For immobile nutrients in plants like zinc, iron, copper, manganese, boron, chlorine, nickel, calcium and sulfur, the deficiency symptoms first show up in the younger leaves. doi: 10.1016/j.bbabio.2013.01.015. 59, 89–113. The effect of foliar application of nickel in the mineral form and urea-Ni complex on fresh weight and nitrogen metabolism of lettuce. HortScience 48, 1145–1153. Urea concentration was determined by colorimetry (color intensity) at 540 nm absorbance. A poorly understood kind, seeds with nickel deficiencies will show poor germination . Chlorophyll fluorescence: a probe of photosynthesis in vivo. The mixture was incubated at 100°C during 5 min. In the greenhouse experiment, soybean plants were cultivated in 4-L pots filled with soil collected from a native forest. Table 1. Crop Sci. Independently of Ni dose, Eu3 line developed normally while eu3-a line presented symptoms of hyponasty and initial necrosis lesions on leaflet tips. Recent studies have demonstrated that fertilization with Ni can increase N assimilation and N metabolite levels in plants (Tan et al., 2000; Khoshgoftarmanesh et al., 2011; Hosseini and Khoshgoftarmanesh, 2013; Dalir and Khoshgoftarmanesh, 2015; Uruç Parlak, 2016). The relationship between WRB soil units and heavy metals content in soils of Catamarca (Argentina). New York, NY: Springer New York. Biplot of the partial principal components analysis of variables related to N metabolism, leaf N concentration and grain yield for 15 soybean genotypes, fertilized with 0.0 mg of Ni kg−1 (−Ni) and 0.5 mg of Ni kg−1 (+Ni), cultivated in field condition. 4. In contrast, the eu3-a mutant presented an increase of 1.1 times in urea concentration. B., and Cakmak, I. J. Hydrog. 13, 181–187. (2012). Energy 39, 18521–18532. One 150-μL aliquot was collected and added to 3.0 mL of color developing reagent. Physiology, biochemistry, and genetics of the uptake hydrogenase in rhizobia. Nickel fertilization positively affected the synthesis of total ureides (allantoin and allantoic acid), which are the main way of exporting N fixed by nodules to other soybean plant tissues (Table 5). B., Xuejing, X., Qin, Z., Miyazawa, M., Ferreira, F. J. F., and Plawiak, R. A. No use, distribution or reproduction is permitted which does not comply with these terms. Sci. Such daily consumption of soybean is far beyond the recommended ingestion standards of in natura grains and soybean products. Integrated Risk Information System (1991). Soil Taxonomy: a Basic System of Soil Classification for Making and Interpreting Soil Surveys. doi: 10.4141/cjps2011-135, Morrison, J. M., Goldhaber, M. B., Lee, L., Holloway, J. M., Wanty, R. B., Wolf, R. E., et al. Nickel fertilization of greenhouse-grown soybean plants promoted increases in grain yield for 12 out of 15 genotypes evaluated and for the Eu3 isogenic line, with increases of up to 2.9 g per plant (Figure 1). doi: 10.1023/A:1006188004189, Winter, G., Todd, C. D., Trovato, M., Forlani, G., and Funck, D. (2015). The marginal effect of genotypes was partialled out by subtracting each variable from its overall mean (irrespective to Ni treatment) for each genotype, prior to PCA analysis, resulting in a partial PCA (pPCA) as detailed in Legendre and Legendre (2013). 721, 83–98. For legume plants that are highly efficient in biological nitrogen fixation (BNF), such as soybean, urease and hydrogenase have a very significant role. Physiological implications of arginine metabolism in plants. Phytochemistry 22, 663–667. This emphasizes the critical role of Ni in N metabolism. DRI: dietary reference intakes for vitamin A, vitamin K, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium, and zinc : a report of the Panel on Micronutrients…and the Standing Committee on the Scientific Evaluation of Dietary Reference Intakes, Food and Nutrition Board, Institute of Medicine. 140, 433–443. Nickel: a micronutrient essential for higher plants. (2014). Grouping of the samples receiving Ni toward the left side of the pPCA biplot indicates increased grain yield, leaf N concentration, leaf ammonia, leaf ureides, and urease activity, associated with decreases in leaf urea, with the opposite for mutant eu3-a (Figures 4, 5). (2017) observed formation of brown color on leaves induced by the presence of Ni inside cells, similarly to what was observed in the eu3-a. Download Adobe Acrobat Reader (free software to read PDF files). 84, 265–273. Can. In addition, the high dependence of this legume on BNF may further increase its demand for Ni. However, standards for Ni-deficient soils have not been established. Photosynthetic function was determined on the third leaf from the top of the plants. However, it has been seen in animals. Bai, C., Reilly, C. C., and Wood, B. W. (2007). The eu3-a mutant was the only treatment to express toxicity with Ni fertilization, as the addition of Ni reduced grain yield by 1.7 g per plant (Figure 1). doi: 10.17660/ActaHortic.2006.721.10, Yusuf, M., Fariduddin, Q., Hayat, S., and Ahmad, A. Long-term toxicologic assessment of nickel in rats and dogs. (2006, 2007) observed that pecan plants under low Ni supply showed an inhibition in the shikimate pathway, disrupting the conversion of free amino acids to other products and, thus, blocking some N pathways. Metais em Fertilizantes Inorgânicos: Avaliação de Risco à Saúde Após a Aplicação. Transporters for uptake and allocation of organic nitrogen compounds in plants. Even though plants usually have a low demand for this micronutrient (Seregin and Kozhevnikova, 2006), it can be expected that Ni-poor soils might also cause a hidden (or latent) deficiency in other plant species (Wood, 2013). In plants, Ni constitutes the active site of two metalloenzymes that are directly involved in nitrogen metabolism (N metabolism): urease (Dixon et al., 1975) and hydrogenase (Evans et al., 1987). The evidence that Ni is an essential plant micronutrient was confirmed four years later, when after thr… In Western Australia, the highly weathered and leached soils are low in cobalt. doi: 10.1016/0003-2697(70)90448-3, Wang, W. H., Köhler, B., Cao, F. Q., and Liu, L. H. (2008). Assessment of the total nickel content and its available forms in the soils around cement plant Lafarge Poland. Environ. Many Abiotic factors exist which can cause plant problems as shown in Table 1. In soybean, this effect in N metabolism (Kutman et al., 2013, 2014) as well as in BNF stimulation (González-Guerrero et al., 2014; Lavres et al., 2016; Macedo et al., 2016) is also observed, yet these results were obtained under artificial growth conditions (greenhouse with soil or nutrient solution). (2017). 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. For these variables, only the mean of Ni-dose effects in the genotypes were presented, since the interaction of genotype x Ni dose was caused by NILs alone (data not shown). 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, ETR, and qN (Table 3). 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. Magnesium is important to calcium and potassium homeostasis. Nickel (Ni) was the latest element to be included in the list of essential nutrients to plants. The editor and reviewers' affiliations are the latest provided on their Loop research profiles and may not reflect their situation at the time of review. Microbiol. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The evidence that Ni is an essential plant micronutrient was confirmed four years later, when after three successive generations of growing barley plants (Hordeum vulgare L.) in Ni-depleted controlled conditions, these plants failed to produce viable grains (Brown et al., 1987). Cu-deficient sweetpotato plants may produce storage roots which are normal in external appearance but contained brown streaks in the flesh (Pillai, et al., 1986). Chim. Field-conditions were more restrictive since the genotypes in this group presented no yield increases (Figures 1, 5), associated mainly with no increases in ureides (Table 5). Bot. (2013) and Lavres et al. Environ. Plant Sci. K. Koch) to Ni deficiency (Wood et al., 2004a,b, 2006). Iowa: Iowa State University Cooperative Extension Service. Sci. Clín. The moisture was determined with an automatic measuring device (Gehaka G650i, Brazil). Ni deficiency in field situations appears to be far more common than Including Ni applications in fertilization programs may provide significant yield benefits in soybean production on low Ni soil. doi: 10.1146/annurev.arplant.57.032905.105421, Keywords: ammonia, biological nitrogen fixation, Glycine max, photosynthesis, urea, urease activity, ureides, Citation: Siqueira Freitas D, Wurr Rodak B, Rodrigues dos Reis A, de Barros Reis F, Soares de Carvalho T, Schulze J, Carbone Carneiro MA and Guimarães Guilherme LR (2018) Hidden Nickel Deficiency? Front. J. Ciênc. doi: 10.1016/S0031-9422(00)86958-7, Hosseini, H., and Khoshgoftarmanesh, A. H. (2013). Without nickel, toxic levels of urea can accumulate within the tissue forming necrotic legions on the leaf tips. 72, 355–367. Statistical analysis was performed through a two-way analysis of variance (ANOVA) and mean values were compared by the Dunnett's test (P = 0.05). 92, 399–405. To be able to transport N-urea to N-sink tissues, soybean plants produce ammonia, as result of urea hydrolysis by urease activity (Wang et al., 2008; Witte, 2011; Polacco et al., 2013; Winter et al., 2015). The extract was centrifuged at 13,200 RPM during 5 min, at 4°C. 6, 1–14. However, more studies are required to set an accurate Ni rate and to verify residual effects of Ni in the soil, especially for oxidic conditions prevalent in tropical agroecosystems. Front. On the contrary, among the 15 field-grown soybean genotypes, 10 showed an increased in grain Ni concentration (mean values without and with Ni ranged from 1.55 to 2.35 mg kg−1) and five—7849, 3730, 2158, 6215, and 620—did not (1.68 to 1.94 mg kg−1). 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