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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Published inFrontiers in plant science Vol. 9; p. 614
Main Authors Siqueira Freitas, Douglas, Wurr Rodak, Bruna, Rodrigues dos Reis, André, de Barros Reis, Fabio, Soares de Carvalho, Teotonio, Schulze, Joachim, Carbone Carneiro, Marco A., Guimarães Guilherme, Luiz R.
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Published Switzerland Frontiers Media S.A 08.05.2018
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Abstract 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 of soil. For this, we used 15 soybean genotypes and two soybean isogenic lines (urease positive, ; urease activity-null, , formerly ). 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 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 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 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.
AbstractList 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.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.
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.
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 of soil. For this, we used 15 soybean genotypes and two soybean isogenic lines (urease positive, ; urease activity-null, , formerly ). 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 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 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 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.
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.
Author Rodrigues dos Reis, André
de Barros Reis, Fabio
Wurr Rodak, Bruna
Schulze, Joachim
Siqueira Freitas, Douglas
Soares de Carvalho, Teotonio
Guimarães Guilherme, Luiz R.
Carbone Carneiro, Marco A.
AuthorAffiliation 2 Laboratory of Biology, School of Science and Engineering, São Paulo State University , Tupã , Brazil
3 CropSolutions Agricultural Research Center , São Gabriel do Oeste , Brazil
4 Laboratory of Plant Nutrition and Crop Physiology, Department of Crop Science, Faculty of Agriculture, University of Göttingen , Göttingen , Germany
1 Laboratory of Soil Microbiology and Environmental Geochemistry, Department of Soil Science, Federal University of Lavras , Lavras , Brazil
AuthorAffiliation_xml – name: 1 Laboratory of Soil Microbiology and Environmental Geochemistry, Department of Soil Science, Federal University of Lavras , Lavras , Brazil
– name: 2 Laboratory of Biology, School of Science and Engineering, São Paulo State University , Tupã , Brazil
– name: 3 CropSolutions Agricultural Research Center , São Gabriel do Oeste , Brazil
– name: 4 Laboratory of Plant Nutrition and Crop Physiology, Department of Crop Science, Faculty of Agriculture, University of Göttingen , Göttingen , Germany
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  surname: Siqueira Freitas
  fullname: Siqueira Freitas, Douglas
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/29868070$$D View this record in MEDLINE/PubMed
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Copyright Copyright © 2018 Siqueira Freitas, Wurr Rodak, Rodrigues dos Reis, de Barros Reis, Soares de Carvalho, Schulze, Carbone Carneiro and Guimarães Guilherme. 2018 Siqueira Freitas, Wurr Rodak, Rodrigues dos Reis, de Barros Reis, Soares de Carvalho, Schulze, Carbone Carneiro and Guimarães Guilherme
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Keywords ureides
photosynthesis
ammonia
urease activity
biological nitrogen fixation
Glycine max
urea
Language English
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Reviewed by: Ümit Bariş Kutman, Gebze Technical University, Turkey; Bahar Yildiz Kutman, Gebze Technical University, Turkey
Edited by: Richard William Bell, Murdoch University, Australia
This article was submitted to Plant Nutrition, a section of the journal Frontiers in Plant Science
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Snippet 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...
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...
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SubjectTerms ammonia
biological nitrogen fixation
Glycine max
photosynthesis
Plant Science
urea
urease activity
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Title Hidden Nickel Deficiency? Nickel Fertilization via Soil Improves Nitrogen Metabolism and Grain Yield in Soybean Genotypes
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