Person: Dumais, J
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Dumais
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Dumais, J
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Publication Generating Helices in Nature(American Association for the Advancement of Science (AAAS), 2011) Forterre, Yoel; Dumais, JMacroscopic helical structures formed by organisms include seashells, horns, plant tendrils, and seed pods (see the figure, panel A). The helices that form are chiral; like wood screws, they have a handedness. Some are helicoids, twisted helices with saddle-like curvature and a straight centerline; others are cylindrical helices with cylindrical curvature and a helical centerline. Studies of the mechanisms underlying the formation of helicoid or helical ribbons and of the transitions between these structures (1–4) have left an important question unanswered: How do the molecular organization of the material and its global geometrical features interact to create a diversity of helical shapes? On page 1726 of this issue, Armon et al. (5) explore the rich phenomenology associated with slender strips made of mutually opposing “molecular” layers, taking a singular botanical structure—the Bauhinia seed pod—as their inspiration. They show that a single component, namely a flat strip with a saddle-like intrinsic curvature, is sufficient to generate a wide variety of helical shapes.Publication Foldable structures and the natural design of pollen grains(Proceedings of the National Academy of Sciences, 2010) Katifori, Eleni; Alben, Silas; Cerda, Enrique; Nelson, David; Dumais, JUpon release from the anther, pollen grains of angiosperm flowers are exposed to a dry environment and dehydrate. To survive this process, pollen grains possess a variety of physiological and structural adaptations. Perhaps the most striking of these adaptations is the ability of the pollen wall to fold onto itself to prevent further desiccation. Roger P. Wodehouse coined the term harmomegathy for this folding process in recognition of the critical role it plays in the survival of the pollen grain. There is still, however, no quantitative theory that explains how the structure of the pollen wall contributes to harmomegathy. Here we demonstrate that simple geometrical and mechanical principles explain how wall structure guides pollen grains toward distinct folding pathways. We found that the presence of axially elongated apertures of high compliance is critical for achieving a predictable and reversible folding pattern. Moreover, the intricate sculpturing of the wall assists pollen closure by preventing mirror buckling of the surface. These results constitute quantitative structure-function relationships for pollen harmomegathy and provide a framework to elucidate the functional significance of the very diverse pollen morphologies observed in angiosperms.Publication Universal rule for the symmetric division of plant cells(Proceedings of the National Academy of Sciences, 2011) Besson, S.; Dumais, JThe division of eukaryotic cells involves the assembly of complex cytoskeletal structures to exert the forces required for chromosome segregation and cytokinesis. In plants, empirical evidence suggests that tensional forces within the cytoskeleton cause cells to divide along the plane that minimizes the surface area of the cell plate (Errera’s rule) while creating daughter cells of equal size. However, exceptions to Errera’s rule cast doubt on whether a broadly applicable rule can be formulated for plant cell division. Here, we show that the selection of the plane of division involves a competition between alternative configurations whose geometries represent local area minima. We find that the probability of observing a particular division configuration increases inversely with its relative area according to an exponential probability distribution known as the Gibbs measure. Moreover, a comparison across land plants and their most recent algal ancestors confirms that the probability distribution is widely conserved and independent of cell shape and size. Using a maximum entropy formulation, we show that this empirical division rule is predicted by the dynamics of the tense cytoskeletal elements that lead to the positioning of the preprophase band. Based on the fact that the division plane is selected from the sole interaction of the cytoskeleton with cell shape, we posit that the new rule represents the default mechanism for plant cell division when internal or external cues are absent.Publication An anisotropic-viscoplastic model of plant cell morphogenesis by tip growth(UPV/EHU Press, 2006) Dumais, J; Shaw, Sidney L.; Steele, Charles R.; Long, Sharon R.; Ray, Peter M.ABSTRACT Plant cell morphogenesis depends critically on two processes: the deposition of new wall material at the cell surface and the mechanical deformation of this material by the stresses resulting from the cell's turgor pressure. We developed a model of plant cell morphogenesis that is a first attempt at integrating these two processes. The model is based on the theories of thin shells and anisotropic viscoplasticity. It includes three sets of equations that give the connection between wall stresses, wall strains and cell geometry. We present an algorithm to solve these equations numerically. Application of this simulation approach to the morphogenesis of tip-growing cells illustrates how the viscoplastic properties of the cell wall affect the shape of the cell at steady state. The same simulation approach was also used to reproduce morphogenetic transients such as the initiation of tip growth and other non-steady changes in cell shape. Finally, we show that the mechanical anisotropy built into the model is required to account for observed patterns of wall expansion in plant cells.Publication The mechanics of tip growth morphogenesis: what we have learned from rubber balloons(Mathematical Sciences Publishers, 2007) Bernal, Roberto; Rojas, Enrique; Dumais, JMorphogenesis of plant, fungal, and bacterial cells depends heavily on surface mechanics and in particular on the stiff wall that surrounds these cells. In this paper, we show that tubular rubber balloons offer a useful physical model of tip growth morphogenesis. In particular, the balloons reproduce accurately the inhomogeneity and anisotropy of surface expansion observed during tip growth. Comparison between the two systems has led to a simple model of tip growth that assumes linear constitutive relations with inhomogeneous material properties. The strain rate profile predicted by the model is a surprisingly good fit to the data given the model’s simplicity. We suggest that a meridional gradient of compliance or extensibility is the key mechanical feature that explains the similar strain rate profiles in tip-growing cells across broad taxonomic groups as well as in rubber balloon analogs.Publication The transcriptional diversity of 25 Drosophila cell lines(Cold Spring Harbor Laboratory Press, 2010) Cherbas, L.; Willingham, A.; Zhang, D.; Yang, L.; Zou, Y.; Eads, B. D.; Carlson, J. W.; Landolin, J. M.; Kapranov, P.; Dumais, J; Samsonova, A.; Choi, J.-H.; Roberts, J.; Davis, C. A.; Tang, H.; van Baren, M. J.; Ghosh, S.; Dobin, A.; Bell, K.; Lin, W.; Langton, L.; Duff, M. O.; Tenney, A. E.; Zaleski, C.; Brent, M. R.; Hoskins, R. A.; Kaufman, T. C.; Andrews, J.; Graveley, B. R.; Perrimon, Norbert; Celniker, S. E.; Gingeras, T. R.; Cherbas, P.Drosophila melanogaster cell lines are important resources for cell biologists. Here, we catalog the expression of exons, genes, and unannotated transcriptional signals for 25 lines. Unannotated transcription is substantial (typically 19% of euchromatic signal). Conservatively, we identify 1405 novel transcribed regions; 684 of these appear to be new exons of neighboring, often distant, genes. Sixty-four percent of genes are expressed detectably in at least one line, but only 21% are detected in all lines. Each cell line expresses, on average, 5885 genes, including a common set of 3109. Expression levels vary over several orders of magnitude. Major signaling pathways are well represented: most differentiation pathways are “off” and survival/growth pathways “on.” Roughly 50% of the genes expressed by each line are not part of the common set, and these show considerable individuality. Thirty-one percent are expressed at a higher level in at least one cell line than in any single developmental stage, suggesting that each line is enriched for genes characteristic of small sets of cells. Most remarkable is that imaginal disc-derived lines can generally be assigned, on the basis of expression, to small territories within developing discs. These mappings reveal unexpected stability of even fine-grained spatial determination. No two cell lines show identical transcription factor expression. We conclude that each line has retained features of an individual founder cell superimposed on a common “cell line“ gene expression pattern.Publication Stochasticity in the symmetric division of plant cells: when the exceptions are the rule(Frontiers Media SA, 2014) Besson, Sebastien; Dumais, JLong before most of the molecular aspects of cell division were uncovered, L. V. Heilbrunn remarked that: “it is easier to make a new theory of cell division than to test an old one” and promised his readers to limit his treatment of cell division to “the factual facts regarding the physical changes which take place during mitosis” (Heilbrunn, 1928). Heilbrunn's barb was directed, first and foremost, to the theories or empirical rules put forward to explain how cells select a plane of division. A perusal of the cell biology literature in the decades preceding Heilbrunn's comment suffices to appreciate the author's cynicism toward cell division theories. By the end of the nineteenth century, at least five different rules had been formulated to predict how cells select a division plane. Of these, the most widely cited rules for plant cells were the Rectangular Section formulated by Sachs (1878) and the Principle of Minimal Area promoted by Berthold (1886) although often attributed to Errera (1888). The presence of exceptions to these rules led to many more “improved” rules and fueled a heated debate that spilled well into the twentieth century. An intriguing feature of this story is that despite the explosion of cell biology research in the twentieth century, the nineteenth century obsession with cell division rules rapidly receded; and ultimately vanished before the tests Heilbrunn so eagerly desired were performed. Although many biologists have cited this early work in reviews (e.g., Smith, 2001; Kwiatkowska, 2004; Dumais, 2007), the classical division rules have laid essentially dormant for a full century. The reasons why these rules were never tested must be sought in the particular mind-set of twentieth century biology. The most important factor is probably the geometrical nature of the rules which did not resonate well with the molecularly-oriented biology of the last century. Certainly, reducing cell division to a geometrical problem adds little to the “factual facts regarding the physical changes which take place during mitosis.” Yet, it is probable that even the most abstract division rule would not have been neglected for so long if it had predicted with great accuracy the selection of division planes in plant cells. Thus, another factor seems to have played an important role: the fact that even within the confine of a specific tissue, cell division seems to escape the determinism embodied by the classical rules. The frequent exceptions to the predicted division planes must have invalidated the division rules to the eye of most biologists. We recently argued that these exceptions may in fact be confirmation of another, more subtle, division rule (Besson and Dumais, 2011). Here we briefly retrace the history leading to this new rule while, at the same time, highlighting the strange turn of events that greatly delayed the acceptance of stochasticity in this particular area of cell biology.Publication Quantifying Green Life: Grand Challenges in Plant Biophysics and Modeling(Frontiers Research Foundation, 2011) Zwieniecki, Maciej A.; Dumais, JPublication Surface Tension Propulsion of Fungal Spores(Company of Biologists, 2009) Noblin, Xavier; Yang, Sylvia; Dumais, JMost basidiomycete fungi actively eject their spores. The process begins with the condensation of a water droplet at the base of the spore. The fusion of the droplet onto the spore creates a momentum that propels the spore forward. The use of surface tension for spore ejection offers a new paradigm to perform work at small length scales. However, this mechanism of force generation remains poorly understood. To elucidate how fungal spores make effective use of surface tension, we performed a detailed mechanical analysis of the three stages of spore ejection: the transfer of energy from the drop to the spore, the work of fracture required to release the spore from its supporting structure and the kinetic energy of the spore after ejection. High-speed video imaging of spore ejection in Auricularia auricula and Sporobolomyces yeasts revealed that drop coalescence takes place over a short distance \((\sim 5 \mu m)\) and energy transfer is completed in less than \(4 \mu s\). Based on these observations, we developed an explicit relation for the conversion of surface energy into kinetic energy during the coalescence process. The relation was validated with a simple artificial system and shown to predict the initial spore velocity accurately (predicted velocity: \(1.2 m s^{-1}\); observed velocity: \(0.8 m s^{-1}\) for A. auricula). Using calibrated microcantilevers, we also demonstrate that the work required to detach the spore from the supporting sterigma represents only a small fraction of the total energy available for spore ejection. Finally, our observations of this unique discharge mechanism reveal a surprising similarity with the mechanics of jumping in animals.Publication How the Venus Flytrap Snaps(Nature Publishing Group, 2005) Forterre, Yoel; Skotheim, Jan M.; Dumais, J; Mahadevan, LakshminarayananThe rapid closure of the Venus flytrap (Dionaea muscipula) leaf in about 100 ms is one of the fastest movements in the plant kingdom. This led Darwin to describe the plant as "one of the most wonderful in the world". The trap closure is initiated by the mechanical stimulation of trigger hairs. Previous studies have focused on the biochemical response of the trigger hairs to stimuli and quantified the propagation of action potentials in the leaves. Here we complement these studies by considering the post-stimulation mechanical aspects of Venus flytrap closure. Using high-speed video imaging, non-invasive microscopy techniques and a simple theoretical model, we show that the fast closure of the trap results from a snap-buckling instability, the onset of which is controlled actively by the plant. Our study identifies an ingenious solution to scaling up movements in non-muscular engines and provides a general framework for understanding nastic motion in plants.