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1.  A correlative microscopy approach relates microtubule behaviour, local organ geometry, and cell growth at the Arabidopsis shoot apical meristem 
Journal of Experimental Botany  2013;64(18):5753-5767.
Cortical microtubules (CMTs) are often aligned in a particular direction in individual cells or even in groups of cells and play a central role in the definition of growth anisotropy. How the CMTs themselves are aligned is not well known, but two hypotheses have been proposed. According to the first hypothesis, CMTs align perpendicular to the maximal growth direction, and, according to the second, CMTs align parallel to the maximal stress direction. Since both hypotheses were formulated on the basis of mainly qualitative assessments, the link between CMT organization, organ geometry, and cell growth is revisited using a quantitative approach. For this purpose, CMT orientation, local curvature, and growth parameters for each cell were measured in the growing shoot apical meristem (SAM) of Arabidopsis thaliana. Using this approach, it has been shown that stable CMTs tend to be perpendicular to the direction of maximal growth in cells at the SAM periphery, but parallel in the cells at the boundary domain. When examining the local curvature of the SAM surface, no strict correlation between curvature and CMT arrangement was found, which implies that SAM geometry, and presumed geometry-derived stress distribution, is not sufficient to prescribe the CMT orientation. However, a better match between stress and CMTs was found when mechanical stress derived from differential growth was also considered.
PMCID: PMC3871827  PMID: 24153420
Arabidopsis thaliana; cortical microtubules; growth; mechanical stress; organ geometry; shoot apical meristem.
2.  Cracking the elusive alignment hypothesis: the microtubule–cellulose synthase nexus unraveled 
Trends in Plant Science  2012;17(11):666-674.
Directed plant cell growth is governed by deposition and alterations of cell wall components under turgor pressure. A key regulatory element of anisotropic growth, and hence cell shape, is the directional deposition of cellulose microfibrils. The microfibrils are synthesized by plasma membrane-located cellulose synthase complexes that co-align with and move along cortical microtubules. That the parallel relation between cortical microtubules and extracellular microfibrils is causal has been named the alignment hypothesis. Three recent studies revealed that the previously identified pom2 mutant codes for a large cellulose synthases interacting (CSI1) protein which also binds cortical microtubules. This review summarizes these findings, provides structure–function models and discusses the inferred mechanisms in the context of plant growth.
PMCID: PMC3492759  PMID: 22784824
3.  Regulatory Role of Cell Division Rules on Tissue Growth Heterogeneity 
The coordination of cell division and cell expansion are critical to normal development of tissues. In plants, cell wall mechanics and the there from arising cell shapes and mechanical stresses can regulate cell division and cell expansion and thereby tissue growth and morphology. Limited by experimental accessibility it remains unknown how cell division and expansion cooperatively affect tissue growth dynamics. Employing a cell-based two dimensional tissue simulation we investigate the regulatory role of a range of cell division rules on tissue growth dynamics and in particular on the spatial heterogeneity of growth. We find that random cell divisions only add noise to the growth and therefore increase growth heterogeneity, while cell divisions following the shortest new wall or along the direction of maximal mechanical stress reduce growth heterogeneity by actively enhancing the regulation of growth by mechanical stresses. Thus, we find that, beyond tissue geometry and topology, cell divisions affect the dynamics of growth, and that their signature is embedded in the statistics of tissue growth.
PMCID: PMC3414725  PMID: 22908023
growth regulation; stochasticity; morphogenesis; mechanical forces; vertex model; cell division
4.  Quantitative imaging strategies pave the way for testable biological concepts 
BMC Biology  2011;9:10.
In developmental biology, the accumulation of qualitative phenotypic descriptions has fueled the need for testable parsimonious hypotheses, giving a fresh impetus to quantitative strategies. As an illustration, thanks to the precise quantification of cell growth and microtubule behavior in a study published in BMC Plant Biology, Zhang and collaborators have identified sequential phases of polarized and isotropic growth in puzzle-shaped leaf epidermal cells, thus providing new clues to explore how growth coordination occurs in this tissue.
PMCID: PMC3045392  PMID: 21352557
5.  Is cell polarity under mechanical control in plants? 
Plant Signaling & Behavior  2011;6(1):137-139.
Plant cells experience a tremendous amount of mechanical stress caused by turgor pressure. Because cells are glued to their neighbors by the middle lamella, supracellular patterns of physical forces are emerging during growth, usually leading to tension in the epidermis. Cortical microtubules have been shown to reorient in response to these mechanical stresses, and to resist them, indirectly via their impact on the anisotropic structure of the cell wall. In a recent study, we show that the polar localization of the auxin efflux carrier PIN1 can also be under the control of physical forces, thus linking cell growth rate and anisotropy by a common mechanical signal. Because of the known impact of auxin on the stiffness of the cell wall, this suggests that the mechanical properties of the extracellular matrix play a crucial signaling role in morphogenesis, notably controlling the polarity of the cell, as observed in animal systems.
PMCID: PMC3122027  PMID: 21258209
development; growth; auxin; microtubule; PIN1; stiffness; cell wall; biophysics; meristem
6.  Alignment between PIN1 Polarity and Microtubule Orientation in the Shoot Apical Meristem Reveals a Tight Coupling between Morphogenesis and Auxin Transport 
PLoS Biology  2010;8(10):e1000516.
Imaging and computational modeling of the Arabidopsis shoot meristem epidermis suggests that biomechanical signals coordinately regulate auxin efflux carrier distribution and microtubule patterning to orchestrate the extent and directionality of growth.
Morphogenesis during multicellular development is regulated by intercellular signaling molecules as well as by the mechanical properties of individual cells. In particular, normal patterns of organogenesis in plants require coordination between growth direction and growth magnitude. How this is achieved remains unclear. Here we show that in Arabidopsis thaliana, auxin patterning and cellular growth are linked through a correlated pattern of auxin efflux carrier localization and cortical microtubule orientation. Our experiments reveal that both PIN1 localization and microtubule array orientation are likely to respond to a shared upstream regulator that appears to be biomechanical in nature. Lastly, through mathematical modeling we show that such a biophysical coupling could mediate the feedback loop between auxin and its transport that underlies plant phyllotaxis.
Author Summary
The proper development of plant organs such as leaves or flowers depends both on localized growth, which can be controlled by the plant hormone auxin, and directional growth, which is dependent on each cell's microtubule cytoskeleton. In this paper we show that at the shoot apex where organs initiate the orientation of the microtubule cytoskeleton is correlated with the orientation of the auxin transporter PIN1, suggesting coordination between growth patterning at the tissue level and directional growth at the cellular level. Recent work has indicated that mechanical signals play a role in orienting the plant microtubule network, and here we show that such signals can also orient PIN1. In addition, we demonstrate through mathematical modeling that an auxin transport system that is coordinated by mechanical signals akin to those we observed in vivo is sufficient to give rise to the patterns of organ outgrowth found in the plant Arabidopsis thaliana.
PMCID: PMC2957402  PMID: 20976043

Results 1-6 (6)