scholarly journals Mechanical stress initiates and sustains the morphogenesis of wavy leaf epidermal cells

2019 ◽  
Author(s):  
Amir J Bidhendi ◽  
Bara Altartouri ◽  
Frédérick P. Gosselin ◽  
Anja Geitmann

Plant cell morphogenesis is governed by the mechanical properties of the cell wall and the resulting cell shape is intimately related to the respective specific function. Pavement cells covering the surface of plant leaves form wavy interlocking patterns in many plants. We use computational mechanics to simulate the morphogenetic process based on experimentally assessed cell shapes, growth dynamics, and cell wall chemistry. The simulations and experimental evidence suggest a multistep process underlying the morphogenesis of pavement cells during tissue differentiation. The mechanical shaping process relies on spatially confined, feedback-augmented stiffening of the cell wall in the periclinal walls, an effect that correlates with experimentally observed deposition patterns of cellulose and de-esterified pectin. We provide evidence for mechanical buckling of the pavement cell walls that can robustly initiate patternsde novoand may precede chemical and geometrical anisotropy.HighlightsA multistep mechano-chemical morphogenetic process underlies the wavy pattern of epidermal pavement cells.Microtubule polarization is preceded by an event that breaks mechanical isotropy in the cell wall.Mechanical models simulate the formation of wavy cell shapes, predict buckling of the cell walls and spatially confined variations in the mechanical properties of leaf epidermal cells.Stress/strain stiffening following the buckling of the cell walls constitutes a crucial element in a positive feedback loop forming interlocking pavement cells.Polarization of cortical microtubules, cellulose microfibrils, and de-esterified pectin occur at the necks of wavy pavement cells, matching thein silicoprediction of cell wall stiffening.

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Lucie Riglet ◽  
Frédérique Rozier ◽  
Chie Kodera ◽  
Simone Bovio ◽  
Julien Sechet ◽  
...  

Successful fertilization in angiosperms depends on the proper trajectory of pollen tubes through the pistil tissues to reach the ovules. Pollen tubes first grow within the cell wall of the papilla cells, applying pressure to the cell. Mechanical forces are known to play a major role in plant cell shape by controlling the orientation of cortical microtubules (CMTs), which in turn mediate deposition of cellulose microfibrils (CMFs). Here, by combining imaging, genetic and chemical approaches, we show that isotropic reorientation of CMTs and CMFs in aged Col-0 and katanin1-5 (ktn1-5) papilla cells is accompanied by a tendency of pollen tubes to coil around the papillae. We show that this coiled phenotype is associated with specific mechanical properties of the cell walls that provide less resistance to pollen tube growth. Our results reveal an unexpected role for KTN1 in pollen tube guidance on the stigma by ensuring mechanical anisotropy of the papilla cell wall.


2021 ◽  
Author(s):  
Wenlong Li ◽  
Sedighe Keynia ◽  
Samuel A. Belteton ◽  
Faezeh Afshar-Hatam ◽  
Daniel B. Szymanski ◽  
...  

AbstractAn integrated, experimental-computational approach is presented to analyze the variation of elastic bending behavior in the primary cell wall of living Arabidopsis thaliana pavement cells and to measure turgor pressure in the cells quantitatively under different osmotic conditions. Mechanical properties, size and geometry of cells and internal turgor pressure greatly influence their morphogenesis. Computational models of plant morphogenesis require values for wall elastic modulus and turgor pressure but very few experiments were designed to validate the results using measurements that deform the entire thickness of the cell wall. Because new wall material is deposited from inside the cell, full-thickness deformations are needed to quantify relevant changes associated with cell development. The approach here uses laser scanning confocal microscopy to measure the three-dimensional geometry of a single pavement cell, and indentation experiments equipped with high magnification objective lens to probe the local mechanical responses across the same cell wall. These experimental results are matched iteratively using a finite element model of the experiment to determine the local mechanical properties, turgor pressure, and cell height. The resulting modulus distribution along the periclinal wall is shown to be nonuniform. These results are consistent with the characteristics of plant cell walls which have a heterogeneous organization. This research and the resulting model will provide a reference for future work associated with the heterogeneity and anisotropy of mechanical properties of plant cell walls in order to understand morphogenesis of the primary cell walls during growth and to predict quantitatively the magnitudes/directions of cell wall forces.One sentence summaryThe distribution of elastic modulus of the periclinal cell walls of livingArabidopsis epidermis is nonuniform as measured by bending the entire thickness of the wall.HighlightsExperimental characterization of the spatial distribution of elastic bending behavior across the periclinal wallQuantification of the turgor pressure of the living plant epidermal cells validated with osmotic treatmentsQuantification of the effect of cell geometry on the measured mechanical responseGraphical abstract


1957 ◽  
Vol 3 (2) ◽  
pp. 171-182 ◽  
Author(s):  
S. T. Bayley ◽  
J. R. Colvin ◽  
F. P. Cooper ◽  
Cecily A. Martin-Smith

The primary walls of epidermal cells in Avena coleoptiles ranging in length from 2 to 40 mm. have been studied in the electron and polarizing microscopes and by the low-angle scattering of x-rays. The outer walls of these cells are composed of multiple layers of cellulose microfibrils oriented longitudinally; initially the number of layers is between 10 and 15 but this increases to about 25 in older tissue. Where epidermal cells touch, these multiple layers fuse gradually into a primary wall of the normal type between cells. In these radial walls, the microfibrils are oriented transversely. Possible mechanisms for the growth of the multilayered outer wall during cell elongation are discussed.


Fibers ◽  
2018 ◽  
Vol 6 (1) ◽  
pp. 6 ◽  
Author(s):  
Camille Goudenhooft ◽  
David Siniscalco ◽  
Olivier Arnould ◽  
Alain Bourmaud ◽  
Olivier Sire ◽  
...  

1966 ◽  
Vol 19 (3) ◽  
pp. 439 ◽  
Author(s):  
MC Probine ◽  
NF Barber

The internodal cells of Nitella opaca L. have been used in earlier studies to assess the part which mechanical properties of the wall may play in the control of cell growth (Probine and Preston 1962). The wall is mechanically anisotropic in both its plastic and elastic properties, and it is shown in this paper by an approximate theoretical treatment that a mat of cellulose microfibrils, embedded in a plastic matrix and having a distribution in the plane of the wall like that observed in Nitella, would lead to longitUdinal and transverse plastic extensions in the ratio observed in the growing cell. Factors which would affect cell shape are discussed.


2017 ◽  
Vol 23 (5) ◽  
pp. 1048-1054 ◽  
Author(s):  
Yunzhen Zheng ◽  
Daniel J. Cosgrove ◽  
Gang Ning

AbstractWe have used field emission scanning electron microscopy (FESEM) to study the high-resolution organization of cellulose microfibrils in onion epidermal cell walls. We frequently found that conventional “rule of thumb” conditions for imaging of biological samples did not yield high-resolution images of cellulose organization and often resulted in artifacts or distortions of cell wall structure. Here we detail our method of one-step fixation and dehydration with 100% ethanol, followed by critical point drying, ultrathin iridium (Ir) sputter coating (3 s), and FESEM imaging at a moderate accelerating voltage (10 kV) with an In-lens detector. We compare results obtained with our improved protocol with images obtained with samples processed by conventional aldehyde fixation, graded dehydration, sputter coating with Au, Au/Pd, or carbon, and low-voltage FESEM imaging. The results demonstrated that our protocol is simpler, causes little artifact, and is more suitable for high-resolution imaging of cell wall cellulose microfibrils whereas such imaging is very challenging by conventional methods.


2016 ◽  
Vol 113 (40) ◽  
pp. 11348-11353 ◽  
Author(s):  
Shundai Li ◽  
Logan Bashline ◽  
Yunzhen Zheng ◽  
Xiaoran Xin ◽  
Shixin Huang ◽  
...  

Cellulose, often touted as the most abundant biopolymer on Earth, is a critical component of the plant cell wall and is synthesized by plasma membrane-spanning cellulose synthase (CESA) enzymes, which in plants are organized into rosette-like CESA complexes (CSCs). Plants construct two types of cell walls, primary cell walls (PCWs) and secondary cell walls (SCWs), which differ in composition, structure, and purpose. Cellulose in PCWs and SCWs is chemically identical but has different physical characteristics. During PCW synthesis, multiple dispersed CSCs move along a shared linear track in opposing directions while synthesizing cellulose microfibrils with low aggregation. In contrast, during SCW synthesis, we observed swaths of densely arranged CSCs that moved in the same direction along tracks while synthesizing cellulose microfibrils that became highly aggregated. Our data support a model in which distinct spatiotemporal features of active CSCs during PCW and SCW synthesis contribute to the formation of cellulose with distinct structure and organization in PCWs and SCWs of Arabidopsis thaliana. This study provides a foundation for understanding differences in the formation, structure, and organization of cellulose in PCWs and SCWs.


2021 ◽  
Vol 118 (51) ◽  
pp. e2111723118
Author(s):  
Yin Chang ◽  
Rox Middleton ◽  
Yu Ogawa ◽  
Tom Gregory ◽  
Lisa M. Steiner ◽  
...  

Chiral asymmetry is important in a wide variety of disciplines and occurs across length scales. While several natural chiral biomolecules exist only with single handedness, they can produce complex hierarchical structures with opposite chiralities. Understanding how the handedness is transferred from molecular to the macroscopic scales is far from trivial. An intriguing example is the transfer of the handedness of helicoidal organizations of cellulose microfibrils in plant cell walls. These cellulose helicoids produce structural colors if their dimension is comparable to the wavelength of visible light. All previously reported examples of a helicoidal structure in plants are left-handed except, remarkably, in the Pollia condensata fruit; both left- and right-handed helicoidal cell walls are found in neighboring cells of the same tissue. By simultaneously studying optical and mechanical responses of cells with different handednesses, we propose that the chirality of helicoids results from differences in cell wall composition. In detail, here we showed statistical substantiation of three different observations: 1) light reflected from right-handed cells is red shifted compared to light reflected from left-handed cells, 2) right-handed cells occur more rarely than left-handed ones, and 3) right-handed cells are located mainly in regions corresponding to interlocular divisions. Finally, 4) right-handed cells have an average lower elastic modulus compared to left-handed cells of the same color. Our findings, combined with mechanical simulation, suggest that the different chiralities of helicoids in the cell wall may result from different chemical composition, which strengthens previous hypotheses that hemicellulose might mediate the rotations of cellulose microfibrils.


2021 ◽  
Vol 12 ◽  
Author(s):  
Kotomi Kikukawa ◽  
Kazuki Yoshimura ◽  
Akira Watanabe ◽  
Takumi Higaki

During cotyledon growth, the pavement cells, which make up most of the epidermal layer, undergo dynamic morphological changes from simple to jigsaw puzzle-like shapes in most dicotyledonous plants. Morphological analysis of cell shapes generally involves the segmentation of cells from input images followed by the extraction of shape descriptors that can be used to assess cell shape. Traditionally, replica and fluorescent labeling methods have been used for time-lapse observation of cotyledon epidermal cell morphogenesis, but these methods require expensive microscopes and can be technically demanding. Here, we propose a silver-nano-ink coating method for time-lapse imaging and quantification of morphological changes in the epidermal cells of growing Arabidopsis thaliana cotyledons. To obtain high-resolution and wide-area cotyledon surface images, we placed the seedlings on a biaxial goniometer and adjusted the cotyledons, which were coated by dropping silver ink onto them, to be as horizontal to the focal plane as possible. The omnifocal images that had the most epidermal cell shapes in the observation area were taken at multiple points to cover the whole surface area of the cotyledon. The multi-point omnifocal images were automatically stitched, and the epidermal cells were automatically and accurately segmented by machine learning. Quantification of cell morphological features based on the segmented images demonstrated that the proposed method could quantitatively evaluate jigsaw puzzle-shaped cell growth and morphogenesis. The method was successfully applied to phenotyping of the bpp125 triple mutant, which has defective pavement cell morphogenesis. The proposed method will be useful for time-lapse non-destructive phenotyping of plant surface structures and is easier to use than the conversional methods that require fluorescent dye labeling or transformation with marker gene constructs and expensive microscopes such as the confocal laser microscope.


HortScience ◽  
1991 ◽  
Vol 26 (6) ◽  
pp. 762B-762
Author(s):  
Martin C. Goffinet ◽  
Roger C. Pearson

Clusters of Vitis labruscana cv. Concord were grown either in full sun or canopy shade, and either not sprayed or sprayed with 3.4 Kg/Ha chlorothalonil every 2 wk from pre-bloom to veraison. Only sun-exposed, sprayed fruit produced skin russeting. Clusters of the very susceptible V. vinifera cv. Rosette were grown in direct sun, sprayed with chlorothalonil 4 times from bloom to veraison, in the presence or absence of purported anti-russeting agents. Heavy russet occurred in all treatments. Russet initiation was similar in the 2 cvs.: epidermal cells first died beneath spray residue in full sun, a phellogen then arose in the hypodermis, followed by periderm. Epidermal death began in `Rosette' within a wk of the bloom spray, but in `Concord' only after 2-3 wk post bloom and 3 sprays. `Concord' russet generally appeared as patches or scabs, whereas `Rosette' russet ranged from freckles, welts, scabs to large smooth burnished areas. In both cvs., unbroken russet consisted of uniform layers of phellum. New, deeper periderm initials arose beneath checks and cracks which formed as fruit enlarged. In `Concord', but not `Rosette', the daughter cells of each such initial were often enclosed in the original cell wall. In all cases of russet, cell walls in the periderm were suberized and sometimes lignified. Cells also contained much phenolic material.


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