Mechanical Shielding of Rapidly Growing Cells Buffers Growth Heterogeneity and Contributes to Organ Shape Reproducibility

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.

The statistics of noisy growth with mechanical feedback in elastic tissues

“…By assuming a solid tissue, we also neglect the possibility of cell rearrangements (T1 transitions) and flow. This assumption usually holds for plant cells (18,19). In animal epithelia, flows and T1's are sometimes significant (6), but there are also cases that exhibit more solid-like behavior.…”

“…Nonetheless, several studies have argued that tissues both in culture (12,(40)(41)(42) and in vivo (43)(44)(45)(46)(47) respond to mechanical stress by modulating the rate and orientation of cell division or by inducing cell death (42,(48)(49)(50). Clones of fast-growing cells in Drosophila wing discs reduce their growth rate through mechanical feedback (8), and similar behavior has been observed in plant systems (19,51) including the Arabidopsis sepal (10). In confluent monolayers, contact inhibition slows mitosis (11,15).…”

“…Here, in contrast, our goal is to explicitly include the effects of mechanical stresses on growth of elastic tissues. An elastic description is typically valid for plants (18,19) and can be applied to animal tissues like the Drosophila wing imaginal disc to the extent that cell rearrangements are rare (20)(21)(22)(23)(24); moreover, the formalism we adopt can be extended to encompass simple models of plastic flow that allow for more frequent rearrangements (25). We expect that noise will lead to growth non-uniformities and thus to the uneven accumulation of cell mass; this, in turn, will generate stresses that can feed back on local growth rates.…”

“…Whether cells more generally adjust their growth rates to their mechanical environment is, however, less obvious. The idea that negative feedback from mechanical stresses could damp out cell density fluctuations was proposed in (27) and has since been incorporated into a number of models (8,18,19,(28)(29)(30)(31)(32)(33)(34)(35)(36)(37).…”

Cytoskeletal organization in isolated plant cells under geometry control

“…Many external signals such as light or hormones can influence MT direction (Zandomeni and Schopfer 1993) . In addition, many studies suggest that mechanical stresses, generated by tissue shape and turgor pressure as well as by external application of force, orient the MTs along their principal direction in the shoot apical meristem (SAM) (Hamant et al 2008) , in leaf cells (Sampathkumar, Yan, et al 2014;Jacques et al 2013) in hypocotyls (Verger et al 2018;Robinson and Kuhlemeier 2018;Hejnowicz et al 2000) , in sepals (Hervieux et al 2017;Hervieux et al 2016) or in single protoplasts (Wymer et al 1996) . The response of MTs to mechanical stress relies on dynamic self-organization of the MTs.…”