Growth directions and stiffness across cell layers determine whether tissues stay smooth or buckle

Abstract

From smooth to buckled, nature exhibits organs of various shapes and forms. How cellular growth patterns produce smooth organ shapes like those of leaves and sepals remains unclear. Here we show that unidirectional growth and comparable stiffness across both epidermal layers of Arabidopsis sepals are essential for smoothness. We identified a mutant with ectopicASYMMETRIC LEAVES 2(AS2) expression that exhibits buckles on the outer epidermis due to conflicting growth directions and unequal epidermal stiffnesses. Aligning growth direction and increasing stiffness restores smoothness. Furthermore, buckling generates outgrowth by influencing auxin efflux transporter protein PIN-FORMED 1 polarity, indicating buckling can initiate organogenesis. Our findings suggest that in addition to molecular cues influencing tissue mechanics, tissue mechanics can also modulate molecular signals, giving rise to well-defined shapes.One-Sentence SummaryThe keys to unlocking sepal smoothness are unidirectional growth and even stiffness; misplace them, it’s time to buckle up!

Modulation of cell differentiation and growth dynamics underlie the shift from bud protection to light capture in cauline leaves

“…However, such growth dynamics is characteristic for some floral organs, such as petals and filaments of the stamen Sauret-Güeto et al, 2013;. The genetic factors driving late-stage acceleration in growth remain unclear but phytohormones such as auxin, jasmonate, and gibberellins are believed to be key players, especially in the growth resumption of the stamen (Nagpal et al, 2005;Reeves et al, 2012;Cecchetti et al, 2013;Huang et al, 2020;He et al, 2023). Given the genetic proximity between cauline leaves and floral organs (Krizek and Meyerowitz, 1996;Pelaz et al, 2001), it would be interesting to investigate whether similar mechanisms govern cauline leaf development to help fulfill its dual function.…”

“…The delay of differentiation combined with the distally localized growth in the early cauline leaf may help to prevent its early unfolding. While the mechanism underlying this change in curvature remains unclear, current evidence suggests that it likely involves differential growth between both organ surfaces (Zhao et al, 2020; Jiao et al, 2021; Yadav et al, 2023). Such growth asymmetry might be controlled by the differential gene expression during the establishment of organ polarity.…”

Multiple feedbacks on self‐organized morphogenesis during plant regeneration

“…For instance, disruptions in PIN1 localization patterns and ensuing biochemical changes impact the mechanical characteristics of cells surrounding the progenitor (Varapparambath et al ., 2022). Such reciprocal interactions are necessary for morphogenesis, and they are also observed during normal development (Yadav et al ., 2023). For instance, during tissue bending (Jonsson et al ., 2021), shoot meristem patterning (Hamant et al ., 2008; Uyttewaal et al ., 2010; Robinson et al ., 2013), emergence of the leaf or flower primordia (Heisler et al ., 2010; Nakayama et al ., 2012), or the LRP (Vermeer et al ., 2014), mechanochemical feedback loops are at play.…”

“…This concept diverged from Turing's reaction–diffusion model, which hinges on morphogen‐driven spatial cues to orchestrate organogenesis (Green, 1992; Selker et al ., 1992). Over the years, mechanical instabilities, such as buckling, folding, or wrinkling, have been incorporated into reaction–diffusion models, during morphogenesis in developing tissues (Shyer et al ., 2015; Yadav et al ., 2023). Interestingly, avian skin patterning's mechanical phenomena resonate with Turing's chemical patterning models, with cellular contractility serving as a local activator and substrate stiffness as a long‐range inhibitor (Shyer et al ., 2017).…”