Regulation of the mechanical properties of the cell wall is a key parameter used by plants to control the growth behavior of individual cells and tissues. Modulation of the mechanical properties ...occurs through the control of the biochemical composition and the degree and nature of interlinking between cell wall polysaccharides. Preferentially oriented cellulose microfibrils restrict cellular expansive growth, but recent evidence suggests that this may not be the trigger for anisotropic growth. Instead, non-uniform softening through the modulation of pectin chemistry may be an initial step that precedes stress-induced stiffening of the wall through cellulose. Here we briefly review the major cell wall polysaccharides and their implication for plant cell wall mechanics that need to be considered in order to study the growth behavior of the primary plant cell wall.
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BFBNIB, NMLJ, NUK, PNG, SAZU, UL, UM, UPUK
The primary plant cell wall is a dynamically regulated composite material of multiple biopolymers that forms a scaffold enclosing the plant cells. The mechanochemical make-up of this polymer network ...regulates growth, morphogenesis, and stability at the cell and tissue scales. To understand the dynamics of cell wall mechanics, and how it correlates with cellular activities, several experimental frameworks have been deployed in recent years to quantify the mechanical properties of plant cells and tissues. Here we critically review the application of biomechanical tool sets pertinent to plant cell mechanics and outline some of their findings, relevance, and limitations. We also discuss methods that are less explored but hold great potential for the field, including multiscale in silico mechanical modeling that will enable a unified understanding of the mechanical behavior across the scales. Our overview reveals significant differences between the results of different mechanical testing techniques on plant material. Specifically, indentation techniques seem to consistently report lower values compared with tensile tests. Such differences may in part be due to inherent differences among the technical approaches and consequently the wall properties that they measure, and partly due to differences between experimental conditions.
Morphogenesis of wavy epidermal pavement cells in plants has fascinated researchers for decades. A mechanical mechanism had been proposed in which the anticlinal cell walls, forming the in-plane cell ...borders, feature contiguous stiff and soft zones that generate waves upon stretching. We replicated this model as designed and also expanded on it to test its validity for three-dimensional (3D) cell geometry. Our results suggest that both the assumptions going into and the predictions arising from this hypothesis do not stand closer scrutiny and may misguide experimentalists. Unlike what the published data seem to suggest, we observed that only waves of negligible magnitude can be formed by this anticlinal stretch model and that these are virtually eliminated when full 3D geometry of the cell is considered. Further, the model produces cell wall stresses that do not match the experimental evidence.
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•Model of wavy cell morphogenesis based on in-plane tension of anticlinal wall tested in 3D•Stress predicted by the model does not match microtubule or cellulose profiles•The periclinal walls of pavement cells are crucial in cell morphogenesis•Simplifying assumptions in modeling approaches must be carefully validated
A mechanical model for plant pavement cell morphogenesis suggested that contiguous stiff and soft zones in the anticlinal walls can produce wavy cell borders upon tension. Bidhendi and Geitmann re-evaluate this model and challenge its function when considering 3D geometry and argue that its predictions are inconsistent with biological data.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
Large language models (LLMs) will benefit science by accelerating task performance. We explored whether answers generated by ChatGPT (generative pretrained transformer) to questions of biology are ...sufficiently diverse. 'Plant awareness' in ChatGPT answers was found to be highly variable, illustrating the importance of scientists being involved in validating the data and methods used to train artificial intelligence (AI) models.
Large language models (LLMs) will benefit science by accelerating task performance. We explored whether answers generated by ChatGPT (generative pretrained transformer) to questions of biology are sufficiently diverse. 'Plant awareness' in ChatGPT answers was found to be highly variable, illustrating the importance of scientists being involved in validating the data and methods used to train artificial intelligence (AI) models.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
The plant cell wall is an extracellular matrix that envelopes cells, gives them structure and shape, constitutes the interface with symbionts, and defends plants against external biotic and abiotic ...stress factors. The assembly of this matrix is regulated and mediated by the cytoskeleton. Cytoskeletal elements define where new cell wall material is added and how fibrillar macromolecules are oriented in the wall. Inversely, the cytoskeleton is also key in the perception of mechanical cues generated by structural changes in the cell wall as well as the mediation of intracellular responses. We review the delivery processes of the cell wall precursors that are required for the cell wall assembly process and the structural continuity between the inside and the outside of the cell. We provide an overview of the different morphogenetic processes for which cell wall assembly is a crucial element and elaborate on relevant feedback mechanisms.
The cytoskeleton plays an integral role in both the assembly and function of the plant cell wall. Chebli et al. review the delivery processes of the precursors required for plant cell wall assembly and the perception of mechanical cues generated by structural changes in the cell wall that mediate intracellular responses.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
Pavement cells form wavy interlocking patterns in the leaf epidermis of many plants. We use computational mechanics to simulate the morphogenetic process based on microtubule organization and cell ...wall chemistry. Based on the in silico simulations and experimental evidence, we suggest that a multistep process underlies the morphogenesis of pavement cells. The in silico model predicts alternatingly located, feedback-augmented mechanical heterogeneity of the periclinal and anticlinal walls. It suggests that the emergence of waves is created by a stiffening of the emerging indented sides, an effect that matches cellulose and de-esterified pectin patterns in the cell wall. Further, conceptual evidence for mechanical buckling of the cell walls is provided, a mechanism that has the potential to initiate wavy patterns de novo and may precede chemical and geometrical symmetry breaking.
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•Mechanical model explains shaping of wavy plant cells•A multistep mechano-chemical process is involved in pavement cell morphogenesis•Microtubules, cellulose, and de-esterified pectin are locally enriched•Cell wall buckling may precede microtubule polarization
Plant epidermal pavement cells often exhibit wavy shapes. A mechanical model by Bidhendi et al. predicts local mechanical heterogeneity to underlie wavy morphogenesis, preceded by buckling triggering microtubule polarization. A positive feedback loop involves polarized deposition of cellulose microfibrils and pectin de-esterification stiffening cell wall regions at indentation sides of waves.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
Simple plant cell morphologies, such as cylindrical shoot cells, are determined by the extensibility pattern of the primary cell wall, which is thought to be largely dominated by cellulose ...microfibrils, but the mechanism leading to more complex shapes, such as the interdigitated patterns in the epidermis of many eudicotyledon leaves, is much less well understood. Details about the manner in which cell wall polymers at the periclinal wall regulate the morphogenetic process in epidermal pavement cells and mechanistic information about the initial steps leading to the characteristic undulations in the cell borders are elusive. Here, we used genetics and recently developed cell mechanical and imaging methods to study the impact of the spatio-temporal dynamics of cellulose and homogalacturonan pectin distribution during lobe formation in the epidermal pavement cells of Arabidopsis (
) cotyledons. We show that nonuniform distribution of cellulose microfibrils and demethylated pectin coincides with spatial differences in cell wall stiffness but may intervene at different developmental stages. We also show that lobe period can be reduced when demethyl-esterification of pectins increases under conditions of reduced cellulose crystallinity. Our data suggest that lobe initiation involves a modulation of cell wall stiffness through local enrichment in demethylated pectin, whereas subsequent increase in lobe amplitude is mediated by the stress-induced deposition of aligned cellulose microfibrils. Our results reveal a key role of noncellulosic polymers in the biomechanical regulation of cell morphogenesis.
In vascular plants, the epidermal surfaces of leaves and flower petals often display cells with wavy geometries forming intricate jigsaw puzzle patterns. The prevalence and diversity of these complex ...epidermal patterns, originating from simple polyhedral progenitor cells, suggest adaptive significance. However, despite multiple efforts to explain the evolutionary drivers behind these geometrical features, compelling validation remains elusive. Employing a multidisciplinary approach that integrates microscopic and macroscopic fracture experiments with computational fracture mechanics, we demonstrate that wavy epidermal cells toughen the plants' protective skin. Through a multi-scale framework, we demonstrate that this energy-efficient patterning mechanism is universally applicable for toughening biological and synthetic materials. Our findings reveal a tunable structural-mechanical strategy employed in the microscale design of plants to protect them from deleterious surface fissures while facilitating and strategically directing beneficial ones. These findings hold implications for targeted plant breeding aimed at enhancing resilience in fluctuating environmental conditions. From an engineering perspective, our work highlights the sophisticated design principles the plant kingdom offers to inspire metamaterials.
Cell growth and organ development in plants are often correlated with the tensile behavior of the primary cell wall. To understand the mechanical behavior of plant material, various mechanical ...testing techniques have been employed, such as tensile testing of excised tissue samples. The onion (Allium cepa L.) epidermis has emerged as a model system for plant tissue mechanics. In this study, we performed tensile tests on strips of adaxial onion epidermis. While the tissue appeared stiffer in the direction along the major growth axis compared with the transverse direction, the tensile strength of tissue was not significantly different between the two orientations, indicating a nontrivial link between the cell wall and tissue mechanical anisotropy. Importantly, we observed the stress-strain behavior of the onion epidermis under tension to be highly nonlinear. Several hyperelastic models were fitted to the test data to evaluate their capacity to describe the nonlinear deformation of onion epidermis. The Yeoh hyperelastic model could successfully simulate the uniaxial tensile test data. This study suggests that accounting for nonlinearity in the deformation of the primary tissue may be essential for the accurate interpretation of mechanical test data, and a better understanding of the mechanics of the primary plant cell wall.
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BF, DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
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