Cellular oscillations and the regulation of growth: the pollen tube paradigm

Abstract

The occurrence of oscillatory behaviours in living cells can be viewed as a visible consequence of stable, regulatory homeostatic cycles. Therefore, they may be used as experimental windows on the underlying physiological mechanisms. Recent studies show that growing pollen tubes are an excellent biological model for these purposes. They unite experimental simplicity with clear oscillatory patterns of both structural and temporal features, most being measurable during real-time in live cells. There is evidence that these cellular oscillators involve an integrated input of plasma membrane ion fluxes, and a cytosolic choreography of protons, calcium and, most likely, potassium and chloride. In turn, these can create positive feedback regulation loops that are able to generate and self-sustain a number of spatial and temporal patterns. Other features, including cell wall assembly and rheology, turgor, and the cytoskeleton, play important roles and are targets or modulators of ion dynamics. Many of these features have similarities with other cell types, notably with apical-growing cells. Pollen tubes may thus serve as a powerful model for exploring the basis of cell growth and morphogenesis. BioEssays 23:86-94, 2001.

Calcium‐regulated anion channels in the plasma membrane of Lilium longiflorum pollen protoplasts

“…Non-oscillatory ionic fluxes of typical permeable ions in cells, such as H + , Ca 2+ , K + and Cl ) , have been observed from the grain and along the tube shank, while the tip zone displays distinctive oscillatory fluxes for the same ions, and usually in the reverse direction to that on the shank (Feijó et al, 1999;Moreno et al, 2007). These oscillatory fluxes have been shown to be essential to tube growth and show a similar period of oscillation to that of growth, although with distinct phase delays (Holdaway-Clarke et al, 1997;Messerli et al, 1999;Feijó et al, 2001;Zonia et al, 2002;Holdaway-Clarke & Hepler, 2003). Early studies by Weisenseel & Jaffe (1976) demonstrated that pollen tube germination and growth have an absolute requirement for extracellular K + , Ca 2+ , a trace of boron, and a somewhat acidic pH.…”

“…The use of noninvasive methods has demonstrated a close link between intracellular ion fluctuations and ionic fluxes across the plasma membrane, and the cellular phenomena that occur during the formation and elongation of the pollen tube (Mascarenhas, 1993;Feijó et al, 1995Feijó et al, , 2001Feijó et al, , 2004Cheung, 1996;Hepler et al, 2001). For example, oscillatory H + gradients have been shown to exist and to be intimately associated with polarized pollen tube growth.…”

“…Several groups have detected the presence of [Ca 2+ ] tip focused gradients (e.g. Holdaway-Clarke et al, 1997;Feijó et al, 2001;Holdaway-Clarke & Hepler, 2003;Michard et al, 2009). Additionally, ion-specific self-referencing electrodes have been used to study ionic fluxes during pollen New Phytologist Research tube growth, demonstrating an uneven distribution of the different fluxes.…”

Gravity Research on Plants: Use of Single-Cell Experimental Models

“…Temporal and spatial control of the vesicle fusion responsible for cell wall assembly at the growing tip is required to determine the rate and direction of growth (Fayant et al, 2010). The influx of calcium through plasma membrane located calcium channels at the tip of the cells plays an important role in the temporal and spatial regulation of the growth process (Hepler, 1997; Feijó et al, 2001; Chebli and Geitmann, 2007). Exocytosis in the tip region is accompanied by membrane endocytosis to ensure a balanced deposition rate of cell wall and membrane material.…”

Dissecting the regulation of pollen tube growth by modeling the interplay of hydrodynamics, cell wall and ion dynamics

“…The pollen tube is a model system for the study of tip growth in plants (Feijo et al, 2001). Essential features of pollen tube growth are polarization of ion fluxes, intracellular ion gradients, and oscillating dynamics.…”