Bundle‐sheath cell regulation of xylem‐mesophyll water transport via aquaporins under drought stress: a target of xylem‐borne ABA?

Abstract

SUMMARYThe hydraulic conductivity of the leaf vascular system (K leaf ) is dynamic and decreases rapidly under drought stress, possibly in response to the stress phytohormone ABA, which increases sharply in the xylem sap (ABA xyl ) during periods of drought. Vascular bundle-sheath cells (BSCs; a layer of parenchymatous cells tightly enwrapping the entire leaf vasculature) have been hypothesized to control K leaf via the specific activity of BSC aquaporins (AQPs). We examined this hypothesis and provide evidence for drought-induced ABA xyl diminishing BSC osmotic water permeability (P f ) via downregulated activity of their AQPs. ABA fed to the leaf via the xylem (petiole) both decreased K leaf and led to stomatal closure, replicating the effect of drought. In contrast, smearing ABA on the leaf blade, while also closing stomata, did not decrease K leaf within 2-3 h of application, demonstrating that K leaf does not depend entirely on stomatal closure. GFP-labeled BSCs showed decreased P f in response to 'drought' and ABA treatment, and a reversible decrease with HgCl 2 (an AQP blocker). These P f responses, absent in mesophyll cells, suggest stress-regulated AQP activity specific to BSCs, and imply a role for these cells in decreasing K leaf via a reduction in P f . Our results support the above hypothesis and highlight the BSCs as hitherto overlooked vasculature sensor compartments, extending throughout the leaf and functioning as 'stress-regulated valves' converting vasculature chemical signals (possibly ABA xyl ) into leaf hydraulic signals.

Measuring the Osmotic Water Permeability Coefficient (P_f) of Spherical Cells: Isolated Plant Protoplasts as an Example

“…These protoplasts were found to have low basal (background) P f levels 7 and can serve as a functional-expression system to enable reproducible P f measurements.…”

The spatio-temporal specificity of PYR1/PYL/RCAR ABA receptors in response to developmental and environmental cues

“…When WT Arabidopsis leaves were xylem-supplied with 10mM ABA, leaf hydraulic conductance (K leaf ) decreased by c. 50%, yet foliar application of the same ABA concentration (while decreasing transpiration rate) had no statistically significant effect on detached leaf K leaf . 12 While application ABA to root medium generally inhibit root growth, McAdam et al recently shown that shoot-derived ABA promotes root growth. 43 It is clear that the different sourced ABA correspondence to its distinct action, even in the same tissues or cells.…”

“…21 While PYL8 mediates the ability of ABA to inhibit primary root growth through the PP2C-SnRK2 pathway, 18 it together with PYL9 promotes lateral root growth recovery from inhibition independently of the core signaling pathway by enhancing MYB77-dependent transcription of auxin-responsive genes. 17,23 The cell-specificities of PYR1/PYL/RCAR ABA receptors It has been shown that application ABA directly enhance plasma membrane water permeability of roots cortical cells 15 and guard cells, 24 while inhibit that of vascular bundle-sheath cells 12 and has not effect to that of mesophyll cells. 12,24 The core signaling component SnRK2.6 has been documented implicated in plasma membrane intrinsic proteins PIP2;1 activation through protein phosphorylation at Ser-121, thus increase in guard cell permeability to water.…”

“…17,23 The cell-specificities of PYR1/PYL/RCAR ABA receptors It has been shown that application ABA directly enhance plasma membrane water permeability of roots cortical cells 15 and guard cells, 24 while inhibit that of vascular bundle-sheath cells 12 and has not effect to that of mesophyll cells. 12,24 The core signaling component SnRK2.6 has been documented implicated in plasma membrane intrinsic proteins PIP2;1 activation through protein phosphorylation at Ser-121, thus increase in guard cell permeability to water. 24 However, how this signaling model involved in PIP inhibition is still not clear, though 4 PIPs dephosphorylation has been documented by a phosphoproteome technology in Arabidopsis leaves following 5-30 min ABA treatment.…”

“…11 It is well known that osmotic stress-derived ABA can reduce leaf hydraulic conductivity and shoot growth, thus reducing the transpiration rate in Arabidopsis leaves, [12][13][14] whereas it can maintain root water uptake by enhancing root growth and root hydraulic conductivity. 8,11,[15][16][17] Recently it is found that the single PYL8 ABA receptor play a key role in mediating ABA-controlled root growth and root response to moisture gradient, means hydrotropism, [17][18] while there is a obvious redundant characteristics of PYR1/PYL/RCAR ABA receptor family in stomatal aperture regulation.…”