Abstract
Sexual reproduction in higher plants relies upon the polarised growth of pollen tubes. The growth-site at the pollen tube tip responds to signalling processes to successfully steer the tube to an ovule. Essential features of pollen tube growth are polarisation of ion fluxes, intracellular ion gradients, and oscillating dynamics. However, little is known about how these features are generated and how they are causally related. We propose that ion dynamics in biological systems should be studied in an integrative and self-regulatory way. Here we have developed a two-compartment model by integrating major ion transporters at both the tip and shank of pollen tubes. We demonstrate that the physiological features of polarised growth in the pollen tube can be explained by the localised distribution of transporters at the tip and shank. Model analysis reveals that the tip and shank compartments integrate into a self-regulatory dynamic system, however the oscillatory dynamics at the tip do not play an important role in maintaining ion gradients. Furthermore, an electric current travelling along the pollen tube contributes to the regulation of ion dynamics. Two candidate mechanisms for growth-induced oscillations are proposed: the transition of tip membrane into shank membrane, and growth-induced changes in kinetic parameters of ion transporters. The methodology and principles developed here are applicable to the study of ion dynamics and their interactions with other functional modules in any plant cellular system.
Highlights
Higher plants reproduce sexually by using the male gametophyte to grow rapidly through sporophytic pistil tissue to effect double-fertilization of the embryo sac, and produce seed
Following the principles for developing compartmental models which are described in the Data S1 in the Supporting Information and using the wealth of biological data on pollen tube growth, we have developed a tip-shank two-compartment model to study ion dynamics and growth and how these are related (Figure 1)
It is known that the tip and shank of a pollen tube possess the following main properties [11,12]: a) ion fluxes across the plasma membrane at the tip and shank are polarised; b) intracellular ion gradients are established between the tip and shank; c) the pollen tube tip possesses the property of oscillatory ion and growth dynamics; and d) the pollen tube shank possesses the property of nonoscillatory ion and growth dynamics
Summary
Higher plants reproduce sexually by using the male gametophyte (the pollen grain) to grow rapidly through sporophytic pistil tissue to effect double-fertilization of the embryo sac, and produce seed. This involves growth of a pollen tube using directional, polar tip growth. Molecular signals affect the position of the polarised growth site and guide the direction of tip growth Interpretation of these signals requires a plethora of proteins and other molecules (recently named the LENS: Localisation Enhancing Network, Selfsustaining [1]). Protein ion transporters and ion channels regulate oscillatory and non-oscillatory flow at both the tip and shank; their influence on flux is likely to be dictated by their sub-cellular distribution, activation and gating properties
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