Solving the Puzzle of Shape Regulation in Plant Epidermal Pavement Cells

2021 ◽  
Vol 72 (1) ◽  
pp. 525-550
Author(s):  
Sijia Liu ◽  
François Jobert ◽  
Zahra Rahneshan ◽  
Siamsa M. Doyle ◽  
Stéphanie Robert
Keyword(s):  
Cell Wall ◽  
Cell Shape ◽  
Current Knowledge ◽  
Regulatory Proteins ◽  
Jigsaw Puzzle ◽  
Environment Protection ◽  
Cell Morphogenesis ◽  
Pavement Cell ◽  
Pavement Cells ◽  
Organ Growth

The plant epidermis serves many essential functions, including interactions with the environment, protection, mechanical strength, and regulation of tissue and organ growth. To achieve these functions, specialized epidermal cells develop into particular shapes. These include the intriguing interdigitated jigsaw puzzle shape of cotyledon and leaf pavement cells seen in many species, the precise functions of which remain rather obscure. Although pavement cell shape regulation is complex and still a long way from being fully understood, the roles of the cell wall, mechanical stresses, cytoskeleton, cytoskeletal regulatory proteins, and phytohormones are becoming clearer. Here, we provide a review of this current knowledge of pavement cell morphogenesis, generated from a wealth of experimental evidence and assisted by computational modeling approaches. We also discuss the evolution and potential functions of pavement cell interdigitation. Throughout the review, we highlight some of the thought-provoking controversies and creative theories surrounding the formation of the curious puzzle shape of these cells.

Local differentiation of cell wall matrix polysaccharides in sinuous pavement cells: its possible involvement in the flexibility of cell shape

Plant Biology ◽  
2018 ◽  
Vol 20 (2) ◽  
pp. 223-237 ◽  
Author(s):  
P. Sotiriou ◽  
E. Giannoutsou ◽  
E. Panteris ◽  
B. Galatis ◽  
P. Apostolakos
Keyword(s):  
Cell Wall ◽  
Cell Shape ◽  
Pavement Cells ◽  
Local Differentiation ◽  
Cell Wall Matrix

scholarly journals Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells

eLife ◽  
2014 ◽  
Vol 3 ◽  
Author(s):  
Arun Sampathkumar ◽  
Pawel Krupinski ◽  
Raymond Wightman ◽  
Pascale Milani ◽  
Alexandre Berquand ◽  
...  
Keyword(s):  
Cell Wall ◽  
Mechanical Stress ◽  
Cell Shape ◽  
Tissue Level ◽  
Pavement Cells ◽  
Force Microscopy ◽  
Atomic Force ◽  
Response To Stress ◽  
Maximal Tensile Stress ◽  
Open Question

Although it is a central question in biology, how cell shape controls intracellular dynamics largely remains an open question. Here, we show that the shape of Arabidopsis pavement cells creates a stress pattern that controls microtubule orientation, which then guides cell wall reinforcement. Live-imaging, combined with modeling of cell mechanics, shows that microtubules align along the maximal tensile stress direction within the cells, and atomic force microscopy demonstrates that this leads to reinforcement of the cell wall parallel to the microtubules. This feedback loop is regulated: cell-shape derived stresses could be overridden by imposed tissue level stresses, showing how competition between subcellular and supracellular cues control microtubule behavior. Furthermore, at the microtubule level, we identified an amplification mechanism in which mechanical stress promotes the microtubule response to stress by increasing severing activity. These multiscale feedbacks likely contribute to the robustness of microtubule behavior in plant epidermis.

scholarly journals Metal-Nano-Ink Coating for Monitoring and Quantification of Cotyledon Epidermal Cell Morphogenesis

2021 ◽  
Vol 12 ◽  
Author(s):  
Kotomi Kikukawa ◽  
Kazuki Yoshimura ◽  
Akira Watanabe ◽  
Takumi Higaki
Keyword(s):  
Epidermal Cell ◽  
Morphological Changes ◽  
Marker Gene ◽  
Time Lapse ◽  
Epidermal Cells ◽  
Jigsaw Puzzle ◽  
Cell Morphogenesis ◽  
Pavement Cells ◽  
Observation Area ◽  
Cell Shapes

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.

The cell shape proteins MreB and MreC control cell morphogenesis by positioning cell wall synthetic complexes

2007 ◽  
Vol 66 (1) ◽  
pp. 174-188 ◽  
Author(s):  
Arun V. Divakaruni ◽  
Cyril Baida ◽  
Courtney L. White ◽  
James W. Gober
Keyword(s):  
Cell Wall ◽  
Cell Shape ◽  
Control Cell ◽  
Cell Morphogenesis

scholarly journals Influence of heterologous MreB proteins on cell morphology of Bacillus subtilis

Microbiology ◽  
2009 ◽  
Vol 155 (11) ◽  
pp. 3611-3621 ◽  
Author(s):  
Kathrin Schirner ◽  
Jeff Errington
Keyword(s):  
Cell Wall ◽  
Bacillus Subtilis ◽  
Cell Shape ◽  
Normal Growth ◽  
Growth Conditions ◽  
Cytoskeletal Protein ◽  
Cell Morphogenesis ◽  
Gram Positive Bacteria ◽  
Related Organism ◽  
Redundant Functions

The prokaryotic cytoskeletal protein MreB is thought to govern cell shape by positioning the cell wall synthetic apparatus at growth sites in the cell. In rod-shaped bacteria it forms helical filaments that run around the periphery of the rod during elongation. Gram-positive bacteria often contain more than one mreB gene. Bacillus subtilis has three mreB-like genes, mreB, mbl and mreBH, the first two of which have been shown to be essential under normal growth conditions. Expression of an mreB homologue from the closely related organism Bacillus licheniformis did not have any effect on cell growth or morphology. In contrast, expression of mreB from the phylogenetically more distant bacterium Clostridium perfringens produced shape defects and ultimately cell death, due to disruption of the endogenous MreB cytoskeleton. However, expression of either mreBB. licheniformis (mreBBl ) or mreBC. perfringens (mreBCp ) was sufficient to confer a rod shape to B. subtilis deleted for the three mreB isologues, supporting the idea that the three proteins have largely redundant functions in cell morphogenesis. Expression of mreBCDBl could fully compensate for the loss of mreBCD in B. subtilis and led to the formation of rod-shaped cells. In contrast, expression of mreBCDCp was not sufficient to confer a rod shape to B. subtilis ΔmreBCD, indicating that a complex of these three cell shape determinants is not enough for cell morphogenesis of B. subtilis.

Review on shape formation in epidermal pavement cells of the Arabidopsis leaf

2014 ◽  
Vol 41 (9) ◽  
pp. 914 ◽  
Author(s):  
Eveline Jacques ◽  
Jean-Pierre Verbelen ◽  
Kris Vissenberg
Keyword(s):  
Arabidopsis Thaliana ◽  
Cell Wall ◽  
Leaf Development ◽  
Current Model ◽  
Pavement Cell ◽  
Pavement Cells ◽  
Regulatory Pathways ◽  
Hard Evidence ◽  
The Moment ◽  
A Current

Epidermal pavement cells appear with a fascinating irregular wavy shape in the Arabidopsis thaliana leaf. This review addresses the questions of why this particular shape is produced during leaf development and how this is accomplished. To answer the first question most probably waviness offers some biomechanical benefits over other organisations. Different positions of lobe-formation are therefore explored and discussed. At the moment, however, no hard evidence that favours any one morphology is available. The latter question comprises the biomechanical accomplishment of shape and refers to the cell wall and cytoskeletal involvement herein. A current model for pavement cell development is discussed but remaining questions and pitfalls are put forward. Moreover, an overview of the genetic and biochemical regulatory pathways that are described up to date in the literature is presented.

scholarly journals FERONIA’s sensing of cell wall pectin activates ROP GTPase signaling in Arabidopsis

2018 ◽  
Author(s):  
Wenwei Lin ◽  
Wenxin Tang ◽  
Charles T. Anderson ◽  
Zhenbiao Yang
Keyword(s):  
Cell Wall ◽  
Cell Shape ◽  
Cell Surface Receptor ◽  
Pavement Cell ◽  
Signaling Mechanism ◽  
Rop Gtpase ◽  
Surface Receptor ◽  
A Cell

ABSTRACTPlant cells need to monitor the cell wall dynamic to control the wall homeostasis required for a myriad of processes in plants, but the mechanisms underpinning cell wall sensing and signaling in regulating these processes remain largely elusive. Here, we demonstrate that receptor-like kinase FERONIA senses the cell wall pectin polymer to directly activate the ROP6 GTPase signaling pathway that regulates the formation of the cell shape in the Arabidopsis leaf epidermis. The extracellular malectin domain of FER directly interacts with de-methylesterified pectin in vivo and in vitro. Both loss-of-FER mutations and defects in the pectin biosynthesis and de-methylesterification caused changes in pavement cell shape and ROP6 signaling. FER is required for the activation of ROP6 by de-methylesterified pectin, and physically and genetically interacts with the ROP6 activator, RopGEF14. Thus, our findings elucidate a cell wall sensing and signaling mechanism that connects the cell wall to cellular morphogenesis via the cell surface receptor FER.

scholarly journals Of puzzles and pavements: a quantitative exploration of leaf epidermal cell shape

2018 ◽  
Author(s):  
Róza V. Vőfély ◽  
Joseph Gallagher ◽  
Grace D. Pisano ◽  
Madelaine Bartlett ◽  
Siobhan A. Braybrook
Keyword(s):  
Aspect Ratio ◽  
Cell Shape ◽  
Molecular Mechanisms ◽  
Vascular Plant ◽  
Plant Morphology ◽  
Pavement Cell ◽  
Pavement Cells ◽  
Stomatal Complexes ◽  
Leaf Epidermal Cell ◽  
Cell Shapes

SummaryThe epidermal cells of leaves lend themselves readily to observation and display many shapes and types: tabular pavement cells, complex trichomes, and stomatal complexes1. Pavement cells fromZea mays(maize) andArabidopsis thaliana(arabidopsis) both have highly undulate anticlinal walls and are held as representative of monocots and eudicots, respectively. In these two model species, we have a nuanced understanding of the molecular mechanisms that generate undulating pavement cell shape2–9. This model-system dominance has led to two common assumptions: first, that particular plant lineages are characterized by particular pavement cell shapes; and second, that undulatory pavement cell shapes are common enough to be model shapes. To test these assumptions, we quantified pavement cell shape in the leaves of 278 vascular plant taxa and assessed cell shape metrics across large taxonomic groups. We settled on two metrics that described cell shape diversity well in this dataset: aspect ratio (degree of cell elongation) and solidity (a proxy for margin undulation). We found that pavement cells in the monocots tended to have weakly undulating margins, pavement cells in ferns had strongly undulating margins, and pavement cells in the eudicots showed no particular degree of undulation. Indeed, we found that cells with strongly undulating margins, like those of arabidopsis and maize, were in the minority in seed plants. At the organ level, we found a trend towards cells with more undulating margins on the abaxial leaf surface vs. the adaxial surface. We also detected a correlation between cell and leaf aspect ratio: highly elongated leaves tended to have highly elongated cells (low aspect ratio), but not in the eudicots. This indicates that while plant anatomy and plant morphology can be connected, superficially similar leaves can develop through very different underlying growth dynamics (cell expansion and division patterns). This work reveals the striking diversity of pavement cell shapes across vascular plants, and lays the quantitative groundwork for testing hypotheses about pavement cell form and function.

scholarly journals Fluctuating auxin response gradients determine pavement cell-shape acquisition

2020 ◽  
Vol 117 (27) ◽  
pp. 16027-16034
Author(s):  
Peter Grones ◽  
Mateusz Majda ◽  
Siamsa M. Doyle ◽  
Daniël Van Damme ◽  
Stéphanie Robert
Keyword(s):  
Cell Shape ◽  
Auxin Response ◽  
Pavement Cell ◽  
Pavement Cells ◽  
Shape Acquisition ◽  
Subcellular Processes ◽  
Specific Localization ◽  
Shape Determination ◽  
Response Gradient

Puzzle-shaped pavement cells provide a powerful model system to investigate the cellular and subcellular processes underlying complex cell-shape determination in plants. To better understand pavement cell-shape acquisition and the role of auxin in this process, we focused on the spirals of young stomatal lineage ground cells ofArabidopsisleaf epidermis. The predictability of lobe formation in these cells allowed us to demonstrate that the auxin response gradient forms within the cells of the spiral and fluctuates based on the particular stage of lobe development. We revealed that specific localization of auxin transporters at the different membranes of these young cells changes during the course of lobe formation, suggesting that these fluctuating auxin response gradients are orchestrated via auxin transport to control lobe formation and determine pavement cell shape.

scholarly journals Real-time conversion of tissue-scale mechanical forces into an interdigitated growth pattern

2021 ◽  
Author(s):  
Samuel A. Belteton ◽  
Wenlong Li ◽  
Makoto Yanagisawa ◽  
Faezeh A. Hatam ◽  
Madeline I. Quinn ◽  
...  
Keyword(s):  
Cell Wall ◽  
Real Time ◽  
Agronomic Traits ◽  
Spatial Scales ◽  
Middle Lamella ◽  
Cell Types ◽  
Adjacent Cell ◽  
Pavement Cell ◽  
Pavement Cells ◽  
Tensile Forces

Abstract The leaf epidermis is a dynamic biomechanical shell that integrates growth across spatial scales to influence organ morphology. Pavement cells, the fundamental unit of this tissue, morph irreversibly into highly lobed cells that drive planar leaf expansion. Here we define how tissue-scale cell wall tensile forces and the microtubule-cellulose synthase systems pattern interdigitated growth in real-time. A morphologically potent subset of cortical microtubules span the periclinal and anticlinal cell faces to pattern cellulose fibers that generate a patch of anisotropic wall. The result is local polarized growth that is mechanically coupled to the adjacent cell via a pectin-rich middle lamella, and this drives lobe formation. Finite element pavement cell models revealed cell wall tensile stress as an upstream patterning element that links cell- and tissue-scale biomechanical parameters to interdigitated growth. Cell lobing in leaves is evolutionarily conserved, occurs in multiple cell types, and is associated with important agronomic traits. Our general mechanistic models of lobe formation provide a foundation to analyze the cellular basis of leaf morphology and function.

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