Growth and size control during development

Vollmer, Jannik; Casares, Fernando; Iber, Dagmar

doi:10.1098/rsob.170190

Cited by 65 publications

(54 citation statements)

References 123 publications

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“…Whereas the MFM incorporates part of the Hippo pathway, a description of growth also requires the integration of extrinsic growth controls, transduced via the dTOR pathway (Vollmer et al, ). The disk also is mechanically connected to the notum, the basement membrane (Domínguez‐Giménez et al, ; Pastor‐Pareja & Xu, ), apical extracellular matrix (Heer & Martin, ), peripodial cells which are opposed to the disk cells (Baena‐López et al, ), and muscles within the larva (Nienhaus et al, ).…”

Section: A Model For the Control Of Disk Sizementioning

confidence: 99%

Growth control in the Drosophila wing disk

Gou

Stotsky

Othmer

2020

WIREs Mechanisms of Disease

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The regulation of size and shape is a fundamental requirement of biological development and has been a subject of scientific study for centuries, but we still lack an understanding of how organisms know when to stop growing. Imaginal wing disks of the fruit fly Drosophila melanogaster, which are precursors of the adult wings, are an archetypal tissue for studying growth control. The growth of the disks is dependent on many inter‐ and intra‐organ factors such as morphogens, mechanical forces, nutrient levels, and hormones that influence gene expression and cell growth. Extracellular signals are transduced into gene‐control signals via complex signal transduction networks, and since cells typically receive many different signals, a mechanism for integrating the signals is needed. Our understanding of the effect of morphogens on tissue‐level growth regulation via individual pathways has increased significantly in the last half century, but our understanding of how multiple biochemical and mechanical signals are integrated to determine whether or not a cell decides to divide is still rudimentary. Numerous fundamental questions are involved in understanding the decision‐making process, and here we review the major biochemical and mechanical pathways involved in disk development with a view toward providing a basis for beginning to understand how multiple signals can be integrated at the cell level, and how this translates into growth control at the level of the imaginal disk. This article is categorized under: Analytical and Computational Methods > Computational Methods Biological Mechanisms > Cell Signaling Models of Systems Properties and Processes > Cellular Models

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Section: A Model For the Control Of Disk Sizementioning

confidence: 99%

Growth control in the Drosophila wing disk

Gou

Stotsky

Othmer

2020

WIREs Mechanisms of Disease

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“…More specifically, distribution of pressure in the tissue could play a role in controlling the rate of cell growth and division, i.e. stem cells under higher pressure in the CZ may divide less frequently than differentiated cells under lower pressure in the PZ (Vollmer et al 2017).…”

Section: Discussionmentioning

confidence: 99%

Cell-Based Model of the Generation and Maintenance of the Shape and Structure of the Multilayered Shoot Apical Meristem of Arabidopsis thaliana

et al. 2018

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One of the central problems in animal and plant developmental biology is deciphering how chemical and mechanical signals interact within a tissue to produce organs of defined size, shape and function. Cell walls in plants impose a unique constraint on cell expansion since cells are under turgor pressure and do not move relative to one another. Cell wall extensibility and constantly changing distribution of stress on the wall are mechanical properties that vary between individual cells and contribute to rates of expansion and orientation of cell division. How exactly cell wall mechanical properties influence cell behavior is still largely unknown. To address this problem, a novel, subcellular element computational model of growth of stem cells within the multilayered shoot apical meristem (SAM) of Arabidopsis thaliana is developed and calibrated using experimental data. Novel features of the model include separate, detailed descriptions of cell wall extensibility and mechanical stiffness, deformation of the middle lamella and increase in cytoplasmic pressure generating internal turgor pressure. The model is used to test novel hypothesized mechanisms of formation of the shape and structure of the growing, multilayered SAM based on WUS concentration of individual cells controlling cell growth rates and layer dependent anisotropic mechanical properties of subcellular components of individual cells determining anisotropic cell expansion directions. Model simulations also provide a detailed prediction of distribution of stresses in the growing tissue which can be tested in future experiments.

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“…Nevertheless, the extra legs of parasite-infested frogs typically reach the right size, as do the extra legs of insects (Heald, Hariharan, & Wake, 2015). How do limbs, or organs in general for that matter, manage to stop growing so precisely (Eder, Aegerter, & Basler, 2017;Hariharan, 2015;Vollmer, Casares, & Iber, 2017)? One idea for vertebrate limbs is that the poles of the feedback loop grow so far apart that they can no longer spur one another (Tanaka, 2016;Verheyden & Sun, 2008), but that trick cannot work for the Dpp-Wg loop due to their perpetual proximity.…”

Section: The Logic Of Monstersmentioning

confidence: 99%

Reflections on Bateson's rule: Solving an old riddle about why extra legs are mirror‐symmetric

Held

Sessions

2019

J Exp Zool Pt B

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William Bateson was an obsessive observer of animal oddities, and at some point in his herculean survey of museum collections leading up to his monumental 1894 monograph (Materials for the study of variation), he noticed a peculiar trend among the preserved specimens (mainly insects) that possessed extra legs: multiple legs that branched from the same socket tended to be mirror images of their adjacent neighbors. He did not know why. These symmetry relationships have come to be known as Bateson's rule, and they have defied a satisfactory explanation for 125 years. In the past few decades, tantalizing clues have emerged from various lines of investigation, and those lines have converged on a possible solution. An attempt is made here to fit all of those clues together to form a coherent picture of the etiology. Two case studies have proven to be pivotal: a fly mutant whose extra legs are caused by patches of dying cells and a frog syndrome whose extra legs are caused by a parasitic flatworm. The conclusion reached is that the extra legs of insects and vertebrates obey Bateson's rule for the same reason, but that reason has nothing to do with the specific molecules in their signaling pathways. Rather, it is an emergent property of the circuitry of the pathways and their polarized alignments along the limb axes. A parade of theoretical models have tried and failed to crack this mystery in the past, and they are reviewed here as part of the narrative.

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Growth and size control during development

Cited by 65 publications

References 123 publications

Growth control in the Drosophila wing disk

Growth control in the Drosophila wing disk

Cell-Based Model of the Generation and Maintenance of the Shape and Structure of the Multilayered Shoot Apical Meristem of Arabidopsis thaliana

Reflections on Bateson's rule: Solving an old riddle about why extra legs are mirror‐symmetric

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