Polar growth in pollen tubes is associated with spatially confined dynamic changes in cell mechanical properties

Abstract

Cellular morphogenesis involves changes to cellular size and shape which in the case of walled cells implies the mechanical deformation of the extracellular matrix. So far, technical challenges have made quantitative mechanical measurements of this process at subcellular scale impossible. We used micro-indentation to investigate the dynamic changes in the cellular mechanical properties during the onset of spatially confined growth activities in plant cells. Pollen tubes are cellular protuberances that have a strictly unidirectional growth pattern. Micro-indentation of these cells revealed that the initial formation of a cylindrical protuberance is preceded by a local reduction in cellular stiffness. Similar cellular softening was observed before the onset of a rapid growth phase in cells with oscillating growth pattern. These findings provide the first quantitative cytomechanical data that confirm the important role of the mechanical properties of the cell wall for local cellular growth processes. They are consistent with a conceptual model that explains pollen tube oscillatory growth based on the relationship between turgor pressure and tensile resistance in the apical cell wall. To further confirm the significance of cell mechanics, we artificially manipulated the mechanical cell wall properties as well as the turgor pressure. We observed that these changes affected the oscillation profile and were able to induce oscillatory behavior in steadily growing tubes.

PECTIN METHYLESTERASE48 Is Involved in Arabidopsis Pollen Grain Germination

“…The reduction of PME48 activity also has consequences later on pollen tube morphology. The pollen tubes are slightly wider in the mutant, which may reflect the role of HG in the mechanical properties of the cell wall (Parre and Geitmann, 2005a;Palin and Geitmann, 2012) and corroborates the predictions made by mechanical simulations (Chebli and Geitmann, 2007;Zerzour et al, 2009;Fayant et al, 2010). The more abundant highly methylesterified HG in the intine wall of pme482/2 pollen grains and at the tip and in the subapical region of pme482/2 pollen tubes provides more viscoelasticity and less rigidity of the cell wall, thus promoting several tips emerging from the pollen grain and wider diameters of pollen tubes, probably due to the internal turgor pressure (Parre and Geitmann, 2005a;Winship et al, 2010).…”

Finite Element Modeling of Shape Changes in Plant Cells

“…This result is consistent with the effect of the pectinase-mediated digestion of pectin, which results in a dramatic apical swelling of the pollen tube (Parre and Geitmann, 2005), presumably through the loss of the modulus gradient. It also accords well with mechanical measurements revealing that the cell wall at the tip of the growing pollen tube is softer and modulates its properties to generate an oscillatory growth pattern (Zerzour et al, 2009). The reciprocation between predictions made by the in silico FE model, experimental validation, refinement of the model, and guidance toward further biological experimentation illustrates the value of FE in the predictive modeling of cell development.…”

“…The wall of the growing pollen tube was represented with a shell of uniform thickness (Box 2) but spatially varying material properties. The apical dome was divided into hoop-shaped subregions in which the elastic modulus (Box 3; Boudaoud, 2010;Dumais, 2013;Niklas, 1992;Huang et al, 2012;Julkunen et al, 2007;Kha et al, 2010;Sun, 2006;Zerzour et al, 2009) could be assigned independently ( Fig. 2A).…”

Self-regulation in tip-growth: The role of cell wall ageing

“…Nevertheless, we may hope that a combination of micromechanical (see e.g. Zerzour et al, 2009) and biochemical (see e.g. Fayant et al, 2010) measurements that probe the local properties of the wall with quantitative measurement on the local rate of exocytosis (see e.g.…”