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Scientia Horticulturae
journal homepage: www.elsevier.com/locate/scihorti
Antioxidant performance and aluminum accumulation in two genotypes of
Solanum lycopersicum in response to low pH and aluminum availability and
under their combined stress
Lucélia Borgo
a,
⁎
, Flávio Henrique Rabêlo
a
, Giselle Carvalho
a
, Thiago Ramires
b
,
Ana Julia Righetto
c
, Fernando Ângelo Piotto
a
, Luis Felipe Boaretto
a
, Ricardo Azevedo
a
a
College of Agriculture Luiz de Queiroz, University of São Paulo, 13418-900, Piracicaba, Brazil
b
Department of Mathematics, Federal University of Technology, 86812-460, Apucarana, Brazil
c
Agronomic Institute of Paraná, 86047-902, Londrina, Brazil
ARTICLE INFO
Keywords:
Enzymatic activity
Lipid peroxidation
Oxidative stress
Tolerance mechanisms
Tomato
ABSTRACT
The mechanisms of Aluminum (Al) tolerance are dependent on the plant species and genotypes, but the results
attributed to the toxic efect of Al can also be infuenced by pH. Our aim was to study the efect of Al and pH in
the antioxidative system of two tomato genotypes in response to Al in hydroponic system. The genotypes
Moneymaker (MM) and Calabash Rouge (CR) were grown in Hoagland and Arnon (1950) nutrient solution pH
6.0 until the complete establishment in hydroponic system. Then the plants were transferred to the treatments:
minimum medium at pH 4.2, minimum medium at pH 6.5 and minimum medium pH 4.2 + 20 mmol L
−1
AlCl
3
.6H
2
O. The sampling of plant material was performed in the times: zero (immediately before exposure to
the treatments), 24 and 48 h after their beginning. Aluminum accumulation in MM roots was higher than in CR
after 48 h. The highest hydrogen peroxide (H
2
O
2
) concentration was observed in the shoots at control and at low
pH without Al in the roots of CR. Malondialdehyde (MDA) concentration in CR roots did not present alteration
along the 48 h, remaining near or below the control, whereas genotype MM presented a lower MDA con-
centration after 48 h in the presence of Al in relation to CR. In the roots of the genotype CR, superoxide dis-
mutase (SOD) activity was lower at pH 4.2+Al and higher at pH 4.2. We evidenced that the antioxidative system
seems more involved in response to low pH than Al toxicity, and that genotype CR presents mechanisms of Al
tolerance possibly more related to the lower Al translocation from roots to shoots than with the protective
activity of antioxidant enzymes.
1. Introduction
The toxicity caused by aluminum (Al) is a limiting factor for food
production in soils with pH values below than 5.5, since in these con-
ditions Al is solubilized and Al
3+
ions are dissolved in the soil solution,
primarily inhibiting the growth of the root system and reducing the
productivity of the crops (Aggarwal et al., 2015). Aluminum directly
afects roots; therefore, the frst damages are caused in the apoplast,
where the cell elongation process is inhibited because of Al ligation to
the cell walls of the rhizodermis and of the external part of the root
cortex, hardening them and preventing them from performing the re-
modeling process, necessary for cell elongation (Kopittke et al., 2015).
Aluminum also afects root growth by interfering in water and nutrient
uptake, such as the cations Ca
2+
, Mg
2+
,K
+
, NH
4
+
(Moustaka et al.,
2016), causing damages to the cell membranes, enzymatic alterations
and inhibition of cell division and nuclear DNA synthesis (Singh et al.,
2017). Another alteration in cell metabolism that can be detected some
minutes after exposure to Al is the rise in production of reactive oxygen
species (ROS) and free radicals, such as superoxides (O
2
%−
), hydroxyls
(OH
%
-), hydrogen peroxides (H
2
O
2
) and singlet oxygen (
1
O
2
)(Liu et al.,
2014). The imbalance between the production of these species and their
degradation can lead to overload of the cellular antioxidative system,
resulting in a process known as oxidative stress, leading to enzyme
inactivation, protein oxidation, lipid peroxidation of the cell mem-
branes, among others (Sharma and Dubey, 2007; Sujkowska-
Rybkowska, 2012; Bhoomika et al., 2013; Matsumoto and Motoda,
2013; Furlan et al., 2018). To counteract these ROS, plants synthesize a
variety of antioxidant enzymes, such as superoxide dismutase (SOD, EC
https://doi.org/10.1016/j.scienta.2019.108813
Received 3 June 2019; Received in revised form 13 August 2019; Accepted 26 August 2019
⁎
Corresponding author.
E-mail addresses: borgolucelia@hotmail.com, lborgo@usp.br (L. Borgo).
Scientia Horticulturae 259 (2020) 108813
0304-4238/ © 2019 Elsevier B.V. All rights reserved.
T