Differential growth of pavement cells of <i>Arabidopsis thaliana</i> leaf epidermis as revealed by microbead labeling

Elsner, J. E.; Lipowczan, Marcin; Kwiatkowska, Dorota

doi:10.1002/ajb2.1021

Cited by 34 publications

(31 citation statements)

References 33 publications

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“…6D, S5D-F) presumably restricting further widening of lobes while promoting anisotropic expansion in length of lobes. These observations and predictions are consistent with anisotropic growth patterns in pavement cells reported by Elsner et al (2018).…”

Section: Discussionsupporting

confidence: 91%

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

Bidhendi

Altartouri

Gosselin

et al. 2019

Preprint

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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 patterns de novo and may precede chemical and geometrical anisotropy.

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Section: Discussionsupporting

confidence: 91%

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

Bidhendi

Altartouri

Gosselin

et al. 2019

Preprint

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“…Upon lobe initiation, expansion at the lobe region may be isotropic, whereas expansion at the neck region is much reduced and primarily parallel to the tangent of the lobe as suggested by the displacement of fiducial markers (Armour et al, 2015). During lobe expansion, the periclinal wall in the lobe seems to undergo anisotropic expansion as reported by Elsner et al (2018), likely promoted by the transverse alignment of cellulose microfibrils at the base of the lobe perpendicular to its long axis (Sampathkumar et al, 2014;Bidhendi et al, 2019).…”

Section: Discussionmentioning

confidence: 87%

“…This arrangement of cellulose microfibrils at the neck region is thought to allow the wall to expand perpendicularly to the direction of the microfibrils and, thus, initiate waviness (Panteris and Galatis, 2005;Szymanski, 2014). At the lobe region of the periclinal wall, two configurations of cellulose microfibrils are suggested: A net-like configuration that allows isotropic expansion of the lobe region (Armour et al, 2015), and an arrangement parallel to the tangent of the lobe tip that allows anisotropic expansion toward the long axis of the lobe (Szymanski, 2014;Elsner et al, 2018). A recent study showed that treatment with cellulase alters Arabidopsis pavement cell shape, but does not prevent the generation of waviness (Higaki et al, 2017).…”

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confidence: 99%

Pectin Chemistry and Cellulose Crystallinity Govern Pavement Cell Morphogenesis in a Multi-Step Mechanism

et al. 2019

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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 (Arabidopsis thaliana) 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.

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“…The subcellular growth patterns associated with lobe initiation are not known. In lobed cells, the growth of periclinal walls is heterogeneous and anisotropic, with maximal extension usually occurring in the direction along the lobe axis (Elsner et al, 2018). The microtubule arrangement in pavement cells is also highly variable in space and time.…”

mentioning

confidence: 99%

Basic Proline-Rich Protein-Mediated Microtubules Are Essential for Lobe Growth and Flattened Cell Geometry

et al. 2019

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Complex cell shapes are generated first by breaking symmetry, and subsequent polar growth. Localized bending of anticlinal walls initiates lobe formation in the epidermal pavement cells of cotyledons and leaves, but how the microtubule cytoskeleton mediates local cell growth, and how plant pavement cells benefit from adopting jigsaw puzzle-like shapes, are poorly understood. In Arabidopsis (Arabidopsis thaliana), the basic Pro-rich protein (BPP) microtubule-associated protein family comprises seven members. We analyzed lobe morphogenesis in cotyledon pavement cells of a BPP1;BPP2;BPP5 triple knockout mutant. New image analysis methods (MtCurv and BQuant) showed that anticlinal microtubule bundles were significantly reduced and cortical microtubules that fan out radially across the periclinal wall did not enrich at the convex side of developing lobes. Despite these microtubule defects, new lobes were initiated at the same frequency as in wild-type cells, but they did not expand into well-defined protrusions. Eventually, mutant cells formed nearly polygonal shapes and adopted concentric microtubule patterns. The mutant periclinal cell wall bulged outward. The radius of the calculated inscribed circle of the pavement cells, a proposed proxy for maximal stress in the cell wall, was consistently larger in the mutant cells during cotyledon development, and correlated with an increase in cell height. These bpp mutant phenotypes provide genetic and cell biological evidence that initiation and growth of lobes are distinct morphogenetic processes, and that interdigitated cell geometry effectively suppresses large outward bulging of pavement cells.

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Differential growth of pavement cells of Arabidopsis thaliana leaf epidermis as revealed by microbead labeling

Abstract: Growth of the anticlinal and outer periclinal walls of leaf pavement cells is heterogeneous. The growth of the lobes resembles cell elongation via diffuse growth rather than tip growth.

Cited by 34 publications

References 33 publications

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

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

Pectin Chemistry and Cellulose Crystallinity Govern Pavement Cell Morphogenesis in a Multi-Step Mechanism

Basic Proline-Rich Protein-Mediated Microtubules Are Essential for Lobe Growth and Flattened Cell Geometry

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