Influence of Heavy Metals on the Nitrogen Metabolism in Plants

*Vitor Nascimento, Glauco Nogueira, Gabriel Monteiro, Waldemar Júnior, Joze Melissa Nunes de Freitas and Cândido Neto*

#### **Abstract**

As an essential element, Nitrogen is needed in large quantities for being an important component of cellular constituents and for plant metabolism, and its deficiency is one of the most common limitations for plant development. The study of the toxic effects of metal in plants involves a complex system of reactions that can be better determined once having a large attention of the different backgrounds of occurence to determinate how to proceed. The objective of this review is to add scientific knowledge, addressing the main functionalities and characteristics of this relation heavy metals – nitrogen metabolism in plant. Increasing industrialization and urbanization had anthropogenic contribution of heavy metals in biosphere and had largest availability in ecosystems. This toxicity in plants varies with plant species, specific metal, concentration, soil composition, as many heavy metals are considered to be essential for plant growth. Were provided data and reviews regarding the effect of heavy metals on nitrogen metabolism of plants and the responses of plants and the cross-talk of heavy metals and various stressors factors. Is clear to understand the relation between metals amount and the benefit or harm caused on plants, determining then, which mechanism should be activated to protect your physiological system.

**Keywords:** Plant physiology, human activities, industrialization, plant stress, toxicity

#### **1. Introduction**

Nitrogen (N) is an essential nutrient required by all living organisms and often limits primary production in aquatic and terrestrial ecosystems. This element is needed in large quantities, as it is an essential component of proteins, nucleic acids and other cellular constituents. Proteins alone comprise 60% or more of the N of plants and microbial cells [1]. It is also an essential element for plant metabolism and its deficiency is one of the most common limitations for plant development [2]. The preference of plants for the source of N can vary according to the selective pressures and consequent physiological adaptations [3].

The most common and available forms in the soil are the nitrate (NO3 − ) and ammonium (NH4 + ) forms, the first being more abundant and better assimilated by plants [4], as a result of the nitrification process by bacteria. However, depending on soil conditions, the ammoniacal form may be the most abundant due to the

#### **Figure 1.**

*Nitrogen metabolism in plants. Source: Biology Experts Notes.*

inhibition of these organisms [5]. Once in the leaves, it is known that different sources of N can affect plant metabolism differently. The accumulation of NH4 + can lead to decreased photosynthesis [6], while the excess of NO3 − can lead to the formation of reactive species inducing oxidative stress [7].

The metabolism of nitrogen is also closely linked to that of carbon (C), and the photorespiratory process is one of the points of connection between these, in addition to being a metabolic route that naturally produces a reactive oxygen species (**Figure 1**).

The study of the toxic effects of metal in plants involves a complex system of reactions that can be better determined once having a large attention of the different backgrounds and regions of occurence to determinate how to proceed. Therefore, the objective of this review is to add scientific knowledge, addressing the main functionalities and characteristics of this relation heavy metals – nitrogen metabolism in plant.

#### **2. Heavy metals**

According to Lenntech [8], heavy metals were significant environmental pollutants because their toxicity is a problem of increasing significance for ecological, evolutionary, environmental and nutritional reasons. Including copper (Cu), manganese (Mn), lead (Pb), cadmium (Cd), nickel (Ni), cobalt (Co), iron (Fe) and others, they are group of metals and metalloids with atomic density greater than 4 g/cm3 , or 5 times or more, greater than water [9]. Environmentally it is defined as total circumstances surrounding an organism or group of organisms especially, the combination of external physical conditions that influence and affect the growth, survival and development of the organisms [10].

Heavy metals are most found in rock formations with a dispersed form. Increasing industrialization and urbanization had anthropogenic contribution of heavy metals in biosphere and had largest availability in soil and aquatic ecosystems

**17**

*Influence of Heavy Metals on the Nitrogen Metabolism in Plants*

and to a relatively smaller portion in atmosphere as vapors or particulates. This toxicity in plants varies with plant species, specific metal, concentration, chemical form, pH and soil composition, as many heavy metals are considered to be essential for plant growth. According to Mildvan [11], some of these heavy metals like Cu and Zn could serve as activators of enzyme reactions and cofactor, exhibiting metallic properties such as ductility, malleability, cation stability, conductivity and ligand specificity were characterized by relatively high density and high relative atomic weight with an atomic number greater than 20, as said by Raskin et al. [12]. In Brazil, the reference levels for investigating the levels of heavy metal and other chemical substances in soils and groundwater are defined in CONAMA Resolution No. 420 [13], which facilitates the assessment of contamination and the creation of indicators that control and take care of the areas exposed to metals and the living beings in it. All forms of life can be affected by the presence of heavy metals depending on the dose and chemical composition [14]. Another key factor to be considered is the degree of exposure that is directly related to the amount of bioavailability in the environment, as the free ions of the metal can be linked to

According to Becher et al. [16], responses of plants to environmental stresses involve defenses, as well as stress-inducible reactions. Stimulation of important tolerance routes, such as enhancement of antioxidant enzymes activity, osmolyte accumulation, induction of membrane-localized transporters. Therefore, plants have developed mechanisms for homeostasis of ions that enable them to cope with a certain limited excess of heavy metals. Plants in the course of evolution demonstrate tolerance or even an adaptation to various biotic and abiotic stress factors. According to Hall and Williams [17] chaperons, chelators and specific transmembrane transporters have evolved. In plants non-adapted to given environmental conditions, that are challenged with excess of ions, an enhanced biosynthesis of complexing substances such as metallothioneins, phytochelatins and/or organic

Nitrogen assimilation is an important plant metabolic process, which not only controls development plant growth but also plays an important role in plant sur-

are major nitrogen sources and are required during different metabolic processes.

Pérez-Tienda et al. [21] reported that nitrate reductase is located in the cytoplasm, while nitrite reductase is located in chloroplast and uses energy and some reductants such as NADH or NADPH from respiration or photosynthesis process

occurs in the cytosol, while the second step occurs in the plastid. Following NH4

production, it has to be incorporated in carbon skeleton, and this process occurs

Moreover, as related by Mevel and Prieur [22], is possible to visualize two isoforms of GS, GOGAT and their localization has been found in a tissue-specific manner, e.g., in roots, GS1 and NADHGOGAT are primarily involved in the assimilation of nitrogen, in leaves the GSII and GOGAT are predominantly involved in the

is converted into nitrite with the action of the enzyme nitrate reductase,

+

−

with the action of nitrite

via a process constituted of two steps; during the first

conversion reaction. The first step of this reaction

and NH4

+

+

vival under stress conditions. As said by Burger and Jackson [20], NO3

+

and in the second step nitrite is converted into NH4

− to NH4 +

*DOI: http://dx.doi.org/10.5772/intechopen.97759*

organic matter, reducing bioavailability [15].

**3. Heavy metals in plants**

acids can occur (**Figure 2**) [18, 19].

Nitrate is converted into NH4

−

to carry out such NO3

nitrogen assimilation.

primarily via GOGAT cycle.

step, NO3

reductase.

*Influence of Heavy Metals on the Nitrogen Metabolism in Plants DOI: http://dx.doi.org/10.5772/intechopen.97759*

and to a relatively smaller portion in atmosphere as vapors or particulates. This toxicity in plants varies with plant species, specific metal, concentration, chemical form, pH and soil composition, as many heavy metals are considered to be essential for plant growth. According to Mildvan [11], some of these heavy metals like Cu and Zn could serve as activators of enzyme reactions and cofactor, exhibiting metallic properties such as ductility, malleability, cation stability, conductivity and ligand specificity were characterized by relatively high density and high relative atomic weight with an atomic number greater than 20, as said by Raskin et al. [12].

In Brazil, the reference levels for investigating the levels of heavy metal and other chemical substances in soils and groundwater are defined in CONAMA Resolution No. 420 [13], which facilitates the assessment of contamination and the creation of indicators that control and take care of the areas exposed to metals and the living beings in it. All forms of life can be affected by the presence of heavy metals depending on the dose and chemical composition [14]. Another key factor to be considered is the degree of exposure that is directly related to the amount of bioavailability in the environment, as the free ions of the metal can be linked to organic matter, reducing bioavailability [15].

#### **3. Heavy metals in plants**

*Nitrogen in Agriculture - Physiological, Agricultural and Ecological Aspects*

inhibition of these organisms [5]. Once in the leaves, it is known that different sources of N can affect plant metabolism differently. The accumulation of NH4

The metabolism of nitrogen is also closely linked to that of carbon (C), and the photorespiratory process is one of the points of connection between these, in addition to being a metabolic route that naturally produces a reactive oxygen species

The study of the toxic effects of metal in plants involves a complex system of reactions that can be better determined once having a large attention of the different backgrounds and regions of occurence to determinate how to proceed. Therefore, the objective of this review is to add scientific knowledge, addressing the main functionalities and characteristics of this relation heavy metals – nitrogen

According to Lenntech [8], heavy metals were significant environmental pollutants because their toxicity is a problem of increasing significance for ecological, evolutionary, environmental and nutritional reasons. Including copper (Cu), manganese (Mn), lead (Pb), cadmium (Cd), nickel (Ni), cobalt (Co), iron (Fe) and others, they are group of metals and metalloids with atomic density greater than

, or 5 times or more, greater than water [9]. Environmentally it is defined as

total circumstances surrounding an organism or group of organisms especially, the combination of external physical conditions that influence and affect the growth,

Heavy metals are most found in rock formations with a dispersed form. Increasing industrialization and urbanization had anthropogenic contribution of heavy metals in biosphere and had largest availability in soil and aquatic ecosystems

can lead to decreased photosynthesis [6], while the excess of NO3

formation of reactive species inducing oxidative stress [7].

*Nitrogen metabolism in plants. Source: Biology Experts Notes.*

survival and development of the organisms [10].

+

can lead to the

−

**16**

4 g/cm3

(**Figure 1**).

**Figure 1.**

metabolism in plant.

**2. Heavy metals**

According to Becher et al. [16], responses of plants to environmental stresses involve defenses, as well as stress-inducible reactions. Stimulation of important tolerance routes, such as enhancement of antioxidant enzymes activity, osmolyte accumulation, induction of membrane-localized transporters. Therefore, plants have developed mechanisms for homeostasis of ions that enable them to cope with a certain limited excess of heavy metals. Plants in the course of evolution demonstrate tolerance or even an adaptation to various biotic and abiotic stress factors.

According to Hall and Williams [17] chaperons, chelators and specific transmembrane transporters have evolved. In plants non-adapted to given environmental conditions, that are challenged with excess of ions, an enhanced biosynthesis of complexing substances such as metallothioneins, phytochelatins and/or organic acids can occur (**Figure 2**) [18, 19].

Nitrogen assimilation is an important plant metabolic process, which not only controls development plant growth but also plays an important role in plant survival under stress conditions. As said by Burger and Jackson [20], NO3 − and NH4 + are major nitrogen sources and are required during different metabolic processes. Nitrate is converted into NH4 + via a process constituted of two steps; during the first step, NO3 − is converted into nitrite with the action of the enzyme nitrate reductase, and in the second step nitrite is converted into NH4 + with the action of nitrite reductase.

Pérez-Tienda et al. [21] reported that nitrate reductase is located in the cytoplasm, while nitrite reductase is located in chloroplast and uses energy and some reductants such as NADH or NADPH from respiration or photosynthesis process to carry out such NO3 − to NH4 + conversion reaction. The first step of this reaction occurs in the cytosol, while the second step occurs in the plastid. Following NH4 + production, it has to be incorporated in carbon skeleton, and this process occurs primarily via GOGAT cycle.

Moreover, as related by Mevel and Prieur [22], is possible to visualize two isoforms of GS, GOGAT and their localization has been found in a tissue-specific manner, e.g., in roots, GS1 and NADHGOGAT are primarily involved in the assimilation of nitrogen, in leaves the GSII and GOGAT are predominantly involved in the nitrogen assimilation.

#### **Figure 2.**

*Morphophysiological responses of plants to metal toxicity in soil.*

Metal toxicity significantly reduces nitrogen assimilation process. However, the level of reduction depends on the sensitivity and localization of enzymes to heavy metal toxicity. Moreover, concentration, mobility and duration of heavy metal ions in growth medium further aggravate alterations in the process of nitrogen assimilation.

The exposure to metals at higher concentrations could result in severe damage to various metabolic activities leading consequently to the death of plants. The exposure of excess levels of metals to plants inhibits physiologically active enzymes [23], inactivates photosystems [24], and can possibly destroy the mineral metabolism. Janas et al. [25] have analyzed the impact of Cu on lipid peroxidation, growth, localization in lentil seedlings and phenolic compound accumulation. According to Xie et al. [26] and Chen [27] previous experiments have reported that dissolved soil organic substances have significant effects on heavy metal transformations by increasing the solubility of metal, plant uptake and root growth.

#### **4. The effects of some heavy metals on plants**

#### **4.1 Cu**

According to Burkhead *et al*. [28], due to the ability to cycle between the reduced Cu and oxidized Cu states, it is involved in biological processes such as

**19**

*Influence of Heavy Metals on the Nitrogen Metabolism in Plants*

oxygen species and harmful interactions at the cellular level.

photosynthesis, respiration, oxygen superoxide scavenging, ethylene sensing, lignification and cell wall metabolism. As an essential element, Cu can also be highly toxic [29]. Cu in a free form catalyzes reactions that generate hydroxyl radicals causing damage to lipids, proteins and DNA [30]. According to Bernal *et al.* [31], copper also has been reported to interfere with iron homeostasis. A highly reduction of plant biomass, inhibition of root growth, chlorosis, and necrosis are the most reported symptoms of a excess od Cu due to increased production of reactive

The roles that zinc plays in cellular processes is a good example of the diverse biological utility of metal ions. Zn is involved in protein, lipid metabolism, carbohydrate and nucleic acid. Moreover, Zn is critical to the control of biological processes regulated by proteins containing DNA-binding Zn-finger motifs and gene transcription [32]. The precise cause of Zn toxicity is unknown, but the metal may bind to inappropriate intracellular ligands, or compete with other metal ions for transporter proteins or enzyme active sites. In order to play these diverse roles in cells, and because it cannot passively diffuse across cell membranes, Zn must be transported into the intracellular compartments of the cell where it is required for

Ni is essential to several metabolic phenomena and is extremely toxic to plants when present at excessive levels in nutrient solutions or in the soil to which plants are exposed. According to Rahman et al. [33], the general signs associated with Ni toxicity in plants, include: reduced shoot and root growth, poor development of the branching system [34], deformation of various plant parts [35], abnormal flower shape [36, 37], decreased biomass production [33], leaf spotting [38], mitotic root tip disturbances [36], inhibition of germination [39], Fe deficiency leading to

According to Chen et al. [43], among all the heavy metals, cadmium (Cd) is considered to have high toxicity to humans and all other living organisms as it has no known biological functions in aquatic or terrestrial organisms. Through its effects on various biochemical and physiological processes in plants, Cd could inhibit plant growth and cause cell death above critical levels [44, 45]. Studies by Hassan et al. [46] reported that cadmium-induced growth reduction might be explained on the basis of inhibition of carbon fixation due to a decrease in photosynthetic rate and

In the presented chapter, we have provided data and reviews regarding the effect of heavy metals on nitrogen metabolism of plants and the responses of plants and the cross-talk of heavy metals and various stressors factors. Moreover, is clear to understand the relation between metals amount and the benefit or harm caused on plants, determining then, which mechanism should be activated to protect your physiological system. Additionally, we briefly show physiologically how this process occurs.

*DOI: http://dx.doi.org/10.5772/intechopen.97759*

these Zn-dependent processes.

chlorosis [40, 41], and foliar necrosis [42].

**4.2 Zn**

**4.3 Ni**

**4.4 Cd**

chlorophyll content.

**5. Conclusion**

*Influence of Heavy Metals on the Nitrogen Metabolism in Plants DOI: http://dx.doi.org/10.5772/intechopen.97759*

photosynthesis, respiration, oxygen superoxide scavenging, ethylene sensing, lignification and cell wall metabolism. As an essential element, Cu can also be highly toxic [29]. Cu in a free form catalyzes reactions that generate hydroxyl radicals causing damage to lipids, proteins and DNA [30]. According to Bernal *et al.* [31], copper also has been reported to interfere with iron homeostasis. A highly reduction of plant biomass, inhibition of root growth, chlorosis, and necrosis are the most reported symptoms of a excess od Cu due to increased production of reactive oxygen species and harmful interactions at the cellular level.

#### **4.2 Zn**

*Nitrogen in Agriculture - Physiological, Agricultural and Ecological Aspects*

Metal toxicity significantly reduces nitrogen assimilation process. However, the level of reduction depends on the sensitivity and localization of enzymes to heavy metal toxicity. Moreover, concentration, mobility and duration of heavy metal ions in growth medium further aggravate alterations in the process of nitrogen assimilation. The exposure to metals at higher concentrations could result in severe damage to various metabolic activities leading consequently to the death of plants. The exposure of excess levels of metals to plants inhibits physiologically active enzymes [23], inactivates photosystems [24], and can possibly destroy the mineral metabolism. Janas et al. [25] have analyzed the impact of Cu on lipid peroxidation, growth, localization in lentil seedlings and phenolic compound accumulation. According to Xie et al. [26] and Chen [27] previous experiments have reported that dissolved soil organic substances have significant effects on heavy metal transformations by

increasing the solubility of metal, plant uptake and root growth.

According to Burkhead *et al*. [28], due to the ability to cycle between the reduced Cu and oxidized Cu states, it is involved in biological processes such as

**4. The effects of some heavy metals on plants**

*Morphophysiological responses of plants to metal toxicity in soil.*

**18**

**4.1 Cu**

**Figure 2.**

The roles that zinc plays in cellular processes is a good example of the diverse biological utility of metal ions. Zn is involved in protein, lipid metabolism, carbohydrate and nucleic acid. Moreover, Zn is critical to the control of biological processes regulated by proteins containing DNA-binding Zn-finger motifs and gene transcription [32]. The precise cause of Zn toxicity is unknown, but the metal may bind to inappropriate intracellular ligands, or compete with other metal ions for transporter proteins or enzyme active sites. In order to play these diverse roles in cells, and because it cannot passively diffuse across cell membranes, Zn must be transported into the intracellular compartments of the cell where it is required for these Zn-dependent processes.

#### **4.3 Ni**

Ni is essential to several metabolic phenomena and is extremely toxic to plants when present at excessive levels in nutrient solutions or in the soil to which plants are exposed. According to Rahman et al. [33], the general signs associated with Ni toxicity in plants, include: reduced shoot and root growth, poor development of the branching system [34], deformation of various plant parts [35], abnormal flower shape [36, 37], decreased biomass production [33], leaf spotting [38], mitotic root tip disturbances [36], inhibition of germination [39], Fe deficiency leading to chlorosis [40, 41], and foliar necrosis [42].

#### **4.4 Cd**

According to Chen et al. [43], among all the heavy metals, cadmium (Cd) is considered to have high toxicity to humans and all other living organisms as it has no known biological functions in aquatic or terrestrial organisms. Through its effects on various biochemical and physiological processes in plants, Cd could inhibit plant growth and cause cell death above critical levels [44, 45]. Studies by Hassan et al. [46] reported that cadmium-induced growth reduction might be explained on the basis of inhibition of carbon fixation due to a decrease in photosynthetic rate and chlorophyll content.

#### **5. Conclusion**

In the presented chapter, we have provided data and reviews regarding the effect of heavy metals on nitrogen metabolism of plants and the responses of plants and the cross-talk of heavy metals and various stressors factors. Moreover, is clear to understand the relation between metals amount and the benefit or harm caused on plants, determining then, which mechanism should be activated to protect your physiological system. Additionally, we briefly show physiologically how this process occurs.

#### **Author details**

Vitor Nascimento1 \*, Glauco Nogueira<sup>2</sup> , Gabriel Monteiro2 , Waldemar Júnior3 , Joze Melissa Nunes de Freitas2 and Cândido Neto2

1 Federal University of Pará (UFPA), Belém, Brazil

2 Federal Rural University of Amazon (UFRA), Belém, Brazil

3 Secretary of State for the Environment and Sustainability (SEMAS), Belém, Brazil

\*Address all correspondence to: vitoresf@gmail.com

© 2021 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

**21**

397. 2013.

*Influence of Heavy Metals on the Nitrogen Metabolism in Plants*

Lenntech, Rotterdamseweg,

Purification.htm. 2004.

Edu 74:1369-1374. 1997.

ary.com/.

290. 1994.

83-100. 2006.

[10] Farlex Incorporated (2005) Definition: environment, the free dictionary, Farlex Inc. Publishing, USA. Available in: http://www.thefreediction

Netherlands Available in: http://www. excelwater.com/thp/filters/Water-

[9] HAWKES J,S. Heavy metals. J Chem

[11] MILDVAN, A.S. Metal in enzymes catalysis. In: Boyer DD (ed) The enzymes, vol 11. Academic Press, London, pp 445-536. 1970.

[12] RASKIN, I.; KUMAR, P.B.A.M.; DUSHENKOV, S.; SALT, D.E.

"Bioconcentration of heavy metals by

Biotechnology, vol. 5, no. 3, pp. 285-

[13] Brasil (2009) Resolução n° 420, de 28 de dezembro de 2009. Diário Oficial

[14] OLIVEIRA, D.L.; ROCHA, C.; MOREIRA, P.C.; MOREIRA, S.O.L. Plantas nativas do Cerrado: uma alternativa para fitorremediação. Estudos 36: 1141- 1159. 2009.

[15] MUNIZ, D.H.F.; OLIVEIRA-FILHO E.C. Metais pesados provenientes de rejeitos de mineração e seus efeitos sobre a saúde e o meio ambiente. Universitas: Ciências da Saúde 4:

[16] BECHER, M.; TALKE, I.N.; KRALL,

microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri.

L.; KRÄMER, U. Cross-species

Plant J. 37, 251-268. 2004.

plants," Current Opinion in

da União 249: 81-84. 2009.

*DOI: http://dx.doi.org/10.5772/intechopen.97759*

[1] VIEIRA, R.S. Ciclo do Nitrogênio em sistemas agrícolas. Empresa Brasileira de Pesquisa Agropecuária (EMBRAPA), Brasília, Brazil. Available in: 2017LV04.

[2] PALLARDYS, S. G. Chapter 9 – Nitrogen metabolism. In: Pallardys, S.G. (Ed.). Physiology of woody plants. 3.ed. San Diego: Academic Press. p.233-254. Available in: http://dx.doi.org/10.1016/ B978-012088765-1.50010-5. 2008.

[3] TERCE-LAFORGUE, T.; GISELA, M.; HIREL, B. New insights towards the function of glutamate dehydrogenase revealed during source-sink transition of tobacco (Nicotiana tabacum L.) plants grown under different nitrogen regimes. Physiologia Plantarum, v.120,

[4] LEA, P.J., AZEVEDO, R.A. Nitrogen use efficiency. 1. Uptake of nitrogen from the soil. Annals of Applied Biology, v.149, n.3, p.243-247. Available in: http://dx.doi.org/10.1111/j.1744-

[5] MILLER, A.J, CRAMER, M.D. Root nitrogen acquisition and assimilation. Plant Soil, v.274, n.1-2, p.1-36. Available in: http://dx.doi.org/10.1007/s11104-

[6] BLACKWELL, R. D.; MURRAY, A. J.

Photosynthesis in Barley with Decreased Levels of Chloroplastic Glutamine Synthetase Activity. Journal of Experimental Botany, v.38, n.11, p.

[7] LI, S. X.; WANG, Z. H.; STEWAR, B.

ammonium and nitrate N. Advances in Agronomy, San Diego, v. 118, p. 205-

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A. Responses of crop plants to

Purification. Water treatment.

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pdf (embrapa.br). 2017.

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*Influence of Heavy Metals on the Nitrogen Metabolism in Plants DOI: http://dx.doi.org/10.5772/intechopen.97759*

#### **References**

*Nitrogen in Agriculture - Physiological, Agricultural and Ecological Aspects*

**20**

**Author details**

Vitor Nascimento1

Joze Melissa Nunes de Freitas2

\*, Glauco Nogueira<sup>2</sup>

2 Federal Rural University of Amazon (UFRA), Belém, Brazil

1 Federal University of Pará (UFPA), Belém, Brazil

\*Address all correspondence to: vitoresf@gmail.com

provided the original work is properly cited.

, Gabriel Monteiro2

and Cândido Neto2

3 Secretary of State for the Environment and Sustainability (SEMAS), Belém, Brazil

© 2021 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium,

, Waldemar Júnior3

,

[1] VIEIRA, R.S. Ciclo do Nitrogênio em sistemas agrícolas. Empresa Brasileira de Pesquisa Agropecuária (EMBRAPA), Brasília, Brazil. Available in: 2017LV04. pdf (embrapa.br). 2017.

[2] PALLARDYS, S. G. Chapter 9 – Nitrogen metabolism. In: Pallardys, S.G. (Ed.). Physiology of woody plants. 3.ed. San Diego: Academic Press. p.233-254. Available in: http://dx.doi.org/10.1016/ B978-012088765-1.50010-5. 2008.

[3] TERCE-LAFORGUE, T.; GISELA, M.; HIREL, B. New insights towards the function of glutamate dehydrogenase revealed during source-sink transition of tobacco (Nicotiana tabacum L.) plants grown under different nitrogen regimes. Physiologia Plantarum, v.120, n.2, p.220-228. 2004.

[4] LEA, P.J., AZEVEDO, R.A. Nitrogen use efficiency. 1. Uptake of nitrogen from the soil. Annals of Applied Biology, v.149, n.3, p.243-247. Available in: http://dx.doi.org/10.1111/j.1744- 7348.2006.00101.x. 2006.

[5] MILLER, A.J, CRAMER, M.D. Root nitrogen acquisition and assimilation. Plant Soil, v.274, n.1-2, p.1-36. Available in: http://dx.doi.org/10.1007/s11104- 004-0965-1. 2004.

[6] BLACKWELL, R. D.; MURRAY, A. J. S.; LEA, P. J. Inhibition of Photosynthesis in Barley with Decreased Levels of Chloroplastic Glutamine Synthetase Activity. Journal of Experimental Botany, v.38, n.11, p. 1799-1809. 1987.

[7] LI, S. X.; WANG, Z. H.; STEWAR, B. A. Responses of crop plants to ammonium and nitrate N. Advances in Agronomy, San Diego, v. 118, p. 205- 397. 2013.

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[21] PÉREZ-TIENDA, J.; CORRÊA, A.; AZCÓN-AGUILAR, C. et al. Transcriptional regulation of host NH4 + transporters and GS/GOGAT pathway in arbuscular mycorrhizal rice roots. Plant Physiol Biochem 75:1-8. 2014.

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[26] XIE, Z.; WU, L.; CHEN, N.; LIU, C.; ZHENG, Y. et al. Phytoextraction of Pb and Cu contaminated soil with maize and microencapsulated EDTA. Int J Phytoremediation 14: 727-740. 2012.

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Cell 24: 738-761. 2012.

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rocks, minerals, metals and

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AZCÓN-AGUILAR, C. et al.

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**22**

[33] RAHMAN H, SABREEN S, ALAM S, KAWAI S. Effects of nickel on growth and composition of metal micronutrients in barley plants grown in nutrient solution. J Plant Nutr 28:393- 404. 2005.

[34] REEVES RD, BAKER AJM, BGRHIDI A, BERAZAÍN R. Nickelaccumulating plants from the ancient serpentine soils of Cuba. New Phytol 133:217-224. 1996.

[35] WRIGHT DA, WELBOURN P (2002) Environmental Toxicology. Cambridge University Press. 2002.

[36] McIlveen WD, Negusanti JJ. Nickel in the terrestrial environment. Sci Total Environ 148:109-138. 1994.

[37] MISHRA D, KAR M. Nickel in plant growth and metabolism. Bot Rev 40:395-452. 1974.

[38] GAJEWSKA E, SKŁODOWSKA M, SŁABA M, Mazur J (2006) Effect of nickel on antioxidative enzyme activities, proline and chlorophyll contents in wheat shoots. Biol Plant 50(4):653-659.

[39] NEDHI A, SINGH LJ, SINGH SI. Effect of cadmium and nickel on germination, early seedling growth and photosynthesis of wheat and pigeon pea. Ind J Trop Agri 8:141-147. 1990.

[40] EWAIS EA (1997) Effects of cadmium, nickel and lead on growth, chlorophyll content and proteins of weeds. Biol Plant 39:403-410.

[41] KIRKBY EA, RÖMHELD V. Micronutrients in plant physiology: Functions, uptake and mobility. Proceedings No. 543, International Fertiliser Society, York, UK. 1-51. 2004.

[42] KUKKOLA E, RAUTIO P, HUTTUNEN S. Stress indications in copper- and nickel-exposed Scots pine seedlings. Environ Exp Bot 43:197- 210. 2000.

[43] CHEN F, DONG J, WANG F, WU F, ZHANG G, LI G, *et al*, Identification of barley genotypes with low grain Cd accumulation and its interactionwith fourmicroelements. Chemosphere **67**:2082-2088. 2007.

[44] POPOVA LP, MASLENKOVA LT, YORDANOVA RY, IVANOVA AP, KRANTEV AP and SZALAI G, Exogenous treatment with salicylic acid attenuates cadmium toxicity in pea seedlings. Plant Physiol Biochem 47:224-231. 2009.

[45] XU J, YIN HX and LI X, Protective effects of proline against cadmium toxicity in micropropagated hyperaccumulator, *Solanum nigrum* L. Plant Cell Rep **28**:325-333. 2009.

[46] HASSAN MJ, WANG F, ALI S and ZHANG G, Toxic effects of cadmium on rice as affected by nitrogen fertilizer form. Plant Soil **277**:359- 365 (2005).

**25**

Section 2

Nitrogen Fertilizers and

Nitrogen Management in

Agriculture

## Section 2
