The contribution of vascular and extra-vascular water pathways to drought-induced decline of leaf hydraulic conductance

Abstract

Drought stress can impair leaf hydraulic conductance (Kleaf), but the relative contribution of changes in the efficiency of the vein xylem water pathway and in the mesophyll route outside the xylem in driving the decline of Kleaf is still debated. We report direct measurements of dehydration-induced changes in the hydraulic resistance (R=1/K) of whole leaf (Rleaf), as well as of the leaf xylem (Rx) and extra-vascular pathways (Rox) in four Angiosperm species. Rleaf, Rx, and Rox were measured using the vacuum chamber method (VCM). Rleaf values during progressive leaf dehydration were also validated with measurements performed using the rehydration kinetic method (RKM). We analysed correlations between changes in Rx or Rox and Rleaf, as well as between morpho-anatomical traits (including dehydration-induced leaf shrinkage), vulnerability to embolism, and leaf water relation parameters. Measurements revealed that the relative contribution of vascular and extra-vascular hydraulic properties in driving Kleaf decline during dehydration is species-specific. Whilst in two study species the progressive impairment of both vascular and extra-vascular pathways contributed to leaf hydraulic vulnerability, in the other two species the vascular pathway remained substantially unaltered during leaf dehydration, and Kleaf decline was apparently caused only by changes in the hydraulic properties of the extra-vascular compartment.

Outside-Xylem Vulnerability, Not Xylem Embolism, Controls Leaf Hydraulic Decline during Dehydration

“…For many species, K leaf in hydrated leaves can be enhanced by many fold under high irradiance likely due to aquaporin expression (Cochard et al, 2007;Scoffoni et al, 2008;Maurel et al, 2015) and such high-light-acclimated leaves show stronger vulnerability before the turgor loss point (Guyot et al, 2012;Sack et al, 2016b). Similarly, a recent study partitioning the vulnerabilities of K x and K ox found that K ox was the strongest determinant of K leaf decline in two of four species (Trifiló et al, 2016), and, for the other two species, both xylem and outsidexylem pathways appeared to be strong drivers of K leaf decline. However, hydraulics measurements were performed in that study under low light, likely minimizing the response of K ox before the turgor loss point.…”

“…However, there has been a lack of information of the number of embolized xylem conduits within given vein orders across the range of leaf water stress and their influence on K leaf (Wylie, 1947;McKown et al, 2010;Sack and Scoffoni, 2013) relative to the potentially strong role of vulnerability of the outside-xylem pathways. Recent work has proposed that outside-xylem hydraulic decline may play a role in K leaf decline (Sade et al, 2014;Scoffoni et al, 2014;HernandezSantana et al, 2016;Trifiló et al, 2016). A study that partitioned the vulnerability of K leaf into that of K x and K ox (Trifiló et al, 2016) found that both contributed, depending on species, but measurements were made under low irradiance, which would minimize the response of K ox before the turgor loss point (Guyot et al, 2012;Sack et al, 2016b).…”

“…Recent work has proposed that outside-xylem hydraulic decline may play a role in K leaf decline (Sade et al, 2014;Scoffoni et al, 2014;HernandezSantana et al, 2016;Trifiló et al, 2016). A study that partitioned the vulnerability of K leaf into that of K x and K ox (Trifiló et al, 2016) found that both contributed, depending on species, but measurements were made under low irradiance, which would minimize the response of K ox before the turgor loss point (Guyot et al, 2012;Sack et al, 2016b). A strong test of the relative roles of K x and K ox depends on their determination for illuminated leaves coupled with direct observations of the formation of emboli in the xylem.…”

Why are leaves hydraulically vulnerable?

“…These studies further showed that K leaf is responsive to internal and external factors that affect both xylem and living tissues, such as temperature, light and water status. In this issue, Trifiló et al (2016) extend the dissection approach to clarify the response of K leaf to dehydration.…”

Stomatal Biology of CAM Plants

“…The mechanisms underlying stomatal sensitivity to VPD remain a controversial and active area of research, with the possibility of liquidand/or vapor-phase signals being involved alongside ABA synthesis and signaling within guard cells (Peak and Mott, 2011;Bauer et al, 2013;Buckley and Mott, 2013;Mott and Peak, 2013;McAdam et al, 2016). Because of the potentially significant metabolic and signaling interactions between guard cells and the mesophyll, integrated investigation of stomatal sensitivity and the dynamic responses of the critical extravascular component of leaf hydraulic conductance in CAM (and C 3 ) species is highly desirable Trifiló et al, 2016). Analysis of the spatiotemporally dynamic expression patterns of aquaporins and of possible interactions between stomatal physiology and mesophyll osmotic properties could be especially fruitful (Pou et al, 2013;Martorell et al, 2015).…”