(Monshausen et al. 2007; Kurepa et al. 2010) which
increases the bioavailable TiO 2 -NPs and thereby the uptake.
The uptake of NPs in plants is determined by various factors
such as plant species and age, and morphological and
chemical properties of NPs (Nair et al. 2010; Rico et al.
2011). In addition, their uptake also depends on exposure
pathways.
2.1 Uptake and Translocation of TiO 2
Nanoparticles Through Roots
Nanoparticles after released into soil biotransformed by the
interaction of humic acid and root exudates, and then uptaken by the surface pores of root cells (Rico et al. 2011).
TiO 2 -NPs first move into root through apoplast. Then, some
of the total amount of TiO 2 -NPs is transported further into
the cell, and some become bound to the cell wall substances.
‘The mechanism of NPs uptake is generally considered as an
active-transport mechanism that includes several other cellular processes such as signaling, recycling and the regulation of plasma membrane’ (Tripathi et al. 2017).
The TiO 2 -NPs’ movement from outside medium into the
root cell wall is a non-metabolic and passive route that is
determined by diffusion or mass flow. After getting entry
through cell wall and plasma membrane in root epidermis,
TiO 2 -NPs reach to stelar vascular tissues (xylem) through
apoplastic or symplastic movements or by both (Larue et al.
2012b; Kurepa et al. 2010) (Fig. 3). Then, from root tissue
they are transported to other regions in plants through unidirectional movement using xylem tissue. Raliya et al.
(2015a, b) reported TiO 2 -NPs accumulation in roots, shoots
and leaves and suggested that once TiO 2 -NPs are uptaken by
tomato plants (either through leaf epidermis or root cell),
they are translocated throughout the plant using xylem and
phloem tissues of plant. TiO 2 -NPs uptaken by leaf cells
follow bidirectional pathways where NPs transported by
phloem tissue.
Wang et al. (2014) suggested that upon foliar application,
due to small size NPs enter in to the plant cells either by
direct penetration or by the mechanism of gaseous uptake.
The rate of NPs translocation and their accumulation in
various plant tissues is dissimilar for both foliar and soil
application and depends on the shape and size of NPs and
the size of pores present on cell wall (Carpita et al. 1979;
Asli and Neumann 2009; Judy et al. 2012) as the root cell
wall is the main site of NPs entry into the plant cells
(Kurepa et al. 2010). Size seems to be one of the main
factors that limit the movement and accumulation of NPs.
NPs having dimension up to 40–50 nm only can move and
accumulate within the cell (Gonzalez-Melendi et al. 2008;
Taylor et al. 2014) while large-sized TiO 2 -NPs cannot enter
into plant cells and thus sieved out (Larue et al. 2011).
However, there are some studies showing the
accumulation/internalization of bigger-sized TiO 2 -NPs of
about 450 nm dimension in plant cells (Santos Filho et al.
2019). It seems that they might have followed another path
to get entry into the cells.
Like some other NPs, TiO 2 -NPs might have induced the
formation of new and large-sized pores on cell wall (Navarro
et al. 2008; Wang et al. 2016; Yan and Chen 2019) and may
directly reach to cytosol without forming endosomes or
encapsulating in any organelle (Serag et al. 2011). Besides,
in order to get successful entry and internalization within the
cell TiO 2 -NPs may bind to some surrounding proteins that
could behave as carrier proteins (Nel et al. 2009). In this
regard, aquaporins have been identified as a potential
transporters for NPs within the plant cell (Rico et al. 2011),
but because of very small size of aquaporins (2.8–3.4 A°)
(Wu et al. 2017), make them dubious path for NPs entry
(Schwab et al. 2015). Besides, they might be integrated into
the cell through invagination of the plasma membrane
forming a vesicle that can move to various cell compartments as endosomes (Etxeberria et al. 2006; Kurepa et al.
2010). Kurepa et al. (2010) demonstrate the presence of
TiO 2 -50% Alizarin red S (ARS) nanocomposites in form of
endosomes (globular bodies) in cotyledons cells and epidermis of petioles and hypocotyls of Arabidopsis thaliana.
They proposed that TiO 2 -NPs internalized both by
clathrin-dependent and independent endocytic pathways as
observed by Onelli et al. (2008) in Nicotiana tabaccum, for
gold NPs. Additionally, the type of NPs and their morphology and physico-chemical properties have also been
observed to play a determining role in NPs uptake (Ma et al.
2010; Rico et al. 2011; Raliya et al. 2016). TiO 2 -NPs within
the plant cell are found to be transported through the plasmodesmata show symplastic movement (Kurepa et al. 2010;
Tripathi et al. 2017; Yan and Chen 2019).
In Arabidopsis, TiO 2 -NPs are found to aggregate in
plasmodesmata and in the cell wall (Kurepa et al. 2010)
suggesting that there may be obstruction of intercellular
communication, due to accumulation of TiO 2 -NPs. Kurepa
et al. (2010) also proposed that the release of H
+ by the plant
root cells resulted into adsorption of TiO 2 -50% ARS
nanocomposites on the surface of root that promotes
micronutrients uptake from the surrounding environment
consequently by lowering the pH of the root zone (Monshausen et al. 2007). Mattiello and Marchiol (2017) reported
TiO 2 -NPs uptake by root tissue and a subsequent translocation and accumulation in barley seedling tissues and in
stroma of chloroplast. Similarly, Kurepa et al. (2010)
observed their accumulation in the shoots of Arabidopsis
thaliana. TiO 2 -NPs was uptaken and accumulated increasingly in tip of root passing when passing through the various
root tissues like root cap, epidermis, columella and initials of
root meristem, sequentially. A transmission electron
Interaction of Titanium Dioxide Nanoparticles …
53
increases the bioavailable TiO 2 -NPs and thereby the uptake.
The uptake of NPs in plants is determined by various factors
such as plant species and age, and morphological and
chemical properties of NPs (Nair et al. 2010; Rico et al.
2011). In addition, their uptake also depends on exposure
pathways.
2.1 Uptake and Translocation of TiO 2
Nanoparticles Through Roots
Nanoparticles after released into soil biotransformed by the
interaction of humic acid and root exudates, and then uptaken by the surface pores of root cells (Rico et al. 2011).
TiO 2 -NPs first move into root through apoplast. Then, some
of the total amount of TiO 2 -NPs is transported further into
the cell, and some become bound to the cell wall substances.
‘The mechanism of NPs uptake is generally considered as an
active-transport mechanism that includes several other cellular processes such as signaling, recycling and the regulation of plasma membrane’ (Tripathi et al. 2017).
The TiO 2 -NPs’ movement from outside medium into the
root cell wall is a non-metabolic and passive route that is
determined by diffusion or mass flow. After getting entry
through cell wall and plasma membrane in root epidermis,
TiO 2 -NPs reach to stelar vascular tissues (xylem) through
apoplastic or symplastic movements or by both (Larue et al.
2012b; Kurepa et al. 2010) (Fig. 3). Then, from root tissue
they are transported to other regions in plants through unidirectional movement using xylem tissue. Raliya et al.
(2015a, b) reported TiO 2 -NPs accumulation in roots, shoots
and leaves and suggested that once TiO 2 -NPs are uptaken by
tomato plants (either through leaf epidermis or root cell),
they are translocated throughout the plant using xylem and
phloem tissues of plant. TiO 2 -NPs uptaken by leaf cells
follow bidirectional pathways where NPs transported by
phloem tissue.
Wang et al. (2014) suggested that upon foliar application,
due to small size NPs enter in to the plant cells either by
direct penetration or by the mechanism of gaseous uptake.
The rate of NPs translocation and their accumulation in
various plant tissues is dissimilar for both foliar and soil
application and depends on the shape and size of NPs and
the size of pores present on cell wall (Carpita et al. 1979;
Asli and Neumann 2009; Judy et al. 2012) as the root cell
wall is the main site of NPs entry into the plant cells
(Kurepa et al. 2010). Size seems to be one of the main
factors that limit the movement and accumulation of NPs.
NPs having dimension up to 40–50 nm only can move and
accumulate within the cell (Gonzalez-Melendi et al. 2008;
Taylor et al. 2014) while large-sized TiO 2 -NPs cannot enter
into plant cells and thus sieved out (Larue et al. 2011).
However, there are some studies showing the
accumulation/internalization of bigger-sized TiO 2 -NPs of
about 450 nm dimension in plant cells (Santos Filho et al.
2019). It seems that they might have followed another path
to get entry into the cells.
Like some other NPs, TiO 2 -NPs might have induced the
formation of new and large-sized pores on cell wall (Navarro
et al. 2008; Wang et al. 2016; Yan and Chen 2019) and may
directly reach to cytosol without forming endosomes or
encapsulating in any organelle (Serag et al. 2011). Besides,
in order to get successful entry and internalization within the
cell TiO 2 -NPs may bind to some surrounding proteins that
could behave as carrier proteins (Nel et al. 2009). In this
regard, aquaporins have been identified as a potential
transporters for NPs within the plant cell (Rico et al. 2011),
but because of very small size of aquaporins (2.8–3.4 A°)
(Wu et al. 2017), make them dubious path for NPs entry
(Schwab et al. 2015). Besides, they might be integrated into
the cell through invagination of the plasma membrane
forming a vesicle that can move to various cell compartments as endosomes (Etxeberria et al. 2006; Kurepa et al.
2010). Kurepa et al. (2010) demonstrate the presence of
TiO 2 -50% Alizarin red S (ARS) nanocomposites in form of
endosomes (globular bodies) in cotyledons cells and epidermis of petioles and hypocotyls of Arabidopsis thaliana.
They proposed that TiO 2 -NPs internalized both by
clathrin-dependent and independent endocytic pathways as
observed by Onelli et al. (2008) in Nicotiana tabaccum, for
gold NPs. Additionally, the type of NPs and their morphology and physico-chemical properties have also been
observed to play a determining role in NPs uptake (Ma et al.
2010; Rico et al. 2011; Raliya et al. 2016). TiO 2 -NPs within
the plant cell are found to be transported through the plasmodesmata show symplastic movement (Kurepa et al. 2010;
Tripathi et al. 2017; Yan and Chen 2019).
In Arabidopsis, TiO 2 -NPs are found to aggregate in
plasmodesmata and in the cell wall (Kurepa et al. 2010)
suggesting that there may be obstruction of intercellular
communication, due to accumulation of TiO 2 -NPs. Kurepa
et al. (2010) also proposed that the release of H
+ by the plant
root cells resulted into adsorption of TiO 2 -50% ARS
nanocomposites on the surface of root that promotes
micronutrients uptake from the surrounding environment
consequently by lowering the pH of the root zone (Monshausen et al. 2007). Mattiello and Marchiol (2017) reported
TiO 2 -NPs uptake by root tissue and a subsequent translocation and accumulation in barley seedling tissues and in
stroma of chloroplast. Similarly, Kurepa et al. (2010)
observed their accumulation in the shoots of Arabidopsis
thaliana. TiO 2 -NPs was uptaken and accumulated increasingly in tip of root passing when passing through the various
root tissues like root cap, epidermis, columella and initials of
root meristem, sequentially. A transmission electron
Interaction of Titanium Dioxide Nanoparticles …
53