A Mechanical Feedback Restricts Sepal Growth and Shape in Arabidopsis

Abstract

How organs reach their final shape is a central yet unresolved question in developmental biology. Here we investigate whether mechanical cues contribute to this process. We analyze the epidermal cells of the Arabidopsis sepal, focusing on cortical microtubule arrays, which align along maximal tensile stresses and restrict growth in that direction through their indirect impact on the mechanical anisotropy of cell walls. We find a good match between growth and microtubule orientation throughout most of the development of the sepal. However, at the sepal tip, where organ maturation initiates and growth slows down in later stages, microtubules remain in a configuration consistent with fast anisotropic growth, i.e., transverse, and the anisotropy of their arrays even increases. To understand this apparent paradox, we built a continuous mechanical model of a growing sepal. The model demonstrates that differential growth in the sepal can generate transverse tensile stress at the tip. Consistently, microtubules respond to mechanical perturbations and align along maximal tension at the sepal tip. Including this mechanical feedback in our growth model of the sepal, we predict an impact on sepal shape that is validated experimentally using mutants with either increased or decreased microtubule response to stress. Altogether, this suggests that a mechanical feedback loop, via microtubules acting both as stress sensor and growth regulator, channels the growth and shape of the sepal tip. We propose that this proprioception mechanism is a key step leading to growth arrest in the whole sepal in response to its own growth.

Floral Organogenesis: When Knowing Your ABCs Is Not Enough

“…The ability to address and ultimately solve such open questions in biology often depends on the development of novel technologies that lead to new experimental approaches, and researchers in the flowering field have always quickly adopted new methods whenever they appeared pertinent. For example, the use of advanced life imaging techniques has yielded unprecedented insights into the cellular and mechanical dynamics during floral organogenesis (Hervieux et al, 2016;Prunet et al, 2016).…”

A Model Analysis of Mechanisms for Radial Microtubular Patterns at Root Hair Initiation Sites

“…Mechanical stresses and strains could serve that purpose. Mechanical stresses in the walls have been suggested to provide a directional signal where cortical microtubules orient along the maximal principal stress direction (Hejnowicz et al, 2000), both at the tissue and at the subcellular levels in shoots, leaves and flowers in Arabidopsis (Hamant et al, 2008; Sampathkumar et al, 2014; Hervieux et al, 2016). Such feedback loop between stress and direction of material anisotropy has been implemented in models which have verified its ability to produce robust regulation of anisotropic growth (Bozorg et al, 2014).…”

Regulation of plant cell wall stiffness by mechanical stress: a mesoscale physical model

“…Existing modeling efforts assessing the feedback mechanism between mechanics and growth in plant tissues rely on a phenomenological black box to express the influence of stress on cell wall stiffness (Hamant et al, 2008;Bozorg et al, 2014;Hervieux et al, 2016). This work is an effort to open this black box by making a first step toward a more quantitative, mechanistic, multiscale analysis of stress-based feedback.…”

“…This allows a reasonable trade-off between modeling expressiveness and computational complexity, but fails at representing efficiently a number of specific properties of higher-dimensional mechanics (Gelder, 1998), such as shear, incompressibility, and anisotropy. To alleviate this difficulty, other authors have adapted the formalism of continuous media to growth (Dumais et al, 2006;Goriely and Amar, 2007;Dyson and Jensen, 2010;Rojas et al, 2011;Fozard et al, 2013;Sassi et al, 2014;Boudon et al, 2015;Bozorg et al, 2016;Hervieux et al, 2016). Boudon et al and Bozorg et al.…”

“…In this approach, stress feedback is taken into account by modulating spring constants according to the angle between the spring and the cells average loading axis. Other authors have instead used a continuous formalism, expressing a coupling between multidimensional stiffness and stress, in Bozorg et al (2014), through triangular biquadratic springs (Delingette, 2008) and in Hervieux et al (2016), through the finite element method (FEM). In the last two implementations, stress is considered as an input-parameter that modulates the main axis of stiffness and its anisotropy.…”