Grapevine petioles are more sensitive to drought induced embolism than stems: evidence from in vivo MRI and microcomputed tomography observations of hydraulic vulnerability segmentation

Abstract

The 'hydraulic vulnerability segmentation' hypothesis predicts that expendable distal organs are more susceptible to water stress-induced embolism than the main stem of the plant. In the current work, we present the first in vivo visualization of this phenomenon. In two separate experiments, using magnetic resonance imaging or synchrotron-based microcomputed tomography, grapevines (Vitis vinifera) were dehydrated while simultaneously scanning the main stems and petioles for the occurrence of emboli at different xylem pressures (Ψx ). Magnetic resonance imaging revealed that 50% of the conductive xylem area of the petioles was embolized at a Ψx of -1.54 MPa, whereas the stems did not reach similar losses until -1.9 MPa. Microcomputed tomography confirmed these findings, showing that approximately half the vessels in the petioles were embolized at a Ψx of -1.6 MPa, whereas only few were embolized in the stems. Petioles were shown to be more resistant to water stress-induced embolism than previously measured with invasive hydraulic methods. The results provide the first direct evidence for the hydraulic vulnerability segmentation hypothesis and highlight its importance in grapevine responses to severe water stress. Additionally, these data suggest that air entry through the petiole into the stem is unlikely in grapevines during drought.

Stomatal Closure, Basal Leaf Embolism, and Shedding Protect the Hydraulic Integrity of Grape Stems

“…To facilitate the observation of leaf appearance at different stages, the same leaf is outlined in red in all three images. accordance with the hydraulic segmentation known in grapevine (Charrier et al, 2016;Hochberg et al, 2016a), the stems of dehydrated grapevine showed only 7% PLC, close to the average value of control plants (Fig. 7).…”

“…Visualization techniques such as microcomputed tomography (microCT) and magnetic resonance imaging (MRI) provide reliable measurements of xylem embolism in intact plants (Scheenen et al, 2007;Cochard et al, 2015) and even embolism propagation over time in the same plant (Holbrook et al, 2001;Brodersen et al, 2010Brodersen et al, , 2013Choat et al, 2015;Hochberg et al, 2016a). However, these approaches also have drawbacks: small field of view, long acquisition times, potentially lethal radiation doses for the imaged plant (in the case of microCT), expense, and limited availability of the equipment.…”

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

“…Thus, changes in outside-xylem pathways with dehydration could be more reversible during drought and recovery cycles than xylem embolism. While xylem embolism requires several hours under no tension to recover by capillarity (Hochberg et al, 2016;Knipfer et al, 2016), in some species, K leaf can partially recover after only 1 h of rehydration , which could be due to the recovery of K ox . Future work should resolve the influence of K x and K ox decline on stomatal conductance and their recovery.…”

Grapevine adaptations to water stress: new perspectives about soil/plant interactions

“…The gas molecules tend to accumulate together causing a disruption of the water column in the xylem and a decrease in hydraulic conductivity. Embolisms occur more frequently in roots and petioles than in shoots, causing 80%PLC (Percent Loss of hydraulic Conductivity) during a moderate water stress in these anatomical compartments compared to the 50% PLC of shoots (Lovisolo et al 2008a;Hochberg et al 2016). Root embolization is thought to limit water use by the plant and be protective against the propagation of low xylem tension to the stem.…”