Genetic Control of Organ Shape and Tissue Polarity

Green, Amelia A.; Kennaway, Richard; Hanna, Andrew I.; Bangham, Jenny; Coen, Enrico

doi:10.1371/journal.pbio.1000537

Cited by 110 publications

(142 citation statements)

References 44 publications

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“…They showed that the difference between these is often not trivial, and even with very simple shapes it is not intuitive how to go from genes to final form. In their simulations (1,(3)(4)(5), plant tissue is modeled as a continuous 2D sheet of material, with any effects from the underlying cellular structure homogenized into the material parameters. Here we have extended this paradigm by considering the effect of the full 3D cellular geometry and topology on cell expansion, both in cellular plant tissues obtained from confocal images and in computer-generated templates.…”

Section: Resultsmentioning

confidence: 99%

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Mechanical constraints imposed by 3D cellular geometry and arrangement modulate growth patterns in the Arabidopsis embryo

Bassel

Stamm

Mosca

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

178

202

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Morphogenesis occurs in 3D space over time and is guided by coordinated gene expression programs. Here we use postembryonic development in Arabidopsis plants to investigate the genetic control of growth. We demonstrate that gene expression driving the production of the growth-stimulating hormone gibberellic acid and downstream growth factors is first induced within the radicle tip of the embryo. The center of cell expansion is, however, spatially displaced from the center of gene expression. Because the rapidly growing cells have very different geometry from that of those at the tip, we hypothesized that mechanical factors may contribute to this growth displacement. To this end we developed 3D finiteelement method models of growing custom-designed digital embryos at cellular resolution. We used this framework to conceptualize how cell size, shape, and topology influence tissue growth and to explore the interplay of geometrical and genetic inputs into growth distribution. Our simulations showed that mechanical constraints are sufficient to explain the disconnect between the experimentally observed spatiotemporal patterns of gene expression and early postembryonic growth. The center of cell expansion is the position where genetic and mechanical facilitators of growth converge. We have thus uncovered a mechanism whereby 3D cellular geometry helps direct where genetically specified growth takes place.computational modeling | quantification | biomechanics | plant development | seed germination C entral to developmental biology is the question of how gene expression leads to morphogenesis and the creation of form (1, 2). However, there are few studies that link genes directly with shape change in a mechanistic way (3-5). In plants, where cells do not move, nearly all shape change and morphogenesis occur through the tightly regulated control over the mechanical properties of the cell wall. Mathematical models of plant cell growth are based on the turgor-driven Lockhart model and its derivatives (6, 7) that link the rate of cell wall expansion to the stress experienced by the wall. This model fits well with the biochemistry of the cell wall, which is composed of a strong cellulose microfibril network embedded in a pectin matrix with cross-links of hemicellulose, structural proteins, and other polysaccharides (8). Stress on the cell wall from turgor pressure causes elastic expansion, which becomes plastic as remodeling enzymes rearrange the network and incorporate new material (8). Thus, the physical manifestation of growth, cell expansion, results from a balance between genetically controlled enzymatic activity and the mechanical forces experienced by the cell wall.A common simplifying assumption is that gene expression associated with cell wall modification directly specifies the rate of growth of cells. This assumption is, however, limited as growthpromoting gene expression rarely correlates well with gradients of active cell expansion (9, 10). This suggests that gene expression patterns alone are not sufficient to pr...

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Section: Resultsmentioning

confidence: 99%

“…However, there are few studies that link genes directly with shape change in a mechanistic way (3)(4)(5). In plants, where cells do not move, nearly all shape change and morphogenesis occur through the tightly regulated control over the mechanical properties of the cell wall.…”

mentioning

confidence: 99%

Mechanical constraints imposed by 3D cellular geometry and arrangement modulate growth patterns in the Arabidopsis embryo

Bassel

Stamm

Mosca

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

178

202

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“…4 D and E and 5A), restoring cell packing. In contrast, the orientation of divisions will tend to alternate in nonstretched monolayers, promoting isotropic monolayer growth, as commonly observed in proliferating plant tissues, where no neighbor exchange occurs (28).…”

Section: Discussionmentioning

confidence: 98%

Emergence of homeostatic epithelial packing and stress dissipation through divisions oriented along the long cell axis

Wyatt

Harris

Lam

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

197

201

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Cell division plays an important role in animal tissue morphogenesis, which depends, critically, on the orientation of divisions. In isolated adherent cells, the orientation of mitotic spindles is sensitive to interphase cell shape and the direction of extrinsic mechanical forces. In epithelia, the relative importance of these two factors is challenging to assess. To do this, we used suspended monolayers devoid of ECM, where divisions become oriented following a stretch, allowing the regulation and function of epithelial division orientation in stress relaxation to be characterized. Using this system, we found that divisions align better with the long, interphase cell axis than with the monolayer stress axis. Nevertheless, because the application of stretch induces a global realignment of interphase long axes along the direction of extension, this is sufficient to bias the orientation of divisions in the direction of stretch. Each division redistributes the mother cell mass along the axis of division. Thus, the global bias in division orientation enables cells to act collectively to redistribute mass along the axis of stretch, helping to return the monolayer to its resting state. Further, this behavior could be quantitatively reproduced using a model designed to assess the impact of autonomous changes in mitotic cell mechanics within a stretched monolayer. In summary, the propensity of cells to divide along their long axis preserves epithelial homeostasis by facilitating both stress relaxation and isotropic growth without the need for cells to read or transduce mechanical signals.T he morphogenesis of animal tissues results from coordinated changes in the shape, size, and packing of their constituent cells (1-3). These include autonomous cell shape changes (4), the response of cells to extrinsic stresses, and the effects of passive tissue deformation (5). When coordinated across a tissue, these active cellular processes and passive responses enable epithelial sheets to undergo shape changes while retaining relatively normal cell packing (6) and help return tissues to their resting state following a perturbation (7). Although the molecular basis of this cooperation is not understood, several studies have suggested a role for mechanical feedback (8, 9). Cell division has been suggested to participate in this feedback (10) because the rate of animal cell proliferation responds to changes in extrinsic forces in several experimental settings (9). Further, division makes an important contribution to tissue morphogenesis in animals (11, 12), accounts for much of the topological disorder observed in epithelia (13), can drive tissue elongation (10), and can facilitate the return to homeostatic cell packing following a deformation (2). Importantly, for each of these functions, the impact of cell division depends critically on the orientation of divisions.At the cellular level, relatively simple rules appear to govern division orientation. These rules were first explored by Hertwig (14), who showed that cells from early em...

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“…However, the mechanisms coordinating cell proliferation and cell size during organ growth remain poorly understood (Johnston and Gallant 2002). Due to the simpler planar structures of their organs, such as leaves and petals, and the absence of cell movement due to rigid cell walls, plants have some experimental advantages for studying organ growth (Green et al 2010).…”

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confidence: 99%

Ubiquitylation activates a peptidase that promotes cleavage and destabilization of its activating E3 ligases and diverse growth regulatory proteins to limit cell proliferation in Arabidopsis

et al. 2017

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The characteristic shapes and sizes of organs are established by cell proliferation patterns and final cell sizes, but the underlying molecular mechanisms coordinating these are poorly understood. Here we characterize a ubiquitinactivated peptidase called DA1 that limits the duration of cell proliferation during organ growth in Arabidopsis thaliana. The peptidase is activated by two RING E3 ligases, Big Brother (BB) and DA2, which are subsequently cleaved by the activated peptidase and destabilized. In the case of BB, cleavage leads to destabilization by the RING E3 ligase PROTEOLYSIS 1 (PRT1) of the N-end rule pathway. DA1 peptidase activity also cleaves the deubiquitylase UBP15, which promotes cell proliferation, and the transcription factors TEOSINTE BRANCED 1/CYCLOIDEA/ PCF 15 (TCP15) and TCP22, which promote cell proliferation and repress endoreduplication. We propose that DA1 peptidase activity regulates the duration of cell proliferation and the transition to endoreduplication and differentiation during organ formation in plants by coordinating the destabilization of regulatory proteins.

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Genetic Control of Organ Shape and Tissue Polarity

Abstract: A combination of experimental analysis and mathematical modelling shows how the genetic control of tissue polarity plays a fundamental role in the development and evolution of form.

Cited by 110 publications

References 44 publications

Mechanical constraints imposed by 3D cellular geometry and arrangement modulate growth patterns in the Arabidopsis embryo

Mechanical constraints imposed by 3D cellular geometry and arrangement modulate growth patterns in the Arabidopsis embryo

Emergence of homeostatic epithelial packing and stress dissipation through divisions oriented along the long cell axis

Ubiquitylation activates a peptidase that promotes cleavage and destabilization of its activating E3 ligases and diverse growth regulatory proteins to limit cell proliferation in Arabidopsis

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