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−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.

Highlights

  • Nickel (Ni) was the latest element to be included in the list of essential nutrients to plants

  • For legume plants that are highly efficient in biological nitrogen fixation (BNF), such as soybean, urease and hydrogenase have a very significant role

  • Analysis of variance of the greenhouse experiment revealed that soybean plant response was dependent on genotypes and Ni doses (A x B) for leaf Ni concentration, grain Ni concentration, grain yield, urease activity, ammonia concentration, urea concentration, SPAD index, electron transport rate (ETR), and qN (Table 3)

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Summary

Introduction

Nickel (Ni) was the latest element to be included in the list of essential nutrients to plants. The first evidence of its essentiality was verified in soybean plants (Glycine max [L.] Merrill) in 1983, under controlled conditions of Ni depletion, when these plants accumulated toxic concentrations of urea in leaflet tips (Eskew et al, 1983). Urease is responsible for hydrolysis of urea into two molecules of ammonia and one of carbon dioxide (Witte, 2011; Polacco et al, 2013), while legume plants in symbiosis with N2-fixing bacteria form root nodules, in which hydrogenase catalyzes the oxidation of molecular hydrogen (H2) into protons and electrons (Shafaat et al, 2013; Bagyinka, 2014; Brazzolotto et al, 2016). For legume plants that are highly efficient in biological nitrogen fixation (BNF), such as soybean, urease and hydrogenase have a very significant role. Nitrogenase reduces N2 to ammonia, and produces molecular hydrogen. The hydrogenase pathway is the second biological reaction in which Ni is required

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