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Current Nanoscience, 2020, 16, 27-41

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ISSN: 1573-4137
eISSN: 1875-6786

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Recent Advances in Plant Nanobionics and Nanobiosensors for Toxicology

Applications

Mohammad Hasan Dad Ansari1, Santosh Lavhale2, Raviraj M. Kalunke3, Prabhakar L. Srivastava4,
Vaibhav Pandit5, Subodh Gade6, Sanjay Yadav7, Peter Laux8, Andreas Luch8, Donato Gemmati9,
Paolo Zamboni10 and Ajay Vikram Singh1,8,*

1
Department of Physical Intelligence, Max Planck Institute for Intelligent Systems, Heisenbergstr. 3, Stuttgart 70569,
Germany; 2Biochemical Sciences Division, CSIR-National Chemical Laboratory, Dr. Homi Bhabha Road, Pashan, Pune
411008, India; 3Institute of Plant and Microbial Biology (IPMB), Academia Sinica, Taipei, Taiwan; 4School of Chemis-
try, Cardiff University, Cardiff, CF10 3AT, United Kingdom; 5Dynex Technologies Inc. 14340 Sullyfield Circle, Chanti-
lly, VA 20151, USA; 6Department of Technology, University of Pune, Ganeshkhind, Pune 411007, India; 7Department of
Orthopedics, Institute of Medical Sciences, BHU, Varanasi, India; 8Department of Chemical and Product Safety, Ger-
man Federal Institute for Risk Assessment (BfR), Max-Dohrn-Strasse 8-10, Berlin 10589, Germany; 9Hemostasis &
Thrombosis Center, Azienda Ospedaliera-Universitaria di Ferrara, via Aldo Moro 8, 44124 Ferrara, Italy;
10
Translational Surgery Unit, Azienda Ospedaliera Universitaria di Ferrara, via Aldo Moro 8, 44124 Ferrara, Italy

ARTICLE HISTORY
Received: October 14, 2018
Revised: January 16, 2019
Accepted: March 26, 2019
DOI:
10.2174/1573413715666190409101305
Keywords: Nanotechnology, agro-ecosystems, nanobionics, engineered nanomaterials, nanosensors, nanotoxicology.
Current Nanoscience
Abstract: Emerging applications in the field of nanotechnology are able to solve a gamut of prob-
lems surrounding the applications of agroecosystems and food technology. Nano Engineered Mate-
rial (NEM) based nanosensors are important tools for monitoring plant signaling pathways and me-
tabolism that are nondestructive, minimally invasive, and can provide real-time analysis of biotic and
abiotic threats for better plant health. These sensors can measure chemical flux even at the single-
molecule level. Therefore, plant health could be monitored through nutrient management, disease
assessment, plant hormones level, environmental pollution, etc. This review provides a comprehen-
sive account of the current trends and practices for the proposed NEM related research and its (i)
structural aspect, (ii) experimental design and performance as well as (iii) mechanisms of field ap-
plication in agriculture and food system. This review also discusses the possibility of integration of
data from NEM based nanosensors in current and emerging trends of precision agriculture, urban
farming, and plant nanobionics to adopt a sustainable approach in agriculture.

1. INTRODUCTION actual plant cells using tobacco plant cells grown in a culture
containing carbon nanotubes thereby, improving the cellular
Plants and animals share many similarities at the cellular
conductivity. The researchers have created a plant inspired
and multicellular level [1]. Majority of the sensory mecha-
electronic sensor which responds to changes in conductivity
nisms share commonalities between animals and plants such
with surrounding temperature fluctuations. This plant based
as sensing temperature, pressure, water content, light, gases
nanosensor is at least 100 times more sensitive than the most
and many more [2-4]. These capabilities in plants gave re- advanced temperature sensors available today [10]. In nature,
searchers conducive opportunities to design bio-inspired
plant roots exhibit a soft bending behavior and have a multi-
structures, which fit in our daily life [5]. While technology is
sensing capability to cooperate from various environmental
often considered separate from nature, many of the human’s
parameters, such as tropisms. These have been mimicked
most significant technological advancements mimic nature
into soft bending actuators via designing the motor power in
[6]. Inspired by plant biology, researchers have developed
a compliant manner following roots [11]. Engineers and sci-
ultra-sensitive temperature, pressure, gas, gravimetric and entists heavily rely on nature and biological materials as in-
humidity sensors using new materials [2, 7-9]. Researchers
spiration as even today, many natural materials exhibit prop-
developed a new temperature sensor that takes this material
erties, which cannot be translated into synthetic counterparts.
concept a step forward, molding synthetic components with
Preliminary work in this context examining fungal and plant
cells cultivated with nano-structures has led to a highly con-
*Address correspondence to this author at the Department of Chemical and
Product Safety, German Federal Institute for Risk Assessment (BfR), Max-
ductive wood like nanomaterial [12, 13]. As shown in Fig.
Dohrn-Strasse 8-10, Berlin 10589, Germany; E-mail: avsingh@is.mpg.de; (1), nanoparticles, being single and multiwall carbon nano-
Ajay-Vikram.Singh@bfr.bund.de tubes are used in a wide variety of modern nanomaterials for

1875-6786/20 $65.00+.00 © 2020 Bentham Science Publishers

28 Current Nanoscience, 2020, Vol. 16, No. 1 Ansari et al.
Precipitation CO2 Radiation Evapotranspiration
(A) Sources of NP’s
Natural and anthropogenic sources of NP’s
(B)
5

Routes of entrance in the ecosystem

1 3
4
Ecosystem Environmental 13
effects on NP
Abiotic interactions
Radiation
Infiltration

Surface runoff 9
Biotic interactions. Uptake. Routes of CO2
entrance in the organisms. Intracellular 2 1 8 8 8
fate. 10
13
effects 11
6
NP’s effects on organisms Nutrient 7 Nutrient
Organism cycling Soil cycling
respiration 8
11 9
8 Soil moisture
Soil CO2 transport
12 Drainage
Population, community, Transfer of the effects. Environmental transport
ecosystem relevance. Risk assessment 12

(C) (D)

Fig. (1). (A) The logical chain of procedures accounting for the toxicity of NP giving an opportunity to design toxicity sensors at various
level. (B) Simplified scheme of aquatic and terrestrial ecosystem processes. [adopted with permission from [126]]. (C) Micro- and ultrastruc-
ture of wood with hierarchy based plant biosensor design. (D) Backscattered electron micrograph of a longitudinal tangential (LT) cut and
cross section through spruce wood infiltrated with Eu:HfO2 nanoparticles. [adopted with permission from refs [127].

their conductive properties, low weight and structural dura-
bility in spite of some cautionary toxicity which may inter-
fere with some biological phenomena [14]. Plant cells are an
excellent model for conductivity studies since their resistiv-
ity responds to tiny changes in environmental temperature
[13]. In the plant cell wall, pectins in wood break apart with
an increase in temperature, which facilitates calcium and
magnesium ions to move with extended freedom which lends
its use to vital applications in thermal sensors with unparal-
leled sensitivity [10]. Plant biology has equipped engineers
with the ability and tools to formulate and develop biohybrid
nanomaterials for potential applications in the fields where
researchers face challenges from both scientific and engi-
neering perspectives. The creation of such nanomaterials is
at the core of technological and scientific innovation vital to
the digital and industrial revolutions in biomedicine. For
example, a touch sensitive plant Mimosa pudica is character-
ized by extremely flexible pressure sensors with low reac-
tion time (<20 ms) and high sensitivity (50.17 kPa(-1)) with
extremely low loading-unloading signal changes over long
cycles [15]. These innovations are only possible in mimick-
ing plant-based pressure sensors. With the increasing role of
artificial intelligence (AI) and algorithm development [16],
these could be integrated into pressure sensitive biomedical
devices to improve the quality of life in debilitating diseases
[17]. These plant-based nanosensor innovations can dramati-
cally change healthcare device development, for example, by
using ubiquitous sensing mechanism in plant biology to de-
velop a cost-effective, ecofriendly and scalable approach to
make flexible e-skins, which offer enhanced sensing capa-
bilities [18, 19]. In this review, we particularly focus on
emerging applications of plant biology as nano biosensors
and nanobionic agents in recent years. We also provide a
brief overview of how knowledge gained from mimicking
plant biology will inspire the next generation of sensors and
bionics interaction with every walk of life.
2. EMERGING FIELD OF PLANT NANOBIONICS
The engineering of living plant for the generation of visi-
ble light and sustainable illumination is interesting because
plants have independent energy requirement, a storage
mechanism and an autonomous self-repair system [20]. Us-
ing advanced nanomaterial engineering, researchers are de-
Plant Nanobionics and Nanobiosensors Current Nanoscience, 2020, Vol. 16, No. 1 29

Outer membrane
(A)
Inner membrane

Stroma

Granum
1.5 μm

Thylakoid
membrane
Thylakoid
Stroma lumen

Nanoparticles
100 nm

(B) (C)

Fig. (2). (A) The natural and artificially engineered photosynthetic materials [adopted with permission from ref. [128]]. (B) Schematic of
hybrid composite design and (C) scanning electron microscopy (SEM) characterization of super tough nanobionic cyberwood production
[adopted with permission from ref. [12].

signing nanoparticle (NPs) based micro-nanosystems to op-
timize transport, synthesis and localization of synthetic cyber
plants mimicking the living organism (Fig. 2). Plants with
high ATP production rates such as spinach (Spinacia ol-
eracea), arugula (Eruca sativa), watercress (Nasturtium offi-
cinale), and kale (Brassica oleracea) are preferred for plant-
based nanobionics study [21]. This has been achieved by
developing NPs of defined size and charge. NPs of 10 nm
size localize in leaf mesophyll and stomata guard cells, while
NPs larger than 100 nm are segregated in the leaf mesophyll.
NPs are inserted in plant leaf by a specially developed
method called the pressurized bath infusion of nanoparticles
(PBIN) [22]. Researchers have developed light-emitting
plants using four chemically interacting nanoparticles as
shown in Fig. (3A-D). A with the following steps i) firefly
luciferase immobilized onto maleimide-functionalized 7 nm
silica nanoparticles (SNP-Luc) to increase stability, ii) D-
luciferin releasing poly (lactic-co-glycolic acid) (PLGA-
LH2) to supply high extracellular flux of luciferin while sup-
pressing local concentration20, iii) chitosan tripolyphos-
phate (CS) carriers to release coenzyme A (CS-CoA) and iv)
semiconductor nanocrystal phosphors. CoA helps in regen-
eration of luciferase and extends its activity. SNP-Luc is
designed to enter mesophyll and stomatal guard cells and
localize near ATP generating organelles namely chloroplast
and mitochondria [23]. PLGA-LH2 and CS-CoA are de-
signed to localize inside the leaf mesophyll cells releasing
luciferin and CoA respectively. These reagents are trans-
ported through the membranes and cell walls [21]. Continu-
ous light formation occurs in two-steps. While the first step
generates photons, the second step is for recycling luciferase.
(1)
(2)
Reactions (1) and (2) have been studied using synthe-
sized NPs, and the authors concluded that the balanced re-
lease of luciferin and its consumption in the first reaction is
crucial for maximizing light production. A reaction mixture
30 Current Nanoscience, 2020, Vol. 16, No. 1 Ansari et al.

(A)

(B) Evaporation (D) b

a Excitation
Excitation
a 6,5 ss(AT)15 SWCNT 7,6 ss(GT)15 SWCNT 250
source

NIR f uorescence

(%air saturation)
200

O2 content
150
0.85 m
Flow direction
Emission
Picric acid (analyte)
OH
O2N NO2
100
blue light on

NIR f uorescence
Long-pass NO2
f lter O2 50

+H2O2
Soil Root Stem Vein/Leaf
(CSTR) (PFR) (PFR) (CSTR)
0
0 100 200 300 400 500
b Quenching
t =1min t =6 min t =10 min t =15 min t =20 min Time (s)
High
Internal H2O2 detection
standard map map c

Chloroplast lantern (ATP1)

CT-Nano-
nIR intensity

t =25 min t =30 min t =36 min t =40 min t =45 min

4,000 CT-Nano-

Intensity (a.u.)
lantern (ATP1)
Low

c t =0 min t =10 min t =20 min t =30 min High

1.6 2,000
I6,5 norm

1.4
2 R7,6 Wild type
nIR intensity

Merge
1
t =40 min t =50 min t =60 min t =70 min 0
0.8 0 2 4 6 8
0 50 100 150 200 0 50 100 150 200 Time (s)
Time (s)
Low

(C) b
Emission
FRET quenching
a FRET
Excitation Excitation Quencher
QD QD
CFP YFP
Binding Analyte
Analyte
domain
Binding
domain

c d H202 +substrate
Analyte HRP Oxidation
Raman intensity

SERS signal
Binding
Excitation Analyte domain
Current
e- Reduction
Conductive e-
AgNP nanomaterial
Binding Electrode
domain Time
Raman tag Raman shift
(cm–1)

e Intensity Wavelength f PZT nanoribbon PPT

change shift

e
trod
Analyte or elec
Amphiphilic ITO Neuronal
polymer cell

SiNX 4
Current (nA)

3
SWNT 2
1
0
–1
–2
–3
0 5 10 15 20 25
Time (s)

Fig. (3). Examples of nanobionic applications and nanosensors in plants. (A) Preparation of nanoparticulate base system for light production
in plant. Reprinted (adapted) with permission from ref. [22]. Copyright (2017) American Chemical Society. (B) Perspective utilization of
light-emitting plants watercress (Nasturtium officinale). [adopted with permission from ref. [28]]. (C) Design and Principles of nanosensors
for plant biology applications. [adopted with permission from ref. [129]]. (a-b) Ratiometric Fluorescence resonance energy transfer (FRET)
Nanosensors to study physiology of small molecules. (c) SERS nanosensor with Raman tag and binding domain. (d) Electrochemical
nanosensor. (e) CoPhMoRe sensor. (f) Piezoelectric (PZT) nanosensor. (D) Examples of nanosensros applied in plant biology. (a) SWNTs
wrapped ratiometric sensor response to H2O2 in-vivo inside leaf section [adopted with permission from ref. [129]]. (b) Dye encapsulated
nano- and micrometer-sized particles for detection of O2 chloroplasts [adopted with permission from ref. [130]]. (c) ATP sensor based CT-
Nano-lantern in chloroplasts [adopted with permission from ref. [131]]. [adopted with permission from ref. [43]].
Plant Nanobionics and Nanobiosensors
containing 1mM PLGA-LH2 produces light for approxi-
mately 21.5 h. The watercress plant emits greater than
1.44×1012 photons/sec or 50% of 1 μW commercial lumines-
cent diodes. The addition of dehydroluciferin and coenzyme
A, leads to “off” and “on” states in the plant, respectively
[24].
3. PLANT NANOBIONICS FOR WIRELESS COM-
MUNICATION AND HAZARDOUS EXPLOSIVE DE-
TECTION
Recent advances in nanotechnology have enabled scien-
tists to introduce non-native functions in living plants using
nanobionics approach. It is well-known in plant biology and
has already been reported that the uptake of organic mole-
cules takes place via roots [25]. It has been proposed that it
is possible to engineer wild plants using specifically de-
signed nanoparticles with properties like microfluidic, stand-
off detector, etc. Recently, several studies have attempted to
introduce bioremediation and detection function in wild
plants using genetic engineering (Fig. 3B).
Explosive weapons in peace and war became the pre-
dominant headache for post-war scenarios and terror-related
events [26]. In addition to that, developing countries have to
deal with the aftermath of implanted mining incidents, which
costs many lives annually [27]. Developing a plant-based
sensor in this context could have a major impact on improv-
ing the socioeconomic status in the developing world. In a
recent study, scientists developed a spinach plant (Spinacia
oleracea) based sensor for the detection of nitroaromatic
compounds like picric acid (model explosive analyte) [28].
They introduced two near-infrared (NIR) fluorescent
nanosensors: Single-walled carbon nanotubes (SWCNTs)
conjugated with Bombolitin II and polyvinyl alcohol acti-
vated (PVA) SWCNTs. SWCNTs emit near-infrared (NIR)
photoluminescence, which is sensitive to its environment.
Bombolitin II is a peptide, which recognizes nitroaromatics
compounds. Peptide-SWCNTs complexes function as a vir-
tual ‘chaperone sensor’, which senses modulation of the pep-
tide secondary structure via changes in NIR photolumines-
cence of SWCNTs. Recognition of nitroaromatics by Bom-
bilitin II leads to a change in the conformation of SWCNTs
which results in the modulation of its NIR photolumines-
cence [29]. The NIR fluorescence intensity of Bombilotin-
SWCNTs quenches in response to picric acid. The NIR fluo-
rescence signal from PVA activated SWCNTs is used as a
reference signal. Authors also demonstrated a miniaturized
and portable standoff detector similar to a portable smart-
phone using Raspberry Pi (without infrared filters) CCD
camera [30].
SWCNTs coated in PVA (P-SWCNTs) and Bombolitin II
(B-SWCNTs) were infiltrated in two regions of leaf lamina
using needleless syringe. The intensity of B-SWCNTs re-
duced in response to the detection of picric acid as compared
to P-SWCNTs. The change in the ratio of B-SWCNTs to P-
SWCNTs was used for the detection of picric acid by plants
[31]. This ratio declined 5-15 minutes after the addition of
picric acid to the solution in which roots of the plant were
submerged.
Nanoparticle-based engineering coupled with plant sen-
sors has also been developed into dopamine-detecting plant
Current Nanoscience, 2020, Vol. 16, No. 1 31
to demonstrate generalization of this technology [32]. It is
possible to develop plants for applications like alerting an
emergency via chemical monitoring and communication
devices to external electronics at standoff distance using
nanobionics [33].
4. NANOSENSOR TECHNOLOGY IN DEVELOP-
MENT OF FUTURISTIC LIVING PLANT SYSTEMS
Plant science plays a vital role in solving some of the
global problems such as food security and fuel demand [34].
The efficiency of product formation can be increased by
various methods such as phenotyping, breeding, genetic en-
gineering, etc. To make them more efficient for product for-
mation, it is important to accurately study/monitor processes
(metabolic pathways) involved in product formation (Fig. 4).
Detailed information of plant characteristics including ana-
tomical, ontogenetical, physiological, and biochemical prop-
erties are crucial prerequisites for phenotyping/breeding [35,
36]. Conventionally, for this kind of analysis, radioisotope
tracer techniques and optical image techniques (thermogra-
phy and fluorescence) are employed, but these tools lack
temporal and spatial resolution [37-40].
Recent developments in nanosensors allow monitoring of
the cellular functions and also spatiotemporal dynamics of
particular analytes [41]. In agriculture, nanobiosensors are
used to detect soil nutrients, contaminants which have helped
to reduce fertilizer consumption, and environmental pollu-
tion [42, 43]. Nanosensors installed in plant enables real-
time monitoring of several important processes like meta-
bolic pathways, signaling cascades, etc. [44, 45].
5. DESIGN AND PRINCIPLES OF NANOSENSORS
FOR PLANT BIOLOGY APPLICATIONS
5.1. Fluorescence Resonance Energy Transfer (FRET)
Nanosensors
FRET nanosensors are used to study small molecules,
protein dynamics, and biophysical parameters [46]. They
have been successfully used for genetic engineering and
biomolecule detection. This type of sensor uses two fluoro-
phores; photoexcitation of one will resonantly transfer en-
ergy to the second one and result in fluorescence release by
the acceptor molecule. Resonance transfer of energy happens
only if the distance between the donor and the receiver is in
the nanoscale range [46, 47]. Using this basic principle, sen-
sors can be designed such that the binding of an analyte
leads to a change in the distance between the donor and the
receiver fluorophore.
The FRET-based nanosensors used in the plants are ge-
netically encoded FRET nanosensors- present in the plant
itself such as fluorescence proteins of two different spectral
variants. These sensors have been successfully used for de-
tection of DNA [48], metal ions [49-51], organic compounds
[52], and are added exogenously as externally synthesized
constructs. b) Nanoparticle-based FRET sensors are devel-
oped using various nanoparticles including gold NPs,
mesoporous silica NPs, polymer NPs, semiconductor quan-
tum dots (QDs), and lanthanide-doped up-conversion
nanoparticles (UCNPs), which act as either a FRET donor or
32 Current Nanoscience, 2020, Vol. 16, No. 1 Ansari et al.

a quencher. QDs provide tunable emission wavelengths [53]
which can be of additional use (Figs. 3C and 3D).
5.2. Surface-enhanced
Nanosensors
SERS is an ultrasensitive nondestructive spectroscopic
technique, efficient enough to detect single molecules of an
analyte. Raman signals of molecules adsorbed on the surface
of metal NPs can be enhanced by a factor of up to 1014.
SERS is described by two mechanisms, namely the long-
range electromagnetic effect (EM) and a short-range chemi-
cal effect (CM) [54]. SERS nanosensors have been utilized
for glucose detection and measurement of redox potential in
humans and animals but not yet in plants.
5.3. Electrochemical Nanosensors
Electrochemical nanosensors consist of a working elec-
trode, counter electrode, and reference electrode. Electro-
chemical electrodes designed with NPs have a broader range
of detection. Gold NPs, carbon nanotubes, graphene-based
nanomaterial can be used for electrode development [55].
These sensors have the potential to detect redox active spe-
cies in the plant to indicate growth and environment condi-
Raman Scattering (SERS) tion. Wang et al. [56] developed a molybdenum-doped Bis-
muth Vandate (BiVO4) nanoparticle-based nanosensor to
detect the antioxidants’ quantity in fresh food and vegetables
(Figs. 3C and 3D).
5.4. Nanosensors Using Corona Phase Molecular Recog-
nition (CoPhMoRe)
CoPhMoRe is based on specific adsorption of a composi-
tionally designed polymer at a nanoparticle interface to en-
able recognition in almost the similar way to an antigen-
antibody interaction [57]. Surfactant and amphiphilic poly-
mer are wrapped on semiconducting single-walled carbon
nanotubes (SWNTs) [14]. Wrapping stabilizes dispersion in
the aqueous medium and modulates the interaction of other
molecules with SWNTs. Wrapping molecules interact with
the nanotube surface and change the configuration of the
complex, which selectively binds to a specific analyte [58,
59]. Binding of the molecule may lead to changes in the di-

(A) (B)
a Treatment chambers (adhesive restraint) b Perfusion chambers (mechanical restraint) a In planta studies b Heterologous studies

Seedling Probing accumulation/elimination rates Screening for novel transporters

Tubing Clone library
Biosensor
response

Analyte

Transporter
Pulsed perfusion with analyte candidate
Coverslip Time
Purple clay Medical adhesive (PDMSglue)
Probing af nity of transport systems
Biosensor
response

[Low] [Med] [High]

Time
Probing mechanismof transport systems Mutant characterization
Liquid growth Support Wire mesh
Biosensor
response

media/water Mock
Protonophore
Sensorized
transport x
Pulsed perfusion with analyte
c Agar chamber d Microf uidics perfusion chambers Time
Pipette
Probing spatiotemporal patterning
Tissue A
Biosensor
response

Tissue B

Interactor characterization
Agar Pipette tip with agar Semisolid PDMSmicrof uidic [n] [n] [n] [n] [n] [n]
chip (lab-on-chip)material Sensorized
Time Time transport
Probing activity in mutants
Biosensor
response

Wild type
Transporter mutant

Pulsed perfusion with analyte

Time

Fig. (4). (A) Schematic illustrations (Left Panel) to show imaging chambers to record plants expressing biosensors. (a) Adhesive restraint to
monitor the plant response to short-term treatments. (b) Perfusion chambers with mechanical restraint to monitor plant responses to various
treatments. (c) Soft Agar mediated approach to monitor variations in biosensor ratio. (d) Perfusion chamber with Microfluidics to monitor
plant root responses. Abbreviation: PDMS, polydimethylsiloxane. (B) Biosensors for studying transport in plants. (a) Genetically encoded
biosensors to monitor elimination and accumulation rates following pulsed application of exogenous analytes. (b) Biosensors used in het-
erologous systems to screen for novel plant transporters [e.g., SWEET1] and, through the use of sensitized transporters, to rapidly cross-
examine the effects of protein interactions and mutations on the activity of plant transporters [e.g., NRT1.1/CHL1/NPF6.3]. [adopted with
permission from ref. [132]].
Plant Nanobionics and Nanobiosensors Current Nanoscience, 2020, Vol. 16, No. 1 33

electric environment surrounding the SWNTs and wave-
length of emitted photons. SWNTs were successfully utilized
for the detection of dopamine, nitric oxide and H2O2 in plants
[60, 61]. CoPhMoRe technique has also been successfully
used to detect ribose, glucose, and arabinose [62].
5.5. Carbon and Ferromagnetic Bionic Materials
Microwave absorbing nature of the carbon-based materi-
als further widens the applications of these SWCNTs hybrid
nanobionics materials. Carbon and its allotropes (nanostruc-
tures, graphite, active carbons, polymer carbon composites)
are easily heated by microwave radiation which yields the
novel functionalities into the carbons with tailored proper-
ties, to be used as microwave absorbers/receptors to ther-
mally actuate other materials indirectly [63]. This further act
as a microwave receptor and catalyst in diverse heterogene-
ous feedbacks since carbon microwave materials are used in
thermal treatments. The use of microwave heating utilizing
SWCNTs and MWCNTs into bionic prosthesis compared
with other methods based on conventional heating has gone
many folds higher. Further microwave absorption properties
make them a good choice for food and food packaging prod-
ucts [64].
Other than carbon, steady short carbon fibers (SCFs)@
TiO2 and γ-Fe2O3@C nanorod-carbon sphere composites
exhibit enhanced low-frequency microwave absorption and
attenuation ability at low and medium frequency. Such tita-
nium-based composites could be very useful for micropros-
thesis of bionic intraoral devices [65, 66]. Amorphous hier-
archical NiCo2O4–CoNiO2 ferromagnetic hybrids and anisot-
ropic copper cobaltate-copper oxide composites are other
efficient electromagnetic wave absorptive materials [67, 68].
5.6. Plasmonic Metamaterials and Photonic Crystals
Optically active or plasmonic NPs from noble metals
such as gold, copper and silver exhibit strong interactions
with incident light and can magnify the local electromagnetic
field, influencing some of the characteristics of the particles
in biology [69]. Albeit these NPs are used in photothermal
therapy, however, these optical NPs can convert light into a
thermal heat even during routine characterization of biologi-
cal system-interaction to serve as sensors for nanotoxicol-
ogy. Nanoparticles’ compatibility in this size with the plas-
monic interaction to evaluate the nanotoxicity has been criti-
cally ignored in the research community [70].
Periodic photonic crystals based optical nanostructures
are used in manipulating light, which will be used in future
bionic eyes and smart biologically engineered interfaces to
mimic and functionally adopt their natural counterparts [5].
5.7. Piezoelectric Nanosensors
Piezoelectricity is a coupling of the electric and mechani-
cal behavior of the material. The piezoelectric effect is the
ability of certain materials to change electric signal and me-
chanical vibration in response to mechanical stress and the
electric field, respectively. Functional oxides of unique class
(e.g., ZnO, SnO2, In2O3, Ga2O3, CdO, and PbO2) exhibit
semiconducting and piezoelectric properties [71]. Piezoelec-
tricity dependent mechanosensors have been successfully
used in biological systems for the study of periosteal/ en-
dosteal surfaces in bone tissues [72], neuromuscular trans-
mission module [73], and to monitor cellular deformations
[74]. These sensors can be utilized in the plant for similar
kind of detection applications.
Using the aforementioned technologies, nanosensors
have been successfully developed for the detection of vari-

a b (A) (B)
Foliar entry Size exclusion limits of barriers of ENP uptake
Cucle
Stomata size (nm)

(A) (B) Hydathodes

Lencels
0.1 1 10 100 1000
Cell walls
Wounds
Extracellular spaces
of cell walls
Phloem

Cell membranes
Xylem

Plasmodesmata
Root entry Casparian strip
Vaseulature
Root ps
Lateral roots Pit membranes
Root hairs Cucles
Rhizodermis Stomata
Ruptures Hydathodes/lencels
40 mm 40 mm Cell wall juncon

c d 100

80 ~76nm
Normalized Frequency %

60 100
Normalized Frequency %

40 80
~47nm
20 60

0 Digestion 40
50 100 150 200
Diameter / nm
20
SP-ICP-MS
SP-ICP-MS 0
25 50 75 100
Diameter/nm

PdNPs
40 mm 40 mm (C)

Fig. (5). (A) Fluorescence microscopic images of roots in control (a), 0.05 (b), 0.1 (c) and 1 (d) mg/L of TiO2-NPs suspensions. Microscopic
images present the remarkable shiny dots inside the roots indicating an increase in aggregations from (a) to (d). TiO2-NPs [adopted with
permission from ref. [133]]. (B) Entry Mode and Size Exclusion Limits of a Series of Barriers for the Uptake and Transport of Nanoparticles
in Plants [adopted with permission from ref. [134]. (C) Sensing bioaccumulation of catalytic NPs cycle [adopted with permission from ref.
[135].
34 Current Nanoscience, 2020, Vol. 16, No. 1 Ansari et al.

ous analytes in plants, such as glucose, nitric oxide, hydro- because of multiple scattering while low reflectance at Short-
gen peroxide, molecular oxygen, adenosine triphosphate, wavelength infrared (SWIR) region due to absorption by
strigolactones, dopamine, and phytoestrogens [75]. Further, water, proteins, and other carbon constituents [83]. Different
they can sense structural changes in plant genomic DNA, pathogens affect different biomolecules; hence some dis-
ethylene and volatile organic compounds, mechanosensing eases may be detected in NIR and some in the middle infra-
of plant growth, high resolution crop monitoring, plant red (MIR) region. Reflectance in the NIR region is high for
pathogen (Xanthomonas axonopodis pv. vesicatoria), toxic leaf tissues, but pigments cannot absorb in this region, so any
metal ion detection (Cu(II), Cd(II), and Pb(II) as shown in change in reflectance in the NIR region is not because of
Figs. (5A-5C) [76, 77]. pigment content but might be because of foliage wilting in
the canopy. Similarly, MIR reflectance region is related to
6. NANOSENSOR BASED MONITORING OF PLANT– water content and reveals water-stress in the canopy.
PATHOGEN INTERACTIONS FOR SUSTAINABLE Raman spectrum can be used for the detection of lower
AGROECOSYSTEMS analyte concentration because of the unique Raman scatter-
Food supply to increased population (11 billion in 2100) ing properties due to water [43]. Raman spectroscopy is
will be one of the biggest challenges in future. It is important effective for carotenoid content analysis in the plants. Caro-
to increase production along with the prevention of loss by tenoid is the most important feature for early detection of
plant diseases [78]. Effective disease management can be Abutilon mosaic virus (AbMV) infection in ornamental
achieved with the help of novel technologies for accurate crops. The intensity of Raman spectra significantly decreases
assessment of severity and early diagnosis. Plant diseases are when the plant is infected by the AbMV [84]. Raman spec-
diagnosed using molecular biology and physical techniques. tral bands related to amino acids and proteins (815, 830,
Molecular biology-based techniques are highly accurate but 852, 918, 926, 970, 1002, 1053, and 1446 cm-1), carbohy-
slow and expensive. Comparatively, physical techniques are drates (905, 1043, 1127, 1208, 1370, 1272, 1340, and 1260-
fast, sensitive, and nondestructive [79, 80]. 1280 cm-1), and lipids (1734, 1736, 1738, 1745, and 1746
cm-1) are characterized for detecting Huanglongbing disease
Vibrational spectroscopy is one of the commonly used caused by the bacteria Candidatus Liberibacter asiaticus on
physical techniques for plant disease diagnosis because of its orange trees [85].
flexibility, efficiency, and cost-effectiveness [81]. Infrared
(IR) and Raman spectroscopy are the two vibrational spec- Nanomaterial-based products, ranging from medicine to
troscopy techniques to measure absorption in the IR region, agro farm applications, are increasingly finding their way to
and vibrational energy associated with chemical bonds in the market. Most of the nanotechnology-based products have
plants. Using these techniques, the concentration of pig- carbon nanotubes (CNTs); these may be single walled
ments, proteins, and water is measured [82]. (SWCNTs) or multi-walled carbon nanotubes (MWCNTs).
SWCNTs show higher antimicrobial property than
Using IR spectroscopy, it is possible to diagnose the dis- MWCNTs [86]. Surface properties of CNTs are important
ease before the appearance of morphological symptoms. A for their activity and toxicity. Wang et al. [87] studied the
healthy plant causes a high reflectance in the NIR region
Environmental variables
(A) (B) Viral Fungal and
replication oomycete
sporulation
Plant cell wall degradation
by soft-rot bacterium

Effect of high temperature Effect of high humidity

Plant physiological status Plant physiological status 5’

RISC 3’

Altered growth pathways Normal growth pathways RNAi

Weaker immune response Temperature
Stronger immune response ETI
OH
Altered abiotic response CO 2 Normal abiotic response O O OH
ABA Bacterial type III effectors

Humidity
ETI
T-DNA transfer
from
Agrobacterium Plant cell

Aqueous
Weaker Plant resistance Stronger apoplast
Disease

(C)
Health

Aqueous
apoplast

O O
N
P. syringae
Stronger Pathogen virulence Weaker PTI
OH
O
replication

Effect of high temperature Effect of high humidity

O
N O

OH

Type III effectors Coronatine

‘Water-soaking’ effectors
O OH
OH
OH
O O OH

Pathogen status Pathogen status ABA SA

Stronger pathogen survival Weaker pathogen survival

ETI
Stronger spore germination Weaker spore germination
ETI
Stronger virulence factor expression Weaker virulence factor expression
Stronger virulence factor delivery Weaker virulence factor delivery
Arabidopsis thaliana

Fig. (6). (A) Impact of environmental variables on plant–pathogen interactions. The temperature and atmospheric CO2 concentration associ-
ated dominant greenhouse effect and water availability are three most important environmental conditions predicted to change in this century
influencing host pathogen interaction. (B) The triangles of molecular actors of environment- plant–pathogen influencing disease. (C) Scheme
depicting the environment-Arabidopsis–Pseudomonas triangular interaction [adopted with permission from ref. [78].
Plant Nanobionics and Nanobiosensors
effect of MWCNTs and modified MWCNTs with different
surface groups (OH-, COOH-, and NH2-) on spores of
Fusarium graminearum. These modified MWCNTs affect
Fusarium graminearum by inhibiting its spore elongation
and germination.
7. NANOSENSORS BASED MONITORING OF
CHANGING CLIMATE CONDITIONS
Plant diseases have a severe effect on the socioeconomic
status at the global scale. Plant pathogens cause direct pro-
duction loss by affecting both quality and quantity. It has
become a challenge for scientists to understand different
aspects of plant diseases such as molecular, epidemiological
and ecological interactions [88]. The severity of loss by
pathogens depends on the type of pathogens (monophagous,
oligophagous, or polyphagous) and their life cycle. Patho-
gens with large host range (polyphagous; ex- Helicoverpa
armigera) and small life cycles are more disastrous than
pathogens with a small host range (monophagous; ex- Try-
poryza incertulus) and long life cycle.
According to the ‘disease triangle’ concept, for a disease
to occur, a triumvirate of the susceptible host, virulent
pathogen and suitable environment is required [78] (Fig. 6).
Optimum environmental conditions are required for the
plants and pathogens for their growth, development and re-
production. Optimal conditions are similarly required for
disease outbreak. Plant disease development is affected by
environmental conditions such as temperature, light and wa-
ter availability, soil fertility, wind speeds, and atmospheric
ozone, methane and CO2 concentrations. Among these, CO 2
concentration, temperature, and water availability are pre-
dicted to be altered significantly in this century.
7.1. CO2 Concentration
After the industrial revolution, atmospheric CO2 concen-
tration is dramatically increasing. Now it has reached to 400
ppm threshold from < 285 ppm at the beginning of the 19th
century [89]. Intergovernmental Panel on Climate Change in
2014 projected that, due to increased greenhouse gases, at
the end of this century, there will be an increase in the global
temperature between 1.5°C and 4.8°C. Increased temperature
affects water availability, which ultimately results in a
change in cultivated areas. It has been observed that due to
increased temperature, pest and pathogen distribution is
moving toward the poles [90]. Higher CO2 concentration
enhances photosynthetic rate in C3 plants [91] while there is
no enhancement in C4 plants [92]. While increased photo-
synthesis improves growth, it also increases disease severity
in C3 plants. The high CO2 level increases susceptibility and
virulence of Fusarium graminearum in both the susceptible
and resistant varieties of wheat [93]. In contrast, the severity
of disease by Peronospora manshurica was found to be de-
creased in the soybean [94]. A modeling study was carried
out to assess the risk of Phytophthora infestans in potato for
the next 60 years and predictions suggest that during the first
half of potato growing season, the severity of the infection
would increase [95]. The predicted results might be due to
the indirect effect of increased CO2 because this model did
not separate the effect of CO2 from the effect of temperature.
In case of wheat, elevated CO2 has no effect on barley yel-
Current Nanoscience, 2020, Vol. 16, No. 1 35
low dwarf virus infection severity [96]. These results are not
sufficient to conclude the effect of CO2 on plant pathogen
interaction; hence a detailed study is required considering the
current state of plants, pathogens and the role of ecosystem.
7.2. Temperature
An optimal temperature range is required for plant-
pathogen interaction. For example, 15°C is required for Glo-
bodera pallida to infect a potato plant [97], while 35°C dur-
ing day and 27°C at night are the conditions for Xantho-
monas oryzae to infect rice [98]. Moreover, the temperature
range of 26°C to 31°C is required for papaya ringspot virus
to infect papaya [99]. Interaction of some plant pathogens is
very sensitive to temperature and environment. Puccinia
striiformis is unable to infect wheat in the laboratory at 21°C
which is the optimum temperature for its infection in the
field [100]. In another case, the fluctuation of 5°C tempera-
ture from the optimum leads to a more susceptible potato
plant for Phytophthora infestans [101]. In tripartite interac-
tion of Banana bunchy top virus (BBTV), the optimum tem-
perature plays an important role in interaction between the
host plant banana and vector aphid (Pentalonia nigroner-
vosa). The optimum temperature for this aphid and for
BBTV infection is 25°C [102, 103]. It can be concluded
from these findings that the projected global temperature
increase will affect plant-pathogen interaction in both posi-
tive and negative ways. To understand the severity of inter-
action, it is important to study the effect of temperature con-
sidering other components of ecosystem such as the concen-
tration of gasses, pH, humidity, pathogen vector, etc.
7.3. Water Availability
Aerial plant parts are severely affected by humidity, be-
cause humidity generally promotes the growth of pathogens.
Soil and air humidity depend on the rain or availability of
water. Virulence of some pathogens increases in high humid-
ity such as Sclerotinia sclerotiorum in tomatoes [104],
Phytophthora capsici causes fruit rot [105], etc. Some
pathogens require wet tissues for infection such as Mag-
naporthe oryzae (rice blast fungus) and Puccinia striiformis
(stripe rust fungus) [106]. In contrast to the above findings,
some pathogens require less humid or dry environment for
the manifestation of pathogenicity such as Magnaporthe
oryzae (rice pathogen) and Streptomyces spp (potato patho-
gen) [107]. A balanced moisture approach can also be used
along with other approaches for effective disease manage-
ment [108].
The combined effect of different environmental factors
may affect the severity of an infection. For example, infec-
tion by turnip mosaic virus (TuMV) becomes more severe in
Arabidopsis thaliana under higher heat and drought condi-
tions [109]. Similarly, the intensity of infection by Botrytis
cinerea in grapes increases under high humidity conditions,
and temperature range between 20°C to 25°C [110]. The
mechanism behind the combined effects is yet to be ex-
plored.
The environment, directly or indirectly, affects various
important processes of plant defense system. These include
PAMP-triggered immunity (PTI), effector-triggered immu-
nity (ETI), Quantitative Resistance Traits, RNA interference
36 Current Nanoscience, 2020, Vol. 16, No. 1 Ansari et al.

Table 1. List of Biosensors developed based on plant tissue or material.

Sr No Plant/Plant Feature Analyte Principle / Method Detection References

Limit

1 Peroxidase from Tobacco Hydrogen Enzymatic reduction of target analyte mediated by ferrocene. 7.5 × 10−7 M [128]
plant peroxide

2 Sulfite oxidase from Malva Sulfite in food Sulfite is converted to sulfate in presence of dissolved O2 by sulfite oxidase. 0.2mM [129]
vulgaris tissue homogenate Consumed oxygen measured by amperometrically.

3 Sulfite oxidase from Arabi- SO2 in food HPLC method with immobilized enzyme reactor (HPLC–IMER) 0.01mg/L [130]
dopsis thaliana

4 Peroxidase from tobacco Dopamine in Dopamine reacts with oxygen and produce hydrogen peroxide. luminol 5.3×10−8 g/ml [30]
rat blood react with hydrogen peroxide and produces Chemiluminescence signal, this
reaction is catalyzed by peroxidase

5 Spinach leaves Glycolic acid Glycolate oxidase from spinach oxidizes glycolic acid in presence of dis- 15µM [131]
solved O2, which generated H2O2. Luminol generates electrochemilumines-
cence in presence of H2O2 and positive potential.

6 Apple tissue containing Total flavanol Polyphenol oxidase catalyzes the oxidation of 1,2-dihydroxybenzene group 4 µM [132]
polyphenol oxidase content in beers of flavonols and forms 1,2-benzoquinone. This product is electrochemically
reduced at the electrode surface.

7 Mesocarp of squash (Cu- L-ascorbic acid Oxygen is consumed for oxidation of analyte by ascorbate oxidase. Con- 0.02–0.57 [133]
curbita pepo) or cucumber centration of oxygen is monitored amperometrically. mmol l−1L-
(Cucumis sativus)

8 Polyphenol oxidase from Catechol Oxydation of catechol leads to formation of quinone is detected by glassy --- [134]
coconut carbon electrode.

(RNAi), and intricate regulation of defense hormone path-
ways. The environment also affects the pathogens’ virulence
by affecting their growth, development, sporulation, etc.
CONCLUSION
Nanotechnology Enabled Emerging Research in Agro-
ecosystem Applicable Nanobiosensors: Opportunities and
Challenges
Current research on the use of ENMs and harnessing of
nanoscale properties in a wide range of agriculture-related
applications demonstrates the opportunity to introduce added
functionality, improve performance, and/or enhance effi-
ciency over current practices and technologies, all of which
aim to advance agriculture sustainability [111]. Plant secon-
dary metabolites play an important role in their adaptation to
diverse and inconstant surroundings. These molecules are
essential components of photosynthetic apparatus, provide
color to the flowers and fruits. They also play a crucial role
in plants as providing protection against microbial infections,
herbivores, UV radiation, acting as signaling agents, and
serving as attractants for pollinators and seed dispersers
[112]. The mechanisms through which ‘nano’ contributes to
this realization have been identified, and important key play-
ers are mentioned in Table 1. This mechanistic insight is
critical to enable continued innovation in product design to
further enhance the desired outcome. Without it, we are left
with a discriminative approach based on phenomenological
results and limited advancement towards design favoring
optimized performance. In order to encourage rapid ad-
vancements and an innovative design that promote agricul-
ture sustainability, several informative guidelines have been
identified from the published literature and review that act as
a source of information for ongoing studies [113]. Compre-
hensive knowledge on the development of ENM or active
ingredients used in formulations is critical. It should always
consist of the molecular mass of ENM in the product or a
formulation, incorporation efficiency (of the ENM or active
ingredient) and the volume or amount and the frequency of
application [114]. Tracking of specific materials through the
system should be included wherever possible. In addition to
this, the design of experiments should always include non-
nano controls, which will be used to identify and quantify
the benefit incurred by the use of nano-enabled products
[69]. Integration of metabolomics, transcriptomics, pro-
teomics and bioinformatics data is also required for the iden-
tification of novel biosynthetic pathways involved in the
biosynthesis of specialized metabolites in plants [115, 116].
The mechanisms underlying how the ‘nano’ aspect of the
design is enabling the observed outcome should be dis-
cussed, which are critical in confirming the nano-aspect,
rather than a non-nano artifact.
In addition to this pointed guidance for ongoing studies,
the research community should also consider establishing a
suggested minimum set of standard testing guidelines [117]
which include, (i) a concentration range and type of crops
used for exposure studies, and (ii) metrics for benefit quanti-
fication (e.g., root and shoot length, yield as dry biomass or
the desired product, nutritional content) for application stud-
ies [118]. These parameters will facilitate the comparison of
results between studies, material efficiency optimization, and
informed design improvements to maximize functional effi-
cacy. This information is necessary to quantify the trade-offs
Plant Nanobionics and Nanobiosensors Current Nanoscience, 2020, Vol. 16, No. 1 37

(a) phy
phot UVR8 cry
(A) (C) UVR8 UVR8

Phototropism Sunscreen production Shade avoidance

(b)

phy
phy phy cry phy
cry ztl cry
(B)

Germination De-etiolation Floral transition Senescense

(c) phot
phot
UVR8

Chloroplast movement Stomata opening

Fig. (7). (A) Agro-defense based Biosensors for food from healthy crops and animals (adopted with permission from refs [136]). (B) Illustra-
tion of bacterial disease symptoms on citrus leaves and fruits. Adapted with permission from refs [137]. (C) Photoreceptors regulate plants
development and adaptation to the light environment. (a) Adaptive responses include phototropism and shade avoidance that maximize ac-
cess to unfiltered sunlight in light-limiting conditions and the biosynthesis of photoprotective pigments in response to UV-B irradiation. (b)
Developmental transitions throughout the life cycle of plants are regulated by photosensory receptors. These include: germination, de-
etiolation, floral transition, and senescence. (c) At the cellular level photoreceptors regulate the position of chloroplasts to maximize light
capture in low light (small arrows) and minimize photodamage in high light (big arrows). They also control the development and opening of
stomata, which represents a key regulatory mechanism controlling gas exchange (CO2 uptake for photosynthesis, transpiration) [Adapted
with permission from refs [138]].

of nano-enabling agriculture early in the design process in an The application of nanosensors for plant environment
effort to preclude future unforeseen consequences [119]. sensing presents a unique set of opportunities to study the
real-time biodistribution and transport of various analytes in
Finally, economics is a critical aspect to consider in the
vivo as shown in Fig. (7). This could vitally contribute to
development of any new product or approach to be applied
plant’s responses to environmental changes, biotic and abi-
to agriculture and food systems. New technologies will only
otic responses, and plants’ signaling and responses during
be realized and advance to fruition if the economics are ad-
their growth and development [121]. The success of nano-
vantageous for both the consumer and the producer, both of
whom are driven by cost minimization. Considering the eco- biosensors depends on the understanding of sensing behavior
and trafficking within the plant, as well as on nanosensor
nomics of the system, not just the cost of the product is criti-
toxicity, specificity, and persistence. Future work will in-
cal to nanotechnologies in particular, since the product may
variably involve the following: (a) Developing new tech-
demand higher capital cost to realize a net positive revenue
niques for the continuous measurement of important plant
stream (e.g., introducing cost effective methods further
metabolites and hormones, and molecular level understand-
downstream via reduction of agrochemical use and/or en-
hanced crop yield) [120]. As with any emerging technology, ing of cellular biosynthetic processes with the help of a high-
throughput multi-omics approach [70]. This will allow the
the novelty of nano-enabled applications in agriculture as
development of strategies for synthetic networks relevant to
well as their predominantly lab-scale production drives high
biosynthetic pathway involved in the production of desired
and uncertain cost. Synthetic pathways for some ENMs are
biomolecules.; (b) Leveraging these new techniques to engi-
in relative infancy, with ongoing efforts to reduce resource
neer plants with highly desirable properties for global food
intensity and increase yields. High initial costs in conjunc-
tion with high levels of uncertainty surrounding widespread security, including high-yield density production, disease
resistance in crop, conferring stress and disease tolerance in
implementation will remain primary obstacles to adoption,
plant, and enhancement of valuable metabolites and nutri-
however, the determination of the level of uncertainty and
tional values in plants [122]; and (c) Developing tools for the
techno-economic approaches in conjunction with life cycle
rapid discovery of important genetic pathways/transcription
assessment can provide guidance for early decision-making
factors in plants, identification of splice variants involved in
in the product design to minimize cost and environmental
impact [22]. important processes, establishing principles for genetic engi-
neering of these pathways into microbes for the production
38 Current Nanoscience, 2020, Vol. 16, No. 1 Ansari et al.

of important metabolites [123] such as: glycosylated, oxy- RNAi = RNA interference
genated, and hydrophobic food components at large scale in SERS = Surface-enhanced Raman scattering
a heterologous system [124]. Increasing interest is also ex-
pected on the use of nanosensor to understand the accumula- SnO2 = Tin dioxide
tion of nitrogen or carbon in plants via the root structure. In SNP-Luc = Silica nanoparticls-luciferase
addition to this, plants have evolved specialized complex SWCNT = Single-walled carbon nanotubes
signaling pathways to protect themselves from various abi-
otic and biotic stresses [125]. The use of selective nanosen- SWIR = short-wave infrared
sors in plants will endow humans with the ability to tap into TuMV = Turnip mosaic virus
these intricate signaling mechanisms, providing us with a UCNP = upconversion nanoparticles
better understanding about plants’ responses against different
environmental stimuli. We envision that such an understand- UV = Ultraviolet
ing will pave the way for creating self-powered photonic ZnO = Zinc oxide
devices as plant nanobionics in the future.
CONSENT FOR PUBLICATION
LIST OF ABBREVIATIONS Not applicable.
AbMV = Abutilon mosaic virus
FUNDING

AMP = Adenosine monophosphate
ATP = Adenosine triphosphate AVS thanks Max Planck Institute for Intelligent Systems
for the grass root project grants in 2017 (M10335) and 2018
BBTV = Banana bunchy top virus (M10338).
BiVO4 = Bismuth Vandate
CONFLICT OF INTEREST
CCD = Charge Coupled Device
CCD = Charge Coupled Device The authors declare no conflict of interest, financial or
otherwise.
Cd(II) = Cadmium ion
CdO = Cadmium oxide ACKNOWLEDGEMENTS
CM = Chemical Declared none.
CNT = Carbon nanotubes
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