Spatial and temporal integration of signalling networks regulating pollen tube growth

Abstract

The overall function of a cell is determined by its contingent of active signal transduction cascades interacting on multiple levels with metabolic pathways, cytoskeletal organization, and regulation of gene expression. Much work has been devoted to analysis of individual signalling cascades interacting with unique cellular targets. However, little is known about how cells integrate information across hierarchical signalling networks. Recent work on pollen tube growth indicates that several key signalling cascades respond to changes in cell hydrodynamics and apical volume. Combined with known effects on cytoarchitecture and signalling from other cell systems, hydrodynamics has the potential to integrate and synchronize the function of the broader signalling network in pollen tubes. This review will explore recent work on cell hydrodynamics in a variety of systems including pollen, and discuss hydrodynamic regulation of cell signalling and function including exocytosis and endocytosis, actin cytoskeleton reorganization, cell wall deposition and assembly, phospholipid and inositol polyphosphate signalling, ion flux, small G-proteins, fertilization, and self-incompatibility. The combined data support a newly emerging model of pollen tube growth.

FIMBRIN1 Is Involved in Lily Pollen Tube Growth by Stabilizing the Actin Fringe

“…Recent studies show that in growing pollen tubes, the front end or leading edge of the cortical actin fringe coincides with a region forming an annulus around the pole of the pollen tube tip, which is thought to correspond to the region of highest exocytosis (Bove et al, 2008;Bou Daher and Geitmann, 2011). Therefore, the cortical actin fringe may serve as a track to target cell wall vesicles to the exocytotic sites on the apical plasma membrane (Bove et al, 2008;Zonia andMunnik, 2008, 2009;Kroeger et al, 2009;Bou Daher and Geitmann, 2011). Our data demonstrate that the cortical actin fringe has only a close connection with growth rate but does not affect the polarity of the pollen tube.…”

“…Myosin II subfragment 1 decoration and electron microscopy studies have further revealed that short and densely packed parallel actin bundles exist in the subapex of pollen tubes and are more densely packed than those in the shank (Lenartowska and Michalska, 2008). The actin fringe appears to function as the track upon which exocytic vesicles are trafficked from the actin cable to the site of exocytosis, which is independent from cytoplasmic streaming (Bove et al, 2008;Zonia andMunnik, 2008, 2009;Kroeger et al, 2009;Bou Daher and Geitmann, 2011). In the apex, the actin cytoskeleton is less abundant but more dynamic (Fu et al, 2001;Staiger et al, 2010).…”

“…On the other hand, in the apical region of the pollen tube, actin filaments reside in certain regions in association with a variety of parameters, including Ca 2+ , pH, phosphorylation, and phosphoinositides (Franklin-Tong, 1999;Cole and Fowler, 2006;Cheung and Wu, 2008;Zonia, 2010). Therefore, it is assumed that the highly ordered and dynamic actin structure in the subapex and apex is regulated spatially and temporally by several classes of ABPs whose spatiotemporal activities are regulated by specific parameters (Fu, 2010;Staiger et al, 2010).…”

The Pollen Tube Oscillator: Integrating Biophysics and Biochemistry into Cellular Growth and Morphogenesis

“…In contrast, a hydrodynamic model has been proposed to explain the mechanism for stochastic and oscillatory growth, which predicts that turgor pressure oscillates during pollen tube growth (Zonia and Munnik 2007;Zonia 2010;Zonia and Munnik 2011). According to this model, turgor pressure is more elevated at the tip compared to the shank, being able to control exocytosis, cell wall mechanical properties and growth (Zonia and Munnik 2011).…”

Molecular evidence that most RNAs required for germination and pollen tube growth are stored in the mature pollen grain in petunia

“…To achieve such a rapid growth, the pollen tube requires a high level of synthesis of the components necessary for the construction of the cytoskeleton, membranes, and cell wall polysaccharides. In addition, during rapid growth, other dynamic cellular events such as calcium oscillation, vesicle transport, and ion fluxes also occur (Cheung and Wu, 2008;Zonia, 2010). However, although many of the processes involved in pollen tube formation and growth have been described, the genes involved in these events are largely unknown.…”