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

Liu J, Hussey PJ - Front Plant Sci (2014)

Bottom Line: Currently, the two main pollen tube growth models, the cell wall model and the hydrodynamic model do not appear to be reconcilable.In this way regulation of pollen tube growth by turgor is context dependent.The novel methodology developed here reveals the underlying context-dependent regulatory principle of pollen tube growth.

View Article: PubMed Central - PubMed

Affiliation: School of Biological and Biomedical Sciences, Durham University Durham, UK.

ABSTRACT
Hydrodynamics, cell wall and ion dynamics are all important properties that regulate pollen tube growth. Currently, the two main pollen tube growth models, the cell wall model and the hydrodynamic model do not appear to be reconcilable. Here we develop an integrative model for pollen tube growth and show that our model reproduces key experimental observations: (1) that the hypertonic condition leads to a much longer oscillatory period and that the hypotonic condition halves the oscillatory period; (2) that oscillations in turgor are experimentally undetectable; (3) that increasing the extracellular calcium concentration or decreasing the pH decreases the growth oscillatory amplitude; (4) that knockout of Raba4d, a member of the Rab family of small GTPase proteins, decreases pollen tube length after germination for 24 h. Using the model generated here, we reveal that (1) when cell wall extensibility is large, pollen tube may sustain growth at different volume changes and maintain relatively stable turgor; (2) turgor increases if cell wall extensibility decreases; (3) increasing turgor due to decrease in osmolarity in the media, although very small, increases volume change. However, increasing turgor due to decrease in cell wall extensibility decreases volume change. In this way regulation of pollen tube growth by turgor is context dependent. By changing the osmolarity in the media, the main regulatory points are extracellular osmolarity for water flow and turgor for the volume encompassed by the cell wall. However, if the viscosity of cell wall changes, the main regulatory points are turgor for water flow and wall extensibility for the volume encompassed by the cell wall. The novel methodology developed here reveals the underlying context-dependent regulatory principle of pollen tube growth.

No MeSH data available.


Related in: MedlinePlus

Knockout of Raba4d, a member of the Rab family of small GTPase proteins, decreases pollen tube length. Osmolarity in the media is 0.36 Osm. Fusion rate parameter is reduced from 21.5 μm3/(mM s) in wild type (wt) to 0.215 μm3/(mM s) in Raba4d mutant, mimicking that Raba4d regulates membrane trafficking. After knockout of Raba4d, membrane trafficking rate decreases. (A) Qualitatively reproduces experimental observations (Szumlanski and Nielsen, 2009): in Raba4d mutant, pollen tube length is shorter than that in wild type (Szumlanski and Nielsen, 2009). Following experimental observations (Szumlanski and Nielsen, 2009), the pollen tube radius is approximately 6 and 12 μm for wt and Raba4d respectively. Our simulations use the corresponding radius respectively. (B) Analyses pollen tube growth rate in both wild type and Raba4d.
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Figure 5: Knockout of Raba4d, a member of the Rab family of small GTPase proteins, decreases pollen tube length. Osmolarity in the media is 0.36 Osm. Fusion rate parameter is reduced from 21.5 μm3/(mM s) in wild type (wt) to 0.215 μm3/(mM s) in Raba4d mutant, mimicking that Raba4d regulates membrane trafficking. After knockout of Raba4d, membrane trafficking rate decreases. (A) Qualitatively reproduces experimental observations (Szumlanski and Nielsen, 2009): in Raba4d mutant, pollen tube length is shorter than that in wild type (Szumlanski and Nielsen, 2009). Following experimental observations (Szumlanski and Nielsen, 2009), the pollen tube radius is approximately 6 and 12 μm for wt and Raba4d respectively. Our simulations use the corresponding radius respectively. (B) Analyses pollen tube growth rate in both wild type and Raba4d.

Mentions: Moreover, modeling predicts the following. (1) Change in turgor is very small when extracellular osmolarity changes and increasing extracellular osmolarity only slightly decreases cellular turgor if cell wall viscosity is low (i.e., cell wall extensibility is large). Moreover, for any fixed osmolarity in the media, oscillations in turgor are experimentally undetectable (<0.0009 MPa) (Figure 3). Experimentally, no oscillatory changes in turgor were observed within a resolution limit of ca. 0.005 MPa (Benkert et al., 1997). (2) Increasing extracellular calcium concentration or decreasing pH decreases growth oscillatory amplitude and increases baseline growth rate, respectively (Messerli and Robinson, 2003) (Figure 4). (3) Knockout of Raba4d decreases the average length of pollen tubes as measured after germination for 24 h in vitro (Szumlanski and Nielsen, 2009) (Figure 5). These modeling results are qualitatively in agreement with experimental observations.


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

Liu J, Hussey PJ - Front Plant Sci (2014)

Knockout of Raba4d, a member of the Rab family of small GTPase proteins, decreases pollen tube length. Osmolarity in the media is 0.36 Osm. Fusion rate parameter is reduced from 21.5 μm3/(mM s) in wild type (wt) to 0.215 μm3/(mM s) in Raba4d mutant, mimicking that Raba4d regulates membrane trafficking. After knockout of Raba4d, membrane trafficking rate decreases. (A) Qualitatively reproduces experimental observations (Szumlanski and Nielsen, 2009): in Raba4d mutant, pollen tube length is shorter than that in wild type (Szumlanski and Nielsen, 2009). Following experimental observations (Szumlanski and Nielsen, 2009), the pollen tube radius is approximately 6 and 12 μm for wt and Raba4d respectively. Our simulations use the corresponding radius respectively. (B) Analyses pollen tube growth rate in both wild type and Raba4d.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4127481&req=5

Figure 5: Knockout of Raba4d, a member of the Rab family of small GTPase proteins, decreases pollen tube length. Osmolarity in the media is 0.36 Osm. Fusion rate parameter is reduced from 21.5 μm3/(mM s) in wild type (wt) to 0.215 μm3/(mM s) in Raba4d mutant, mimicking that Raba4d regulates membrane trafficking. After knockout of Raba4d, membrane trafficking rate decreases. (A) Qualitatively reproduces experimental observations (Szumlanski and Nielsen, 2009): in Raba4d mutant, pollen tube length is shorter than that in wild type (Szumlanski and Nielsen, 2009). Following experimental observations (Szumlanski and Nielsen, 2009), the pollen tube radius is approximately 6 and 12 μm for wt and Raba4d respectively. Our simulations use the corresponding radius respectively. (B) Analyses pollen tube growth rate in both wild type and Raba4d.
Mentions: Moreover, modeling predicts the following. (1) Change in turgor is very small when extracellular osmolarity changes and increasing extracellular osmolarity only slightly decreases cellular turgor if cell wall viscosity is low (i.e., cell wall extensibility is large). Moreover, for any fixed osmolarity in the media, oscillations in turgor are experimentally undetectable (<0.0009 MPa) (Figure 3). Experimentally, no oscillatory changes in turgor were observed within a resolution limit of ca. 0.005 MPa (Benkert et al., 1997). (2) Increasing extracellular calcium concentration or decreasing pH decreases growth oscillatory amplitude and increases baseline growth rate, respectively (Messerli and Robinson, 2003) (Figure 4). (3) Knockout of Raba4d decreases the average length of pollen tubes as measured after germination for 24 h in vitro (Szumlanski and Nielsen, 2009) (Figure 5). These modeling results are qualitatively in agreement with experimental observations.

Bottom Line: Currently, the two main pollen tube growth models, the cell wall model and the hydrodynamic model do not appear to be reconcilable.In this way regulation of pollen tube growth by turgor is context dependent.The novel methodology developed here reveals the underlying context-dependent regulatory principle of pollen tube growth.

View Article: PubMed Central - PubMed

Affiliation: School of Biological and Biomedical Sciences, Durham University Durham, UK.

ABSTRACT
Hydrodynamics, cell wall and ion dynamics are all important properties that regulate pollen tube growth. Currently, the two main pollen tube growth models, the cell wall model and the hydrodynamic model do not appear to be reconcilable. Here we develop an integrative model for pollen tube growth and show that our model reproduces key experimental observations: (1) that the hypertonic condition leads to a much longer oscillatory period and that the hypotonic condition halves the oscillatory period; (2) that oscillations in turgor are experimentally undetectable; (3) that increasing the extracellular calcium concentration or decreasing the pH decreases the growth oscillatory amplitude; (4) that knockout of Raba4d, a member of the Rab family of small GTPase proteins, decreases pollen tube length after germination for 24 h. Using the model generated here, we reveal that (1) when cell wall extensibility is large, pollen tube may sustain growth at different volume changes and maintain relatively stable turgor; (2) turgor increases if cell wall extensibility decreases; (3) increasing turgor due to decrease in osmolarity in the media, although very small, increases volume change. However, increasing turgor due to decrease in cell wall extensibility decreases volume change. In this way regulation of pollen tube growth by turgor is context dependent. By changing the osmolarity in the media, the main regulatory points are extracellular osmolarity for water flow and turgor for the volume encompassed by the cell wall. However, if the viscosity of cell wall changes, the main regulatory points are turgor for water flow and wall extensibility for the volume encompassed by the cell wall. The novel methodology developed here reveals the underlying context-dependent regulatory principle of pollen tube growth.

No MeSH data available.


Related in: MedlinePlus