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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

Variation of growth rate for (A) different calcium concentrations in the media, and (B) different pH in the media. Osmolarity in the media is 0.36O sm. (A) At time t1, [Ca2+] in the media increases from 0.13 to 1.3 mM (the reference value used in this work is 1 mM). The oscillatory amplitude of growth rate decreases and the baseline growth rate increases. At time t2, [Ca2+] returns the original 0.13 mM. The oscillatory amplitude of growth rate increases and the baseline growth rate decreases. (B) At time t1, pH in the media decreases to 5.1 from 5.7 (the reference value used in this work is 5.7). The oscillatory amplitude of growth rate decreases and the baseline growth rate slightly increases. At time t2, pH returns the original 5.7. The oscillatory amplitude of growth rate increases and the baseline growth rate slightly decreases. These results are qualitatively in agreement with experimental observations (Messerli and Robinson, 2003), although the range of varying pH in experiments (Messerli and Robinson, 2003) is much wider. Modeling results show that, when [Ca2+] in the media increases from 0.13 to 1.3 mM, although oscillatory amplitudes of growth rate change, the average growth rates for the two media conditions are approximately the same. The reason is as follows. The 10-fold increase (from 0.13 to 1.3 mM) of [Ca2+] in the media only leads to a change of 0.04 and 0.4% in the osmolarity in the media. Thus, the contribution of this 10-fold of [Ca2+] increase to the osmolarity in the media is insignificant.
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Figure 4: Variation of growth rate for (A) different calcium concentrations in the media, and (B) different pH in the media. Osmolarity in the media is 0.36O sm. (A) At time t1, [Ca2+] in the media increases from 0.13 to 1.3 mM (the reference value used in this work is 1 mM). The oscillatory amplitude of growth rate decreases and the baseline growth rate increases. At time t2, [Ca2+] returns the original 0.13 mM. The oscillatory amplitude of growth rate increases and the baseline growth rate decreases. (B) At time t1, pH in the media decreases to 5.1 from 5.7 (the reference value used in this work is 5.7). The oscillatory amplitude of growth rate decreases and the baseline growth rate slightly increases. At time t2, pH returns the original 5.7. The oscillatory amplitude of growth rate increases and the baseline growth rate slightly decreases. These results are qualitatively in agreement with experimental observations (Messerli and Robinson, 2003), although the range of varying pH in experiments (Messerli and Robinson, 2003) is much wider. Modeling results show that, when [Ca2+] in the media increases from 0.13 to 1.3 mM, although oscillatory amplitudes of growth rate change, the average growth rates for the two media conditions are approximately the same. The reason is as follows. The 10-fold increase (from 0.13 to 1.3 mM) of [Ca2+] in the media only leads to a change of 0.04 and 0.4% in the osmolarity in the media. Thus, the contribution of this 10-fold of [Ca2+] increase to the osmolarity in the media is insignificant.

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)

Variation of growth rate for (A) different calcium concentrations in the media, and (B) different pH in the media. Osmolarity in the media is 0.36O sm. (A) At time t1, [Ca2+] in the media increases from 0.13 to 1.3 mM (the reference value used in this work is 1 mM). The oscillatory amplitude of growth rate decreases and the baseline growth rate increases. At time t2, [Ca2+] returns the original 0.13 mM. The oscillatory amplitude of growth rate increases and the baseline growth rate decreases. (B) At time t1, pH in the media decreases to 5.1 from 5.7 (the reference value used in this work is 5.7). The oscillatory amplitude of growth rate decreases and the baseline growth rate slightly increases. At time t2, pH returns the original 5.7. The oscillatory amplitude of growth rate increases and the baseline growth rate slightly decreases. These results are qualitatively in agreement with experimental observations (Messerli and Robinson, 2003), although the range of varying pH in experiments (Messerli and Robinson, 2003) is much wider. Modeling results show that, when [Ca2+] in the media increases from 0.13 to 1.3 mM, although oscillatory amplitudes of growth rate change, the average growth rates for the two media conditions are approximately the same. The reason is as follows. The 10-fold increase (from 0.13 to 1.3 mM) of [Ca2+] in the media only leads to a change of 0.04 and 0.4% in the osmolarity in the media. Thus, the contribution of this 10-fold of [Ca2+] increase to the osmolarity in the media is insignificant.
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Related In: Results  -  Collection

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Figure 4: Variation of growth rate for (A) different calcium concentrations in the media, and (B) different pH in the media. Osmolarity in the media is 0.36O sm. (A) At time t1, [Ca2+] in the media increases from 0.13 to 1.3 mM (the reference value used in this work is 1 mM). The oscillatory amplitude of growth rate decreases and the baseline growth rate increases. At time t2, [Ca2+] returns the original 0.13 mM. The oscillatory amplitude of growth rate increases and the baseline growth rate decreases. (B) At time t1, pH in the media decreases to 5.1 from 5.7 (the reference value used in this work is 5.7). The oscillatory amplitude of growth rate decreases and the baseline growth rate slightly increases. At time t2, pH returns the original 5.7. The oscillatory amplitude of growth rate increases and the baseline growth rate slightly decreases. These results are qualitatively in agreement with experimental observations (Messerli and Robinson, 2003), although the range of varying pH in experiments (Messerli and Robinson, 2003) is much wider. Modeling results show that, when [Ca2+] in the media increases from 0.13 to 1.3 mM, although oscillatory amplitudes of growth rate change, the average growth rates for the two media conditions are approximately the same. The reason is as follows. The 10-fold increase (from 0.13 to 1.3 mM) of [Ca2+] in the media only leads to a change of 0.04 and 0.4% in the osmolarity in the media. Thus, the contribution of this 10-fold of [Ca2+] increase to the osmolarity in the media is insignificant.
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