The pollen tube oscillator: Integrating biophysics and biochemistry into cellular growth and morphogenesis

Abstract

Individual cells generate ultradian rhythms in different systems and levels of organisation. A cell biology approach is necessary to better understand the intrinsic nature of these biological oscillators and their evolutionary significance. In this respect, pollen tubes provide a useful working model because, unlike other cells, their growth can be conveniently followed in vitro and it is known to involve structural, biochemical as well as biophysical oscillations. As commonly seen in complex systems, these oscillations involve almost all cellular components but, in this case, their causal relations have not yet been fully identified. Most studies consider growth as a reference to establish the relation with other oscillating variables, interpreted to be a cause if its peak occurs before and as a consequence if it occurs after that of the variable in question. Today, it is known that this group of oscillating variables include at least ion fluxes and internal free concentrations (calcium, chloride, protons and potassium), the cytoskeleton, membrane trafficking and cell wall synthesis. Despite the progress made in this domain, however, a central core-controlling mechanism is still missing, and even less is known about how all components interact to produce the macroscopic outcome, i.e. structurally and temporally organised apical growth. In other words, we can see the arms of the clock and many underlying moving parts but still miss which work as pendulum, escapement and anchor. Here, we review the recent advances in this field and critically address some of the pitfalls and inconsistencies in the data and models presently available. Some conceptual outlines and future directions of research are also discussed.