scholarly journals Pavement cells and the topology puzzle

2017 ◽  
Author(s):  
Ross Carter ◽  
Yara E. Sánchez-Corrales ◽  
Verônica A. Grieneisen ◽  
Athanasius F. M. Marée

AbstractD’Arcy Thompson emphasised the importance of surface tension as a potential driving force in establishing cell shape and topology within tissues. Leaf epidermal pavement cells grow into jigsaw-piece shapes, highly deviating from such classical forms. We investigate the topology of developing Arabidopsis leaves composed solely of pavement cells. Image analysis of around 50,000 cells reveals a clear and unique topological signature, deviating from previously studied epidermal tissues. This topological distribution is however established early during leaf development, already before the typical pavement cell shapes emerge, with topological homestasis maintained throughout growth and unaltered between division and maturation zones. Simulating graph models, we identify a heuristic cellular division rule that reproduces the observed topology. Our parsimonious model predicts how and when cells effectively place their division plane with respect to their neighbours. We verify the predicted dynamics through in vivo tracking of 800 mitotic events, and conclude that the distinct topology is not a direct consequence of the jigsaw-like shape of the cells, but rather owes itself to a strongly life-history-driven process, with limited impact from cell surface mechanics.Summary statementDevelopment of the Arabidopsis leaf epidermis topology is driven by deceptively simple rules of cell division, independent of surface tension, cell size and, often complex, cell shape.

2018 ◽  
Author(s):  
Róza V. Vőfély ◽  
Joseph Gallagher ◽  
Grace D. Pisano ◽  
Madelaine Bartlett ◽  
Siobhan A. Braybrook

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.


2020 ◽  
Author(s):  
Steve Runser ◽  
Lisa Conrad ◽  
Harold Gómez ◽  
Christine Lang ◽  
Mathilde Dumond ◽  
...  

ABSTRACTDuring lung development, epithelial branches expand preferentially in longitudinal direction. This bias in outgrowth has been linked to a bias in cell shape and in the cell division plane. How such bias arises is unknown. Here, we show that biased epithelial outgrowth occurs independent of the surrounding mesenchyme. Biased outgrowth is also not the consequence of a growth factor gradient, as biased outgrowth is obtained with uniform growth factor cultures, and in the presence of the FGFR inhibitor SU5402. Furthermore, we note that epithelial tubes are largely closed during early lung and kidney development. By simulating the reported fluid flow inside segmented narrow epithelial tubes, we show that the shear stress levels on the apical surface are sufficient to explain the reported bias in cell shape and outgrowth. We use a cell-based vertex model to confirm that apical shear forces, unlike constricting forces, can give rise to both the observed bias in cell shapes and tube elongation. We conclude that shear stress may be a more general driver of biased tube elongation beyond its established role in angiogenesis.


Development ◽  
1978 ◽  
Vol 47 (1) ◽  
pp. 1-15
Author(s):  
K. F. Heintzelman ◽  
H. M. Phillips ◽  
G. S. Davis

Emerging chick limb-buds at first grow only in length, not width. The growth parameters of limb mesoderm — cell shapes, distributions, division patterns and cleavage orientations — are incompatible with representations of this tissue as an elongating solid composed of proliferating but immobile cells. We observe that samples of both early limb mesoderm and also surrounding flank mesoderm round up like liquid droplets in organ culture. Therefore, liquid-like tissue rearrangments, including cell shuffling movements and neighbor exchanges, may occur in limb and flank mesoderm during in vivo limb budding. If so, differences in limb-flank surface tension properties would have to be present to keep these two fluid cell populations segregated into distinct tissues and properly positioned underneath limb and flank ectoderm. Previous studies have shown that tissue surface tensions are reflected in the spreading behavior of fused pairs of cell aggregates. To determine whether or not they possess differing surface tension properties, we pair excised pieces of early leg-bud, wing-bud or intervening flank mesoderm with pieces of 5¾-day heart or liver in hanging drop cultures. For more rapid determinations of relative liquid-tissue cohesiveness than can be obtained in conventional, long-term experiments, aggregate pairs are fixed shortly after fusion. Since partial-envelopment configurations depend upon relative aggregate sizes as well as their tissue surface tensions, new procedures are used to deduce relative aggregate cohesiveness from cross-sections of these briefly fused aggregate pairs. The envelopment tendencies of aggregates fixed 6–9 h after fusion are similar to those fixed 15–19 h after fusion: heart tends to surround leg; heart and wing surround each other with similar frequencies, but flank tends to surround heart. Also, liver tends to surround leg and wing, but flank tends to surround liver. When the effects of relative aggregate size are taken into account, these non-random, tissue-specific patterns of aggregate envelopment indicate that the relative cohesiveness of these tissues falls into the sequence: leg > heart ∼ wing > liver > flank. The in vitro behavior of early limb-bud and neighboring flank mesoderm in these studies suggests that they are not simply mechanically identical portions of a single liquid tissue. We have previously proposed that early limb-bud mesoderm may act like a non-dispersing, cohesive liquid droplet which is embedded within a less cohesive fluid layer of flank tissue (and which is molded distally into paddle-shaped conformations by solid-like limb ectoderm and/or subjacent extracellular matrix). This proposal is not only compatible with the growth parameters of limb-bud mesoderm in vivo, but is also consistent with our observation that flank mesoderm surrounds tissues which surround limb mesoderm in these aggregate-fusion-experiments. Our model suggests that differences in the surface tension properties of limb vs. flank mesoderm may combine with differential cell proliferation, and possibly with active limb ectoderm expansion, to generate initial proximodistal limb outgrowth.


2017 ◽  
Author(s):  
Yara E. Sánchez-Corrales ◽  
Matthew Hartley ◽  
Jop van Rooij ◽  
Athanasius F. M. Marée ◽  
Verônica A. Grieneisen

AbstractQuantifying cell morphology is fundamental to the statistical study of cell populations, and can help us unravel mechanisms underlying cell and tissue morphogenesis. Current methods, however, require extensive human intervention, are highly sensitive to parameter choice, or produce metrics that are difficult to interpret biologically. We therefore developed a novel method, Lobe Contribution Elliptical Fourier Analysis (LOCO-EFA), which generates from digitalised cell outlines meaningful descriptors that can be directly matched to morphological features. We show that LOCO-EFA provides a tool to phenotype efficiently and objectively populations of cells by applying it to the complex shaped pavement cells of Arabidopsis thaliana wild type and speechless leaves. To further validate our method, we analysed computer-generated tissues, where cell shape can be specified in a controlled manner. LOCO-EFA quantifies deviations between the specified shape that an individual in silico cell takes up when in isolation and the resultant shape when they are allowed to interact within a confluent tissue, thereby assessing the role of cell-cell interactions on population cell shape distributions.Summary statementNovel method (LOCO-EFA) quantifies complex cell shapes, extracting meaningful biological features such as protrusion number and amplitude; here shown for plant pavement cells and validated on in silico tissues.


Development ◽  
1991 ◽  
Vol 111 (1) ◽  
pp. 23-33 ◽  
Author(s):  
M.L. Condic ◽  
D. Fristrom ◽  
J.W. Fristrom

Imaginal discs of Drosophila are simple epithelial tissues that undergo dramatic changes in shape during metamorphosis, including elongation to form adult appendages such as legs and wings. We have examined the cellular basis of leg disc morphogenesis by staining filamentous actin to outline cell boundaries in discs and observing cell shapes with scanning confocal laser microscopy (SCLM). Surprisingly, we found that prior to the onset of morphogenesis, cells in the dorsal-lateral regions of leg discs are compressed in the proximal-distal axis and greatly elongated circumferentially. These cells are also asymmetric in the apical-basal axis, being more elongated in the apical-most region of the cell than they are subapically, and frequently contacting different sets of neighbors apically and basally. Elongated cells were first observed in early third instar discs, and persisted through several rounds of cell division as the discs matured. During appendage elongation in vivo and trypsin-accelerated elongation in vitro, these highly asymmetric cells became isometric. As the apical cell profiles changed shape, apical and basal cell contacts came into register. Measurements of apical cell dimensions suggest that changes in cell shape account for most of the elongation in the basitarsal and tibial leg segments between 0 and 6 h after puparium formation (AP). The conversion of a stable population of anisometric cells to isometric dimensions constitutes a novel mechanism for altering the proportions of an epithelial sheet during development.


2018 ◽  
Author(s):  
Wenwei Lin ◽  
Wenxin Tang ◽  
Charles T. Anderson ◽  
Zhenbiao Yang

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.


2020 ◽  
Vol 117 (27) ◽  
pp. 16027-16034
Author(s):  
Peter Grones ◽  
Mateusz Majda ◽  
Siamsa M. Doyle ◽  
Daniël Van Damme ◽  
Stéphanie Robert

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.


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.


2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Jacqueline Nowak ◽  
Ryan Christopher Eng ◽  
Timon Matz ◽  
Matti Waack ◽  
Staffan Persson ◽  
...  

AbstractCell shape is crucial for the function and development of organisms. Yet, versatile frameworks for cell shape quantification, comparison, and classification remain underdeveloped. Here, we introduce a visibility graph representation of shapes that facilitates network-driven characterization and analyses across shapes encountered in different domains. Using the example of complex shape of leaf pavement cells, we show that our framework accurately quantifies cell protrusions and invaginations and provides additional functionality in comparison to the contending approaches. We further show that structural properties of the visibility graphs can be used to quantify pavement cell shape complexity and allow for classification of plants into their respective phylogenetic clades. Therefore, the visibility graphs provide a robust and unique framework to accurately quantify and classify the shape of different objects.


Blood ◽  
2002 ◽  
Vol 99 (8) ◽  
pp. 2851-2858 ◽  
Author(s):  
Yukari Okamoto ◽  
Daniel C. Douek ◽  
Richard D. McFarland ◽  
Richard A. Koup

Abstract Immune reconstitution is a critical component of recovery after treatment of human immunodeficiency virus (HIV) infection, cancer chemotherapy, and hematopoietic stem cell transplantation. The ability to enhance T-cell production would benefit such treatment. We examined the effects of exogenous interleukin-7 (IL-7) on apoptosis, proliferation, and the generation of T-cell receptor rearrangement excision circles (TRECs) in human thymus. Quantitative polymerase chain reaction demonstrated that the highest level of TRECs (14 692 copies/10 000 cells) was present in the CD1a+CD3−CD4+CD8+stage in native thymus, suggesting that TREC generation occurred following the cellular division in this subpopulation. In a thymic organ culture system, exogenous IL-7 increased the TREC frequency in fetal as well as infant thymus, indicating increased T-cell receptor (TCR) rearrangement. Although this increase could be due to the effect of IL-7 to increase thymocyte proliferation and decrease apoptosis of immature CD3− cells, the in vivo experiments using NOD/LtSz-scid mice given transplants of human fetal thymus and liver suggested that IL-7 can also directly enhance TREC generation. Our results provide compelling evidence that IL-7 has a direct effect on increasing TCR-αβ rearrangement and indicate the potential use of IL-7 for enhancing de novo naı̈ve T-cell generation in immunocompromised patients.


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