Uncoupling secretion and tip growth in lily pollen tubes: evidence for the role of calcium in exocytosis

Roy, Stéphane; Holdaway‐Clarke, Terena L.; Hackett, Grant; Kunkel, Joseph G.; Lord, Elizabeth M.; Hepler, Peter K.

doi:10.1046/j.1365-313x.1999.00515.x

Cited by 103 publications

(75 citation statements)

References 38 publications

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“…These two events are thus as much as 1408 out of phase, and yet it is a paradigm in plant and animal cells (Battey et al, 1999), including pollen tubes (Roy et al, 1999;Camacho and Malhó , 2003), that Ca 2+ stimulates secretion. How do we explain this apparent lack of correlation between Ca 2+ and secretion?…”

Section: Oscillation Of the Intracellular [Ca 2+ ] Does Not Regulate mentioning

confidence: 99%

“…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%

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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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Section: Oscillation Of the Intracellular [Ca 2+ ] Does Not Regulate mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

et al. 2009

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“…Alternative energyproducing machinery may be induced to some degree upon a Ca 2+ -CaM signaling deficiency that allows FM endocytic uptake, in accordance with an up-regulated PDC bypass as the energy source for FM internalization (Parton et al, 2001;Gass et al, 2005). In contrast, accumulating evidence has confirmed that the dissipation of the tip-focused Ca 2+ gradient may contribute to the decrease in vesicle accumulation and fusion (Roy et al, 1999). We found a gradual decrease in AcPase activity and a differential display of secretory pathway-related proteins (spots 12 and 57), providing direct evidence for reduced exocytic vesicular trafficking in TFP-treated pollen tubes.…”

Section: Proteins Involved In Cellular Structure/secretory Pathway Asmentioning

confidence: 99%

“…It is well accepted that Ca 2+ has a profound effect on the oriented transport of vesicles toward the cell wall in the extreme pollen tube tip (Roy et al, 1999). Rapid turnover of the intracellular pool of UDPG has been reported during pollen tube elongation, which attests to the metabolic specialization of pollen tubes for rapid wall synthesis (Gibeaut, 2000).…”

Section: Proteins Involved In Polysaccharide Synthesis As the Tertiarmentioning

confidence: 99%

Combined Proteomic and Cytological Analysis of Ca2+-Calmodulin Regulation inPicea meyeriPollen Tube Growth

Chen

et al. 2008

Plant Physiology

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Ca 2+ -calmodulin (Ca 2+ -CaM) is a critical molecule that mediates cellular functions by interacting with various metabolic and signaling pathways. However, the protein expression patterns and accompanying serial cytological responses in Ca 2+ -CaM signaling deficiency remain enigmatic. Here, we provide a global analysis of the cytological responses and significant alterations in protein expression profiles after trifluoperazine treatment in Picea meyeri, which abrogates Ca 2+ -CaM signaling. Ninety-three differentially displayed proteins were identified by comparative proteomics at different development stages and were assigned to different functional categories closely related to tip growth machinery. The inhibition of Ca 2+ -CaM signaling rapidly induced an increase in extracellular Ca 2+ influx, resulting in dramatically increased cytosolic Ca 2+ concentrations and ultrastructural abnormalities in organelles as the primary responses. Secondary and tertiary alterations included actin filament depolymerization, disrupted patterns of endocytosis and exocytosis, and cell wall remodeling, ultimately resulting in perturbed pollen tube extension. In parallel with these cytological events, time-course experiments revealed that most differentially expressed proteins showed time-dependent quantitative changes (i.e. some signaling proteins and proteins involved in organelle functions and energy production changed first, followed by alterations in proteins related to cytoskeletal organization, secretory pathways, and polysaccharide synthesis). Taken together, Ca 2+ -CaM dysfunction induced serial cytological responses and temporal changes in protein expression profiles, indicating the pivotal role of Ca 2+ -CaM in the regulation of tip growth machinery.

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“…A number of Ca 2+ -regulated cellular activities, such as cytoskeleton dynamics, exocytosis, and endocytosis, are directly or indirectly involved in the regulation of pollen tube growth (Roy et al, 1999;Hwang et al, 2005;Helling et al, 2006;Konrad et al, 2011). Based on the observation that Ca 2+ is known to regulate the activity of ion channels in many other physiological processes, Ca 2+ and its downstream components are assumed to play crucial roles in modulating ion channel activity during pollen tube growth.…”

Section: Introductionmentioning

confidence: 99%

Ca2+-Dependent Protein Kinase11 and 24 Modulate the Activity of the Inward Rectifying K+ Channels inArabidopsisPollen Tubes

et al. 2013

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Potassium (K+) influx into pollen tubes via K+ transporters is essential for pollen tube growth; however, the mechanism by which K+ transporters are regulated in pollen tubes remains unknown. Here, we report that Arabidopsis thaliana Ca2+-dependent protein kinase11 (CPK11) and CPK24 are involved in Ca2+-dependent regulation of the inward K+ (K+ in) channels in pollen tubes. Using patch-clamp analysis, we demonstrated that K+ in currents of pollen tube protoplasts were inhibited by elevated [Ca2+]cyt. However, disruption of CPK11 or CPK24 completely impaired the Ca2+-dependent inhibition of K+ in currents and enhanced pollen tube growth. Moreover, the cpk11 cpk24 double mutant exhibited similar phenotypes as the corresponding single mutants, suggesting that these two CDPKs function in the same signaling pathway. Bimolecular fluorescence complementation and coimmunoprecipitation experiments showed that CPK11 could interact with CPK24 in vivo. Furthermore, CPK11 phosphorylated the N terminus of CPK24 in vitro, suggesting that these two CDPKs work together as part of a kinase cascade. Electrophysiological assays demonstrated that the Shaker pollen K+ in channel is the main contributor to pollen tube K+ in currents and acts as the downstream target of the CPK11-CPK24 pathway. We conclude that CPK11 and CPK24 together mediate the Ca2+-dependent inhibition of K+ in channels and participate in the regulation of pollen tube growth in Arabidopsis.

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Uncoupling secretion and tip growth in lily pollen tubes: evidence for the role of calcium in exocytosis

Abstract: SummaryCytoplasmic calcium concentration ([Ca 2+ ] i ) and extracellular calcium (Ca

Cited by 103 publications

References 38 publications

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

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

Combined Proteomic and Cytological Analysis of Ca2+-Calmodulin Regulation inPicea meyeriPollen Tube Growth

Ca2+-Dependent Protein Kinase11 and 24 Modulate the Activity of the Inward Rectifying K+ Channels inArabidopsisPollen Tubes

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