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

Leaf hydraulic supply is crucial to maintaining open stomata for CO₂ capture and plant growth. During drought-induced dehydration, the leaf hydraulic conductance (K leaf) declines, which contributes to stomatal closure and, eventually, to leaf death. Previous studies have tended to attribute the dec...

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Bibliographic Details
Published in:Plant physiology (Bethesda) 2017-02, Vol.173 (2), p.1197-1210
Main Authors: Scoffoni, Christine, Albuquerque, Caetano, Brodersen, Craig R., Townes, Shatara V., John, Grace P., Bartlett, Megan K., Buckley, Thomas N., McElrone, Andrew J., Sack, Lawren
Format: Article
Language:English
Subjects:
Biological Transport
Computer Simulation
Dehydration
Droughts
ECOPHYSIOLOGY AND SUSTAINABILITY
Magnoliopsida - physiology
Models, Biological
Plant Leaves - physiology
Species Specificity
Water - physiology
X-Ray Microtomography
Xylem - physiology
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Summary:Leaf hydraulic supply is crucial to maintaining open stomata for CO₂ capture and plant growth. During drought-induced dehydration, the leaf hydraulic conductance (K leaf) declines, which contributes to stomatal closure and, eventually, to leaf death. Previous studies have tended to attribute the decline of K leaf to embolism in the leaf vein xylem. We visualized at high resolution and quantified experimentally the hydraulic vulnerability of xylem and outside-xylem pathways and modeled their respective influences on plant water transport. Evidence from all approaches indicated that the decline of K leaf during dehydration arose first and foremost due to the vulnerability of outside-xylem tissues. In vivo x-ray microcomputed tomography of dehydrating leaves of four diverse angiosperm species showed that, at the turgor loss point, only small fractions of leaf vein xylem conduits were embolized, and substantial xylem embolism arose only under severe dehydration. Experiments on an expanded set of eight angiosperm species showed that outside-xylem hydraulic vulnerability explained 75% to 100% of K leaf decline across the range of dehydration from mild water stress to beyond turgor loss point. Spatially explicit modeling of leaf water transport pointed to a role for reduced membrane conductivity consistent with published data for cells and tissues. Plant-scale modeling suggested that outside-xylem hydraulic vulnerability can protect the xylem from tensions that would induce embolism and disruption of water transport under mild to moderate soil and atmospheric droughts. These findings pinpoint outside-xylem tissues as a central locus for the control of leaf and plant water transport during progressive drought.
ISSN:0032-0889
1532-2548
DOI:10.1104/pp.16.01643