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Title: Outside-xylem pathways, not xylem embolism, drive leaf hydraulic decline with dehydration

item SCOFFONI, CHRISTINE - University Of California
item ALBUQUERQUE, CAETANO - University Of California
item BRODERSEN, CRAIG - Yale University
item TOWNES, SHATARA - University Of California
item JOHN, GRACE - University Of California
item BARTLETT, MEGAN - University Of California
item BUCKLEY, THOMAS - University Of Sydney
item McElrone, Andrew
item SACK, LAWREN - University Of California

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/3/2017
Publication Date: 2/20/2017
Citation: Scoffoni, C., Albuquerque, C., Brodersen, C., Townes, S., John, G., Bartlett, M., Buckley, T., McElrone, A.J., Sack, L. 2017. Outside-xylem pathways, not xylem embolism, drive leaf hydraulic decline with dehydration. Plant Physiology. 173(2):1197-1210.

Interpretive Summary: Water scarcity threatens plant growth in natural and agricultural ecosystems worldwide. We studied how drought induced water stress alters the ability of leaves to transport water to the sites where it is exchanged for carbon dioxide. Using a variety of techniques including x-ray micro computed tomography, we found that changes in leaf mesophyll properties drive leaf and whole plant hydraulic decline with dehydration, protecting plants from catastrophic embolism (i.e. air bubble blockages) in xylem conduits of several species.

Technical Abstract: Leaf hydraulic supply is crucial to enable the maintenance of open stomata for CO2 capture and plant growth. During drought-induced leaf dehydration, the capacity for water flow through the leaf (Kleaf) declines, a phenomenon surprisingly attributed for the past fifty years solely to the formation of gas bubbles in the leaf veins, neglecting the potential impact of dysfunction in outside-xylem pathways which account for a great portion of the leaf hydraulic resistance. We combined unique hydraulic measurements, x-ray microtomography visualization, and modeling to quantify the vulnerability of the xylem and outside-xylem pathways to hydraulic decline and their influence on whole-plant water transport. Outside-xylem pathways played the major role in shaping Kleaf and whole plant hydraulic vulnerability, whereas xylem conductance was maintained in dehydrating leaves, and very few gas-filled conduits were observed even when Kleaf had declined by 80%. Models suggested that membrane permeability and reduced cell wall thickness may play a role in outside-xylem hydraulic decline. Overall these findings provide unprecedented resolution for partitioning the drivers of leaf hydraulic decline, and pinpoint the leaf mesophyll as a central locus for the dynamic control of water transport especially during progressive drought.