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

The 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.