Cell division plane orientation based on tensile stress inArabidopsis thaliana

Abstract

Cell geometry has long been proposed to play a key role in the orientation of symmetric cell division planes. In particular, the recently proposed Besson-Dumais rule generalizes Errera's rule and predicts that cells divide along one of the local minima of plane area. However, this rule has been tested only on tissues with rather local spherical shape and homogeneous growth. Here, we tested the application of the Besson-Dumais rule to the divisions occurring in the Arabidopsis shoot apex, which contains domains with anisotropic curvature and differential growth. We found that the Besson-Dumais rule works well in the central part of the apex, but fails to account for cell division planes in the saddle-shaped boundary region. Because curvature anisotropy and differential growth prescribe directional tensile stress in that region, we tested the putative contribution of anisotropic stress fields to cell division plane orientation at the shoot apex. To do so, we compared two division rules: geometrical (new plane along the shortest path) and mechanical (new plane along maximal tension). The mechanical division rule reproduced the enrichment of long planes observed in the boundary region. Experimental perturbation of mechanical stress pattern further supported a contribution of anisotropic tensile stress in division plane orientation. Importantly, simulations of tissues growing in an isotropic stress field, and dividing along maximal tension, provided division plane distributions comparable to those obtained with the geometrical rule. We thus propose that division plane orientation by tensile stress offers a general rule for symmetric cell division in plants.cell division plane | mechanical forces | meristem | vertex model | Arabidopsis

Forces behind plant cell division

“…Previous investigation from the same group had inferred the presence of strong tensional stresses along the axis of the crease (10). The alignment of the division planes with the direction of maximal tension and not with the shorter axis of the cell has led Louveaux et al (9) to conclude that stress is a better predictor of the orientation of the division plane in this region. To test more specifically the role of stresses in directing cell division, Louveaux et al (9) proceeded to produce lesions within the central region of the meristem, where the least-area division rule is normally a robust predictor of division plane orientation.…”

“…Louveaux et al (9) present two new experimental results indicating that wall tension is important in determining the position of the division plane. Their first result emerges from a careful analysis of cell division within distinct regions of the Arabidopsis inflorescence meristem.…”

“…The alignment of the division planes with the direction of maximal tension and not with the shorter axis of the cell has led Louveaux et al (9) to conclude that stress is a better predictor of the orientation of the division plane in this region. To test more specifically the role of stresses in directing cell division, Louveaux et al (9) proceeded to produce lesions within the central region of the meristem, where the least-area division rule is normally a robust predictor of division plane orientation. To their surprise, the authors found that divisions were now redirected to be mostly parallel to the free edges created by the lesion, irrespective of cell geometry.…”

“…It is thought that a substantial fraction of this "inner pressure" is transferred to the cells of the tunica (11,12). Because there is no way for the cell to distinguish between the two sources of stresses-both are experienced as tensions within the wall-Louveaux et al (9) suggest that the cell will align its division plane with the direction of greatest tension as a whole. This hypothesis immediately raises two questions that will have to be answered fully before we can safely say that tensional forces within the cell wall are what align the division planes of plant cells.…”

“…Thus, the two theories may have more in common mechanistically than might be expected at first sight. With their work, Louveaux et al (9) have managed to bring wall stresses to the forefront of cell biology. Even though many details remain to be ironed out, future studies of plant cell division cannot neglect stresses as a possible contributor to the cell-division process.…”