A cytoplasmic gradient of Ca2+ is correlated with the growth of lily pollen tubes

Rathore, Keerti S.; Cork, R. J.; Robinson, Kenneth R.

doi:10.1016/0012-1606(91)90278-b

Cited by 196 publications

(142 citation statements)

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“…A cytosolic Ca 21 gradient as well as its oscillation is considered to play a central role in the regulation of pollen germination and tube growth (Rathore et al, 1991;Miller et al, 1992;Pierson et al, 1994;Malhó and Trewavas, 1996; Holdaway-Clarke et al, 1997; for review, see Feijó et al, 1995;Holdaway-Clarke and Hepler, 2003). Several lines of evidence suggest that PM Ca 21 channels may be prominently involved in the regulation of this Ca 21 gradient (Pierson et al, 1994(Pierson et al, , 1996Malhó et al, 1995).…”

Section: Discussionmentioning

confidence: 99%

“…It is well known that extracellular Ca 21 is required for pollen germination and tube growth (for review, see Steer and Steer, 1989;Taylor and Hepler, 1997;Malhó , 1998;Franklin-Tong, 1999), which indicates a possible involvement of Ca 21 influx in pollen germination and tube growth. Upon pollen hydration and germination, cytoplasmic Ca 21 concentration ([Ca 21 ] i ) at the germinal aperture where the pollen tube emerges increases to a higher level than other regions, and a tip-focused Ca 21 gradient is then established and sustained while a pollen tube grows forward (Rathore et al, 1991;Pierson et al, 1994;Feijó et al, 1995). Disruption or modification of the Ca 21 gradient inhibits pollen tube growth (Miller et al, 1992) or changes its growth direction (Malhó and Trewavas, 1996).…”

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Ca2+-Permeable Channels in the Plasma Membrane of Arabidopsis Pollen Are Regulated by Actin Microfilaments

et al. 2004

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Cytosolic free Ca 21 and actin microfilaments play crucial roles in regulation of pollen germination and tube growth. The focus of this study is to test the hypothesis that Ca 21 channels, as well as channel-mediated Ca 21 influxes across the plasma membrane (PM) of pollen and pollen tubes, are regulated by actin microfilaments and that cytoplasmic Ca 21 in pollen and pollen tubes is consequently regulated. In vitro Arabidopsis (Arabidopsis thaliana) pollen germination and tube growth were significantly inhibited by Ca 21 channel blockers La 31 or Gd 31 and F-actin depolymerization regents. The inhibitory effect of cytochalasin D (CD) or cytochalasin B (CB) on pollen germination and tube growth was enhanced by increasing external Ca 21 . Ca 21 fluorescence imaging showed that addition of actin depolymerization reagents significantly increased cytoplasmic Ca 21 levels in pollen protoplasts and pollen tubes, and that cytoplasmic Ca 21 increase induced by CD or CB was abolished by addition of Ca 21 channel blockers. By using patch-clamp techniques, we identified the hyperpolarization-activated inward Ca 21 currents across the PM of Arabidopsis pollen protoplasts. The activity of Ca 21 -permeable channels was stimulated by CB or CD, but not by phalloidin. However, preincubation of the pollen protoplasts with phalloidin abolished the effects of CD or CB on the channel activity. The presented results demonstrate that the Ca 21 -permeable channels exist in Arabidopsis pollen and pollen tube PMs, and that dynamic actin microfilaments regulate Ca 21 channel activity and may consequently regulate cytoplasmic Ca 21 .The primary function of pollen and pollen tubes is to deliver sperms to egg apparatus for double fertilization that is required for sexual reproduction of flowering plants. Pollen germination and pollen tube growth are a continuous and highly polarized process characteristic of tip growth; thus pollen and pollen tubes provide an ideal model system for the study of cell polarity control and tip growth. It is well known that extracellular Ca 21 is required for pollen germination and tube growth (for review, see Steer and Steer, 1989;Taylor and Hepler, 1997;Malhó , 1998;Franklin-Tong, 1999), which indicates a possible involvement of Ca 21 influx in pollen germination and tube growth. Upon pollen hydration and germination, cytoplasmic Ca 21 concentration ([Ca 21 ] i ) at the germinal aperture where the pollen tube emerges increases to a higher level than other regions, and a tip-focused Ca 21 gradient is then established and sustained while a pollen tube grows forward (Rathore et al., 1991;Pierson et al., 1994;Feijó et al., 1995). Disruption or modification of the Ca 21 gradient inhibits pollen tube growth (Miller et al., 1992) or changes its growth direction (Malhó and Trewavas, 1996). The tip-focused Ca 21 gradient oscillates in the pollen tubes of lily (Lilium longiflorum) and other species (Holdaway-Clarke et al., 1997;Messerli and Robinson, 1997;Messerli et al., 2000). Ca 21 mobilization from intracellular Ca...

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

Ca2+-Permeable Channels in the Plasma Membrane of Arabidopsis Pollen Are Regulated by Actin Microfilaments

et al. 2004

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“…As with serotonin, there is thought to be a soluble auxin receptor (Dharmasiri et al, 2003;Woodward and Bartel, 2005a,b). Most interestingly, auxin has been suggested to move under electrophoretic control Rathore and Goldsworthy, 1985;Rathore et al, 1988;Rathore and Robinson, 1989;Wang et al, 1989;Rathore et al, 1991;Fischer et al, 1997;Fischer-Iglesias et al, 2001;Rober-Kleber et al, 2003). Paponov et al (2005) proposed an auxin-flow canalization hypothesis: auxin flow, starting by diffusion, induces formation of polar transport system.…”

Section: Comparison To Other Morphogen Gradientsmentioning

confidence: 99%

Mathematical model of morphogen electrophoresis through gap junctions

Esser

Smith

Weaver

et al. 2006

Developmental Dynamics

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Gap junctional communication is important for embryonic morphogenesis. However, the factors regulating the spatial properties of small molecule signal flows through gap junctions remain poorly understood. Recent data on gap junctions, ion transporters, and serotonin during left-right patterning suggest a specific model: the net unidirectional transfer of small molecules through long-range gap junctional paths driven by an electrophoretic mechanism. However, this concept has only been discussed qualitatively, and it is not known whether such a mechanism can actually establish a gradient within physiological constraints. We review the existing functional data and develop a mathematical model of the flow of serotonin through the early Xenopus embryo under an electrophoretic force generated by ion pumps. Through computer simulation of this process using realistic parameters, we explored quantitatively the dynamics of morphogen movement through gap junctions, confirming the plausibility of the proposed electrophoretic mechanism, which generates a considerable gradient in the available time frame. The model made several testable predictions and revealed properties of robustness, cellular gradients of serotonin, and the dependence of the gradient on several developmental constants. This work quantitatively supports the plausibility of electrophoretic control of morphogen movement through gap junctions during early left-right patterning. This conceptual framework for modeling gap junctional signaling-an epigenetic patterning mechanism of wide relevance in biological regulation-suggests numerous experimental approaches in other patterning systems.

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“…This essential ion (Brewbaker and Kwack, 1963) forms a steep tipfocused gradient at the extreme apex of the tube (Rathore et al, 1991;Miller et al, 1992;Malhó et al, 1994;Pierson et al, 1994;Roy et al, 1999) where it may stimulate exocytosis (Battey et al, 1999;Roy et al, 1999). Further studies have revealed that the Ca 2+ gradient oscillates in magnitude with the same period as growth rate; however, it follows the increase in growth rate by 10 to 408 (Messerli et al, 2000;Cá rdenas et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

Exocytosis Precedes and Predicts the Increase in Growth in Oscillating Pollen Tubes

et al. 2009

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We examined exocytosis during oscillatory growth in lily (Lilium formosanum and Lilium longiflorum) and tobacco (Nicotiana tabacum) pollen tubes using three markers: (1) changes in cell wall thickness by Nomarski differential interference contrast (DIC), (2) changes in apical cell wall fluorescence in cells stained with propidium iodide (PI), and (3) changes in apical wall fluorescence in cells expressing tobacco pectin methyl esterase fused to green fluorescent protein (PME-GFP). Using PI fluorescence, we quantified oscillatory changes in the amount of wall material from both lily and tobacco pollen tubes. Measurement of wall thickness by DIC was only possible with lily due to limitations of microscope resolution. PME-GFP, a direct marker for exocytosis, only provides information in tobacco because its expression in lily causes growth inhibition and cell death. We show that exocytosis in pollen tubes oscillates and leads the increase in growth rate; the mean phase difference between exocytosis and growth is -988 6 38 in lily and -1248 6 48 in tobacco. Statistical analyses reveal that the anticipatory increase in wall material predicts, to a high degree, the rate and extent of the subsequent growth surge. Exocytosis emerges as a prime candidate for the initiation and regulation of oscillatory pollen tube growth.

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A cytoplasmic gradient of Ca2+ is correlated with the growth of lily pollen tubes

Cited by 196 publications

References 25 publications

Ca2+-Permeable Channels in the Plasma Membrane of Arabidopsis Pollen Are Regulated by Actin Microfilaments

Ca2+-Permeable Channels in the Plasma Membrane of Arabidopsis Pollen Are Regulated by Actin Microfilaments

Mathematical model of morphogen electrophoresis through gap junctions

Exocytosis Precedes and Predicts the Increase in Growth in Oscillating Pollen Tubes

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