Chemically Mediated Mechanical Expansion of the Pollen Tube Cell Wall

Abstract

Morphogenesis of plant cells is tantamount to the shaping of the stiff cell wall that surrounds them. To this end, these cells integrate two concomitant processes: 1), deposition of new material into the existing wall, and 2), mechanical deformation of this material by the turgor pressure. However, due to uncertainty regarding the mechanisms that coordinate these processes, existing models typically adopt a limiting case in which either one or the other dictates morphogenesis. In this report, we formulate a simple mechanism in pollen tubes by which deposition causes turnover of cell wall cross-links, thereby facilitating mechanical deformation. Accordingly, deposition and mechanics are coupled and are both integral aspects of the morphogenetic process. Among the key experimental qualifications of this model are: its ability to precisely reproduce the morphologies of pollen tubes; its prediction of the growth oscillations exhibited by rapidly growing pollen tubes; and its prediction of the observed phase relationships between variables such as wall thickness, cell morphology, and growth rate within oscillatory cells. In short, the model captures the rich phenomenology of pollen tube morphogenesis and has implications for other plant cell types.

Rice Morphology Determinant-Mediated Actin Filament Organization Contributes to Pollen Tube Growth

“…Massive secretion during cell wall formation at the pollen tube tip is critical for the incorporation of materials into the apical plasma membrane, which are subsequently retrieved by endocytic membrane recycling and cytoplasmic streaming movement (Rojas et al, 2011;Chebli et al, 2012;Grebnev et al, 2017). The pollen tube wall has a unique organization, with the growing tip consisting mainly of pectin and the flanks containing a callose layer (Bosch and Hepler, 2005).…”

“…Highly methoxylated homogalacturonans are accumulated at the apical region through exocytosis to loosen the cell wall and form the thick, soft tip wall with a lower stressyield point, allowing the pollen tube to deform more easily. Thus, as the cell wall thickens, the polar growth rate increases in the direction of the tip (McKenna et al, 2009;Zerzour et al, 2009;Rojas et al, 2011;Rounds and Bezanilla, 2013). In this process, the bidirectional reverse-fountain cytoplasmic streaming between the shank region and the subapex is presumably essential to ensure a sufficient supply of materials required for cell expansion (Cheung and Wu, 2008;Grebnev et al, 2017).…”

Finite Element Modeling of Shape Changes in Plant Cells

“…To represent a normally growing tube, the model had to produce a self-similar shape profile, and the strain pattern resulting from the deformation of the wall had to reproduce those observed experimentally (Rojas et al, 2011). Two key mechanical parameters were analyzed for their ability to shape the tube: (1) the profile of the elastic modulus gradient from tip to shank; and (2) the degree of material anisotropy expressing how different the material responds to loads applied in different directions.…”

Multiscale Systems Analysis of Root Growth and Development: Modeling Beyond the Network and Cellular Scales

“…Veytsman and Cosgrove (1998) used thermodynamic principles to relate the stiffness and yield stress to properties of the microfibril/hemicellulose network. In a study of growing pollen tubes, Rojas et al (2011) modeled a network of calcium cross-links to show how the extensibility of the pectin gel relates to its stiffness and cross-link dissociation rate; their model connects chemical and deposition kinetics to wall expansion rates. Building on the conceptual framework of Passioura and Fry (1992), Dyson et al (2012) used transient viscoelastic network theory to describe the evolution of hemicellulose cross-links in an elongating cell wall, recovering yielding behavior reminiscent of a Lockhart model.…”