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Gating of aqùaporins by light and reactive oxygen species in leaf parenchyma cells of the midrib of Zea mays.

Kim YX, Steudle E - J. Exp. Bot. (2008)

Bottom Line: The effects of HL on T(1/2) were similar to those caused by H(2)O(2) treatment in the presence of Fe(2+), which produced *OH (Fenton reaction; reversible oxidative gating of aquaporins).The results provide evidence that the varying light climate adjusts water flow at the cell level; that is, water flow is maximized at a certain light intensity and then reduced again by HL.Light effects are discussed in terms of an oxidative gating of aquaporins by ROS.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Ecology, Bayreuth University, D-95440 Bayreuth, Germany.

ABSTRACT
Changes of the water permeability aqùaporin (AQP) activity of leaf cells were investigated in response to different light regimes (low versus high). Using a cell pressure probe, hydraulic properties (half-time of water exchange, T(1/2) infinity 1/water permeability) of parenchyma cells in the midrib tissue of maize (Zea mays L.) leaves have been measured. A new perfusion technique was applied to excised leaves to keep turgor constant and to modify the environment around cells by perfusing solutions using a pressure chamber. In response to low light (LL) of 200 micromol m(-2) s(-1), T(1/2) decreased during the perfusion of a control solution of 0.5 mM CaCl(2) by a factor of two. This was in line with earlier results from leaf cells of intact maize plants at a constant turgor. In contrast, high light (HL) at intensities of 800 micromol m(-2) s(-1) and 1800 micromol m(-2) s(-1) increased the T(1/2) in two-thirds of cells by factors of 14 and 35, respectively. The effects of HL on T(1/2) were similar to those caused by H(2)O(2) treatment in the presence of Fe(2+), which produced *OH (Fenton reaction; reversible oxidative gating of aquaporins). Treatments with 20 mM H(2)O(2) following Fe(2+) pre-treatments increased the T(1/2) by a factor of 30. Those increased T(1/2) values could be partly recovered, either when the perfusion solution was changed back to the control solution or when LL was applied. 3mM of the antioxidant glutathione also reversed the effects of HL. The data suggest that HL could induce reactive oxygen species (ROS) such as *OH, and they affected water relations. The results provide evidence that the varying light climate adjusts water flow at the cell level; that is, water flow is maximized at a certain light intensity and then reduced again by HL. Light effects are discussed in terms of an oxidative gating of aquaporins by ROS.

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Two types of response to high light (HL) treatment. (A) HL of 800 μmol m−2 s−1 (black bars, n=4 cells) and 1800 μmol m−2 s−1 (grey bars, n=3 cells) increased the T1/2 at constant turgor in CaCl2 solution. The increase in T1/2 began ∼10 min after HL was turned on. The largest T1/2s caused by HL were significantly larger than those measured at ambient light (AL) intensity before HL treatments (P <0.05, t-test). During 15 min after the light was switched off, T1/2s remained large, i.e. not reversible within 15 min. (B) There were cells in which T1/2 did not increase but decreased due to the effect of HL of 1800 μmol m−2 s−1 (grey bars, n=5 cells). Values are means ±SD and are shown as relative changes. The absolute values of T1/2 are shown in the inset.
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fig6: Two types of response to high light (HL) treatment. (A) HL of 800 μmol m−2 s−1 (black bars, n=4 cells) and 1800 μmol m−2 s−1 (grey bars, n=3 cells) increased the T1/2 at constant turgor in CaCl2 solution. The increase in T1/2 began ∼10 min after HL was turned on. The largest T1/2s caused by HL were significantly larger than those measured at ambient light (AL) intensity before HL treatments (P <0.05, t-test). During 15 min after the light was switched off, T1/2s remained large, i.e. not reversible within 15 min. (B) There were cells in which T1/2 did not increase but decreased due to the effect of HL of 1800 μmol m−2 s−1 (grey bars, n=5 cells). Values are means ±SD and are shown as relative changes. The absolute values of T1/2 are shown in the inset.

Mentions: Although there was an overall trend of a reduction of T1/2 following HL treatment, this was statistically not significant. As during the LL treatment, there was a substantial variability between cells. For example, HL of 800 μmol m−2 s−1 and 1800 μmol m−2 s−1 reduced the T1/2 during the first 5–10 min of the 15 min period of illumination, but then T1/2 increased substantially by factors of 14 and 35, respectively (Fig. 6A, n=3–4 cells; type-1 response). In total, 10 cells showed an increase in T1/2 due to HL. The 15 min treatment was chosen as the maximum treatment which could be applied at constant turgor and with stable cells. Longer HL treatments caused a continuous decrease in turgor pressure, which indicated damage to the cells. In this respect, punctured cells could have been more prone to damage in the presence of light stress than other cells (see Discussion). In eight out of 10 cells, the T1/2s remained large when light was turned off for 30 min, which was the maximum period of time measured. There were, however, cells, which were hardly affected by HL, as seen in Fig. 6B (n=5 cells; type-2 response). In those cells, there was only a 37–86% reduction within 15 min. Those five cells were from two leaves, and no cells in those leaves showed a type-1 response. Maximum temperature changes on the leaf surface due to illumination with 800 μmol m−2 s−1 and 1800 μmol m−2 s−1 were 3 °C and 7 °C, respectively.


Gating of aqùaporins by light and reactive oxygen species in leaf parenchyma cells of the midrib of Zea mays.

Kim YX, Steudle E - J. Exp. Bot. (2008)

Two types of response to high light (HL) treatment. (A) HL of 800 μmol m−2 s−1 (black bars, n=4 cells) and 1800 μmol m−2 s−1 (grey bars, n=3 cells) increased the T1/2 at constant turgor in CaCl2 solution. The increase in T1/2 began ∼10 min after HL was turned on. The largest T1/2s caused by HL were significantly larger than those measured at ambient light (AL) intensity before HL treatments (P <0.05, t-test). During 15 min after the light was switched off, T1/2s remained large, i.e. not reversible within 15 min. (B) There were cells in which T1/2 did not increase but decreased due to the effect of HL of 1800 μmol m−2 s−1 (grey bars, n=5 cells). Values are means ±SD and are shown as relative changes. The absolute values of T1/2 are shown in the inset.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC2651454&req=5

fig6: Two types of response to high light (HL) treatment. (A) HL of 800 μmol m−2 s−1 (black bars, n=4 cells) and 1800 μmol m−2 s−1 (grey bars, n=3 cells) increased the T1/2 at constant turgor in CaCl2 solution. The increase in T1/2 began ∼10 min after HL was turned on. The largest T1/2s caused by HL were significantly larger than those measured at ambient light (AL) intensity before HL treatments (P <0.05, t-test). During 15 min after the light was switched off, T1/2s remained large, i.e. not reversible within 15 min. (B) There were cells in which T1/2 did not increase but decreased due to the effect of HL of 1800 μmol m−2 s−1 (grey bars, n=5 cells). Values are means ±SD and are shown as relative changes. The absolute values of T1/2 are shown in the inset.
Mentions: Although there was an overall trend of a reduction of T1/2 following HL treatment, this was statistically not significant. As during the LL treatment, there was a substantial variability between cells. For example, HL of 800 μmol m−2 s−1 and 1800 μmol m−2 s−1 reduced the T1/2 during the first 5–10 min of the 15 min period of illumination, but then T1/2 increased substantially by factors of 14 and 35, respectively (Fig. 6A, n=3–4 cells; type-1 response). In total, 10 cells showed an increase in T1/2 due to HL. The 15 min treatment was chosen as the maximum treatment which could be applied at constant turgor and with stable cells. Longer HL treatments caused a continuous decrease in turgor pressure, which indicated damage to the cells. In this respect, punctured cells could have been more prone to damage in the presence of light stress than other cells (see Discussion). In eight out of 10 cells, the T1/2s remained large when light was turned off for 30 min, which was the maximum period of time measured. There were, however, cells, which were hardly affected by HL, as seen in Fig. 6B (n=5 cells; type-2 response). In those cells, there was only a 37–86% reduction within 15 min. Those five cells were from two leaves, and no cells in those leaves showed a type-1 response. Maximum temperature changes on the leaf surface due to illumination with 800 μmol m−2 s−1 and 1800 μmol m−2 s−1 were 3 °C and 7 °C, respectively.

Bottom Line: The effects of HL on T(1/2) were similar to those caused by H(2)O(2) treatment in the presence of Fe(2+), which produced *OH (Fenton reaction; reversible oxidative gating of aquaporins).The results provide evidence that the varying light climate adjusts water flow at the cell level; that is, water flow is maximized at a certain light intensity and then reduced again by HL.Light effects are discussed in terms of an oxidative gating of aquaporins by ROS.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Ecology, Bayreuth University, D-95440 Bayreuth, Germany.

ABSTRACT
Changes of the water permeability aqùaporin (AQP) activity of leaf cells were investigated in response to different light regimes (low versus high). Using a cell pressure probe, hydraulic properties (half-time of water exchange, T(1/2) infinity 1/water permeability) of parenchyma cells in the midrib tissue of maize (Zea mays L.) leaves have been measured. A new perfusion technique was applied to excised leaves to keep turgor constant and to modify the environment around cells by perfusing solutions using a pressure chamber. In response to low light (LL) of 200 micromol m(-2) s(-1), T(1/2) decreased during the perfusion of a control solution of 0.5 mM CaCl(2) by a factor of two. This was in line with earlier results from leaf cells of intact maize plants at a constant turgor. In contrast, high light (HL) at intensities of 800 micromol m(-2) s(-1) and 1800 micromol m(-2) s(-1) increased the T(1/2) in two-thirds of cells by factors of 14 and 35, respectively. The effects of HL on T(1/2) were similar to those caused by H(2)O(2) treatment in the presence of Fe(2+), which produced *OH (Fenton reaction; reversible oxidative gating of aquaporins). Treatments with 20 mM H(2)O(2) following Fe(2+) pre-treatments increased the T(1/2) by a factor of 30. Those increased T(1/2) values could be partly recovered, either when the perfusion solution was changed back to the control solution or when LL was applied. 3mM of the antioxidant glutathione also reversed the effects of HL. The data suggest that HL could induce reactive oxygen species (ROS) such as *OH, and they affected water relations. The results provide evidence that the varying light climate adjusts water flow at the cell level; that is, water flow is maximized at a certain light intensity and then reduced again by HL. Light effects are discussed in terms of an oxidative gating of aquaporins by ROS.

Show MeSH