| 1. |
- Hervieux, Nathan, et al.
(författare)
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Mechanical Shielding of Rapidly Growing Cells Buffers Growth Heterogeneity and Contributes to Organ Shape Reproducibility
- 2017
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Ingår i: Current Biology. - : Elsevier BV. - 0960-9822 .- 1879-0445. ; 27:22, s. 3468-3479.e4
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Tidskriftsartikel (refereegranskat)abstract
- A landmark of developmental biology is the production of reproducible shapes, through stereotyped morphogenetic events. At the cell level, growth is often highly heterogeneous, allowing shape diversity to arise. Yet, how can reproducible shapes emerge from such growth heterogeneity? Is growth heterogeneity filtered out? Here, we focus on rapidly growing trichome cells in the Arabidopsis sepal, a reproducible floral organ. We show via computational modeling that rapidly growing cells may distort organ shape. However, the cortical microtubule alignment along growth-derived maximal tensile stress in adjacent cells would mechanically isolate rapidly growing cells and limit their impact on organ shape. In vivo, we observed such microtubule response to stress and consistently found no significant effect of trichome number on sepal shape in wild-type and lines with trichome number defects. Conversely, modulating the microtubule response to stress in katanin and spiral2 mutant made sepal shape dependent on trichome number, suggesting that, while mechanical signals are propagated around rapidly growing cells, the resistance to stress in adjacent cells mechanically isolates rapidly growing cells, thus contributing to organ shape reproducibility.
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| 2. |
- Hong, Lilan, et al.
(författare)
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Heterogeneity and Robustness in Plant Morphogenesis : From Cells to Organs
- 2018
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Ingår i: Annual Review of Plant Biology. - : Annual Reviews. - 1543-5008 .- 1545-2123. ; 69, s. 469-495
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Forskningsöversikt (refereegranskat)abstract
- Development is remarkably reproducible, producing organs with the same size, shape, and function repeatedly from individual to individual. For example, every flower on the Antirrhinum stalk has the same snapping dragon mouth. This reproducibility has allowed taxonomists to classify plants and animals according to their morphology. Yet these reproducible organs are composed of highly variable cells. For example, neighboring cells grow at different rates in Arabidopsis leaves, sepals, and shoot apical meristems. This cellular variability occurs in normal, wild-type organisms, indicating that cellular heterogeneity (or diversity in a characteristic such as growth rate) is either actively maintained or, at a minimum, not entirely suppressed. In fact, cellular heterogeneity can contribute to producing invariant organs. Here, we focus on how plant organs are reproducibly created during development from these highly variable cells.
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| 3. |
- Mirabet, Vincent, et al.
(författare)
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The self-organization of plant microtubules in three dimensions enables stable cortical localization and sensitivity to external cues
- 2017
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Ingår i: bioRxiv. - : Cold Spring Harbor Laboratory.
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Annan publikation (övrigt vetenskapligt/konstnärligt)abstract
- Many cell functions rely on the ability of microtubules to self-organize as complex networks. In plants, cortical microtubules are essential to determine cell shape as they guide the deposition of cellulose microfibrils, and thus control mechanical anisotropy in the cell wall. Here we analyze how, in turn, cell shape may influence microtubule behavior. Using a computational model of microtubules enclosed in a three-dimensional space, We show that the microtubule network has spontaneous configurations that could explain many experimental observations without resorting to specific regulation. In particular, we find that the preferred localization of microtubules at the cortex emerges from directional persistence of the microtubules, combined with their growth mode. We identified microtubule parameters that seem relatively insensitive to cell shape, such as length or number. In contrast, microtubule array anisotropy depends strongly on local curvature of the cell surface and global orientation follows robustly the longest axis of the cell. Lastly, we found that the network is capable of reorienting toward weak external directional cues. Altogether our simulations show that the microtubule network is a good transducer of weak external polarity, while at the same time, it easily reaches stable global configurations.Author summary Plants exhibit an astonishing diversity in architecture and shape. A key to such diversity is the ability of their cells to coordinate and grow to reach a broad spectrum of sizes and shapes. Cell growth in plants is guided by the microtubule cytoskeleton. Here, we seek to understand how microtubules self-organize close to the cell surface. We build upon previous two-dimensional models and we consider microtubules as lines growing in three dimensions, accounting for interactions between microtubules or between microtubules and the cell surface. We show that microtubule arrays are able to adapt to various cell shapes and to reorient in response to factors such as signals or environment. Altogether, our results help to understand how the microtubule cytoskeleton contributes to the diversity of plant shapes and to how these shapes adapt to environment.
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| 4. |
- Mirabet, Vincent, et al.
(författare)
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The self-organization of plant microtubules inside the cell volume yields their cortical localization, stable alignment, and sensitivity to external cues
- 2018
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Ingår i: PLoS Computational Biology. - : Public Library of Science (PLoS). - 1553-7358. ; 14:2
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Tidskriftsartikel (refereegranskat)abstract
- Many cell functions rely on the ability of microtubules to self-organize as complex networks. In plants, cortical microtubules are essential to determine cell shape as they guide the deposition of cellulose microfibrils, and thus control mechanical anisotropy of the cell wall. Here we analyze how, in turn, cell shape may influence microtubule behavior. Buidling upon previous models that confined microtubules to the cell surface, we introduce an agent model of microtubules enclosed in a three-dimensional volume. We show that the microtubule network has spontaneous aligned configurations that could explain many experimental observations without resorting to specific regulation. In particular, we find that the preferred cortical localization of microtubules emerges from directional persistence of the microtubules, and their interactions with each other and with the stiff wall. We also identify microtubule parameters that seem relatively insensitive to cell shape, such as length or number. In contrast, microtubule array anisotropy depends on local curvature of the cell surface and global orientation follows robustly the longest axis of the cell. Lastly, we find that geometric cues may be overcome, as network is capable of reorienting toward weak external directional cues. Altogether our simulations show that the microtubule network is a good transducer of weak external polarity, while at the same time, easily reaching stable global configurations.
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| 5. |
- Sampathkumar, Arun, et al.
(författare)
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Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells
- 2014
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Ingår i: eLife. - 2050-084X. ; 3
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Tidskriftsartikel (refereegranskat)abstract
- 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.
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| 6. |
- Tsugawa, Satoru, et al.
(författare)
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Clones of cells switch from reduction to enhancement of size variability in Arabidopsis sepals
- 2017
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Ingår i: Development. - : The Company of Biologists. - 0950-1991 .- 1477-9129. ; 144:23, s. 4398-4405
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Tidskriftsartikel (refereegranskat)abstract
- Organs form with remarkably consistent sizes and shapes during development, whereas a high variability in growth is observed at the cell level. Given this contrast, it is unclear how such consistency in organ scale can emerge from cellular behavior. Here, we examine an intermediate scale, the growth of clones of cells in Arabidopsis sepals. Each clone consists of the progeny of a single progenitor cell. At early stages, we find that clones derived from a small progenitor cell grow faster than those derived from a large progenitor cell. This results in a reduction in clone size variability, a phenomenon we refer to as size uniformization. By contrast, at later stages of clone growth, clones change their growth pattern to enhance size variability, when clones derived from larger progenitor cells grow faster than those derived from smaller progenitor cells. Finally, we find that, at early stages, fast growing clones exhibit greater cell growth heterogeneity. Thus, cellular variability in growth might contribute to a decrease in the variability of clones throughout the sepal.
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| 7. |
- Zhu, Mingyuan, et al.
(författare)
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Robust organ size requires robust timing of initiation orchestrated by focused auxin and cytokinin signalling
- 2020
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Ingår i: Nature Plants. - : Springer Science and Business Media LLC. - 2055-0278. ; 6, s. 686-698
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Tidskriftsartikel (refereegranskat)abstract
- The shape of plant organs shows low variability. Sepals of the same age look the same. Here the authors identify one transcription factor (DRMY1) crucial for sepal size reproducibility, and its effect on initiation timing and growth of the organ. Organ size and shape are precisely regulated to ensure proper function. The four sepals in each Arabidopsis thaliana flower must maintain the same size throughout their growth to continuously enclose and protect the developing bud. Here we show that DEVELOPMENT RELATED MYB-LIKE 1 (DRMY1) is required for both timing of organ initiation and proper growth, leading to robust sepal size in Arabidopsis. Within each drmy1 flower, the initiation of some sepals is variably delayed. Late-initiating sepals in drmy1 mutants remain smaller throughout development, resulting in variability in sepal size. DRMY1 focuses the spatiotemporal signalling patterns of the plant hormones auxin and cytokinin, which jointly control the timing of sepal initiation. Our findings demonstrate that timing of organ initiation, together with growth and maturation, contribute to robust organ size.
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