Anisotropic growth is achieved through the additive mechanical effect of material anisotropy and elastic asymmetry

Abstract

Fast directional growth is a necessity for the young seedling; after germination, it needs to quickly penetrate the soil to begin its autotrophic life. In most dicot plants, this rapid escape is due to the anisotropic elongation of the hypocotyl, the columnar organ between the root and the shoot meristems. Anisotropic growth is common in plant organs and is canonically attributed to cell wall anisotropy produced by oriented cellulose fibers. Recently, a mechanism based on asymmetric pectin-based cell wall elasticity has been proposed. Here we present a harmonizing model for anisotropic growth control in the dark-grown Arabidopsis thaliana hypocotyl: basic anisotropic information is provided by cellulose orientation) and additive anisotropic information is provided by pectin-based elastic asymmetry in the epidermis. We quantitatively show that hypocotyl elongation is anisotropic starting at germination. We present experimental evidence for pectin biochemical differences and wall mechanics providing important growth regulation in the hypocotyl. Lastly, our in silico modelling experiments indicate an additive collaboration between pectin biochemistry and cellulose orientation in promoting anisotropic growth.

Disentangling loosening from softening: insights into primary cell wall structure

“…Coupling of indentation mechanics with tensile mechanics is often assumed, though not actually measured, in studies that attempt to connect the results of surface indentation assays to growth and development (Peaucelle et al ., ; Milani et al ., ; Braybrook and Jonsson, ; Bou Daher et al ., ). Our results provide examples where changes in indentation properties did not correlate with changes in tensile stiffness and creep.…”

“…Other studies correlated changes in homogalacturonan esterification in vivo with changes in cell growth and wall stiffness as probed by surface indentation (e.g. Peaucelle et al ., , ; Bou Daher et al ., ). Tensile compliances of the wall were not actually measured in these latter studies and changes in homogalacturonan esterification may be accompanied by other changes that impact wall structure and mechanics.…”

“…Indentations of living cells may be influenced by turgor pressure which pre‐stresses and stiffens the wall in a manner dependent on cell geometry (Forouzesh et al ., ; Beauzamy et al ., ; Weber et al ., ). Indentations may also be sensitive to the presence of anticlinal walls of the epidermis and underlying cell layers (Peaucelle et al ., ; Bou Daher et al ., ) and to connections with neighboring cells (Mosca et al ., ). Moreover, forces applied to living cells induce hydraulic flows that may influence cell and tissue deformations.…”

Modeling the nonlinear elastic behavior of plant epidermis

“…The outcome of the mechanical assessment of plant cells and tissues has led to insight on cellgrowth-related features such as mechanical anisotropy of the cell wall and enzymatic activity. Many studies have attempted to correlate the subcellular mechanical behavior of the cell wall with cell growth (Bolduc et al 2006;Fayant et al 2010;Sanati Nezhad et al 2013;Carter et al 2017) or, at a larger scale, with tissue growth and organogenesis (Braybrook and Peaucelle 2013;Peaucelle et al 2015;Bou Daher et al 2018). Experimental strategies to study the mechanics of primary plant cells and tissue mostly rely on the application of some type of force and examining the response of the tissue.…”

Deviating from the Beaten Track: New Twists in Brassinosteroid Receptor Function

“…However, the cell wall also feeds back on BR signalling [153]. The state of pectin, an important component of the plant cell wall and a dynamic regulator of its properties [154][155][156][157], is relayed to the BR receptor complex by RECEPTOR-LIKE PROTEIN44 (RLP44), which directly interacts with both BRI1 and BAK1, likely acting as a scaffold to promote their association [103,158,159]. In line with this notion, RLP44 is sufficient to promote BR signalling, at least partially independent of BRs [103].…”