Plant Cell Wall-Like Soft Materials: Micro- and Nanoengineering, Properties, and Applications

Abstract

Plant cell wall (CW)-like soft materials, referred to as artificial CWs, are composites of assembled polymers containing micro-/nanoparticles or fibers/fibrils that are designed to mimic the composition, structure, and mechanics of plant CWs. CW-like materials have recently emerged to test hypotheses pertaining to the intricate structure-property relationships of native plant CWs or to fabricate functional materials. Here, research on plant CWs and CW-like materials is reviewed by distilling key studies on biomimetic composites primarily composed of plant polysaccharides, including cellulose, pectin, and hemicellulose, as well as organic polymers like lignin. Micro- and nanofabrication of plant CW-like composites, characterization techniques, and in silico studies are reviewed, with a brief overview of current and potential applications. Micro-/nanofabrication approaches include bacterial growth and impregnation, layer-by-layer assembly, film casting, 3-dimensional templating microcapsules, and particle coating. Various characterization techniques are necessary for the comprehensive mechanical, chemical, morphological, and structural analyses of plant CWs and CW-like materials. CW-like materials demonstrate versatility in real-life applications, including biomass conversion, pulp and paper, food science, construction, catalysis, and reaction engineering. This review seeks to facilitate the rational design and thorough characterization of plant CW-mimetic materials, with the goal of advancing the development of innovative soft materials and elucidating the complex structure-property relationships inherent in native CWs.

Keywords: Acellular wall; Biomimicry; Composites; Living materials; Soft matter; Synthetic plants.

Fig. 1

CW architecture and composition. a A cut-out schematic of a wood CW shows its layered structure, featuring a network-like arrangement in the PCW and aligned fibrils in the SCW. b The composition of wood CW in each layer after lignification. The light blue region shows the content of other compounds in the layers. c PCW schematic based on a molecular model, showing a load-bearing network of CMF in a matrix of pectin and xyloglucan. d A schematic of the SCW based on a molecular model, illustrating lignin deposits within an oriented cellulose matrix. The CMF are bound by xylan hemicelluloses, with limited interactions between cellulose and lignin. The PCW and SCW schemes were inspired by [29] and [37], respectively

Fig. 2

Fabrication of plant CW-like materials via bacterial cellulose pellicle growth and impregnation or LbL assembly techniques. a A culture of cellulose-synthesizing bacteria, assembling cellulose within a growth medium, containing CW polysaccharides and other biopolymers. b Deep-etch freeze-fracture TEM micrographs of bacterial cellulose, showing differences in the arrangement of CMF with or without xyloglucan. Scale bars are 5 µm. Adapted (cropped and labeled) with permission [46]. Copyright Wiley, 1995. c Effect of expansin on the extension of hemicellulose-cellulose composites, showing a significant increase in displacement under a constant load for cellulose-xyloglucan composites with the addition of expansin. Adapted with permission. Copyright Wiley, 2000 [39]. d Schematic of the LbL assembly method, showing the formation of alternating cellulose fibril and xyloglucan layers on a primer-coated substrate. e The thickness of CNC-xyloglucan films, formed via spin coating, as a function of deposited layer number demonstrates the linear growth of layers when the xyloglucan concentration is 0.5 or 1 g mL⁻¹. Adapted with permission [62]. Copyright American Chemical Society, 2010. f AFM topographical images show the non-uniformity of pectin and extensin layers in a pectin-extensin composite material, attributed to the imbalanced charge density between the components. Adapted with permission [65]. Copyright American Chemical Society, 2010

Fig. 3

Fabrication of plant CW-like materials via film casting and 3D templating techniques. a Schematic of the film casting technique for constructing a plant CW-like film by combining CW polysaccharides, followed by solvent removal through either evaporation, crosslinking, or filtration. b Nano-indentation modulus of in situ lignified cast films, showing that an increase in lignin content and a decrease in cellulose content reduced stiffness. Adapted under terms of the CC-BY license [69]. Copyright 2017, The Authors, published by Springer Nature. c Tensile stress–strain of cast films, containing c-CLPs, showing an initial increase in both strength and elongation at break by increasing the lignin content (e.g., tensile strength at break increases from 132 to 160 MPa as c-CLPs increased from 0 to 10%), followed by a rapid decrease for films containing 20% and 50% c-CLPs [74]. Values next to c-CLP on the curves indicate the lignin content (wt%) of films. H bonding stands for hydrogen bonding. Adapted under terms of the CC-BY license [74]. Copyright 2019, The Authors, published by American Chemical Society. d LbL assembly of CW-mimetic microcapsules using liquid- or solid-based 3D templating and particle coating techniques, resulting in hollow microcapsules when the core was removed. e SEM images of microcapsules composed of CNC, isolated from bacteria or algae with varying AR, showing differences in the morphology of droplets and inter-droplet bridging. Core spheres are polystyrene particles, representing the oil droplets. Adapted with permission [85]. Copyright Royal Society of Chemistry, 2013. f Plantosomes prepared using liposome templating mimicked the mechanism of turgor pressure in native plant cells by undergoing reversible deformations and the formation of microtubular protrusions when the pH was increased from 8 to 8.6. Adapted under terms of the CC-BY license [87]. Copyright 2020, The Authors, published by Springer Nature

Fig. 4

In silico studies of plant CWs using MD simulations. a Top and side views of a four-lamella CW after equilibration (Scale bars are 200 nm) along with their corresponding close-ups (Scale bars are 25 nm). Reproduced with permission [29]. Copyright Science, 2021. b Stress–strain behavior of PCW, consisting of CMF, xyloglucan, and pectin, showing that the stress is mainly tolerated by CMF. Reproduced with permission [29]. Copyright Science, 2021. c Normalized average end-to-end length of CMF (L_E/L_E0, where L_E is the average end-to-end length and L_E0 is its initial value at strain of 0%) as a function of strain, applied via the uniaxial stretching of single lamellae at varying CMF orientations of 0°, 30°, 45°, 60°, or 90°. Reproduced with permission [29]. Copyright Science, 2021. d Stress–strain response of onion epidermal CW during cyclic loading and unloading, showing a large hysteresis, stemming from energy dissipation and irreversible (plastic) deformation in the epidermal wall. Reproduced with permission [29]. Copyright Science, 2021. e Molecular model of wood CW, encompassing CNC, hemicellulose, and lignin molecules, assembled in a layered nanocomposite. M1 and M2 indicate the molecular orientation of CW matrix during yielding and sliding, respectively. Reproduced with permission [91]. Copyright Elsevier, 2015. f Stress–strain response in the CW model (blue), indicating 3 separate regimes: an initial elastic regime and two plastic regimes. The unloading (red) and reloading (green) curves indicate the irreversible deformation of CW after yielding. Reproduced with permission [91]. Copyright Elsevier, 2015

Fig. 5

Varying techniques for mechanical, morphological, structural and chemical characterizations of natural and artificial plant CWs. Abbreviations are defined as follows: AFM (atomic force microscopy), SEM (scanning electron microscopy), TEM (transmission electron microscopy), SAXS (small angle X-ray scattering), WAXS (wide angle X-ray scattering), SANS (small angle neutron scattering), QCM (quartz crystal microbalance), QCM-D (quartz crystal microbalance with dissipation monitoring), FTIR (Fourier transform infrared), NMR (nuclear magnetic resonance), and SFG (sum frequency generation). Some abbreviations have been redefined here as per the request of a reviewer

Fig. 6

Morphological and structural characterizations of plant CW-like materials. a AFM height images of xyloglucan chains and xyloglucan assemblies. Reproduced under terms of the CC-BY license [95]. Copyright 2015, The Authors, published by Springer Nature. b AFM images of bacterial cellulose, bacterial cellulose-pectin, and bacterial cellulose-pectin-xyloglucan composites. Adapted under terms of the CC-BY license [96] Copyright 2010, The Authors, published by Institute of Agrophysics. c SEM images of physically and chemically crosslinked composites, consisting of cellulose/glucomannan/lignin, showing the extensive aggregation of lignin particles in physically crosslinked composites compared with the chemical analog. Reproduced with permission [73]. Copyright Elsevier, 2022. d QCM-based frequency changes (Δf) versus deposited pectin (Pect) and extensin (Ext) layer number. Reproduced with permission [65]. Copyright Langmuir, 2010. e QCM-D-derived normalized frequency shift (Δf/n) of hemicelluloses, including xyloglucan (XG), galactoglucomannan (GGM), and water-soluble xylan (WXY), initially deposited on bacterial cellulose films, showing the effect of HRP adsorption on polysaccharides over time. Reproduced with permission [54]. Copyright Springer Nature, 2021. f QCM-D-derived dissipation shift (ΔD) versus Δf/n of hemicellulose adsorption to CNF. Reproduced with permission [54]. Copyright Springer Nature, 2021. g QCM-derived Δf for xyloglucan adsorption to CNC-spin-coated quartz crystals versus time. Reproduced with permission [62]. Copyright Langmuir, 2010. h The 2D SAXS pattern of water-swollen horizontally-oriented individual single flax fiber. Reproduced with permission [106]. Copyright American Chemical Society, 1998. i Azimuthal integration of X-ray diffractograms in wet-spun filaments, obtained at a scattering vector of 15.8 nm⁻¹. Reproduced under terms of the CC-BY license [112]. Copyright 2016, The Authors, published by Springer Nature. j A representative core–shell model, proposed for the structure of hydrated bacterial cellulose-xyloglucan composites. Reproduced with permission [119]. Copyright Royal Society of Chemistry, 2016

Fig. 7

Mechanical characterizations of plant CW-like materials. a Uniaxial creep test setup to measure the time-dependent displacement of viscoelastic CW-like materials at a constant tension. Adapted with permission [121]. Copyright Springer Nature, 1989. b A customized and unique biaxial tensile testing setup was used to apply pressure to films and hydrogels from one side while measuring the corresponding deflections, providing insights into their mechanical responses. Adapted with permission [51]. Copyright Springer Nature, 2002. c Topological image and indentation modulus of poplar fiber CW layers, obtained using AFM, which show three distinct regions, ML/PCW, S1 layer, and S2 layer. Cell corner is denoted as cc. Reproduced under terms of the CC-BY license [69]. Copyright 2017, The Authors, published by Springer Nature

Fig. 8

Chemical characterizations of plant CWs and CW-like materials. a A representative 2D ¹³C NMR spectrum of maize lignin (represented by S, G, H, and FA labels) and cellulose (i: interior, s: surface), showing cross-peaks that represent interactions between the components. S, G, H, and FA are maize lignin residues. Xn1-4 (2f, 3f), OMe, and cellu. stand for C1-C4 of xylan (twofold and threefold conformations, respectively), lignin methoxy group, and cellulose, respectively. The spectrum provides information on the quantity of cross-peaks between lignin and polysaccharides or lignin and xylan. Reproduced under terms of the CC-BY license [37]. Copyright 2019, The Authors, published by Springer Nature. b FTIR spectrum of CNC-polyethyleneimine microcapsules, showing the peak associated with vibrational OH stretching at 3342 cm⁻¹, which typically appears at 3500 cm⁻¹. Reproduced with permission [140]. Copyright American Chemical Society, 2015. FTIR microspectroscopy spectra of c initial, d stressed, or e relaxed plant cells, including parallel (positive, solid line) and perpendicular (positive, dashed line) polarization and subtraction (mainly negative, solid line) spectra. Reproduced with permission [143]. Copyright Oxford University Press, 2000. f Nano-FTIR spectra of SCW and ML of poplar fibers along with Nano-FTIR absorbance versus location of AFM tip for wavenumbers pertaining to polysaccharides (1162 cm⁻¹) and lignin (1269 cm⁻¹). Absorbance normalization was conducted via standard normal variate (SNV) transformation method: [(absorbance – average absorbance from all wavenumbers) / absorbance standard deviation]). Reproduced with permission [124]. Copyright American Chemical Society, 2022. g SFG spectrum of randomly-packed (red) and uniaxially-aligned (black) cellulose Iβ crystals with corresponding AFM images (i) and (ii), respectively. Reproduced with permission [148]. Copyright Royal Society of Chemistry, 2014. h SFG spectra of the SCW of several land plants, including flax, ramie, cotton, Brachypodium, poplar, Arabidopsis, pine, maize, and switchgrass. Reproduced with permission [148]. Copyright Royal Society of Chemistry, 2014. i SFG spectra of biological tissues, including algal CWs (Glaucocystis, Oocystis, Valonia, and Cladophora), cellulose biofilm produced from G. xylinus, Halocynthia mantle, onion epidermis, and Arabadopsis aerial tissue [148], showing that the relative intensity of the hydroxyl to alkyl signals was significantly greater for these PCWs (as shown in panel i) compared with most SCWs (panel h). The higher intensity suggested that PCWs had a lower degree of antiparallel CMF orientation over the SFG coherence length scale. Reproduced with permission [148]. Copyright Royal Society of Chemistry, 2014