Barriers, pathways and processes for uptake, translocation and accumulation of nanomaterials in ...

76 Pages·2015·16.63 MB·English

by  Detlef Schrott

This is an Accepted Manuscript of an article published by Informa Healthcare in Nanotoxicology in 2015, available
online: http://informahealthcare.com/doi/abs/10.3109/17435390.2015.1048326 .
Barriers, Pathways and Processes for Uptake, Trans-
1"
location, and Accumulation of Nanomaterials in
2"
Plants—Critical Review
3"
4" Fabienne Schwab1,2, Guangshu Zhai3, Meaghan Kern3, Amalia Turner1,2, Jerald L.
5" Schnoor3, Mark R. Wiesner1,2*
6" 1) Department of Civil and Environmental Engineering, Duke University, Durham, North Caro-
7" lina 27708, USA
8" 2) Center for the Environmental Implications of Nanotechnology (CEINT), Duke University,
9" Durham, North Carolina 27708, USA.
10" 3) Department of Civil and Environmental Engineering, The University of Iowa, Iowa City, Io-
11" wa 52242, USA
12"
13" * Corresponding author: Tel: [phone], [email protected]
14"
15"
16" Keywords: plant physiology, nanoparticles, engineered nanomaterials, internalization, excretion
17"
Nanotoxicology 2015. 1/76
This is an Accepted Manuscript of an article published by Informa Healthcare in Nanotoxicology in 2015, available
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Abstract
18"
19" Uptake, transport and toxicity of engineered nanomaterials (ENMs) into plant cells are complex
20" processes that are currently still not well understood. Parts of this problem are the multifaceted
21" plant anatomy, and analytical challenges to visualize and quantify ENMs in plants. We critically
22" reviewed the currently known ENM uptake, translocation, and accumulation processes in plants.
23" A vast number of studies showed uptake, clogging, or translocation in the apoplast of plants,
24" most notably of nanoparticles with diameters much larger than the commonly assumed size ex-
25" clusion limit of the cell walls of ~5-20 nm. Plants that tended to translocate less ENMs were
26" those with low transpiration, drought–tolerance, tough cell wall architecture, and tall growth. In
27" the absence of toxicity, accumulation was often linearly proportional to exposure concentration.
28" Further important factors strongly affecting ENM internalization are the cell wall composition,
29" mucilage, symbiotic microorganisms (mycorrhiza), absence of a cuticle (submerged plants), and
30" stomata aperture. Mostly unexplored are the roles of root hairs, leaf repellency, pit membrane
31" porosity, xylem segmentation, wounding, lateral roots, nodes, the Casparian band, hydathodes,
32" lenticels, and trichomes. The next steps towards a realistic risk assessment of nanoparticles in
33" plants are to measure ENM uptake rates, the size exclusion limit of the apoplast, and to unravel
34" plant physiological features favoring uptake.

35"
Nanotoxicology 2015. 2/76
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Abbreviations
36"
37" (C)FPE, (clathrin–mediated) fluid–phase endocytosis; EDS, energy dispersive X-ray spectros-
38" copy; ENMs, engineered nanomaterials, MSNs, mesoporous silica nanoparticles; NPs, nanopar-
39" ticles; QDs, quantum dots; (S)TEM, (scanning) transmission electron microscopy;
40" SWCNTs/MWCNTs, single–walled/multi–walled carbon nanotubes; SEL, size exclusion limit;
41" SPIONs, super paramagnetic iron oxide nanoparticles; µ-XANES synonym µ-NEXAFS, µ-X-ray
42" absorption near edge structure; µ-XRF, µ-X-ray fluorescence spectroscopy.
Nano- and Microparticles Discussed
43"
44" Various coatings and functionalizations: Nano-Ag, nano-Au, nano-CeO , nano-141CeO , China
2 2
45" ink, nano-CuO, nano-Fe O , ferritins, fullerenes, liquid crystalline nanoparticles, mesoporous
x y
46" silica nanoparticles, nano-MgO, [Mo Br ]2− clusters, nano-Pb, nano-Pd, polystyrene
6 14
47" nano-spheres, phytoliths, nano-Pt, quantum dots, nano-Rh, single–walled and multi–walled car-
48" bon nanotubes, nano-SiO , super paramagnetic iron oxide nanoparticles, nano-TiO , transparent
2 2
49" exopolymer particles, viral nucleic-acid–protein complexes, viruses, zero–valent
50" nano-iron (nZVI), nano-ZnO, nano-Yb O .
2 3

51"
Nanotoxicology 2015. 3/76
This is an Accepted Manuscript of an article published by Informa Healthcare in Nanotoxicology in 2015, available
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Index
52"
53" 1 INTRODUCTION ................................................................................................................... 6
54" 2 CELL–LEVEL NANOPARTICLE INTERACTIONS ....................................................... 9
55" 2.1 SYMBIOTIC BACTERIA AND MYCORRHIZAE. ...................................................................... 10
56" 2.2 MUCILAGE AND EXUDATES ............................................................................................... 12
57" 2.3 CUTICLE ............................................................................................................................ 17
58" 2.4 THE CELL WALL AND PECTINS .......................................................................................... 20
59" 2.5 UPTAKE ACROSS THE CELL MEMBRANE ........................................................................... 24
60" 2.5.1 Endocytosis ................................................................................................................ 25
61" 2.5.2 Non–endocytic Pathways ........................................................................................... 26
62" 2.6 CELL-LEVEL IMAGING OF NANOPARTICLE INTERACTIONS ................................................ 28
63" 3 PLANT LOOPHOLES ......................................................................................................... 29
64" 3.1 WOUNDS ............................................................................................................................ 29
65" 3.2 LATERAL ROOT—RUPTURED EPIDERMIS .......................................................................... 30
66" 3.3 ROOT HAIRS—WATER & NUTRIENT TRANSPORTERS ....................................................... 31
67" 3.4 HYDATHODES—WATER SAFETY VALVES ......................................................................... 32
68" 3.5 STOMATA—GAS TRANSPORTERS ...................................................................................... 32
69" 3.6 LENTICELS—GAS SAFETY VALVES ................................................................................... 34
70" 3.7 TRICHOMES—DEFENSIVE APPENDAGES ............................................................................ 35
71" 4 PLASMODESMATA ............................................................................................................ 37
72" 4.1 STRUCTURE AND SIZE EXCLUSION LIMIT (SEL) ................................................................ 37
73" 4.2 FLEXIBLE SIZE EXCLUSION LIMIT ...................................................................................... 38
Nanotoxicology 2015. 4/76
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74" 4.3 DIRECTLY OBSERVED NP TRANSPORT .............................................................................. 39
75" 4.4 INDIRECTLY OBSERVED NP TRANSPORT ........................................................................... 40
76" 5 VASCULATURE ................................................................................................................... 41
77" 5.1 THE CASPARIAN STRIP ...................................................................................................... 43
78" 5.2 PIT MEMBRANES ............................................................................................................... 44
79" 5.3 NODES ............................................................................................................................... 45
80" 6 VASCULAR AND NON–VASCULAR TRANSPORT PROCESSES ............................. 45
81" 6.1 APOPLASTIC VS. SYMPLASTIC TRANSPORT ........................................................................ 45
82" 6.2 UPTAKE RATES .................................................................................................................. 47
83" 7 CONCLUSIONS AND GAP ANALYSIS ........................................................................... 51
84" 7.1 UNDERSTUDIED OR OVERLOOKED UPTAKE PROCESSES .................................................... 51
85" 7.2 UPTAKE AND TRANSLOCATION RATES (IN SOIL) ............................................................... 52
86" 7.3 DEFENSE MECHANISMS ..................................................................................................... 53
87" 7.4 WANTED REPORTING DATA .............................................................................................. 53
88" 7.5 PLANT–SOIL INTERACTIONS .............................................................................................. 54
89" 7.6 VALIDATED ANALYTICS AND VISUALIZATION ................................................................... 54
90" DECLARATION OF INTEREST ............................................................................................. 55
91" REFERENCES ............................................................................................................................ 56
92" " "
Nanotoxicology 2015. 5/76
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1 Introduction
93"
94" Naturally occurring nanoparticles (NPs), in enormous quantities and varieties, are distrib-
95" uted throughout the atmosphere, oceans, soil systems, terrestrial freshwater systems, and in/on
96" most living organisms (Wiesner et al., 2009; Colvin, 2003; Hochella Jr. et al., 2008). Concern
97" over the possible environmental and toxicological impacts of increasingly manufactured and
98" used engineered nanomaterials (ENMs) has stimulated research on the potential for
99" plant (cell) uptake, accumulation, and transformation of ENMs—materials that several decades
100" ago might have been simply described as dissolved by virtue of their ability to pass through
101" a 0.45 micron membrane (USEPA, 1996; Dietz & Herth, 2011; von Moos et al., 2014;
102" Scheringer, 2008). Plant–ENM interactions, in the process, have led plant biologists to rethink
103" the role of (nano)particles as sorbents and/or sources of heavy metals, pesticides, and essential
104" nutrients to plants and phytoplankton (Schwab et al., 2013; Santner et al., 2012; Baken et al.,
105" 2014; Van Moorleghem et al., 2013).
106" Two decades ago, research on the uptake of ENMs by plants was motivated primarily by
107" interest in their capability as vehicles for gene transfer (Wang et al., 1988; Torney et al., 2007;
108" Fisk & Dandekar, 1993). Over the last decade (Figure 1), scientists have begun to consider
109" plant–ENM bioaccumulation and -transformation as processes affecting the environmental fate
110" of ENMs. Their ecotoxicity, and their behavior in ecosystems include propagation within food
111" webs (Klaine et al., 2008; Navarro et al., 2008; Zhu et al., 2008; Al-Salim et al., 2011). The fre-
112" quency of publications addressing nanoparticle uptake by plants jumped over the last five years
113" to >40 peer reviewed original publications per year in 2013 (Figure 1).
Nanotoxicology 2015. 6/76
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114" Both terrestrial and aquatic plants, including phytoplankton, are expected to be exposed
115" to ENMs from ENM–containing sewage sludges (predicted annual input ~1.01-2380 µg
116" ENMs kg-1yr-1 sludge treated soil, where land application is allowed), supposedly quickly in-
117" creasing levels of novel nano-formulations of pesticides or fertilizers (Gardea-Torresdey et al.,
118" 2014), wastewater treatment effluent (0.001-15 ng L-1yr-1), and atmospheric sources from factory
119" or laboratory exhaust including contaminated rainfall (<<1 µg m-3yr-1; Hendren et al., 2011;
120" Gottschalk et al., 2009). In soil, the exposure concentrations are predicted to be five orders of
121" magnitude higher than those in water, and aerial exposure is expected to be much lower. Still,
122" determining which compartment is relevant for plant NP uptake is challenging due to the differ-
123" ent mobility of the NPs, e.g. in absence or presence of natural organic matter (Ek et al., 2004;
124" Zhao, LJ et al., 2012). Also, the ability of different plants to take up NPs is currently unpredicta-
125" ble (Dietz & Herth, 2011).
126" In the water compartment, at least for types of ENMs well–dispersible in water
127" (Wilkinson et al., 1997), NP–plant accumulation is well documented (Colman et al., 2014; Glenn
128" et al., 2012). Depending on the background particles, ENMs agglomerate more or less rapidly
129" (Therezien et al., 2014). Agglomerated ENMs can again re–suspend due to many natural pro-
130" cesses, e.g. turbulence in rivers (Gottschalk & Nowack, 2011), or suspension by natural organic
131" matter (Hyung et al., 2006; Schwyzer et al., 2012; Schwyzer et al., 2013). Submerged hydro-
132" phytes, as compared to terrestrial plants, must exhibit much faster mass transfer rates to acquire
133" enough CO and other dissolved gases from the water (Sculthorpe, 1967). These mass transfer
2
134" rates are enabled by an underdeveloped or absent epidermis and/or protective lipophilic cuticle
135" (Sculthorpe, 1967). As a consequence, well–dispersed ENMs can interact directly with the cellu-
136" lose cell wall. This can facilitate uptake.
Nanotoxicology 2015. 7/76
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137" In the terrestrial compartment, ENM accumulation in plants is favored due to exposure
138" concentrations in the µg-mg kg-1 range (Gardea-Torresdey et al., 2014; Gottschalk & Nowack,
139" 2011). The mobility of the NPs, and uptake into plants was found to be low (Gardea-Torresdey et
140" al., 2003). Eight different ENMs in a system resembling a sandy groundwater aquifer were
141" transported maximally 14 m (organic NPs), and 2.4 m respectively (inorganic NPs) (Lecoanet et
142" al., 2004). Nanoparticle mobility in soil was found to be even lower (Darlington et al., 2009).
143" Keeping in mind that under environmental conditions, biovoids, mucilage and exudates from
144" roots, hyphae, and bacteria significantly alter soil porosity and transport (Oades, 1993; Zhao, LJ
145" et al., 2012), this low mobility of ENMs shows that (a) NPs can accumulate in the first few me-
146" ters or centimeters of the soil, in close interaction with the rhizosphere (Gardea-Torresdey et al.,
147" 2014; McNear Jr., 2013; Walker et al., 2003; Hawes et al., 2000) (i.e. the root system environ-
148" ment where mucilage and exudates act) and (b) the key process keeping plant–ENM accumula-
149" tion low in soil is slow desorption kinetics or sequestration (Zhao et al., 2014; Avanasi et al.,
150" 2014; Wang, P et al., 2013; Zhao, LJ et al., 2012).
151" To date, ~200 peer–reviewed original publications have addressed ENM–plant up-
152" take (Figure 1). Recent reviews have addressed toxic and stimulating NP effects, summarized
153" NP concentrations found in plants, and discussed how plants are exposed to NPs in soil, water,
154" and air (Klaine et al., 2008; Handy, R. D. et al., 2008; Ma, XM et al., 2010; Navarro et al., 2008;
155" Gardea-Torresdey et al., 2003; Jackson et al., 2013; von Moos et al., 2014; Husen & Siddiqi,
156" 2014; Miralles & Church & et al., 2012). Central, not recently systematically addressed topics
157" are the actual barriers, pathways, and transport processes that NPs face in plants. What kind of
158" chemical and physiological barriers of plant cells do NPs have to cross before they reach the cy-
159" toplasm? How (fast) do—particularly non–dissolving—nanoparticles translocate within plants?
Nanotoxicology 2015. 8/76
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160" Which anatomical features of plants favor uptake? Where in plants will NPs accumulate? And do
161" plants, at all, excrete insoluble NPs again? (Dietz & Herth, 2011) provided an initial overview
162" for several hypothetic pathways for NPs into plants in 2011. Recent studies have begun to reveal
163" which of these processes are significant. New or scarcely described sites of uptake, transport,
164" accumulation, and excretion have been studied, such as plant–associated microorgan-
165" isms (mycorrhiza), mucilage, the cuticle, non–endocytic uptake across cell membrane, necrotic
166" tissue, root hairs, and trichomes. Other topics continue to cause confusion, such as the actual size
167" and morphology of "pores across the cell wall", and several other types of "pores" or "channels".
168" The goal of this review is therefore to (a) provide an update on pathways for NPs into
169" plants; (b) systematically describe, for the first time, the micro–architecture of these and all other
170" major pathways for NPs in plants, including uptake, translocation, and excretion, with special
171" attention to less explored, but potentially relevant pathways (termed here "loop-
172" holes"); (c) mathematically describe uptake processes based on the gained knowledge on NP
173" transport within plants; and (d) identify priorities for research on NP–plant interactions.
2 Cell–Level Nanoparticle Interactions
174"
175" Plants and phytoplankton exhibit specific barriers against intruders and ENMs (Figure 2;
176" McNear Jr., 2013; Fahn, 1982). The thickness and architecture of the barriers varies with species,
177" tissues, and environmental conditions, e.g. in drought–tolerant plants, where the cell wall, cuticle
178" and the Casparian strip are tighter to minimize water loss (Fahn, 1982), and the xy-
179" lem (section 5) is strongly sectored (Choat et al., 2008). The plant itself, by depositing cell mate-
180" rials, can create additional barriers. For instance, cell wall thickenings such as papilla, or callose,
181" suberin, and lignin deposits represent plant responses to the mechanical intrusion of patho-
Nanotoxicology 2015. 9/76
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182" gens (Figure 2A; Carpita & Gibeaut, 1993; Basavaraju et al., 2009; Voigt, 2014). The following
183" subsections describe all cell–level pathways and barriers for NPs in detail.
184"
185" 2.1 Symbiotic Bacteria and Mycorrhizae.
186" Nearly all pathogenic and symbiotic relationships in roots are initiated in the extending cell wall
187" region of elongation (Hawes et al., 2000), where they strongly interact with mucilage and exu-
188" dates of the plant (section 2.2). Microorganisms living associated with plants create a variety of
189" symbiotic microenvironments (McNear Jr., 2013; Larran et al., 2007) and soil aggregates
190" (Oades, 1993) or biomineralized products (Emerson et al., 1999; Aznar et al., 2014). Symbiotic
191" microenvironments can affect metal and metal (oxide) NP mobility and uptake in plants. For in-
192" stance, arbuscular mycorrhizal fungi known to confer heavy metal resistance to plants signifi-
193" cantly increased the soil porosity near nano-Ag and nano-FeO exposed roots, and reduced the
194" uptake of nano-Ag for clover (Trifolium repens, Feng et al., 2013). Another example is the root
195" bacterium Pseudomonas chlororaphis O6 that significantly affected the levels of bioavailable
196" metal nutrients in nano-CuO and nano-ZnO exposed mung bean (Phaseolus vulgaris, Dimkpa et
197" al., 2015). Below, symbiotic bacteria- and fungi-based microenvironments are discussed in de-
198" tail.
199" Virtually all food crops heavily depend on microorganisms, most obvious in soy-
200" bean (Glycine max, colonized by rhizobia) (Guo & Chi, 2014), a key ingredient in many live-
201" stock diets. Rhizobia, symbionts of legumes (Fabaceae) are N–fixing bacteria (e.g. Rhizobium
202" leguminosarum). They erode few µm sized holes in the root hair cell wall (Mateos et al., 2001)
203" to induce bacteria–containing nodules (McNear Jr., 2013). These nodules can alleviate heavy
204" metal accumulation in symbiotic legume hosts (soybean, cadmium 22% reduced as compared to
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