Modulation of tissue growth heterogeneity by responses to mechanical stress

Fruleux, Antoine; Boudaoud, Arezki

doi:10.1073/pnas.1815342116

Cited by 21 publications

(14 citation statements)

References 53 publications

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“…In other words, the cell's response to mechanical stress needs to be suboptimal to promote developmental robustness. This result echoes plant-based computational simulations suggesting the ambivalent nature of mechanical stress in growth heterogeneity [11,65] and opens several avenues to test whether comparable conclusions can be reached in animal systems.…”

Section: A Suboptimal Response To Mechanical Stress Buffers Growth Variationssupporting

confidence: 73%

Microtubule Response to Tensile Stress Is Curbed by NEK6 to Buffer Growth Variation in the Arabidopsis Hypocotyl

et al. 2020

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Section: A Suboptimal Response To Mechanical Stress Buffers Growth Variationssupporting

confidence: 73%

Microtubule Response to Tensile Stress Is Curbed by NEK6 to Buffer Growth Variation in the Arabidopsis Hypocotyl

et al. 2020

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“…Fluctuation stretching, the enlargement of the lengthscale of fluctuations by medium expansion, is predicted by different models of expanding media, the early universe [16] and living tissues [14, 15]. Fluctuation stretching can be understood with the help of FIG.1 and is formally derived in section Datasets and Methods.…”

Section: Resultsmentioning

confidence: 99%

“…Recent models of tissue mechanics and growth accounted for temporal and spatial fluctuations of growth and investigated their role in robustness of morphogenesis [26][27][28]. Temporal fluctuations are characterised by their degree of persistence, quantified with the persistence time (or correlation time), the characteristic time over which memory of previous fluctuations is lost.…”

Section: Introductionmentioning

confidence: 99%

Growth couples temporal and spatial fluctuations of tissue properties during morphogenesis

Fruleux,

Hong,

Roeder

et al. 2023

Preprint

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Living tissues display fluctuations -- random spatial and temporal variations of tissue properties around their reference values -- at multiple scales. It is believed that such fluctuations may enable tissues to sense their state or their size. Recent theoretical studies developed specific models of fluctuations in growing tissues and predicted that fluctuations of growth show long-range correlations. Here we elaborated upon these predictions and we tested them using experimental data. We first introduced a minimal model for the fluctuations of any quantity that has some level of temporal persistence or memory, such as concentration of a molecule, local growth rate, or mechanical properties. We found that long-range correlations are generic, applying to to any such quantity, and that growth couples temporal and spatial fluctuations. We then analysed growth data from sepals of the model plant Arabidopsis and we quantified spatial and temporal fluctuations of cell growth using the previously developed Cellular Fourier Transform. Growth appears to have long-range correlations. We compared different genotypes and growth conditions: mutants with altered response to mechanical stress have lower temporal correlations and longer-range spatial correlations than wild-type plants. Finally, we used a theoretical prediction to collapse experimental data from all conditions and developmental stages, validating the notion that temporal and spatial fluctuations are coupled by growth. Altogether, our work reveals kinematic constraints on spatiotemporal fluctuations that have an impact on the robustness of morphogenesis.

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“…In an alternative scenario, growth heterogeneity may decrease, either because the presence of adjacent cells rather fuels growth heterogeneity, as observed in shoot apical meristems (Uyttewaal et al, 2012), or because the supracellular averaging of individual cells growing at different speed may produce more reproducible organs than large sectors of cells growing at different speed, as shown in sepals (Hong et al, 2016). The ambivalent nature of mechanical conflicts in growth heterogeneity has recently been analyzed in computer simulations (Fruleux and Boudaoud, 2019). In a more complex scenario, plasmodemata may have a direct role in organ twisting.…”

Section: Discussionmentioning

confidence: 99%

Mechanical Conflicts in Twisting Growth Revealed by Cell-Cell Adhesion Defects

2019

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Many plants grow organs and tissues with twisted shapes. Arabidopsis mutants with impaired microtubule dynamics exhibit such a phenotype constitutively. Although the activity of the corresponding microtubule regulators is better understood at the molecular level, how large-scale twisting can emerge in the mutants remains largely unknown. Classically, oblique cortical microtubules would constrain the deposition of cellulose microfibrils in cells, and such conflicts at the cell level would be relaxed at the tissue scale by supracellular torsion. This model implicitly assumes that cell-cell adhesion is a key step to transpose local mechanical conflicts into a macroscopic twisting phenotype. Here we tested this prediction using the quasimodo1 mutant, which displays cell-cell adhesion defects. Using the spriral2/tortifolia1 mutant with hypocotyl helical growth, we found that qua1 -induced cell-cell adhesion defects restore straight growth in qua1-1 spr2-2 . Detached cells in qua1-1 spr2-2 displayed helical growth, confirming that straight growth results from the lack of mechanical coupling between cells rather than a restoration of SPR2 activity in the qua1 mutant. Because adhesion defects in qua1 depend on tension in the outer wall, we also showed that hypocotyl twisting in qua1-1 spr2-2 could be restored when decreasing the matrix potential of the growth medium, i.e., by reducing the magnitude of the pulling force between adjacent cells, in the double mutant. Interestingly, the induction of straight growth in qua1-1 spr2-2 could be achieved beyond hypocotyls, as leaves also displayed a flat phenotype in the double mutant. Altogether, these results provide formal experimental support for a scenario in which twisted growth in spr2 mutant would result from the relaxation of local mechanical conflicts between adjacent cells via global organ torsion.

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Modulation of tissue growth heterogeneity by responses to mechanical stress

Cited by 21 publications

References 53 publications

Microtubule Response to Tensile Stress Is Curbed by NEK6 to Buffer Growth Variation in the Arabidopsis Hypocotyl

Microtubule Response to Tensile Stress Is Curbed by NEK6 to Buffer Growth Variation in the Arabidopsis Hypocotyl

Growth couples temporal and spatial fluctuations of tissue properties during morphogenesis

Mechanical Conflicts in Twisting Growth Revealed by Cell-Cell Adhesion Defects

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