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 ◽  
...  

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.

1997 ◽  
Vol 48 (2) ◽  
pp. 165 ◽  
Author(s):  
J. R. Wilson ◽  
R. D. Hatfield

Legume and grass stems decrease substantially in digestibility as they mature. This review evaluates how anatomical and chemical factors restrict digestion of cell walls in legume and grass stems. Cells that make up legume stems fall into 2 groups: cells with high (≅ 100%) digestibility (e.g. cortex and pith) and cells that appear indigestible (e.g. xylem). The digestibility of xylem cells is restricted by the highly lignified secondary walls (SW). Although cortex and pith cells may develop SW or thickened primary walls, digestibility is high because these cell types do not undergo lignification. In contrast, as grass stems mature, SW thickening and lignification occur in all main cell types. However, lignified SW in grass is readily digested when accessible to rumen microorganisms. Analysis of tissue and cell architecture in grasses strongly supports the hypothesis that observed poor digestion of lignified SW in vivo is due to limits imposed by anatomical structure. Compositional limitation to wall digestion lies in the lignified, indigestible middle lamella–primary wall. This structure confines SW digestion to inner (lumen) surfaces of cells with an open end. Low sclerenchyma SW degradation in vivo can be explained by limited movement of bacteria into sclerenchyma cells and low surface area on interior walls. For example, the ratio of surface area to total cell wall volume for sclerenchyma cells is 100-fold lower than for mesophyll cells. Apparent relationships of some wall constituents–chemical structures to wall digestibility may be the result of the increasing SW and, therefore, may simply reflect limitations imposed by anatomical structure.


IAWA Journal ◽  
2016 ◽  
Vol 37 (3) ◽  
pp. 383-401 ◽  
Author(s):  
Jong Sik Kim ◽  
Geoffrey Daniel

Although there is considerable information on anatomy and gross chemistry of oak wood, little is known on the ultrastructure and chemistry at the individual cell wall level. In particular, differences in ultrastructure and chemistry within the same cell type between earlywood (EW) and latewood (LW) are poorly understood. This study investigated the ultrastructure and chemistry of (vasicentric) tracheids, vessels, (libriform) fibers and axial/ray parenchyma cells of English oak xylem (Quercus robur L.) using light-, fluorescence- and transmission electron microscopy combined with histo/cytochemistry and immunohisto/ cytochemistry. EW tracheids showed several differences from LW tracheids including thinner cell walls, wider middle lamella cell corner (MLcc) regions and lesser amounts of mannan epitopes. Fibers showed thicker cell walls and higher amounts of mannan epitopes than tracheids. EW vessels were rich in guaiacyl (G) lignin with a characteristic non-layered cell wall organization (absence of S1–3 layers), whereas LW vessels were rich in syringyl (S) lignin with a three layered cell wall structure (S1–3 layers). Formation of a highly lignified and wide protective layer (PL) inside axial/ray parenchyma cells was detected only in EW. Distribution of mannan epitopes varied greatly between cell types and between EW and LW, whereas distribution of xylan epitopes was almost identical in all cell types within a growth ring. Together, this study demonstrates that there are great variations in ultrastructure and chemistry of cell walls within a single growth ring of English oak xylem.


2014 ◽  
Vol 41 (9) ◽  
pp. 914 ◽  
Author(s):  
Eveline Jacques ◽  
Jean-Pierre Verbelen ◽  
Kris Vissenberg

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.


2019 ◽  
Vol 21 (1) ◽  
pp. 81
Author(s):  
Eleni Giannoutsou ◽  
Basil Galatis ◽  
Panagiotis Apostolakos

The distribution of highly de-esterified homogalacturonans (HGs) in dividing protodermal cells of the monocotyledon Zea mays, the dicotyledon Vigna sinensis, and the fern Asplenium nidus was investigated in order to examine whether the cell wall region adjoining the preprophase band (PPB) is locally diversified. Application of immunofluorescence revealed that de-esterified HGs were accumulated selectively in the cell wall adjacent to the PPB in: (a) symmetrically dividing cells of stomatal rows of Z. mays, (b) the asymmetrically dividing protodermal cells of Z. mays, (c) the symmetrically dividing guard cell mother cells (GMCs) of Z. mays and V. sinensis, and (d) the symmetrically dividing protodermal cells of A. nidus. A common feature of the above cell types is that the cell division plane is defined by extrinsic cues. The presented data suggest that the PPB cortical zone-plasmalemma and the adjacent cell wall region function in a coordinated fashion in the determination/accomplishment of the cell division plane, behaving as a continuum. The de-esterified HGs, among other possible functions, might be involved in the perception and the transduction of the extrinsic cues determining cell division plane in the examined cells.


1999 ◽  
Vol 276 (2) ◽  
pp. R363-R372 ◽  
Author(s):  
Chris K. C. Wong ◽  
D. K. O. Chan

High-purity viable cells with low mitochondria (pavement cells) and mitochondria-rich content (chloride cells) were successfully isolated from the gill epithelium of Japanese eels, using three-step Percoll gradient low-speed centrifugation. Cytochemistry (silver staining for chloride, rhodamine-123, and Mitotracker for mitochondria and actin/spectrin immunofluorescence) and scanning electron microscope images were used to identify the cell types in the gill epithelium of the eel. Pavement cells were isolated at 97 and 98% purity for freshwater- and seawater-adapted eels, respectively, and chloride cells were obtained at 89 and 92% purity. The enzymatic activities of the isolated cells were determined. Na+-K+-ATPase, Mg2+-ATPase, and succinate dehydrogenase were found mainly in the chloride cell. Alkaline Ca2+-ATPase and low- and high-affinity Ca2+-ATPase were about twice as high in the chloride cell compared with the pavement cell. Transfer of eels to seawater resulted in enlargement of chloride cell sizes and significant increases in Na+-K+-ATPase, Mg2+-ATPase, and succinate dehydrogenase activities, while all Ca2+-ATPases declined by ∼60–80%. This is the first report demonstrating the successful isolation of freshwater chloride cells and also an exclusive method of getting high-purity seawater chloride cells. The isolated cells are viable and suitable for further cytological and molecular studies to elucidate the mechanisms of ionic transport.


2021 ◽  
Vol 72 (1) ◽  
pp. 525-550
Author(s):  
Sijia Liu ◽  
François Jobert ◽  
Zahra Rahneshan ◽  
Siamsa M. Doyle ◽  
Stéphanie Robert

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.


Author(s):  
S. E. Keckler ◽  
D. M. Dabbs ◽  
N. Yao ◽  
I. A. Aksay

Cellular organic structures such as wood can be used as scaffolds for the synthesis of complex structures of organic/ceramic nanocomposites. The wood cell is a fiber-reinforced resin composite of cellulose fibers in a lignin matrix. A single cell wall, containing several layers of different fiber orientations and lignin content, is separated from its neighboring wall by the middle lamella, a lignin-rich region. In order to achieve total mineralization, deposition on and in the cell wall must be achieved. Geological fossilization of wood occurs as permineralization (filling the void spaces with mineral) and petrifaction (mineralizing the cell wall as the organic component decays) through infiltration of wood with inorganics after growth. Conversely, living plants can incorporate inorganics into their cells and in some cases into the cell walls during growth. In a recent study, we mimicked geological fossilization by infiltrating inorganic precursors into wood cells in order to enhance the properties of wood. In the current work, we use electron microscopy to examine the structure of silica formed in the cell walls after infiltration of tetraethoxysilane (TEOS).


2021 ◽  
Author(s):  
Keiko U Torii

Abstract Background Stomata are adjustable pores on the surface of plant shoots for efficient gas exchange and water control. The presence of stomata is essential for plant growth and survival, and the evolution of stomata is considered as a key developmental innovation of the land plants, allowing colonization on land from aquatic environments some 450 million years ago. In the past two decades, molecular genetic studies using the model plant Arabidopsis thaliana identified key genes and signalling modules that regulate stomatal development: master-regulatory transcription factors that orchestrate cell-state transitions and peptide-receptor signal transduction pathways, which, together, enforce proper patterning of stomata within the epidermis. Studies in diverse plant species, ranging from bryophytes to angiosperm grasses, have begun to unravel the conservation and uniqueness of the core modules in stomatal development. Scope Here, I review the mechanisms of stomatal development in the context of epidermal tissue patterning. First, I introduce the core regulatory mechanisms of stomatal patterning and differentiation in the model species Arabidopsis thaliana. Subsequently, experimental evidence is presented supporting the idea that different cell types within the leaf epidermis, namely stomata, hydathodes pores, pavement cells, and trichomes, either share developmental origins or mutually influence each other’s gene regulatory circuits during development. Emphasis is taken on extrinsic and intrinsic signals regulating the balance between stomata and pavement cells, specifically by controlling the fate of Stomatal-Lineage Ground Cells (SLGCs) to remain within the stomatal-cell lineage or differentiate into pavement cells. Finally, I discuss the influence of inter-tissue-layer communication between the epidermis and underlying mesophyll/vascular tissues on stomatal differentiation. Understanding the dynamic behaviors of stomatal precursor cells and their differentiation in the broader context of tissue and organ development may help design plants tailored for optimal growth and productivity in specific agricultural applications and a changing environment.


Crop Science ◽  
2011 ◽  
Vol 51 (5) ◽  
pp. 1956-1964 ◽  
Author(s):  
Muhammet Sakiroglu ◽  
Kenneth J. Moore ◽  
E. Charles Brummer

1976 ◽  
Vol 22 (2) ◽  
pp. 403-411 ◽  
Author(s):  
M.J. Packard ◽  
S.M. Stack

Numerous vesicles were observed among the microtubules of the “preprophase” band in prophase cells from root tips of Allium cepa. The content of these vesicles looks similar to the matrix of adjacent cell walls, and these vesicles often appear to be involved in exocytosis. In addition, the cell walls perpendicular to the plane of (beneath) the preprophase band are often differentially thickened compared to the walls lying parallel to the plane of the band. Our interpretation of these observations is that the preprophase band may direct or channel vesicles containing precursors of the cell wall to localized regions of wall synthesis. The incorporation of constituents of the cell wall into a narrow region defined by the position of the preprophase band may be a mechanism that ensures unidirecitonal growth of meristematic cells.


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