One thousand and one oscillators at the pollen tube tip: The quest for a central pacemaker revisited

Abstract

Pollen tube growth and oscillations constitute a prime system to study polarized cell growth, warranting the expansion of mathematical models in recent years. Although it is unlikely to have a myriad of distinct independent oscillators at the pollen tube tip, the tendency to describe as many new oscillators as there are objects of study is likely to continue. The same process has happened for over 60 years of studies in circadian rhythms and, similarly, in other biological phenomena displaying oscillatory behavior. Here, we take the opportunity to revise pollen tube oscillator models with cautionary tales learned in other systems. Currently the nature of the core negative feedback loop generating the oscillations, as well as the role and regulation of Ca2+ and growth, seems elusive. The vast majority of mathematical models assume that intracellular Ca2+ is primarily controlled by stretch-activated channels and, thus, relies on membrane tension and growth. Counterpoints to these canonical assumptions will be given as to evidence the gaps in achieving a comprehensive view of pollen tube oscillations. Finally, inspiration stemming from systems involving intracellular polarity and chemotaxis motivates a proposal for the existence of two putatively coupled and yet distinct oscillatory systems involved in pollen tube growth: A signaling-based oscillator at the tip and a motion-based oscillator at the shank, which could be coupled by intracellular signals as Ca2+waves. This proposition may account for the oscillations observed in nongrowing tubes, as both oscillators could be uncoupled in certain regimes, resolving the conundrum entailed by current model.