Leaf hydraulic maze; Differential effect of ABA on bundle-sheath, palisade, and spongy mesophyll hydraulic conductance

Abstract

Leaf hydraulic conductance (Kleaf) facilitates water for transpiration, enabling the continuation of CO2 upsurge while maintaining water status. Nevertheless, radial water flow out–of–the–xylem and its regulation under well and stress conditions remain vague. We hypothesized that bundle–sheath and mesophyll cells play key roles in the radial flow of water out of the xylem and the regulation of that flow under optimal and stress conditions. We generated transgenic Arabidopsis plants that were insensitive to abscisic acid (ABA) exclusively in their bundle sheath (BSabi) or mesophyll (MCabi). BSabi plants showed greater Kleaf and transpiration under optimal conditions, with stomatal apertures and index and vein density like those of the wild type. MCabi exhibited even higher Kleaf and transpiration, as well as larger stomatal apertures, a higher stomatal index and greater vascular diameter and biomass, relative to the wild type. In response to xylem–fed ABA, both transgenic lines exhibited reduced Kleaf and transpiration, while their leaf water potentials remained unchanged. The greater osmotic water permeability (Pf) of the wild types' spongy mesophyll was reduced by ABA; whereas the lower (Pf) of the palisade mesophyll was not affected by ABA. Genetically modified, ABA–insensitive spongy mesophyll cells had a low (Pf) ; whereas ABA–insensitive bundle–sheath cells had a higher (Pf) . The flow over the symplastic water pathway was increased by ABA, but its contribution to Kleaf was negligible. High levels of ABA appear to regulate the (Pf) of bundle–sheath and spongy mesophyll cells, to control Kleaf. Under optimal conditions, ABA limits transpiration and Kleaf via physiological, morphological, and developmental modifications of bundle–sheath and mesophyll cells. The bundle sheath–spongy mesophyll pathway controls Kleaf and leaf water balance under both optimal and drought conditions.

The dynamic multi‐functionality of leaf water transport outside the xylem

“…During drought, ABA transported in xylem sap may be sensed at the BS membranes, triggering deactivation of aquaporins and reduction of membrane permeability for water transfer to the mesophyll (Shatil‐Cohen et al ., 2011; Pantin et al ., 2013). The resulting reduced K leaf would accelerate mesophyll dehydration, causing increased ABA production and potentially driving stomatal closure (Yaaran et al ., 2023). At the same time, ABA appears to increase symplastic flow from xylem to BS through plasmodesmata, possibly to help equilibrate water potential (Ψ) across cells (Yaaran et al ., 2023).…”

“…The resulting reduced K leaf would accelerate mesophyll dehydration, causing increased ABA production and potentially driving stomatal closure (Yaaran et al ., 2023). At the same time, ABA appears to increase symplastic flow from xylem to BS through plasmodesmata, possibly to help equilibrate water potential (Ψ) across cells (Yaaran et al ., 2023). More work is needed to disentangle the roles of the different outside‐xylem pathways, and how these depend on membrane proteins and vary across species of diverse anatomies.…”

“…1; Buckley et al, 2015Buckley et al, , 2017. In most hypostomatous species, palisade mesophyll is relatively hydraulically isolated, sustaining photosynthesis during mild dehydration (Yaaran et al, 2023). Many recent studies of leaf water transport have focused on BS cells (Buckley et al, 2015(Buckley et al, , 2017), yet the microroutes for water movement from the xylem into the BS remain unclear.…”

A tale of two pumps: Blue light and ABA alter Arabidopsis leaf hydraulics via bundle sheath cells’ H+-pumps and channels

“…Quantification of abi1-1 expression in WT, abi1-1 and SCR:abi1-1 plants by restriction enzymes was as described by (Negin et al, 2019; Yaaran et al, 2022).…”