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Berg, Science
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EDITORIAL EXPRESSION OF CONCERN 14 September 2017. See first page.
R ES E A RC H

◥ signal (movies S1 and S2). In comparison with the


REPORT ovules grown in the absence of pigment, we did
not observe morphological differences from a sim-
ple visual inspection (fig. S5). On day 20 of incu-
BIOLOGICAL MATERIALS bation, the harvested ovules showed a yellow
coloration of fibers (Fig. 1E) and strong fluores-

Biological fabrication of cellulose cence (Fig. 1, F and G). Using diffuse reflectance
UV–visible spectroscopy, we calculated the uptake
to be 4.8 ± 0.2% on the basis of the band centered at
fibers with tailored properties 497 nm and the respective calibration curve (fig. S6).
Imaging under confocal laser scanning micros-
Filipe Natalio,1,2* Regina Fuchs,3 Sidney R. Cohen,4 Gregory Leitus,4 copy (CLSM; emission wavelength, 490 nm) revealed
Gerhard Fritz-Popovski,5,6 Oskar Paris,5 Michael Kappl,3 Hans-Jürgen Butt3 tubular fluorescent morphology in the three-
dimensional (3D) reconstruction (Fig. 1H), and
Cotton is a promising basis for wearable smart textiles. Current approaches that rely the presence of fluorescent features in the cytosol
on fiber coatings suffer from function loss during wear. We present an approach that (Fig. 1I) confirmed our hypothesis that 6CF-Glc is
allows biological incorporation of exogenous molecules into cotton fibers to tailor the transported through the ovule tissue, metabo-
material’s functionality. In vitro model cultures of upland cotton (Gossypium hirsutum) are lized by the epidermal cellulose-producing cells,
incubated with 6-carboxyfluorescein–glucose and dysprosium–1,4,7,10-tetraazacyclododecane- and integrated into the cotton fibers (Fig. 1J).
1,4,7,10-tetraacetic acid–glucose, where the glucose moiety acts as a carrier capable of Structural characterization of the fluorescent
traveling from the vascular connection to the outermost cell layer of the ovule epidermis, fibers containing 6CF-Glc, termed FGIO fibers
becoming incorporated into the cellulose fibers. This yields fibers with unnatural properties (Fig. 2A), dispelled any suspicion of surface con-
such as fluorescence or magnetism. Combining biological systems with the appropriate tamination during incubation or handling. FGIO
molecular design offers numerous possibilities to grow functional composite materials and wide-angle x-ray scattering (WAXS) patterns
implements a material-farming concept. showed only one broad peak (Fig. 2B, upper panel,

S
red), whereas the raw fiber WAXS patterns
mart or responsive textiles and wearable of traveling from the vascular connection to the attributed to the native cellulose I-b crystal struc-
technologies are fabrics that react to exter- outermost cell layer of the ovule epidermis and ture showed overlapping (110) and (110) peaks at
nal stimuli, such as a change in temperature (ii) a functional molecule (either an optical tracer scattering vector length (q) = 1.05 and 1.18 Å−1,
or humidity (1, 2). Many synthetic polymers or magnetic complex). as well as the (200) peak at 1.62 Å−1 (Fig. 2B,
can be adapted to achieve high perform- We started by exploring the uptake selectivity upper panel, black) (22, 23). The absence of these
ance and multifunctionality by coating fiber sur- of pigments that either were devoid of glucose peaks in the FGIO WAXS signal indicates that
faces by means of chemical treatments (3–5). Such (6-carboxyfluorescein, carminic acid, and indigo) 6CF-Glc induces structural amorphization, which
fibers can have multiple applications (6–14), but or were glucose derivatives (carmine) in the is corroborated by the lack of any evident angular
they suffer from wear. Furthermore, the prefer- millimeter-size fertilized ovules (21) (Fig. 1A). Car- dependence of the pattern obtained by azimuthal
ences of end consumers are for natural fibers mine is a carminic acid glycoside—i.e., carminic integration of the FGIO WAXS peak (Fig. 2B,
because of issues of sensation, skin irritation, acid is bound to the anomeric carbon (C1) of the lower panel). For both fiber types, the azimuthal
smoothness, and weight. This makes biological glucose moiety. The pigments were added to ovule’s profiles obtained from 2D small-angle x-ray
materials a prime choice, spurring intense eco- medium and kept under standard conditions (32°C, scattering (SAXS) patterns (fig. S7, A and B)
nomic interest and research aimed at a compre- 5% CO2) for 20 days. For the pigments devoid of showed clear preferred orientation (fig. S8, blue
hensive understanding of the physiology and glucose, we observed neither an intracellular color- and red)—with the raw fibers showing a higher
biochemistry of cotton fiber development (15). The ation of the epidermal layer (fig. S1, right column) degree of orientation (0.24) than FGIO fibers
identification of the intermembrane cellulose/ nor coloration of the fibers (fig. S1, left column). (0.12)—indicating the presence of oriented fibrous
sucrose synthase complex, its role in promoting For glucose derivatives, namely carmine, we found nanostructures in the size range of a few nano-
glucose polymerization into cellulosic chains (b-1,4- red coloration of the epidermal layer (fig. S2A) but meters. Influence on the SAXS signal from cracks
glucans) (16, 17), and insights into epidermal cell not of the fibers. These results allowed us to infer developing during fiber drying was eliminated
differentiation mechanics were foundational in that the glucose moiety has a role in reaching the by analyzing radial cuts of SAXS patterns of the
establishing the current cellulose biosynthesis path- outermost epidermal layer and that C1 is essential aligned fibers (fig. S9).
ways and cotton in vitro growth models (18–20). for polymerization of glucose units into fibers. Differential scanning calorimetry (DSC) showed
We used upland cotton (Gossypium hirsutum) These results suggested that molecules carrying two major endothermic peaks with minima at
ovules as an in vitro model for biological fabri- a functionality and a glucose moiety with free C1 297° and 400°C for FGIO fibers (Fig. 2C, red) and
cation of cotton fiber composites with fluores- and C4 positions, such as 6-carboxyfluorescein– 324° and 418°C for raw fibers (Fig. 2C, black).
cent and magnetic properties. We synthesized glucose (6CF-Glc), could be transported from the They correspond to the thermal decomposition
two glucose derivatives containing (i) a sugar external medium into the outermost epidermal by depolymerization and volatilization of levo-
moiety (glucose) that acts as a carrier capable layer of the ovule, intracellularly metabolized, glucosans and to charcoal formation, respectively
and biologically integrated into the cellulose fibers. (24). In comparison with the raw fiber peaks, the
1
Institut für Chemie–Anorganische Chemie,
Using peptide chemistry, we synthesized 6CF-Glc FGIO peak located at 297°C is broader and less
Naturwissenschaftliche Fakultät II–Chemie, Physik und by reacting the free amino group located at C2 intense. The FGIO peak at 400°C is sharper and
Mathematik, Martin-Luther-Universität Halle-Wittenberg, of the acetyl-protected glucosamine moiety with more intense. The 27°C temperature offset be-
Kurt-Mothes-Straße 2, Halle 06120, Germany. 2Kimmel the carboxylate from 6-carboxyfluorescein (fig. S3). tween the first endothermic peaks for FGIO
Center for Archaeological Science, Weizmann Institute of
Science, Rehovot 76100, Israel. 3Max Planck Institut für
We incubated 6CF-Glc with fertilized ovules under and raw fibers indicates an increase in the amor-
Polymerforschung, Ackermannweg 10, 55128 Mainz, standard conditions and imaged their development phous cellulose content in FGIO fibers (24), in
Germany. 4Department of Chemical Research Support, under white and ultraviolet (UV) light (365 nm) (fig. agreement with our WAXS results.
Weizmann Institute of Science, Rehovot 76100, Israel. S4). Figure 1C (i to vi) shows a sequence of images Fourier-transform infrared spectroscopy with
5
Institut für Physik, Montanuniversität Leoben, Franz-Josef-
Straße 18, A-8700 Leoben, Austria. 6Materials Center Leoben
acquired under white light after 0, 4, 8, 12, 15, and attenuated total reflectance (FT-IR ATR) analysis
Forschung, Roseggerstraße 12, 8700 Leoben, Austria. 20 days, which demonstrate that the fibers acquired of FGIO fibers showed a decrease in the intensity
*Corresponding author. Email: filipe.natalio@weizmann.ac.il a yellow coloration coincident with the fluorescent of the bands at 2850 and 2915 cm−1 (asymmetric

Natalio et al., Science 357, 1118–1122 (2017) 15 September 2017 1 of 5


EDITORIAL EXPRESSION OF CONCERN 14 September 2017. See first page.
R ES E A RC H | R E PO R T

CH2 stretching), 1727 cm−1 (C=O stretching from responding to O(2)H–O(6) (3465 cm−1), O(3)H–O(5) rupture forces showed substantial scatter, we re-
esters, waxes, fatty acids, and noncellulosic polysac- (3351 cm−1), and O(6)H–O(3) (3262 cm−1), re- frained from converting rupture forces into tensile
charides), 1422 cm−1 (CH2 symmetric deformation), spectively (Fig. 2E), for the raw fibers; for FGIO strength in terms of force per unit area. However,
and 1243 cm−1 (C=O stretching). Furthermore, a fibers, these bands were shifted toward higher given that raw and FGIO fibers have comparable
band appeared at 1204 cm−1 (COH in-plane bending wave numbers (Fig. 2F), revealing disturbances average thicknesses and widths (fig. S10, A and
and structural organization), and the bands at in the H-bond network between the cellulose chains B), and assuming the same degree of twisting, we
1155 cm−1 (antisymmetric stretching of C–O–C (26). In addition, we found two new bands at lower are able to compare the rupture forces for raw
glycosidic bonds), 1053 cm−1 (structural and second- wave numbers (3021 and 3139 cm−1), which we and FGIO fibers under tensile loading. We found
ary wall synthesis), and 896 cm−1 (b-1,4-glycosidic attributed to hydrogen bonding between 6CF-Glc that fiber rupture occurred more often at the edges
bonds) became sharper (21, 25). Scanning electron and the cellulose chains, with expected implica- than in the middle section of the fibers, most likely
microscopy (SEM) imaging revealed comparable tions for the fiber’s mechanical properties. because of stress concentration at the clamp-
average thicknesses (1.7 ± 0.4 and 1.5 ± 0.3 mm) To verify this hypothesis, we conducted tensile ing points (table S1). During the initial phase of
and widths (21 ± 5 and 24 ± 5 mm) for the raw tests on single fibers (fig. S11). Figure 2G shows straining, we observed jumps in the force curves
and FGIO fibers, respectively (fig. S10, A and B), typical force-displacement curves for raw (black) (Fig. 2G) owing to untwisting of the single fibers
indicating that the modifications occur only at and FGIO (red) single fibers. Mean rupture forces with increasing strain (Fig. 2H for FGIO fibers
the structural level. Peak fitting and decon- were 16 ± 6 and 7 ± 3 mN, respectively. The and fig. S12 for raw fibers). Despite the fact that
volution of the region corresponding to the OH standard deviation is attributed to variations in we observed an increase in H bonds between
band (3000 to 3600 cm−1) revealed two intra- the cross-sectional area of the fibers. Because the the cellulose chains and 6CF-Glc and thus would
molecular bonds and one intermolecular bond cor- cross-sectional area varies along the fiber and the expect an increase in rupture force, the global

Fig. 1. Biological incorpora-


tion of fluorescent-tagged
glucose (6CF-Glc) into cot-
ton fibers. (A) A G. hirsutum
flower grown under hydro-
ponic conditions. (B) Sche-
matic representation of the
development of the in vitro
cotton culture model. BT,
Beasley-Ting. (C) Sequence
of microscopic images taken
under “white” illumination
and standard conditions
(32°C, 5% CO2) at 0, 4,
8, 12, 15, and 20 days.
(D) Corresponding sequence
of images taken under UV
illumination (wavelength,
365 nm). (E) A representative
ovule after day 20 of incuba-
tion with 6CF-Glc, showing
yellow coloration of the fibers.
(F) Similar to (E), but under
UV illumination (365 nm),
showing fluorescent fibers.
(G) Binocular image of the
fibers under UV illumination
(365 nm). (H) CLSM 3D
image stack of isolated
fibers displaying a fluorescent
tubular morphology. (I) High-
magnification CLSM image
of a fiber, showing fluorescent
features in the cytosol.
(J) Schematic representation
of the transport of 6CF-Glc
through the embryo to the
outermost layer of the
epidermis, uptake and
metabolism by the cellulose-
producing cells, and integra-
tion into the cotton fibers.

Natalio et al., Science 357, 1118–1122 (2017) 15 September 2017 2 of 5


EDITORIAL EXPRESSION OF CONCERN 14 September 2017. See first page.
R ES E A RC H | R E PO R T

structural amorphization seems to have a predom- i to iv). Visual inspection revealed no morpho- appeared to be dewetted regions (holes) of a depth
inant effect of mechanically weakening FGIO logical differences relative to the control [Fig. 3C of 20 to 25 nm (Fig. 3E).
fibers. and fig. S15 for DOTA-Dy(III)]. Despite the yellow FiDy WAXS diffraction patterns showed a broad
Our second model exemplifies the application to color of the complex, treated fibers remained peak with a maximum at q = 1.35 Å−1 and a distinct
inorganic compounds. We synthesized a water-soluble white (Fig. 3D). Structural characterization was shoulder at about 1.55 Å−1 (Fig. 3F, upper panel,
glucose macrocycle caging dysprosium [Glc-DOTA- thus required to validate the integration of the red). Although the shoulder roughly agreed with
Dy(III); DOTA, 1,4,7,10-tetraazacyclododecane- Glc-DOTA-Dy(III) complex into the fibers. the (200) peak seen in the raw fibers at 1.62 Å−1
1,4,7,10-tetraacetic acid; ground term 6H15/2, spin By using inductively coupled plasma mass (Fig. 3F, upper panel, black), the weaker (110)
angular momentum S = 5/2, orbital angular mo- spectrometry, we detected the presence of Dy(III) and (110) peaks of the cellulose I-b crystal struc-
mentum L = 5, total angular momentum J = 15/2, at a concentration of 2.25% (weight/weight) in ture were absent, indicating partial amorphization
g-factor = 4/3, Curie temperature C = 14.17 electro- the fibers incubated with Glc-DOTA-Dy(III), and partial retention of the original polymeric
magnetic units (emu) K mol–1] to confer magnetic termed FiDy fibers, whereas raw fibers and fibers nanocrystallites (22, 23). This is supported by the
properties to the fibers. As for 6CF-Glc, we used incubated with DOTA-Dy(III) contained no detect- partial loss of preferential orientation, relative to
peptide chemistry to synthesize Glc-DOTA-Dy(III) able dysprosium. To eliminate the suspicion of raw fibers, seen in the azimuthal cuts of FiDy fibers
by reacting the free amino group of glucosamine surface contamination, we characterized the fiber (Fig. 3F, lower panel), indicating the presence of
located at C2 with DOTA-N-hydroxysuccinimide structure at different levels. Atomic force micros- Dy(III) between the chains. Azimuthal profiles
ester to form an amide bond. Afterward, Dy(III) copy (AFM) imaging revealed a distinct contrast obtained from 2D SAXS patterns (fig. S7C) showed
was coordinated inside DOTA (Fig. 3A, fig. S13 for in texture between FiDy and raw fibers. Whereas that the fibers retained a preferential orientation
the complete synthesis, and fig. S14 for dc mag- the raw fibers exhibited typical fibrillar morphol- (fig. S8, green) and preserved a fibrous nano-
netic measurements) (27). ogy (fig. S16) with a surface roughness (root mean structure in the size range of a few nanometers
The ovule development was monitored for square, RMS) of about 12 nm for a 3-by-3-mm image, with a ratio of 0.17—a value lower than that
20 days after addition of Glc-DOTA-Dy(III) to the FiDy fibers exhibited a relatively smooth sur- found for raw fibers (0.24) but higher than for
the medium under standard conditions (Fig. 3B, face (RMS roughness, 2.5 to 3.5 nm) with what FGIO fibers (0.12).

Fig. 2. Structural characterization of fibers after biological integration deconvolution of the infrared spectrum in the OH band region (3000 to
of 6CF-Glc. (A) Microscopic view of the yellow cotton fibers. (B) WAXS 3600 cm−1) for raw (E) and FGIO (F) fibers, showing the FGIO bands shifted
spectra of raw (black) and FGIO (red) fibers, showing induced structural toward higher wave numbers and the two new additional bands, reflecting
amorphization. (C) DSC of raw (black) and FGIO (red) fibers. FGIO fibers had differences between inter- and intrachain H-bond networks. (G) Force-
a lower temperature of crystallization (297°C) than raw fibers (324°C), in displacement curves of single raw (black) and FGIO (red) fibers obtained
agreement with WAXS. (D) FT-IR ATR spectra of raw (black) and FGIO (red) during tensile testing. (H) Sequence of images from single-fiber tensile
fibers, showing a structural modification. The inset shows detailed spectral testing probed with a force-puller setup and recorded in situ until fracture (vi).
differences in the range between 1100 and 1900 cm−1. (E and F) Spectral White arrows indicate the direction of the force. a.u., arbitrary units.

Natalio et al., Science 357, 1118–1122 (2017) 15 September 2017 3 of 5


EDITORIAL EXPRESSION OF CONCERN 14 September 2017. See first page.
R ES E A RC H | R E PO R T

We conducted tensile tests on single FiDy fibers of cellular stress response and not induced by red lines)—a feature typically associated with dia-
(Fig. 3G and fig. S17 for force-displacement curves Dy(III). magnetic behavior. At 2 K, we found that fibers con-
and an SEM image after fracture). As with FGIO With this in mind, we investigated the Dy(III) taining Glc-DOTA-Dy(III) had a superparamagnetic
fibers, we observed jumps in the force curves environment by means of magnetic measurements, behavior at fields –20 kOe < H < 20 kOe, reach-
during the initial phase of straining and avoided using a superconducting quantum interference ing magnetic saturation at these values. Additionally,
converting tensile strength to force per unit area. device. Figure 3H shows the temperature (T ) de- fibers containing Glc-DOTA-Dy(III) displayed a
We found an average rupture force of 9 ± 4 mN pendence of a mass magnetic susceptibility (cmass) negative slope at high magnetic fields (–60 kOe <
for FiDy fibers. Although this value is smaller plot measured at a magnetic field strength (H) of H < –20 kOe and 20 kOe < H < 60 kOe), differing
than the one found for raw fibers (16 ± 6 mN), 5 kOe. We found a strong paramagnetic behavior from that of the inorganic complex alone (Fig. 3H,
if we consider FiDy fibers’ average width of above 30 K (Fig. 3H, red) and a magnetic suscep- inset, blue), thus confirming that the Glc-DOTA-
18 ± 6 mm and average thickness of 1 ± 0.3 mm tibility product of 14.12 cm3 K mol−1 at 300 K, Dy(III) is located in a different environment, as
(fig. S10C), and if we take into account that the decreasing to 10.97 cm3 K mol−1 at 2 K (fig. S18) illustrated in Fig. 3I.
estimated cross-sectional areas are about half because of thermal depopulation of the Stark Here we demonstrate that exogenous mole-
that of the raw fibers, the rupture force should sublevels of the Dy(III) ground state (27). In cules carrying a glucose moiety and functionality
be reduced by a factor of 2 when compared with contrast, the raw fibers showed a diamagnetic such as fluorescence or magnetism can be biolog-
that for raw fibers. Unlike FGIO fibers, the pres- behavior (negative magnetic moment) through- ically incorporated into cotton cellulosic fibers by
ence of Glc-DOTA-Dy(III) and structural amor- out the full temperature range (Fig. 3H, black). using G. hirsutum in vitro cultures. The biofabri-
phization (Fig. 3F) do not seem to meaningfully We measured magnetization versus magnetic field cation of composite functional materials need not
affect the fiber’s mechanical properties. This sim- by sweeping the magnetic field between –60 and be limited to cotton but could be expanded to
ilarity could challenge the assumption that Dy(III) +60 kOe at T = 300 and 2 K (Fig. 3H, inset). At other biological systems such as bacteria, bamboo,
was incorporated into the fibers and that the 300 K, both raw and FiDy fibers displayed a neg- silk, and flax. With the appropriate molecular de-
amorphization found in WAXS is a consequence ative slope throughout the full range (black and sign, this approach offers numerous options for

Fig. 3. Biological incorpora-


tion of a magnetic Dy(III)-
based complex into cotton
fibers. (A) Structure of
the Glc-DOTA-Dy(III) complex.
(B) Sequence of microscopic
images taken at 2, 6, 15, and
20 days under “white”
illumination and standard
conditions (32°C, 5% CO2).
(C and D) Ovules at day 20.
The incorporation of Glc-
DOTA-Dy(III) does not result
in (macro)morphological
differences. (E) AFM image
from an end-clamped single
FiDy fiber, showing a
relatively smooth surface.
(F) WAXS spectra of raw
(black) and FiDy (red)
fibers, showing structural
amorphization. (G) Sequence
of images from tensile testing
of FiDy fibers, probed with
a force-puller setup and
recorded in situ until fracture
(iv). White arrows indicate
the direction of the force.
(H) Temperature versus cmass
at 5 kOe for raw (black) and
FiDy (red) fibers, showing
diamagnetic and paramagnetic
behavior below 30 K,
respectively. The inset shows
magnetization versus
magnetic field (H) at 300 K of
raw (black) and FiDy (red)
fibers that remain unchanged
throughout the temperature
range. Blue points represent
FiDy fibers at 2 K. FiDy
exhibits superparamagnetic
behavior between –20 and +20 kOe and diamagnetic behavior at 20 kOe < H < –20 kOe. (I) Schematic representation of the biological incorporation of
Glc-DOTA-Dy(III) into the cellulose fibers.

Natalio et al., Science 357, 1118–1122 (2017) 15 September 2017 4 of 5


EDITORIAL EXPRESSION OF CONCERN 14 September 2017. See first page.
R ES E A RC H | R E PO R T

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Natalio et al., Science 357, 1118–1122 (2017) 15 September 2017 5 of 5


Biological fabrication of cellulose fibers with tailored properties
Filipe Natalio, Regina Fuchs, Sidney R. Cohen, Gregory Leitus, Gerhard Fritz-Popovski, Oskar Paris, Michael Kappl and
Hans-Jürgen Butt

Science 357 (6356), 1118-1122.


DOI: 10.1126/science.aan5830

More than just a cotton shirt


Responsive or functional fabrics include coatings or secondary materials with properties such as changing color with
temperature or generating electricity with movement. The challenge is that anything added to a fabric can get washed or worn
away. Hence, Natalio et al. opted to build the functionality directly into cotton grown in vitro, through the addition of glucose
modified at the C 2 position to the culture medium. By this process, fibers can be made that naturally fluoresce or have

Downloaded from http://science.sciencemag.org/ on September 14, 2017


magnetic properties, for instance.
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