Epidermal restriction confers robustness to organ shapes

Abstract

The shape of comparable tissues and organs is consistent among individuals of a given species, but how this consistency or robustness is achieved remains an open question. The interaction between morphogenetic factors determines organ formation and subsequent shaping, which is ultimately a mechanical process. Using a computational approach, we show that the epidermal layer is essential for the robustness of organ geometry control. Specifically, proper epidermal restriction allows organ asymmetry maintenance, and the tensile epidermal layer is sufficient to suppress local variability in growth, leading to shape robustness. The model explains the enhanced organ shape variations in epidermal mutant plants. In addition, differences in the patterns of epidermal restriction may underlie the initial establishment of organ asymmetry. Our results show that epidermal restriction can answer the longstanding question of how cellular growth noise is averaged to produce precise organ shapes, and the findings also shed light on organ asymmetry establishment.

A crosstalk between auxin and brassinosteroid regulates leaf shape by modulating growth anisotropy

“…Thus, epidermal BR signaling is downstream of auxin to promote proximodistal growth. This model is in line with the proposal that epidermal restriction plays an important role in organ shape determination (Kutschera and Niklas, 2007;Boudon et al, 2015;Qi et al, 2017;Zhou et al, 2020). Note that the phenotype of arf6 arf8 leaves is milder than that of the strong dwf4-102 allele, suggesting the potential involvement of additional ARF genes and other genes in regulating DWF4 expression.…”

“…ARF8 was also enriched in the floral primordium epidermis, whereas ARF6 was enriched in the epidermis of young floral primordia but was also expressed in the inner cells of older floral primordia (Figure 1G). Since epidermal restriction plays an important role in organ shape determination (Kutschera and Niklas, 2007;Boudon et al, 2015;Qi et al, 2017;Zhou et al, 2020), we speculate that epidermal auxin signaling mediated by ARF6 and ARF8 affects proximodistal growth.…”

What is quantitative plant biology?

“…is coordination involves various mechanisms ranging from mechanical stress to mobile morphogens controlled by cell-to-cell communications (e.g., Hervieux et al, 2017). Importantly, local cellular growth variability can be as well used by the plant to buffer shape variations at the organ or tissue level, as shown, for instance, during Arabidopsis sepal development (Hong et al, 2016), or leaf primordia initiation at the shoot apical meristem (Uyttewaal et al, 2012), with a primary role of the epidermis (Malivert et al, 2018;Zhou et al, 2020). Finally, shape definition during plant development is a multiscale and integrated process, which is plastic by nature.…”

What shoots can teach about theories of plant form

“…At the same time, mechanical feedback mediated by microtubules amplifies growth differences, generating variability in cell size and maintaining a robust form at the SAM 70 . A role for mechanical resistance to growth of the epidermis has also been proposed in generating robust tissue shapes 77 . A plausible hypothesis is that form emergence is not only influenced by, but also uses both structured and random changes in geometry and mechanical stress distribution as cues for the dynamic generation of form.…”