Integrating cell biology, image analysis, and computational mechanical modeling to analyze the contributions of cellulose and xyloglucan to stomatal function

Rui, Yue; Yi, Hojae; Kandemir, Baris; Wang, James; Puri, Virendra M.; Anderson, Charles T.

doi:10.1080/15592324.2016.1183086

Cited by 11 publications

(13 citation statements)

References 26 publications

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“…However, we observed significant asymmetry in many of the imaging-based FEMs we constructed, both at the subcellular scale, as evidenced by surface “bumpiness,” and at the cellular scale, with guard cells bulging slightly on the opposite ends as their sister cells (Figure 8 , Supplemental Figure 2 ). These observations call into question the assumption that stomatal complexes are perfectly symmetrical, both longitudinally and transversely, when developing analytical and numerical models to represent stomatal dynamics (Cooke et al, 1976 ; Rui et al, 2016 ; Marom et al, 2017 ; Woolfenden et al, 2017 ).…”

Section: Discussionmentioning

confidence: 99%

Mechanical Effects of Cellulose, Xyloglucan, and Pectins on Stomatal Guard Cells of Arabidopsis thaliana

Rui

Kandemir

et al. 2018

Front. Plant Sci.

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Stomata function as osmotically tunable pores that facilitate gas exchange at the surface of plants. Stomatal opening and closure are regulated by turgor changes in guard cells that result in mechanically regulated deformations of guard cell walls. However, how the molecular, architectural, and mechanical heterogeneities that exist in guard cell walls affect stomatal dynamics is unclear. In this work, stomata of wild type Arabidopsis thaliana plants or of mutants lacking normal cellulose, hemicellulose, or pectins were experimentally induced to close or open. Three-dimensional images of these stomatal complexes were collected using confocal microscopy, images were landmarked, and three-dimensional finite element models (FEMs) were constructed for each complex. Stomatal opening was simulated with a 5 MPa turgor increase. By comparing experimentally measured and computationally modeled changes in stomatal geometry across genotypes, anisotropic mechanical properties of guard cell walls were determined and mapped to cell wall components. Deficiencies in cellulose or hemicellulose were both predicted to stiffen guard cell walls, but differentially affected stomatal pore area and the degree of stomatal opening. Additionally, reducing pectin molecular mass altered the anisotropy of calculated shear moduli in guard cell walls and enhanced stomatal opening. Based on the unique architecture of guard cell walls and our modeled changes in their mechanical properties in cell wall mutants, we discuss how each polysaccharide class contributes to wall architecture and mechanics in guard cells. This study provides new insights into how the walls of guard cells are constructed to meet the mechanical requirements of stomatal dynamics.

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Section: Discussionmentioning

confidence: 99%

Mechanical Effects of Cellulose, Xyloglucan, and Pectins on Stomatal Guard Cells of Arabidopsis thaliana

Rui

Kandemir

et al. 2018

Front. Plant Sci.

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“…Then, we employ mechanical models for biological materials (Bar-On and Wagner, 2013 ) to correlate these parameters with the bio-composite, and, thereby, present an analytical explanation of the role of each bio-composite phase (cellulose microfibrils and matrix material) on the stomatal aperture and opening area. These analytical relations quantitatively illuminate the effect of the structure and composition of on stomatal opening, and they complete the extensive recent studies in the field (Jones et al, 2003 , 2005 ; Rui and Anderson, 2016 ; Rui et al, 2016 ; Carter et al, 2017 ; Woolfenden et al, 2017 ).…”

Section: Introductionmentioning

confidence: 52%

“…In addition, stomatal functionality, i.e., the effects of water pressure on stomatal opening characteristics such as the aperture and the pore opening, have also been extensively studied (Franks et al, 1998 , 2001 ; Franks, 2003 ; Franks and Farquhar, 2007 ). In parallel with these experimental investigations, mechanical models that attempted to correlate between the stomatal architecture and its deformation were developed both by analytical means (Aylor et al, 1973 ; DeMichele and Sharpe, 1973 ; Sharpe and Wu, 1978 ; Wu and Sharpe, 1979 ; Wu et al, 1985 ) and by numerical simulations (e.g., Finite-Element, FE) (Cooke et al, 1976 , 1977 ; Rui et al, 2016 ; Carter et al, 2017 ; Woolfenden et al, 2017 ). Despite the scientific consensus that guard cells possess high structural-mechanical anisotropy (that is crucial for stomatal functionality), some of these modeling approaches were based on the inappropriate assumption of mechanical isotropy.…”

Section: Introductionmentioning

confidence: 99%

“…Later studies abandoned the numerical approach for almost four decades, until it was recently revisited in a series of experimentally based FE simulations, which aimed to isolate the key structural, compositional, and mechanical parameters of the guard cell that govern stomatal opening. Recently, Rui et al (Rui and Anderson, 2016 ; Rui et al, 2016 ) used mutants to analyze the effect of variations in cellulose and in the inter-cellulose xylogucan on stomatal opening; these effects were implemented in their FE models via effective changes in the mechanical anisotropy of the guard cell wall. They found that the loss of xyloglucan, which effectively increase the mechanical stiffness anisotropy, facilitates stomatal opening, while cellulose deficiency, which effectively reduces the mechanical anisotropy, has a complementary effect and reduces stomatal opening.…”

Section: Introductionmentioning

confidence: 99%

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Stomatal Opening: The Role of Cell-Wall Mechanical Anisotropy and Its Analytical Relations to the Bio-composite Characteristics

2017

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Stomata are pores on the leaf surface, which are formed by a pair of curved, tubular guard cells; an increase in turgor pressure deforms the guard cells, resulting in the opening of the stomata. Recent studies employed numerical simulations, based on experimental data, to analyze the effects of various structural, chemical, and mechanical features of the guard cells on the stomatal opening characteristics; these studies all support the well-known qualitative observation that the mechanical anisotropy of the guard cells plays a critical role in stomatal opening. Here, we propose a computationally based analytical model that quantitatively establishes the relations between the degree of anisotropy of the guard cell, the bio-composite constituents of the cell wall, and the aperture and area of stomatal opening. The model introduces two non-dimensional key parameters that dominate the guard cell deformations—the inflation driving force and the anisotropy ratio—and it serves as a generic framework that is not limited to specific plant species. The modeling predictions are in line with a wide range of previous experimental studies, and its analytical formulation sheds new light on the relations between the structure, mechanics, and function of stomata. Moreover, the model provides an analytical tool to back-calculate the elastic characteristics of the matrix that composes the guard cell walls, which, to the best of our knowledge, cannot be probed by direct nano-mechanical experiments; indeed, the estimations of our model are in good agreement with recently published results of independent numerical optimization schemes. The emerging insights from the stomatal structure-mechanics “design guidelines” may promote the development of miniature, yet complex, multiscale composite actuation mechanisms for future engineering platforms.

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“…Recent biomechanical modelling has focussed on the geometry and material properties of cell walls (Rui et al, 2016(Rui et al, , 2018Shtein et al, 2017;Woolfenden et al, 2017;Carter et al, 2017;Marom et al, 2017;Yi et al, 2018) and confirmed old ideas on the importance of anisotropic wall properties and in particular circumferentially aligned cellulose microfibrils. To determine the key biomechanical ingredients for stomatal movement, (Woolfenden et al, 2017;Marom et al, 2017) used simplified models with idealised geometries.…”

Section: Force-velocity Trade-offs and Snap-bucklingmentioning

confidence: 83%

How water flow, geometry, and material properties drive plant movements

Morris

Blyth

2019

Journal of Experimental Botany

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Plants are dynamic. They adjust their shape for feeding, defence, and reproduction. Such plant movements are critical for their survival. We present selected examples covering a range of movements from single cell to tissue level and over a range of time scales. We focus on reversible turgor-driven shape changes. Recent insights into the mechanisms of stomata, bladderwort, the waterwheel, and the Venus flytrap are presented. The underlying physical principles (turgor, osmosis, membrane permeability, wall stress, snap buckling, and elastic instability) are highlighted, and advances in our understanding of these processes are summarized.

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Integrating cell biology, image analysis, and computational mechanical modeling to analyze the contributions of cellulose and xyloglucan to stomatal function

Cited by 11 publications

References 26 publications

Mechanical Effects of Cellulose, Xyloglucan, and Pectins on Stomatal Guard Cells of Arabidopsis thaliana

Mechanical Effects of Cellulose, Xyloglucan, and Pectins on Stomatal Guard Cells of Arabidopsis thaliana

Stomatal Opening: The Role of Cell-Wall Mechanical Anisotropy and Its Analytical Relations to the Bio-composite Characteristics

How water flow, geometry, and material properties drive plant movements

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