÑONES, A.; FORNER-GINER, M. Á.; RODRÍGUEZ-GAMIR, J.; LEGAZ, F.; PRIMO-MILLO, E.; IGLESIAS, D. J. Flooding affects uptake and distribution of carbon and nitrogen in citrus seedlings. Journal of Plant Physiology, v. 169, n. 12, p. 1150-1157, 2012. https://doi.org/10.1016/j.jplph.2012.03.016

MASLOVA, T. G.; MARKOVSKAYA, E. F.; SLEMNEV, N. N. Functions of carotenoids in leaves of higher plants. Biology Bulletin Reviews, v. 11, n. 5, p. 476-487, 2021. https://doi.org/10.1134/S2079086421050078

MÜLLER, C.; SILVEIRA, S. F. S.; DALOSO, D. M.; MENDES, G. C.; MERCHANT, A.; KUKI, K. N.; OLIVA, M. A.; LOUREIRO, M. E.; ALMEIDA, A. M. Ecophysiological responses to excess iron in lowland and upland rice cultivars. Chemosphere, v. 189, n. 24, p. 123-133, 2017. https://doi.org/10.1016/j.chemosphere.2017.09.033

PEDO, T.; KOCH, F.; MARTINAZZO, E. G.; VILLELA, F. A.; AUMONDE, T. Z. Physiological attributes, growth and expression of vigor in soybean seeds under soil waterlogging. African Journal of Agricultural Research, v. 10, n. 39, p. 3791-3797, 2015. https://doi.org/10.5897/AJAR2015.9661

PEREIRA, E. G.; OLIVA, M. A.; ROSADO-SOUZA, L.; MENDES, G. C.; COLARES, D. S.; STOPATO, C. H.; ALMEIDA, A. M. Iron excess affects rice photosynthesis through stomatal and non-stomatal limitations. Plant Science, v. 201-202, n. 3, p. 81-92, 2013. https://doi.org/10.1016/j.plantsci.2012.12.003

QUAGGIO, J. A.; VAN RAIJ, B.; MALAVOLTA, E. Alternative use of the SMP‐buffer solution to determine lime requirement of soils. Communications in Soil Science and Plant Analysis, v. 16, n. 3, p. 245-260, 1985. https://doi.org/10.1080/00103628509367600

R Development Core Team (2019) R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Disponível em: https://www.R-project.org/

RHINE, M. D.; STEVENS, G.; SHANNON, G.; WRATHER, A.; SLEPER, D. Yield and nutritional responses to waterlogging of soybean cultivars. Irrigation Science, v. 28, n. 2, p. 135-142, 2010. https://doi.org/10.1007/s00271-009-0168-x

RODRÍGUEZ-GAMIR, J.; ANCILLO, G.; CARMEN GONZÁLEZ-MAS, M.; PRIMO-MILLO, E.; IGLESIAS, D. J.; FORNER-GINER, M. A. Root signalling and modulation of stomatal closure in flooded citrus seedlings. Plant Physiology and Biochemistry, v. 49, n. 6, p. 636-645, 2011. https://doi.org/10.1016/j.plaphy.2011.03.003

SAIRAM, R. K.; DHARMAR, K.; CHINNUSAMY, V.; MEENA, R. C. Waterlogging-induced increase in sugar mobilization, fermentation, and related gene expression in the roots of mung bean (Vigna radiata). Journal of Plant Physiology, v. 166, n. 6, p. 602-616, 2009. https://doi.org/10.1016/j.jplph.2008.09.005

SANTOS, H. G.; JACOMINE, P. K. T.; ANJOS, L. H. C.; OLIVEIRA, V. A.; LUMBRERAS, J. F.; COELHO, M. R.; ALMEIDA, J. A.; CUNHA, T. J. F.; OLIVEIRA, J. B. Sistema brasileiro de classificação de solos. 3.ed. Brasília: Embrapa, 2013. 353p.

SCHULZE E. D.; BECK E.; BUCHMANN N.; CLEMENS S.; MÜLLER-HOHENSTEIN K.; SCHERER-LORENZEN M. In: Plant Ecology. Springer, Berlin, Heidelberg, 2019. p. 143-164. https://doi.org/10.1007/978-3-662-56233-8_5

SHIMAMURA, S.; YAMAMOTO, R.; NAKAMURA, T.; SHIMADA, S.; KOMATSU, S. Stem hypertrophic lenticels and secondary aerenchyma enable oxygen transport to roots of soybean in flooded soil. Annals of botany, v. 106, n. 2, p. 277-284, 2010. https://doi.org/10.1093/aob/mcq123

SINGH, S. P.; SETTER, T. L. Effect of waterlogging on element concentrations, growth and yield of wheat varieties under farmer’s sodic field conditions. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences, v. 87, n. 2, p. 513-520, 2017. https://doi.org/10.1007/s40011-015-0607-9

SOUZA, S. C. R.; MAZZAFERA, P.; SODEK, L. Flooding of the root system in soybean: biochemical and molecular aspects of N metabolism in the nodule during stress and recovery. Amino acids, v. 48, n. 5, p. 1285-1295, 2016. https://doi.org/10.1007/s00726-016-2179-2

THOMAS, A. L.; GUERREIRO, S. M. C.; SODEK, L. Aerenchyma formation and recovery from hypoxia of the flooded root system of nodulated soybean. Annals of Botany, v. 96, n. 7, p. 1191-1198, 2005. https://doi.org/10.1093/aob/mci272

TIAN, L.; LI, J.; BI, W.; ZUO, S.; LI, L.; LI, W.; SUN, L. Effects of waterlogging stress at different growth stages on the photosynthetic characteristics and grain yield of spring maize (Zea mays L.) under field conditions. Agricultural Water Management, v. 218, n. 8, p. 250-258, 2019. https://doi.org/10.1016/j.agwat.2019.03.054

VELASCO, N. F.; LIGARRETO, G. A.; DÍAZ, H. R.; FONSECA, L. P. M. Photosynthetic responses and tolerance to root-zone hypoxia stress of five bean cultivars (Phaseolus vulgaris L.). South African Journal of Botany, v. 123, n. 4, p. 200-207, 2019. https://doi.org/10.1016/j.sajb.2019.02.010

VOESENEK, L. A. C. J.; COLMER, T. D.; PIERIK, R.; MILLENAAR, F. F.; PEETERS, A. J. M. How plants cope with complete submergence. New phytologist, v. 170, n. 2, p. 213-226, 2006. https://doi.org/10.1111/j.1469-8137.2006.01692.x

WANG, S., ZHOU, H., FENG, N., XIANG, H., LIU, Y., WANG, F., LI, W.; FENG, S.; LIU M.; ZHENG, D. Physiological response of soybean leaves to uniconazole under waterlogging stress at R1 stage. Journal of Plant Physiology, v. 268, n. 1, p. 153579, 2022. https://doi.org/10.1016/j.jplph.2021.153579

WIENTJES, E.; PHILIPPI, J.; BORST, J. W.; VAN AMERONGEN, H. Imaging the Photosystem I/Photosystem II chlorophyll ratio inside the leaf. Biochimica et Biophysica Acta (BBA)-Bioenergetics, v. 1858, n. 3, p. 259-265, 2017. https://doi.org/10.1016/j.bbabio.2017.01.008

XING, W.; LI, D.; LIU, G. Antioxidative responses of Elodea nuttallii (Planch.) H. St. John to short-term iron exposure. Plant Physiology and Biochemistry, v. 48, n. 10-11, p. 873-878, 2010. https://doi.org/10.1016/j.plaphy.2010.08.006

XU, S.; LIN, D.; SUN, H.; YANG, X.; ZHANG, X. Excess iron alters the fatty acid composition of chloroplast membrane and decreases the photosynthesis rate: a study in hydroponic pea seedlings. Acta Physiologiae Plantarum, v. 37, n. 10, p. 1-9, 2015. https://doi.org/10.1007/s11738-015-1969-6

XU, Y.; SUN, X.; ZHANG, Q.; LI, X.; YAN, Z. Iron plaque formation and heavy metal uptake in Spartina alterniflora at different tidal concentrations and waterlogging conditions. Ecotoxicology and environmental safety, v. 153, n. 7, p. 91-100, 2018. https://doi.org/10.1016/j.ecoenv.2018.02.008

YAN, K.; ZHAO, S.; CUI, M.; HAN, G.; WEN, P. Vulnerability of photosynthesis and photosystem I in Jerusalem artichoke (Helianthus tuberosus L.) exposed to waterlogging. Plant Physiology and Biochemistry, v. 125, n. 4, p. 239-246, 2018. https://doi.org/10.1016/j.plaphy.2018.02.017

ZHANG, F.; ZHU, K.; WANG, Y. Q.; ZHANG, Z. P.; LU, F.; YU, H. Q.; ZOU, J. Q. Changes in photosynthetic and chlorophyll fluorescence characteristics of sorghum under drought and waterlogging stress. Photosynthetica, v. 57, n. 4, p. 1156-1164, 2019. https://doi.org/10.32615/ps.2019.136

ZHANG, Y.; CHEN, Y.; LU, H.; KONG, X.; DAI, J.; LI, Z.; DONG, H. Growth, lint yield and changes in physiological attributes of cotton under temporal waterlogging. Field Crops Research, v. 194, p. 83-93, 2016. https://doi.org/10.1016/j.fcr.2016.05.006

ZHENG, X. D.; ZHOU, J. Z.; TAN, D. X.; WANG, N.; WANG, L.; SHAN, D. Q.; KONG, J. Melatonin improves waterlogging tolerance of Malus baccata (Linn.) Borkh. seedlings by maintaining aerobic respiration, photosynthesis and ROS migration. Frontiers in Plant Science, v. 8, p. 483, 2017. https://doi.org/10.3389/fpls.2017.00483

Publicado

2022-08-20 — Atualizado em 2023-10-06

Versões

Como Citar

Lapaz, A. M. de, Yoshida, C. . H. P., Bogas, C. L. P. ., Camargos, L. S. de ., Figueiredo, P. A. M. de, Aguilar, J. V., Lima, R. C., & Tomaz, R. S. (2023). SOIL WATERLOGGING ASSOCIATED WITH IRON EXCESS POTENTIATES PHYSIOLOGICAL DAMAGE TO SOYBEAN LEAVES. Nativa, 10(3), 319–327. https://doi.org/10.31413/nativa.v10i3.13332 (Original work published 20º de agosto de 2022)

Edição

Seção

Agronomia / Agronomy