Chapter 9

Tolerance of Plants to Toxicity Induced by

Micronutrients

Allan Klynger da Silva Lobato, Emily Juliane Alvino Lima,

Elaine Maria Silva Guedes Lobato, Gabriel Mascarenhas Maciel and
Douglas José Marques

Additional information is available at the end of the chapter

http://dx.doi.org/10.5772/62046

Abstract

Micronutrient elements such as zinc, boron copper, iron, manganese, molybdenum, and
chlorine are frequently responsible by the regulatory activity of the cell organelles, being
nutrients that are absorbed and found in lower concentrations in plant tissues, they also
contribute to supply the nutritional exigency of the plant. Study with Zea mays plants ex‐
posed to Zn toxicity + Si presented significant increases in stomatal conductance, net pho‐
tosynthetic rate, transpiration rate, and water use efficiency, respectively, in comparison
with treatment only with Zn. In relation to chlorophylls a, b and total and carotenoids
presented non-significant increases, when compared to plants exposed to Zn toxicity.
This study revealed the positive contribution of the Si on gas exchange and reduction of
the negative effects provoked on chlorophylls and carotenoids in maize plants under Zn
toxicity. Other results described that prolonged exposure to excessive Cu resulted in seri‐
ous toxic effects on the rice seedlings. In contrast, Tre pretreatment has been shown to be
beneficial in alleviating Cu toxicity, which was mainly attributed to the ability of Tre to
restrict Cu uptake and accumulation to maintain Cu homeostasis, and to induce produc‐
tion of antioxidant and Gly enzymes to alleviate excessive Cu-triggered oxidative stress.
Stress caused by the excessive supply of micronutrients to plants frequently promotes re‐
percussions on oxidant system, inducing the overproduction of reactive oxygen species.
The oxidative damage is a situation characterized by the large ROS accumulation and in‐
sufficient detoxification promoted by antioxidant enzymes, such as catalase and gluta‐
thione peroxidase. Different mechanisms have been proposed to explain the tolerance of
plants to toxicity induced by micronutrients, as uses of other elements and substances, in
which it can positively act with specific transporters, metal ion homeostasis and compart‐
mentalization of micronutrients into the vacuole.

Keywords: gas exchange, antioxidant metabolism, metals, photosynthetic pigments

© 2016 The Author(s). Licensee InTech. 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.
230 Abiotic and Biotic Stress in Plants - Recent Advances and Future Perspectives

1. Introduction

Large amounts of minerals and organic materials can be found in soil [1]; and some of these
materials have great significance in the anatomical development and plant morphology. The
soil fertility is an important factor of agronomic order. It is related to provision of essential
elements in the soil, where the plant will absorb adequate levels of important substances to
work with its metabolism [2]. The nutrients are arranged in ionic form, which can interact with
the root system of plants via three mechanisms: interception root, diffusion, or mass flow [3].
The plants require basic conditions to develop and supply the essential elements to aid with
the metabolism and produce simple and/or complex compounds [4]. These are divided into
non-minerals and minerals, which are sub-divided into macro and micronutrients.

2. Non-mineral nutrients

The non-mineral nutrients are hydrogen (H), oxygen (O), and carbon (C). These elements help
in the formation of tissues. They are responsible for the composition of lipids, carbohydrates,
proteins, nucleic acids, and hormones in plants [5]. Hydrogen (H) is the element that contrib‐
utes to nitrogen fixation and photosynthesis; this is due to their reducing capacity molecules,
being a nutrient assimilated from the water. Oxygen (O) is extracted from atmosphere and
water, it is used during the process of cell respiration, where sugar transferred by the photo‐
synthetic process is transformed into energy. The plant captures the Carbon (C) in the form of
CO2 from atmosphere. It is an organic nutrient with function to ensure the occurrence of
physical, chemical, and biological cycles, ensuring the maintenance of energy reserves
throughout vegetative growth.

3. Nutrients minerals

These are elements essential for plant to complete its cycle [6]. They are divided into macro
and micronutrients [7].

3.1. Macronutrients

The macronutrients are composed by nitrogen (N), phosphorus (P), potassium (K), calcium
(Ca), magnesium (Mg), and sulphur (S). Large amount of these elements are required for plants
to develop and meet its physiological activity. The macronutrients play a vital role in plant
structure [8].

3.2. Micronutrients

These elements are responsible for the regulatory activity of the cell organelles. These nutrients
are absorbed and found in lower concentrations in plant tissues and supply the nutritional
exigency of the plant [9].
 Tolerance of Plants to Toxicity Induced by Micronutrients 231
http://dx.doi.org/10.5772/62046

3.2.1. Zinc (Zn)

Zinc is an essential component in thousands of proteins in plants, in which it performs the role
of enzymatic activator in various processes related to plant metabolism, such as dehydrogen‐
ases, aldolases, isomerases and transphorylases [10]. Its deficiency affects plant development,
with stems and leaf expansion directly affected, and also reported to have consequences on
chlorophyll levels and possibly necrosis [11].

3.2.2. Boron (B)

Boron is a nutrient that works with the carbohydrate metabolism and transport of sugars
through membranes. This element acts in the formation of the cell wall, sap movement, cell
division, development of leaves and inflorescence, and confer resistance to tissues [12]. Its
deficiency causes disorder in meristematic activities and reserve mechanisms can be directly
affected, with the stem apex, flowers and fruits suffer deformations [13].

3.2.3. Copper (Cu)

The copper activity is related to photosynthetic and respiration processes, fixation, and
distribution of the nitrogen, all being necessary during plant cycle [14]. When the plant does
not absorb adequate amount of this element for their development, it may present negative
characteristics, such as changes of colour and structure in leaf [15].

3.2.4. Iron (Fe)

Iron is an essential micronutrient used in photosynthesis, cell division, nitrogen fixation, and
formation and morphology of plants [16-17]. The excess of this element affects the leaf, and
their growth is strongly reduced [18]. The deficiency induces chlorosis [19].

3.2.5. Manganese (Mn)

Manganese is a micronutrient of essential character. It plays the metabolic activities of direct
or indirect orders, with capacity to activate enzymes responsible for the control of oxidation-
reduction processes, such as the production of chlorophylls [20]. The low concentration of this
micronutrient causes loss of leaf due to appearance of small spots on leaves and chlorosis, and
structural development of the plant normally is compromised [21].

3.2.6. Molybdenum (Mo)

Molybdenum is a micronutrient that helps in nitrogen fixation and nitrate assimilation [22].
With the deficiency of this nutrient, plants are affected by chlorotic spots and marginal
necrosis, thus the plant yield is negatively affected [23].

3.2.7. Chlorine (Cl)

Chlorine acts in the photosynthetic process of plants, aside from interacting with water and
during transpiration process [24]. The lack of chlorine causes chlorosis and necrosis, roots
232 Abiotic and Biotic Stress in Plants - Recent Advances and Future Perspectives

suffer atrophy, affecting the development of the plant [25]. The excess of chlorine in the soil is
more common than the deficiency. Indication of its excess is signalled by the burn of the leaf
edges [26].

4. Toxicity of micronutrients

Despite micronutrients be required in higher plants, in higher concentrations frequently is

toxic and provokes negative effects [27], as reduction in photosynthetic pigments [28], minor
integrity and permeability of membranes [29], increase of the oxidative stress related with
production and accumulation of reactive oxygen species (ROS), besides to increase the
activities of antioxidant enzymes [30], and in levels more extremes to induce cell death [31].
Stress caused by the excessive supply of nutrients to plants promotes repercussion on oxidant
system [32-33], inducing the overproduction of reactive oxygen species (ROS) as superoxide
radical (O2-) and hydrogen peroxide (H2O2) [34]. The oxidative damage is a situation charac‐
terized by the large ROS accumulation and insufficient detoxification promoted by antioxidant
enzymes, such as catalase and glutathione peroxidase [35].
Different mechanisms have been proposed to explain the tolerance of plants to toxicity induced
by heavy metals and nutrients. Two specific transporters are metal ion homeostasis and
compartmentalization of metals into the vacuole [36-37]. However, responses linked to
contribution of Si in plants submitted to Zn excess, more specifically on gas exchanges and
photosynthetic pigments, are unknown.
Beneficial repercussions related to Si uses in higher plants are intensively found [38-40]. Isa et
al. [41] reported that Si is largely accumulated in leaves. Silva et al. [42] described increases in
chlorophylls produced by exogenous Si application. Si also induces higher mechanical
resistance from cell wall [43]. Chen et al. [44] found better light reception and increasing net
photosynthesis rate and CO2 capitation after Si treatment.

5. Objectives

This chapter aim to: (i) define what nutrient toxicity is; (ii) present the modifications produced
in the biochemical and physiological levels; (iii) explain the consequences to plant induced by
the nutrient toxicity.

6. Effects of zinc toxicity in gas exchange

Study conducted by Paula et al. [45] with Zea mays plants under Zn toxicity and treated with
Si (silicon) evaluating the gas exchanges and photosynthetic pigments was shown in Figure
1. Zinc toxicity produced a negative interaction promoting stomatal closing, and consequently,
 Tolerance of Plants to Toxicity Induced by Micronutrients 233
http://dx.doi.org/10.5772/62046

reduction in stomatal conductance. This effect can be attributed to Zn excess, in which it will
induce a minor density and size of these structures, with structural differences in adaxial and
abaxial sides, besides minor stomatal aperture sizes [46]. Similar results were obtained by
Pavlíková et al. [47] in Nicotiana tabacum plants submitted to stress by Zn.

Figure 1. Stomatal Conductance (A), Photosynthesis Rate (B), Transpiration Rate (C), and Water Use Efficiency (D) in
Zea mays plants subjected to silicon and zinc toxicity. Different letters to treatments indicate significant differences
from the Skott-Knott test (P < 0.05). Columns represent the mean values from four repetitions, and bars represent the
standard deviations [45].

Zn induced a reduction in net photosynthetic rate, as explained by the stomatal limitation,

arising of minor stomatal conductance, and consequent decrease of the CO2 assimilation to
photosynthetic process [48-49]. Similar results were found by Shi and Cai [50] working with
Arachis hypogaea plants submitted to Zn stress, corroborating with results obtained in this
research.
234 Abiotic and Biotic Stress in Plants - Recent Advances and Future Perspectives

The reduction of the transpiration in plants under exogenous application of Zn was possibly
attributed to decrease in stomatal conductance. This stomatal limitation reduces the transpi‐
ration rate, promoting minor water loss from plant to atmosphere, and consequently limited
nutrients reposition, in form of adsorbed ions into substrate with water, using the via root
system [51]. In other words, the transpiration is responsible with the dynamic of nutrient
transport form substrate in direction root and leaf [52], thus avoid the cavitation in xylem [53].
Fernàndez et al. It was also described thatthere is a significant reduction in transpiration rate
in Populus deltoides plants submitted to high Zn concentrations [54].

The exogenous application of Si promoted an increase in water use efficiency (WUE), this result
can be explained by the increase in net photosynthetic rate (PN) and maintenance in transpi‐
ration rate (E). The ratio between photosynthesis and transpiration will result in WUE [55],
being a physiological parameter that describes quantitatively the behavior momentaneous of
the gas exchanges in leaf, it also reveals the efficiency that the plant utilizes the water resource
[56]. Our results are corroborated by Moussa [57] working with Zea mays seedlings under
exogenous application of Si.

7. Zinc toxicity and silicon benefits on photosynthetic pigments

Figure 2 shows the same study conducted by Paula et al. [45] on photosynthetic pigments in
Zea mays plants under Zn toxicity and Si. The decrease in CHL a occurred due to Zn toxicity,
being probably related to minor biosynthesis rate of CHL a [58]. The Zn excess negatively
interferes in NADPH availability into chloroplasts [59], because the NADPH is one of the
substrates of the divinyl chlorophyllide an 8-vinyl-reductase enzyme, which is responsible to
CHL a synthesis [60].

The chlorophylls are responsible to the photochemical and biochemical reactions during light
capitation [61], while carotenoids present an important role related to photoprotection against
excessive sunlight [62], given that both pigments work simultaneously into photosynthetic
machinery [63]. However, the excessive B supply represents a problem to photosynthetic
pigments, with consequent decrease in chlorophylls [64-65].

The Zn excess promoted a decrease in CHL b level, and this result can be explained by the
oxidative stress induced by the overproduction of reactive species oxygen (ROS), such as
H2O2 [66-67]. The H2O2 aside from being toxic in chloroplasts, is considered an inhibitor of the
carbon metabolism, [68], resulting in acceleration of leaf senescence through of the lipid
peroxidation and oxidative damages [69]. Similar results were reported by Bettaieb [70]
evaluating Solanum tuberosum cultivars.

The CHL total levels were reduced after Zn toxicity, which is related to magnesium (Mg)
substitution in molecule of chlorophyll by the Zn. It will result to the inadequate work of the
light-harvesting complex (LHCII), and consequently the photosynthesis limitation [71-73]. Our
results on reduction in CHL total were corroborated by Bassi and Sarma [74] in Triticum
aestivum seedlings.
 Tolerance of Plants to Toxicity Induced by Micronutrients 235
http://dx.doi.org/10.5772/62046

Figure 2. Chlorophyll a (A), Chlorophyll b (B), Total Chlorophyll (C) and Carotenoids (D) in Zea mays plants subjected
to silicon and zinc toxicity. Different letters to treatments indicate significant differences from the Skott-Knott test (P <
0.05). Columns represent the mean values from four repetitions, and bars represent the standard deviations [45].

8. Boron toxicity induces modifications in nitrogen metabolism

Silva et al. [75] working with Schizolobium parahyba plants exposed to progressive boron levels
determined amino acids total and proline is depicted in Figure 2. The total amino acids
accumulated in leaf must be associated to proteases enzyme activity and concomitantly to
inhibition of the protein biosynthesis rate, due to the high B levels. According to Paula et al.
[76], the increases in proteases activities promote the breakdown and consequent decrease of
proteins, increasing the total AA amount, which will be used in synthesis of other AA, like as
PRO. Cervilla et al. [77] evaluating the effects of the B toxicity in Solanum lycopersicum plants
found similar results.
236 Abiotic and Biotic Stress in Plants - Recent Advances and Future Perspectives

Figure 3. Electrolyte Leakage (A), Total Amino Acids (B), Proline (C) of young Schizolobium parahyba var. amazonicum
plants subjected to boron toxicity. Different letters for boron levels indicate significant differences from the Skott-Knott
test (P<0.05). Columns represent the mean values from 5 repetitions, and bars represent the standard deviations [75].

The proline concentration was maximized and this result is related to the amino acid acting in
detoxification process of ROS and membrane protection against lipid peroxidation [78-79];
associated with ROS antagonist, it aims to attenuate the oxidative stress and to avoid the cell
death. In other activities, the PRO protects the protein structure against denaturation and it
will stabilize the cell membranes during interaction with phospholipids [80]. Contreras et al.
[81] evaluating the B and NaCl effects in Solanum lycopersicum plants verified similar results
of this research.

Proline is an amino acid synthetized into nitrogen metabolism with functions related to
osmoprotection [82] and cellular homeostasis [83], which can contribute to improve the plant
tolerance under situations of abiotic stress, as B toxicity.
 Tolerance of Plants to Toxicity Induced by Micronutrients 237
http://dx.doi.org/10.5772/62046

9. Effects of the copper toxicity and exogenous trehalose on antioxidant

enzymes

In agreement with Mostofa et al. [84], the regulating Cu homeostasis is crucial in maintaining
the intracellular Cu level to avoid toxicity. Plants have developed various mechanisms to restrict
Cu toxicity, such as inhibition of Cu uptake by binding with root exudates like organic acids,
intracellular sequestration by strong ligands like cysteine-rich compounds and phytochela‐
tins, and exclusion of excessive Cu from the cells by sugar alcohols like trehalose (Tre) [26–28].
Tre, a non-reducing disaccharide of glucose, protects plant cells against long-term desiccation
by stabilizing enzymes, proteins, and biological membranes under dehydration [29].

In relation to antioxidant enzymes superoxide dismutase (SOD), catalase (CAT), glutathione

peroxidase (GPX), and glutathione reductase (GST), the pretreatment with non-reducing
disaccharide Tre induces increases in enzyme activities when compared with control or Cu
stress treatments (Figure 4).

Figure 4. Effect of exogenous trehalose on the activities of antioxidant enzymes in rice seedlings with or without Cu
stress. (a) Superoxide Dismutase (SOD), (b) Catalase (CAT), (c) Glutathione Peroxidase (GPX), and (d) Glutathione Re‐
ductase (GST). Control, Tre, Cu, and Tre + Cu correspond to control, 10 mM trehalose, 100 μM CuSO4, and 10 mM
trehalose + 100 μM CuSO4, respectively. Bars represent standard deviation (SD) of the mean (n = 3). Different letters
indicate significant differences among treatments at p < 0.05, according to Duncan’s multiple range test [84].
238 Abiotic and Biotic Stress in Plants - Recent Advances and Future Perspectives

NBT staining indicated an increased amount of O2– as scattered dark blue spots in the leaf
plate of the Cu-stressed seedlings compared with the non-treated control (Figure 5a).
Similarly, DAB staining confirmed a marked increase in brown polymerization products,
which indicated the over-accumulation of H2O2 in the leaves of the Cu-stressed seedlings
relative to control (Figure 5b) [84].

Results described by Mostofa et al. [84] indicate that prolonged exposure to excessive Cu
resulted in serious toxic effects on the rice seedlings. In contrast, Tre pretreatment has been
shown to be beneficial in alleviating Cu toxicity, which was mainly attributed to the ability
of Tre (i) to restrict Cu uptake and accumulation to maintain Cu homeostasis, and (ii) to
induce production of antioxidant and Gly enzymes to alleviate excessive Cu-triggered
oxidative stress [84].

Figure 5. Effect of exogenous trehalose on ROS accumulation in leaves of rice seedlings with or without Cu stress. (a)
Superoxide (O2−) and (b) Hydrogen Peroxide (H2O2) production in rice leaves were detected using nitro-blue tetrazoli‐
um (NBT) solution and 3,3'-diaminobenzidine (DAB), respectively, at day 7 of Cu stress. Control, Tre, Cu, and Tre + Cu
correspond to control, 10 mM trehalose, 100 μM CuSO4, and 10 mM trehalose + 100 μM CuSO4, respectively [84].

10. Final considerations

Micronutrient elements such as zinc, boron copper, iron, manganese, molybdenum, and
chlorine are responsible to the regulatory activity of the cell organelles. These nutrients are
absorbed and found in lower concentrations in plant tissues, and contribute to supply the
nutritional exigency of the plant.

Study with Zea mays plants exposed to Zn toxicity + Si presented more significant increases in
stomatal conductance, net photosynthetic rate, transpiration rate, and water use efficiency
 Tolerance of Plants to Toxicity Induced by Micronutrients 239
http://dx.doi.org/10.5772/62046

compared with the treatment only with Zn. On the contrary, chlorophylls a, b and total and
carotenoids presented non-significant increases when compared with plants exposed to Zn
toxicity.

This study also revealed the positive contribution of the Si on gas exchange and reduction of
the negative effects provoked on chlorophylls and carotenoids in Zea mays plants under Zn
toxicity. Other result described that prolonged exposure to excessive Cu resulted in serious
toxic effects on the rice seedlings. In contrast, Tre pretreatment has been shown to be beneficial
in alleviating Cu toxicity, which was mainly attributed to the ability of Tre to restrict Cu uptake
and accumulation to maintain Cu homeostasis. It induced production of antioxidant and Gly
enzymes to alleviate excessive Cu-triggered oxidative stress.

Stress caused by the excessive supply of micronutrients to plants promotes repercussion on

oxidant system, inducing the overproduction of reactive oxygen species. The oxidative
damage is a situation characterized by the large ROS accumulation and insufficient detoxifi‐
cation promoted by antioxidant enzymes, such as catalase and glutathione peroxidase.
Different mechanisms have been proposed to explain the tolerance of plants to toxicity induced
by micronutrients, as uses of other elements and substances, in which it can positively act with
specific transporters, metal ion homeostasis and compartmentalization of micronutrients into
the vacuole.

Acknowledgements

This chapter had financial support from Fundação Amazônia Paraense de Amparo à Pesquisa
(FAPESPA/Brazil), Universidade Federal Rural da Amazônia (UFRA/Brazil) and Conselho
Nacional de Pesquisa (CNPq/Brazil) to Lobato AKS.

Author details

Allan Klynger da Silva Lobato1*, Emily Juliane Alvino Lima1,

Elaine Maria Silva Guedes Lobato1, Gabriel Mascarenhas Maciel2 and
Douglas José Marques3

*Address all correspondence to: [email protected]

1 Núcleo de Pesquisa Vegetal Básica e Aplicada, Universidade Federal Rural da Amazônia,

Paragominas, Brazil

2 Instituto de Ciências Agrárias, Universidade Federal de Uberlândia, Monte Carmelo,

Brazil

3 Setor de Olericultura e Experimentação, Universidade José do Rosário Vellano

(UNIFENAS), Alfenas, Brazil
240 Abiotic and Biotic Stress in Plants - Recent Advances and Future Perspectives

References

[1] Pavinato, P.S. and Rosolem, C.A. Disponibilidade de nutrientes no solo - Decomposi‐
ção e liberação de compostos orgânicos de resíduos vegetais. Revista Brasileira de
Ciência do Solo. 2008;32:911-920. DOI: 10.1590/S0100-06832008000300001.

[2] Arnon, D.I. and Stout, P.R.. The essentiality of certain elements in minute quantity
for plants with special reference to copper. Plant Physiology. 1939;14(2):371-375.

[3] Epstein, E. and Hagen, C.E. A kinetic study of the absorption of alkali cations by bar‐
ley roots. Plant Physiology. 1952;27:457-474. DOI: 10.1104/pp.27.3.457.

[4] Laviola, B.G and Dias, A.S. Teor e acúmulo de nutrientes em folhas e frutos de pin‐
hão-manso. Revista Brasileira de Ciencia do Solo. 2008;32:1969-1975.

[5] Malavolta, E. Manual de nutrição mineral de plantas.1ed. São Paulo: Agronômica

Ceres; 2006.638p.

[6] Borkert, C.M., Gaudêncio, C.A., Pereira, J.E., Pereira, L.R., Oliveira, A.J. Junior. Nu‐
trientes minerais na biomassa da parte aérea em culturas de cobertura de solo. Pes‐
quisa Agropecuária Brasileira. 2003;38:143-153. DOI: 10.1590/
S0100-204X2003000100019.

[7] Mengel, K., Kirkby, E. Principles of plant nutrition. 5ed. Dordrecht/Boston/London:

Kluwer Academic Publishers; 2001.849p.

[8] Coelho, V.A.T., Rodas, C.L., Coelho, L.C, Carvalho, J.G., Almeida, E.F.A., Figueiredo,
M.A. Caracterização de sintomas visuais de deficiências de macronutrientes e boro
em plantas de gengibre. Revista Brasileira de Horticultura Ornamental. 2012;18:
47-55.

[9] Welch, R.M and Shuman, R. Micronutrient Nutrition of Plants. Plant Sciences.
1995;14(1):49-82. DOI: 10.1080/07352689509701922.

[10] Andreotti, M., Souza, E.C.A., Crusciol, C.A.C. Componentes morfológicos e produ‐
ção de matéria seca de milho em função da aplicação de calcário e zinco. Scientia Ag‐
ricola. 2001;58:321-327.

[11] Cakmak, I.. Possible role of zinc in protecting plant cells from damage by reactive
oxygen species. New Phytologist. 2000;146:185–205.

[12] Bastos, A.R.R. and Carvalho, J.G. Absorção radicular e redistribuição do boro pelas
plantas, e seu papel na parede celular. Revista Univiversidade Rural, Série Ciencias
da Vida. 2004.;24:47-66.

[13] Viégas, I.J.M., Thomaz, M.A.A., Silva, J.F., Conceição, H.E.O., Naiff, A.P.M. Efeito da
omissão de macronutrientes e boro no crescimento, nos sintomas de deficiências nu‐
tricionais e na composição mineral de plantas de camucamuzeiro. Revista Brasileira
de Fruticultura. 2004;26:315-319.
 Tolerance of Plants to Toxicity Induced by Micronutrients 241
http://dx.doi.org/10.5772/62046

[14] Luchese, A.V., Gonçalves, A.C.J., Luchese, E.B., Braccini, M.C.L. Emergência e absor‐
ção de cobre por plantas de milho (Zea mays) em resposta ao tratamento de sementes
com cobre. Ciência Rural. 2004;34:1949-1952.

[15] Yruela,I.. Copper in plants. Brazilian Journal Plant Physiology. 2005;17(1):145-156.

[16] Marenco, R.A., Lopes, N.F.. Fisiologia Vegetal: Fotossíntese, respiração, relações
hídricas e nutrição mineral.Viçosa: Editora UFV; 2005. 451p.

[17] Alexander J.R., Oliveira, M.L.F., Santos, T.C.S., Canton, G.C., Conceição, J.M, Eutró‐
pio, F.J., Cruz, Z.M.A., Dobbss, L.B., Ramos, A.C. Zinco e ferro: de micronutrientes a
contaminantes do solo. ESFA [online] http://www.naturezaonline.com.br. 2012 ;10(1):
23-28.

[18] Kuki, K.N., Oliva, M.A., Costa, A.C. The simulated effects of iron dust and acidity
during the early stages of establishment of two coastal plant Species. Water Air Soil
Pollution. 2009;196:287–295.

[19] Hellín, E., Hernández-Cortés, J.A., Piqueras, A., Olmos, E., Sevilla, F. The influence of
the iron content on the superoxide dismutase activity and chloroplast ultrastructure
of Citrus limon. Developments in Plant and Soil Sciences. 1995;59:247-254. DOI:
10.1007/978-94-011-0503-3_36.

[20] Hoagland, D.R. and Arnon, D.L. The water culture methods for growing plants with‐
out soil. California Agriculture Experiment Station. 1950.;347:1-32.

[21] Fernandes, D.S., Soratto, R.P., Kulczynski, S.M., Biscaro, G.A., Reis, C.J. Produtivi‐
dade e qualidade fisiológica de sementes de feijão em conseqüência da aplicação fo‐
liar de manganês. Pesquisa Agropecuária Brasileira. 2007;42:419-426.

[22] Dechen, A.R., Haag, H.P., Carmello, Q.A.C. Mecanismos de absorção e de transloca‐
ção de micronutrientes In: FERREIRA, M.E., CRUZ, M.C.P. (Ed.) Micronutrientes na
agricultura. Piracicaba: Potafós/CNPq, 1991. 134p, p.79-97.

[23] Yuri, J.E., Resende, G.M., Mota, J.H., Gonçalves, L.D.,Souza, R.J. Doses e épocas de
aplicação de molibdênio na produção e qualidade de alface americana. Horticultura
Brasileira. 2004;22:589-592.

[24] Broyer, T.C., Carlton, A.B., Johson, C.M., Stout, P.R. Chlorine: a micronutrient ele‐
ment for higher plants. Plant Physiology. 1954;29:526-532.DOI 10.1104/pp.29.6.526.

[25] Xu, S., Huang, H.K., Kaiser, P., Latterich, M., Hunter, T. Phosphorylation and spindle
pole body localization of the Cdc15p mitotic regulatory protein kinase in budding
yeast. Current Biology. 2000;10(6):329-32.

[26] Mascarenhas, H.A.A., Neptune, A.M.L., Muraoka, T., Bulisani, E.A., Hiroce, R. Ab‐
sorção de nutrientes por cultivares de soja (Glicine max (L.) Merril). Revista Brasileira
de Ciência do Solo. 1980;4:92-96.
242 Abiotic and Biotic Stress in Plants - Recent Advances and Future Perspectives

[27] Garbisu, C. and Alkorta, I. Basic concepts on heavy metal soil bioremediation. Euro‐
pean Journal of Mineral Processing and Environmental Protection. 2003;3:58-66.

[28] Radic, S., Babic, M., Skobic, D., Roje, V. Ecotoxicological effects of aluminum and
zinc on growth and antioxidants in Lemna minor L. Ecotoxicology and Environmental
Safety. 2010;73(3):336-342. DOI: 10.1016/j.ecoenv.2009.10.014.

[29] Stoyanova, Z. and Doncheva S. The effect of zinc supply and succinate treatment on
plant growth and mineral uptake in pea plant. Brazilian Journal of Plant Physiology.
2002;14:111-116. DOI: 10.1590/S1677-04202002000200005.

[30] Jain, R., Srivastava, S., Solomon, S., Shrivastava, A.K., Chandra A. Impact of excess
zinc on growth parameters, cell division, nutrient accumulation, photosynthetic pig‐
ments and oxidative stress of sugarcane (Saccharum spp.). Acta Physiologiae Planta‐
rum. 2010;32:979-986. DOI: 10.1007/s11738-010-0487-9.

[31] Chang, H.B., Lin, C.W., Huang, H.J. Zinc-induced cell death in rice (Oryza sativa L.)
roots. Plant Growth Regulation. 2005;46(3):261-266. DOI: 10.1007/s10725-005-0162-0.

[32] Molassiotis, A., Sotiropoulos, T., Tanou, G., Diamantidis, G., Therios, I. Boron-in‐
duced oxidative damage and antioxidant and nucleolytic responses in shoot tips cul‐
ture of the apple rootstock EM 9 (Malus domestica Borkh). Environmental and
Experimental Botany. 2006;56(1):54-62. DOI: 10.1016/j.envexpbot.2005.01.002.

[33] Wang, J.Z., Tao, S.T., Qi, K.J., Wu, J., Wu, H.Q., Zhang, G.S.L. Changes in photosyn‐
thetic properties and antioxidative system of pear leaves to boron toxicity. African
Journal of Biotechnology. 2011;10:19693-19700.

[34] Landi, M., Remorini, D., Pardossi A., Guidi, L. Boron excess affects photosynthesis
and antioxidant apparatus of greenhouse Cucurbita pepo and Cucumis sativus. Journal
of Plant Research. 2013;126(6):775-786. DOI: 10.1007/s10265-013-0575-1.

[35] Gill, S.S. and Tuteja, N. Reactive oxygen species and antioxidant machinery in abiotic
stress tolerance in crop plants. Plant Physiology and Biochemistry. 2010;48(12):
909-930. DOI: 10.1016 / j.plaphy.2010.08.016.

[36] Verkleij, J.A.C., Koevoets, P.L.M., Mechteld, M.A., Blake‐Kalff, M.M.A., Chardon‐
nens A. Evidence for an important role of the tonoplast in the mechanism of natural‐
ly selected zinc tolerance in Silene vulgaris. Journal of Plant Physiology. 1998;153(1-2):
188-191. DOI: 10.1016/S0176-1617(98)80064-3.

[37] Williams, G.M., Kroes, R., Munro, I.C. Safety Evaluation and Risk Assessment of the
Herbicide Roundup and Its Active Ingredient, Glyphosate, for Humans. Elsevier.
2000;31(2):117-165. DOI: doi:10.1006/rtph.1999.1371.

[38] Lobato, A.K.S., Coimbra, G.K., Neto, M.A.M., Costa, R.C.L., Santos Filho, B.G., Oli‐
veira Neto, C.F., Luz, L.M., Barreto, A.G.T., Pereira, B.W.F., Alves, G.A.R., Monteiro,
B.S., Marochio, C.A. Protective action of silicon on relations and photosynthetic pig‐
 Tolerance of Plants to Toxicity Induced by Micronutrients 243
http://dx.doi.org/10.5772/62046

ments in pepper plants induced to water deficit. Research Journal of Biological Scien‐
ces. 2009;4(5):617-623.

[39] Pereira, T.S., Lobato, A.K.S., Tan, D.K.Y., Costa, D.V., Uchôa, E.B., Ferreira, R.N., Per‐
eira, E.S., Avila, F.W., Marques, D.J., Guedes, E.M.S. Positive interference of silicon
on water relations, nitrogen metabolism, and osmotic adjustment in two pepper
(Capsicum annuum) cultivars under water deficit. Australian Journal of Crop Science.
2013;7(8):1064-1071.

[40] Marques, D.J., Ferreira, M.M., Lobato, A.K.S., Carvalho, J.G., Carvalho, J.Á., Freitas,
W.A., Bastos, A.R.R., Pereira, F.J., Castro, E.M. CaSiO3 improves water potential and
gas exchange but not contribute to the production parameters of maize plants ex‐
posed to different irrigation depths. Australian Journal of Crop Science. 2014;8(8):
1257-1265.

[41] Isa, M., Bai S., Yokoyama, T., Ma, J.F., Ishibashi, Y., Yuasa, T., Iwaya-Inoue, M. Sili‐
con enhances growth independent of silica deposition in a low-silica rice mutant,
lsi1. Plant and Soil. 2010;331(1-2):361-375. DOI: 10.1007/s11104-009-0258-9.

[42] Silva, O.N., Lobato, A.K.S., Avila, F.W., Costa, R.C.L., Oliveira Neto, C.F., Santos Fil‐
ho, B.G., Martins Filho, A.P., Lemos, R.P., Pinho, J.M., Medeiros, M.B.C.L., Cardoso,
M.S., Andrade, I.P. Silicon-induced increase in chlorophyll is modulated by the leaf
water potential in two water-deficient tomato cultivars. Plant Soil And Environment.
2012;58(11):481-486.

[43] Kim, S.G., Kim, K.W., Park, E.W., Choi, D. Silicon-induced cell wall fortification of
rice leaves: A possible cellular mechanism of enhanced host resistance to blast. Phy‐
topathology. 2002;92(10):1095-1103. DOI: 10.1094/PHYTO.2002.92.10.1095.

[44] Chen, W., Yao, X., Cai, K., Chen, J. Silicon alleviates drought stress of rice plants by
improving plant water status, photosynthesis and mineral nutrient absorption. Bio‐
logical Trace Element Research. 2011;142(1):67–76. DOI: 10.1007/s12011-010-8742-x.

[45] Paula, L.S., Silva, B.C., Pinho, W.C.S., Barbosa, M.A.M., Lobato, E.M.S.G., Batista,
B.L., Barbosa Júnior, F., Lobato, A.K.S. Silicon (Si) ameliorates the gas exchange and
reduces negative impacts on photosynthetic pigments in maize plants under Zn tox‐
icity. Australian Journal of Crop Science. 2015;9: paper in press.

[46] Sagardoy, R., Vázquez, S., Florez-Sarasa, I.D., Albacete, A., Ribas-Carbó, M., Flexas,
J., Abadía, J., Morales, F. Stomatal and mesophyll conductances to CO2 are the main
limitations to photosynthesis in sugar beet (Beta vulgaris) plants grown with excess
zinc. New Phytologist. 2010;187(1):145-158. DOI: 10.1111/j.1469-8137.2010.03241.x.

[47] Pavlíková, D., Pavlík, M., Procházková, D., Zemanová, V., Hnilicka, F., Wilhelmová,
N. Nitrogen metabolism and gas exchange parameters associated with zinc stress in
tobacco expressing an ipt gene for cytokinin synthesis. Journal of Plant Physiology.
2014;171:559-564.
244 Abiotic and Biotic Stress in Plants - Recent Advances and Future Perspectives

[48] Ripley, B.S., Gilbert, M.E., Ibrahim, D.G., Osborne, C.P. Drought constraints on C4
photosynthesis: stomatal and metabolic limitations in C3 and C4 subspecies of Allo‐
teropsis semialata. Journal of Experimental Botany. 2007;58(6):1351-1363.

[49] Flexas, J., Ribas-Carbó, M., Bota, J., Galmés, J., Henkle, M., Martínez-Cañellas, S., Me‐
drano, H. Decreased rubisco activity during water stress is not induced by decreased
relative water content but related to conditions of low stomatal conductance and
chloroplast CO2 concentration. New Phytologist. 2006;172(1):73-82.

[50] Shi, G.R. and Cai, Q.S. Photosynthetic and anatomic responses of peanut leaves to
zinc stress. Biologia Plantarum. 2009;53(2):391-394.

[51] Mott, K.A. and Franks, P.J. The role of epidermal turgor in stomatal interactions fol‐
lowing a local perturbation in humidity. Plant Cell and Environment. 2001;24(6):
657-662. DOI: 10.1046/j.0016-8025.2001.00705.x.

[52] Ronda, R.J., Bruin, H.A.R., Holtslag, A.A.M. Representation of the canopy conduc‐
tance in modelling the surface energy budget for low vegetation. Journal of Applied
Meteorology. 2001;40(8):1431-1444. DOI: http://dx.doi.org/10.1175/1520-0450
(2001)040<1431:ROTCCI>2.0.CO;2.

[53] Sperry, J.S. Hydraulic constraints on plant gas exchange. Agricultural and Forest Me‐
teorology. 2000;104:13-23.

[54] Fernàndez, J., Zacchini, M., Fleck, I. Photosynthetic and growth responses of Populus
clones Eridano and I-214 submitted to elevated Zn concentrations. Journal of Geo‐
chemical Exploration. 2012;123:77-86. DOI: 10.1016/j.gexplo.2012.01.010.

[55] Ma, C.C., Gao, Y.B., Guo, H.Y., Wang, J.L. Photosynthesis, transpiration and water
use efficiency of Caragana microphylla, C. intermedia and C. korshinskii. Photosynthe‐
tica. 2004;42(1):65-70.

[56] Silva, C.E.M., Gonçalves, J.F.C., Feldpausch, T.R. Water-use efficiency of tree species
following calcium and phosphorus application on an abandoned pasture, central
Amazonia, Brazil. Environmental and Experimental Botany. 2008;64(2):189-195. DOI:
10.1016/j.envexpbot.2008.03.001.

[57] Moussa, H.R. Influence of exogenous application of silicon on physiological response

of salt-stressed maize (Zea mays L.). International Journal of Agriculture and Biology.
2006;2:293-297.

[58] Manivasagaperumal, R., Balamurugan, S., Thiyagarajan, G., Sekar, J. Effect of zinc on
germination, seedling growth and biochemical content of cluster bean (Cyamopsiste‐
tragonoloba (L.) Taub). Current Botany. 2011;2:11-15.

[59] Mousavi, S.R. Zinc in crop production and interaction with phosphorus. Australian
Journal of Basic and Applied Sciences. 2011;5(9):1503-1509.
 Tolerance of Plants to Toxicity Induced by Micronutrients 245
http://dx.doi.org/10.5772/62046

[60] Parham, R. And Rebeiz, C.A. Chloroplast Biogenesis 72: A [4-vinyl] chlorophyllide a
reductase assay using divinyl chlorophyllide a as an exogenous substrate. Analytical
Biochemistry. 1995;231(1):164-169.

[61] Streit, N.M., Canterle, L.P., Canto, M.W., Hecktheuer, L.H.H. The chlorophylls. Cien‐
cia Rural. 2005;35:748-755. DOI: 10.1590/S0103-84782005000300043.

[62] Cazzonelli, C.I. Carotenoids in nature: insights from plants and beyond. Functional
Plant Biology. 2011;38(11):833–847. DOI: 10.1071/FP11192.

[63] Croce, R., Müller, M.G., Bassi, R., Holzwarth, A.R. Carotenoid-to-chlorophyll energy
transfer in recombinant major light-harvesting complex (LHCII) of higher plants. I.
Femtosecond transient absorption measurements. Biophysical Journal. 2001;80(2):
901-915. DOI: 10.1016/S0006-3495(01)76069-9.

[64] Papadakis, I. E., Dimassi, K.N., Bosabalidis, A.M., Therios, I.N., Patakas, A., Gianna‐
koula, A. Boron toxicity in ‘Clementine’ mandarin plants grafted on two rootstocks.
Plant Science. 2004;166(2):539-547. DOI: 10.1016/j.plantsci.2003.10.027.

[65] Tepe, M. And Aydemir, T. Antioxidant responses of lentil and barley plants to boron
toxicity under different nitrogen sources. African Journal of Biotechnology.
2011;10:10882-10891. DOI: 10.5897/AJB10.1076.

[66] Madhava, R.K.V. and Sresty, T.V.S. Antioxidative parameters in the seedlings of pi‐
geon-pea (Cajanus cajan (L.) Millspaugh) in response to Zn and Ni stresses. Plant Sci‐
ence. 2000;157(1):113-128.

[67] López, M.A.F., Ellis D.R., Grusak M.A. Effect of zinc and manganese supply on the
activities of superoxide dismutase and carbonic anhydrase in Medicago truncatula
wild type and raz mutant plants. Plant Science. 2005;168:1015-1022. DOI: 10.1016/
j.plantsci.2004.11.018.

[68] Hung, S.H., Yu, C.W., Lin, C.H. Hydrogen peroxide functions as a stress signal in
plants. Botanical Bulletin of Academia Sinica. 2005;46:1-10.

[69] Sairam, R.K. and Srivastava, G.C. Induction of oxidative stress and antioxidant activ‐
ity by hydrogen peroxide treatment in tolerant and susceptible wheat genotypes. Bi‐
ologia Plantarum. 2000;43(2):381-386. DOI: 10.1023/A:1026730008917.

[70] Bettaieb, T., Denden, M., Mhamdi, M. In vitro regeneration and physiological charac‐
terization of Gladiolus (Gladiolus grandiflorus Hort.) Somaclonal variants tolerant to
low temperatures. Tropicultura. 2008;26:10-16.

[71] Kowalewska, G., Lotocka, M., Latala, A. Formation of the copper-chlorophyll com‐
plexes in cells of phytoplankton from the Baltic Sea. Polskie Archiwum Hydrobiolo‐
gii. 1992;39:41-49.

[72] Wettstein, D.V., Gough, S., Kannangara, C.G. Chlorophyll biosynthesis. Plant Cell.
1995;7(7):1039-1057. DOI: 10.1105/tpc.7.71039.
246 Abiotic and Biotic Stress in Plants - Recent Advances and Future Perspectives

[73] Küpper, H., Küpper, F., Spiller, M. Environmental relevance of heavy metal substitut‐
ed chlorophylls using the example of water plants. Journal of Experimental Botany.
1996;47(2):259–266. DOI: 10.1093/jxb/47.2.259.
[74] Bassi, R. and Sharma, S.S. Proline accumulation in wheat seedlings exposed to zinc
and copper. Phytochemistry. 1993; 33:1339-1342.

[75] Silva, P.F.N., Lobato, E.M.S.G., Souza, P.R., Santos, H.J.M., Braga, R.O., Lobato,
A.K.S.

[76] Proline and total glutathione are accumulated in leaf of young Schizolobium parahyba
var. amazonicum plants exposed to boron toxicity. Brazilian Journal of Botany.
2015;38: paper in press.

[77] Paula, M.T., Filho, B.G.S., Cordeiro, Y.E.M., Conde, R.A., Neves, P.A.P.F.G. Eco‐
physiology the brazilian mahogany (Swietenia macrophylla King) agroforestry systems
in Santa Barbara-Pa. Enciclopedia Biosfera. 2013;9:813-824.

[78] Cervilla, L.M., Blasco, B., Ríos, J.J., Rosales, M.A., Rubio-Wilhelmi, M.M., Rodríguez, E.S.,
Romero, L., Ruiz, J.M. Response of nitrogen metabolism to boron toxicity in tomato
plants. Plant Biology. 2009;11(5):671-677. DOI: 10.1111/j.1438-8677.2008.00167.x.
[79] Hong, Z., Lakkineni, K., Zhang, Z., Verma, D.P.S. Removal of feedback inhibition of
Δ1-pyrroline-5- carboxylate synthetase results in increased proline accumulation and
protection of plants from osmotic stress. Plant Physiology. 2000;122:1129-1136. DOI:
http://dx.doi.org/10.1104/pp.122.4.1129.

[80] Cervilla, L.M., Blasco, B., Rios, J.J., Rosales, M.A., Sánchez-Rodríguez, E., Rubio-
Wilhelmi, M.M., Romero, L., Ruiz, J.M. Parameters symptomatic for boron toxicity in
leaves of tomato plants. Journal Botany. 2012;2012:1-17. DOI: 10.1155/2012/726206
[81] Cervilla, L.M., Blasco, B., Ríos, J.J., Romero, L., Ruiz, J.M. Oxidative stress and antiox‐
idants in tomato (Solanum lycopersicum) plants subjected to boron toxicity. Annals of
Botany. 2007;100(4):747-756. DOI: 10.1093/aob/mcm156.

[82] Contreras, C., Montoya, A., Pacheco, P., Martinez-Ballesta, M.C., Carvajal, M., Bastias,
E. The effects of the combination of salinity and excess boron on the water relations of
tolerant tomato (Solanum lycopersicum L.) cv. Poncho Negro, in relation to aquaporin
functionality. Spanish Journal of Agricultural Research. 2011;9:494-503.
[83] Costa, R.C.L., Lobato, A.K.S., Silveira, J.A.G., Laughinhouse, I.V.H.D. ABA-mediated
proline synthesis in cowpea leaves exposed to water deficiency and rehydration.
Turkish Journal of Agriculture and Forestry. 2011;35:309-317.

[84] Szabados, L. and Savouré, A. Proline: a multifunctional amino acid. Trends Plant Sci‐
ence. 2010;15(2):89-97. DOI: 10.1016/j.tplants.

[85] Mostofa, M.G., Hossain, M.A., Fujita, M., Tran, L.S. Physiological and biochemical
mechanisms associated with trehalose-induced copper-stress tolerance. Scientific Re‐
post. 2014;5:11433. DOI: 10.1038/srep11433.