Subscriber access provided by Binghamton University | Libraries
Article
Uptake, distribution and transformation of CuO NPs in a floating plant Eichhornia crassipes and related stomatal responses Jian Zhao, Wenting Ren, Yanhui Dai, Lijiao Liu, Zhenyu Wang, Xiaoyu Yu, Junzhe Zhang, Xiangke Wang, and Baoshan Xing Environ. Sci. Technol., Just Accepted Manuscript • Publication Date (Web): 06 Jun 2017 Downloaded from http://pubs.acs.org on June 10, 2017
Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a free service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are accessible to all readers and citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.
Environmental Science & Technology is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.
Page 1 of 30
Environmental Science & Technology
1
Uptake, distribution and transformation of CuO NPs in a floating
2
plant Eichhornia crassipes and related stomatal responses
3
Jian Zhao,a Wenting Ren,a Yanhui Dai,a Lijiao Liu,a Zhenyu Wang,*,b,c Xiaoyu Yu,a
4
Junzhe Zhang,a Xiangke Wang,d and Baoshan Xing*,e
5 6
a
7
Laboratory of Marine Environment and Ecology, Ocean University of China, Qingdao 266100,
8
China
9
b
College of Environmental Science and Engineering, and Ministry of Education Key
Institute of Environmental Processes and Pollution Control, and School of Environmental
10
and Civil Engineering, Jiangnan University, Wuxi 214122, China
11
c
12
Marine Science and Technology, Qingdao 266071, China
13
d
14
Beijing 102206, China
15
e
16
01003, USA
Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for
School of Environment and Chemical Engineering, North China Electric Power University,
Stockbridge School of Agriculture, University of Massachusetts, Amherst, Massachusetts
17 18 19
*Corresponding authors
20
Tel.: +1 413 545 5212; fax: +1 413 577 0242
21
E-mail address:
[email protected] (Dr. Baoshan Xing);
[email protected] (Dr. Zhenyu
22
Wang)
23 1
ACS Paragon Plus Environment
Environmental Science & Technology
24
Abstract.
25
Engineered nanoparticles (NPs) are releasing into aquatic environments with their
26
increasing applications. In this work, we investigated the interaction of CuO NPs with a
27
floating plant, water hyacinth (Eichhornia crassipes). CuO NPs (50 mg/L) showed significant
28
growth inhibition on both roots and shoots of E. crassipes after 8-day exposure, much higher
29
than the bulk CuO particles (50 mg/L) and corresponding dissolved Cu2+ ions (0.30 mg/L).
30
Scanning electron and light microscopic observations showed that root caps and meristematic
31
zone of E. Crassipes were severely damaged after CuO NP exposure, with disordered cell
32
arrangement and destroyed elongation zone of root tips. It is confirmed that CuO NPs could be
33
translocated to shoot from both roots and submerged leaves. As detected by X-ray absorption
34
near-edge spectroscopy analysis (XANES), CuO NPs were observed in roots, submerged
35
leaves, and emerged leaves. Cu2S and other Cu species were also detected in these tissues,
36
providing solid evidence on the transformation of CuO NPs. In addition, stomatal closure was
37
observed during CuO NPs-leaf contact, which was induced by the production of H2O2 and
38
increased Ca level in leaf guard cells. These findings are helpful for better understanding the
39
fate of NPs in aquatic plants and related biological responses.
40
2
ACS Paragon Plus Environment
Page 2 of 30
Page 3 of 30
41
Environmental Science & Technology
TOC Art
42 43
3
ACS Paragon Plus Environment
Environmental Science & Technology
44
INTRODUCTION
45
CuO nanoparticles (NPs) are commonly used in pesticides, paints, textiles, plastics,
46
sensors and catalysts.1,2 Rapid growth in production and application of CuO NPs will
47
inevitably result in the introduction of NPs into aqueous environments. As a type of high-toxic
48
NPs, toxicological researches on CuO are widely conducted towards various species including
49
terrestrial plants, algae and bacteria.3-6 However, little nanotoxicological information is
50
available for aquatic plants in comparison with above species.7 Aquatic plants are critical
51
components of aquatic ecosystems, functioning as sources of organic matters, food for aquatic
52
animals, and sinks for nutrients.8 Currently, there are only three reports on the toxicity of CuO
53
NPs towards aquatic plants. Perreault et al. found that growth and photosynthesis of Lemna
54
gibba L. were inhibited after CuO NP exposure, and the release of Cu2+ ions was identified as
55
a main reason for the observed toxicity.1 However, the nanoparticulate CuO rather than soluble
56
Cu2+ ions caused reduction in growth of both duckweeds (Landoltia punctata)9 and soft-stem
57
bulrush (Schoenoplectus tabernaemontani).10 These contradictory results suggest that the
58
contribution of nanoparticulate CuO to the total toxicity is unclear for aquatic plants. The
59
toxicity mechanism of CuO NPs and related biological responses of aquatic plants deserve
60
further investigations.
61
The roots and submerged leaves of aquatic plants will directly interact with CuO NPs in
62
water columns during exposure. CuO NPs (23-50 nm, 50 mg/L) were evidenced first to be
63
accumulated in root tissues of the aquatic plant Schoenoplectus tabernaemontani,10 in which
64
CuO NPs were aggregated around organelle after penetrating cell wall and plasma membrane.
65
But the limited root-shoot translocation potential was suggested in this study. For rice which is
4
ACS Paragon Plus Environment
Page 4 of 30
Page 5 of 30
Environmental Science & Technology
66
commonly recognized as a semi-aquatic or terrestrial plant, CuO NP (43 ± 9 nm, 100 mg/L)
67
transport from its roots to leaves was confirmed based on X-ray absorption near edge structure
68
(XANES) analysis.2 Maize could also root-shoot transport CuO NPs (20-40 nm, 100 mg/L) via
69
xylem.11 One possible reason for this difference on NPs transport between aquatic and
70
terrestrial plants is the more extensive roots in terrestrial plants. In addition, terrestrial plants
71
have highly-developed xylem which has been confirmed as a main pathway for NP transport.
72
It is still unknown whether the poorly-developed xylem vessels in roots of aquatic plants could
73
effectively transport NPs. For submerged leaves of most aquatic plants, the cuticle and its
74
waxes are much thinner or absent as compared to terrestrial plants to facilitate foliar uptake of
75
water and nutrients.12 Therefore, submerged leaf of aquatic plants could be an excellent model
76
to investigate foliar uptake mechanism of water-exposed NPs. Aquatic plants are thus
77
hypothesized to accumulate NPs from water column through both roots and submerged leaves,
78
and the latter is expected to have a higher contribution on CuO NP accumulation in shoots. To
79
confirm this hypothesis, a new device is designed in an emergent treatment with the separation
80
of leaves from water column in this work. In addition, dissolution and sulphidation could be
81
two transformation processes of CuO NPs in aqueous phase, especially in the presence of
82
natural organic matter.13 After internalized by freshwater algae (Chlorella pyrenoidosa), CuO
83
NPs were partially transformed to Cu2O.5 Cu2S was detected in the plants of both maize
84
(xylem sap)11 and wheat (shoot)3 while it was not found in either roots or shoots of rice.2 The
85
specific processes of CuO NP transformation in aquatic plants needs to be explored. Moreover,
86
the stomata on submerged leaf is a key organ for acquirement of CO2 and nutrients, and uptake
87
of exogenous matters such as heavy metals,14 mineral particles15 and nanopesticides.16 It is
5
ACS Paragon Plus Environment
Environmental Science & Technology
88
hypothesized that CuO NPs could be internalized through stomata during foliar uptake, which
89
is a possible mechanism for CuO NP toxicity. The responses of stomata when interacting with
90
CuO NPs and the relevant signaling pathway will be investigated in the present work.
91
Overall, the main objectives are thus to investigate (1) the toxicity of CuO NPs to aquatic
92
plants and related damages on roots and leaves; (2) root uptake, root-shoot translocation and
93
foliar uptake of CuO NPs; (3) transformation of CuO NPs in aquatic plants; and (4) stomatal
94
responses of leaves upon CuO NPs and related mechanism for CuO NP-induced stomatal
95
closure. Water hyacinth is selected in this study because it is a representative free-floating
96
plant that can float on the surface of water column. Leaves of water hyacinth could be
97
submerged in water or emerged atop the water column, which is helpful for investigating the
98
contribution of foliar uptake of NPs. The newly generated information on accumulation,
99
distribution and transformation of CuO NPs in water hyacinth will be helpful for
100
understanding the behavior and ultimate fate of NPs in aquatic plants and potential risk of NPs
101
transfer through aquatic food chains because water hyacinths are sources of food for aquatic
102
animals.
103
MATERIALS AND METHODS
104
Materials.
105
CuO NPs (No. 544868,
