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

Feijó, José A.; Sainhas, Joaquim; Holdaway‐Clarke, Terena L.; Cordeiro, M. Sofia; Kunkel, Joseph G.; Hepler, Peter K.

doi:10.1002/1521-1878(200101)23:1<86::aid-bies1011>3.0.co;2-d

Cited by 147 publications

(56 citation statements)

References 62 publications

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“…The oscillations in elongation of pollen tubes are thought to reflect either the rapid usage of growth components, which must be reaccumulated to support the next phase of growth, or feedback in either the regulatory or metabolic machinery supporting tip growth (Feijo et al, 2001). Until recently, whether such oscillatory patterns represent an element in the process of root hair tip growth has been unclear.…”

Section: Discussionmentioning

confidence: 99%

Imaging of the Yellow Cameleon 3.6 Indicator Reveals That Elevations in Cytosolic Ca2+ Follow Oscillating Increases in Growth in Root Hairs of Arabidopsis

2008

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(M.A.M.) In tip-growing cells, the tip-high Ca 21 gradient is thought to regulate the activity of components of the growth machinery, including the cytoskeleton, Ca 21 -dependent regulatory proteins, and the secretory apparatus. In pollen tubes, both the Ca 21 gradient and cell elongation show oscillatory behavior, reinforcing the link between the two. We report that in growing root hairs of Arabidopsis (Arabidopsis thaliana), an oscillating tip-focused Ca 21 gradient can be resolved through imaging of a cytosolically expressed Yellow Cameleon 3.6 fluorescence resonance energy transfer-based Ca 21 sensor. Both elongation of the root hairs and the associated tip-focused Ca 21 gradient show a similar dynamic character, oscillating with a frequency of 2 to 4 min 21 . Crosscorrelation analysis indicates that the Ca 21 oscillations lag the growth oscillations by 5.3 6 0.3 s. However, growth never completely stops, even during the slow cycle of an oscillation, and the concomitant tip Ca 21 level is always slightly elevated compared with the resting Ca 21 concentration along the distal shaft, behind the growing tip. Artificially increasing Ca 21 using the Ca 21 ionophore A23187 leads to immediate cessation of elongation and thickening of the apical cell wall. In contrast, dissipating the Ca 21 gradient using either the Ca 21 channel blocker La 31 or the Ca 21 chelator EGTA is accompanied by an increase in the rate of cell expansion and eventual bursting of the root hair tip. These observations are consistent with a model in which the maximal oscillatory increase in cytosolic Ca 21 is triggered by cell expansion associated with tip growth and plays a role in the subsequent restriction of growth.

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Section: Discussionmentioning

confidence: 99%

Imaging of the Yellow Cameleon 3.6 Indicator Reveals That Elevations in Cytosolic Ca2+ Follow Oscillating Increases in Growth in Root Hairs of Arabidopsis

2008

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“…An important feature of pollen tube elongation is that the growth rate oscillates (Pierson et al, 1995(Pierson et al, , 1996Geitmann et al, 1996;Feijó et al, 2001;Holdaway-Clarke and Hepler, 2003;Moreno et al, 2007). In lily (Lilium longiflorum and Lilium formosanum), pollen tube growth rates typically vary continuously from a minimum of 100 nm s 21 to >500 nm s 21 with a period of 20 to 50 s (Pierson et al, 1996;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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“…The [pH] cyt of the pollen tube shank is an approximate pH of 6.9 to 7.11 (Fricker et al, 1997;Messerli and Robinson, 1998). There has been much debate about the [pH] cyt gradient, comprising an apical domain with an approximate pH of 6.8 and a subapical alkaline band with an approximate pH of 7.2 to 7.8 in Lilium longiflorum and Lilium formosanum pollen tubes (Fricker et al, 1997;Messerli and Robinson, 1998;Feijó et al, 2001;Lovy-Wheeler et al, 2006). Oscillations of [pH] cyt between approximate pH values of 6.9 and 7.3 have been linked to tip growth in L. formosanum pollen tubes (Lovy-Wheeler et al, 2006).…”

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confidence: 99%

Self-Incompatibility-Induced Programmed Cell Death in Field Poppy Pollen Involves Dramatic Acidification of the Incompatible Pollen Tube Cytosol

et al. 2015

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Self-incompatibility (SI) is an important genetically controlled mechanism to prevent inbreeding in higher plants. SI involves highly specific interactions during pollination, resulting in the rejection of incompatible (self) pollen. Programmed cell death (PCD) is an important mechanism for destroying cells in a precisely regulated manner. SI in field poppy (Papaver rhoeas) triggers PCD in incompatible pollen. During SI-induced PCD, we previously observed a major acidification of the pollen cytosol. Here, we present measurements of temporal alterations in cytosolic pH ([pH] cyt ); they were surprisingly rapid, reaching pH 6.4 within 10 min of SI induction and stabilizing by 60 min at pH 5.5. By manipulating the [pH] cyt of the pollen tubes in vivo, we show that [pH] cyt acidification is an integral and essential event for SI-induced PCD. Here, we provide evidence showing the physiological relevance of the cytosolic acidification and identify key targets of this major physiological alteration. A small drop in [pH] cyt inhibits the activity of a soluble inorganic pyrophosphatase required for pollen tube growth. We also show that [pH] cyt acidification is necessary and sufficient for triggering several key hallmark features of the SI PCD signaling pathway, notably activation of a DEVDase/caspase-3-like activity and formation of SI-induced punctate actin foci. Importantly, the actin binding proteins Cyclase-Associated Protein and ActinDepolymerizing Factor are identified as key downstream targets. Thus, we have shown the biological relevance of an extreme but physiologically relevant alteration in [pH] cyt and its effect on several components in the context of SI-induced events and PCD.

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

Cited by 147 publications

References 62 publications

Imaging of the Yellow Cameleon 3.6 Indicator Reveals That Elevations in Cytosolic Ca2+ Follow Oscillating Increases in Growth in Root Hairs of Arabidopsis

Imaging of the Yellow Cameleon 3.6 Indicator Reveals That Elevations in Cytosolic Ca2+ Follow Oscillating Increases in Growth in Root Hairs of Arabidopsis

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

Self-Incompatibility-Induced Programmed Cell Death in Field Poppy Pollen Involves Dramatic Acidification of the Incompatible Pollen Tube Cytosol

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