Hidden Nickel Deficiency? Nickel Fertilization via Soil Improves Nitrogen Metabolism and Grain Yield in Soybean Genotypes

Nickel (Ni)—a component of urease and hydrogenase—was the latest nutrient to be recognized as an essential element for plants. However, to date there are no records of Ni deficiency for annual species cultivated under field conditions, possibly because of the non-appearance of obvious and distinctiv...

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Main Authors: Douglas Siqueira Freitas, Bruna Wurr Rodak, André Rodrigues dos Reis, Fabio de Barros Reis, Teotonio Soares de Carvalho, Joachim Schulze, Marco A. Carbone Carneiro, Luiz R. Guimarães Guilherme
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-05-01
Series:Frontiers in Plant Science
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fpls.2018.00614/full
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spelling doaj-c4eef22dec424275b989fff476053e3b2020-11-24T23:23:10ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2018-05-01910.3389/fpls.2018.00614328382Hidden Nickel Deficiency? Nickel Fertilization via Soil Improves Nitrogen Metabolism and Grain Yield in Soybean GenotypesDouglas Siqueira Freitas0Bruna Wurr Rodak1André Rodrigues dos Reis2Fabio de Barros Reis3Teotonio Soares de Carvalho4Joachim Schulze5Marco A. Carbone Carneiro6Luiz R. Guimarães Guilherme7Laboratory of Soil Microbiology and Environmental Geochemistry, Department of Soil Science, Federal University of Lavras, Lavras, BrazilLaboratory of Soil Microbiology and Environmental Geochemistry, Department of Soil Science, Federal University of Lavras, Lavras, BrazilLaboratory of Biology, School of Science and Engineering, São Paulo State University, Tupã, BrazilCropSolutions Agricultural Research Center, São Gabriel do Oeste, BrazilLaboratory of Soil Microbiology and Environmental Geochemistry, Department of Soil Science, Federal University of Lavras, Lavras, BrazilLaboratory of Plant Nutrition and Crop Physiology, Department of Crop Science, Faculty of Agriculture, University of Göttingen, Göttingen, GermanyLaboratory of Soil Microbiology and Environmental Geochemistry, Department of Soil Science, Federal University of Lavras, Lavras, BrazilLaboratory of Soil Microbiology and Environmental Geochemistry, Department of Soil Science, Federal University of Lavras, Lavras, BrazilNickel (Ni)—a component of urease and hydrogenase—was the latest nutrient to be recognized as an essential element for plants. However, to date there are no records of Ni deficiency for annual species cultivated under field conditions, possibly because of the non-appearance of obvious and distinctive symptoms, i.e., a hidden (or latent) deficiency. Soybean, a crop cultivated on soils poor in extractable Ni, has a high dependence on biological nitrogen fixation (BNF), in which Ni plays a key role. Thus, we hypothesized that Ni fertilization in soybean genotypes results in a better nitrogen physiological function and in higher grain production due to the hidden deficiency of this micronutrient. To verify this hypothesis, two simultaneous experiments were carried out, under greenhouse and field conditions, with Ni supply of 0.0 or 0.5 mg of Ni kg−1 of soil. For this, we used 15 soybean genotypes and two soybean isogenic lines (urease positive, Eu3; urease activity-null, eu3-a, formerly eu3-e1). Plants were evaluated for yield, Ni and N concentration, photosynthesis, and N metabolism. Nickel fertilization resulted in greater grain yield in some genotypes, indicating the hidden deficiency of Ni in both conditions. Yield gains of up to 2.9 g per plant in greenhouse and up to 1,502 kg ha−1 in field conditions were associated with a promoted N metabolism, namely, leaf N concentration, ammonia, ureides, urea, and urease activity, which separated the genotypes into groups of Ni responsiveness. Nickel supply also positively affected photosynthesis in the genotypes, never causing detrimental effects, except for the eu3-a mutant, which due to the absence of ureolytic activity accumulated excess urea in leaves and had reduced yield. In summary, the effect of Ni on the plants was positive and the extent of this effect was controlled by genotype-environment interaction. The application of 0.5 mg kg−1 of Ni resulted in safe levels of this element in grains for human health consumption. Including Ni applications in fertilization programs may provide significant yield benefits in soybean production on low Ni soil. This might also be the case for other annual crops, especially legumes.http://journal.frontiersin.org/article/10.3389/fpls.2018.00614/fullammoniabiological nitrogen fixationGlycine maxphotosynthesisureaurease activity
collection DOAJ
language English
format Article
sources DOAJ
author Douglas Siqueira Freitas
Bruna Wurr Rodak
André Rodrigues dos Reis
Fabio de Barros Reis
Teotonio Soares de Carvalho
Joachim Schulze
Marco A. Carbone Carneiro
Luiz R. Guimarães Guilherme
spellingShingle Douglas Siqueira Freitas
Bruna Wurr Rodak
André Rodrigues dos Reis
Fabio de Barros Reis
Teotonio Soares de Carvalho
Joachim Schulze
Marco A. Carbone Carneiro
Luiz R. Guimarães Guilherme
Hidden Nickel Deficiency? Nickel Fertilization via Soil Improves Nitrogen Metabolism and Grain Yield in Soybean Genotypes
Frontiers in Plant Science
ammonia
biological nitrogen fixation
Glycine max
photosynthesis
urea
urease activity
author_facet Douglas Siqueira Freitas
Bruna Wurr Rodak
André Rodrigues dos Reis
Fabio de Barros Reis
Teotonio Soares de Carvalho
Joachim Schulze
Marco A. Carbone Carneiro
Luiz R. Guimarães Guilherme
author_sort Douglas Siqueira Freitas
title Hidden Nickel Deficiency? Nickel Fertilization via Soil Improves Nitrogen Metabolism and Grain Yield in Soybean Genotypes
title_short Hidden Nickel Deficiency? Nickel Fertilization via Soil Improves Nitrogen Metabolism and Grain Yield in Soybean Genotypes
title_full Hidden Nickel Deficiency? Nickel Fertilization via Soil Improves Nitrogen Metabolism and Grain Yield in Soybean Genotypes
title_fullStr Hidden Nickel Deficiency? Nickel Fertilization via Soil Improves Nitrogen Metabolism and Grain Yield in Soybean Genotypes
title_full_unstemmed Hidden Nickel Deficiency? Nickel Fertilization via Soil Improves Nitrogen Metabolism and Grain Yield in Soybean Genotypes
title_sort hidden nickel deficiency? nickel fertilization via soil improves nitrogen metabolism and grain yield in soybean genotypes
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2018-05-01
description Nickel (Ni)—a component of urease and hydrogenase—was the latest nutrient to be recognized as an essential element for plants. However, to date there are no records of Ni deficiency for annual species cultivated under field conditions, possibly because of the non-appearance of obvious and distinctive symptoms, i.e., a hidden (or latent) deficiency. Soybean, a crop cultivated on soils poor in extractable Ni, has a high dependence on biological nitrogen fixation (BNF), in which Ni plays a key role. Thus, we hypothesized that Ni fertilization in soybean genotypes results in a better nitrogen physiological function and in higher grain production due to the hidden deficiency of this micronutrient. To verify this hypothesis, two simultaneous experiments were carried out, under greenhouse and field conditions, with Ni supply of 0.0 or 0.5 mg of Ni kg−1 of soil. For this, we used 15 soybean genotypes and two soybean isogenic lines (urease positive, Eu3; urease activity-null, eu3-a, formerly eu3-e1). Plants were evaluated for yield, Ni and N concentration, photosynthesis, and N metabolism. Nickel fertilization resulted in greater grain yield in some genotypes, indicating the hidden deficiency of Ni in both conditions. Yield gains of up to 2.9 g per plant in greenhouse and up to 1,502 kg ha−1 in field conditions were associated with a promoted N metabolism, namely, leaf N concentration, ammonia, ureides, urea, and urease activity, which separated the genotypes into groups of Ni responsiveness. Nickel supply also positively affected photosynthesis in the genotypes, never causing detrimental effects, except for the eu3-a mutant, which due to the absence of ureolytic activity accumulated excess urea in leaves and had reduced yield. In summary, the effect of Ni on the plants was positive and the extent of this effect was controlled by genotype-environment interaction. The application of 0.5 mg kg−1 of Ni resulted in safe levels of this element in grains for human health consumption. Including Ni applications in fertilization programs may provide significant yield benefits in soybean production on low Ni soil. This might also be the case for other annual crops, especially legumes.
topic ammonia
biological nitrogen fixation
Glycine max
photosynthesis
urea
urease activity
url http://journal.frontiersin.org/article/10.3389/fpls.2018.00614/full
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