Mechanical regulation of organ asymmetry in leaves

Abstract

How appendages, such as plant leaves or animal limbs, develop asymmetric shapes remains a fundamental question in biology. Although ongoing research has revealed the genetic regulation of organ pattern formation, how gene activity ultimately directs organ shape remains unclear. Here, we show that leaf dorsoventral (adaxial-abaxial) polarity signals lead to mechanical heterogeneity of the cell wall, related to the methyl-esterification of cell-wall pectins in tomato and Arabidopsis. Numerical simulations predicate that mechanical heterogeneity is sufficient to produce the asymmetry seen in planar leaves. Experimental tests that alter pectin methyl-esterification, and therefore cell wall mechanical properties, support this model and lead to polar changes in gene expression, suggesting the existence of a feedback mechanism for mechanical signals in morphogenesis. Thus, mechanical heterogeneity within tissue may underlie organ shape asymmetry.

A wall with integrity: surveillance and maintenance of the plant cell wall under stress

“…The primary wall of growing cells is a three-dimensional dynamic network composed of cellulose, hemicelluloses, pectins and a small amount of structural proteins (Somerville et al, 2004;Cosgrove, 2005;Lampugnani et al, 2018). Pectin chemistrysuch as HG de-methylesterification, Ca 2+ -mediated HG crosslinking, and borate crosslinking of RG-IIaffects the stiffness of the wall and, as a result, cell and organ growth (O'Neill et al, 2001;Peaucelle et al, 2008Peaucelle et al, , 2011Peaucelle et al, , 2015Qi et al, 2017;Rui et al, 2017;Bou Daher et al, 2018). Each cellulose microfibril is composed of b-1,4-linked glucan chains synthesized at the cell surface by cellulose synthase (CESA) complexes (CSCs), which are highly mobile membrane proteins (Paredez et al, 2006;McFarlane et al, 2014;Kieber & Polko, 2019).…”

“…Their major structural domains include homogalacturonan (HG), rhamnogalacturonan-I (RG-I), and rhamnogalacturonan-II (RG-II) (Atmodjo et al, 2013). Pectin chemistrysuch as HG de-methylesterification, Ca 2+ -mediated HG crosslinking, and borate crosslinking of RG-IIaffects the stiffness of the wall and, as a result, cell and organ growth (O'Neill et al, 2001;Peaucelle et al, 2008Peaucelle et al, , 2011Peaucelle et al, , 2015Qi et al, 2017;Rui et al, 2017;Bou Daher et al, 2018). In addition, evidence from solid-state nuclear magnetic resonance (ssNMR) studies reveals that RG-I and a portion of HG interact with cellulose non-covalently (Wang et al, 2012(Wang et al, , 2015, but the nature and mechanical effect of these interactions are not yet clear (Cosgrove, 2018).…”

On the electrophoretic mobilities of partially charged oligosaccharides as a function of charge patterning and degree of polymerization

“…This work focuses on calculating the electrophoretic mobilities of fully or partially charged oligogalacturonide species as a function of charge patterning and degree of polymerization. This choice was motivated by the prior existence of data for several of these fragments, generated from the digestion of pectin by endo‐polygalacturonse II (endo‐PG II) from Aspergillus niger and their importance for many areas of plant science .…”

A microtubule-mediated mechanical feedback controls leaf blade development in three dimensions

“…The models of leaf development proposed in the literature --e.g. (7,11,12) -10 -are in 2 dimensions. Therefore, out-of-plane walls are not taken into account, although they could significantly impact the mechanics of the system.…”

“…According to our model, once asymmetry is established in a primordium, the CMTmediated mechanical feedback would amplify the asymmetry to form a plenary leaf blade. Initial 9 symmetry breaking can result from the asymmetric gene expression patterns at the shoot meristem, and likely involves asymmetric patterns of cell wall stiffness and expansion during early stages of development, in particular at the leaf margins (12,24,25).…”