N. Michèle Holbrook

Harvard University

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Maciej A. Zwieniecki

University of California, Davis

Fulton E. Rockwell

Harvard University Press

Timothy J. Brodribb

University of Tasmania

Guillermo Goldstein

University of Miami

Abraham D. Stroock

Cornell University

Francis E. Putz

University of Florida

Lawren Sack

University of California, Los Angeles

Uri Hochberg

Agricultural Research Organization

Frederick C. Meinzer

Pacific Northwest Research Station

Peter J. Melcher

Ithaca College

Cooperative Institutions

Harvard University

Harvard University Press

Australian National University

University of California, Berkeley

United States Department of Agriculture

University of California, Los Angeles

Hebrew University of Jerusalem

Agricultural Research Organization

Cornell University

University of California, Davis

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Loss of plasma membrane conductance in outside-xylem zone explains non-stomatal control of transpiration

bioRxiv (Cold Spring Harbor Laboratory) (2025)

Piyush Jain Sabyasachi Sen Fulton E. Rockwell Robert J. Twohey Annika E. Huber

The conventional assumption is that stomatal conductance (gs) dominates the regulation of water and carbon dioxide fluxes between leaves and the atmosphere. Here, a nanoreporter of water status at the mesophyll cell surface and local xylem within intact maize leaves documents significant undersaturation of water vapor in the outside-xylem zone (OXZ) and a large loss of conductance of this zone (goxz) at moderate xylem water stress (no turgor loss). The ratio of the resistances (1/goxz)/(1/gs) serves as a predictive phenotype of undersaturation, non-stomatal regulation of transpiration, errors in standard gas exchange analysis, and an increase of intrinsic water use efficiency (iWUE). Cell scale access to water status reveals symplasmic-apoplasmic disequilibrium and informs a biophysical model that can explain experimental observations quantitatively based on localization of variable conductance to the plasma membrane. This work opens new paths of inquiry into the molecular basis and functional consequences of non-stomatal regulation of transpiration.

Stomatal Conductance

10.1101/2025.02.15.638441

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Reversible Deformation of Transfusion Tracheids in Taxus baccata Is Associated with a Reversible Decrease in Leaf Hydraulic Conductance

PLANT PHYSIOLOGY (2014)

Yong‐Jiang Zhang Fulton E. Rockwell James K. Wheeler N. Michèle Holbrook

Declines in leaf hydraulic conductance (Kleaf) with increasing water stress have been attributed to cavitation of the leaf xylem. However, in the leaves of conifers, the reversible collapse of transfusion tracheids may provide an alternative explanation. Using Taxus baccata, a conifer species without resin, we developed a modified rehydration technique that allows the separation of declines in Kleaf into two components: one reversible and one irreversible upon relaxation of water potential to −1 MPa. We surveyed leaves at a range of water potentials for evidence of cavitation using cryo-scanning electron microscopy and quantified dehydration-induced structural changes in transfusion tracheids by cryo-fluorescence microscopy. Irreversible declines in Kleaf did not occur until leaf water potentials were more negative than −3 MPa. Declines in Kleaf between −2 and −3 MPa were reversible and accompanied by the collapse of transfusion tracheids, as evidenced by cryo-fluorescence microscopy. Based on cryo-scanning electron microscopy, cavitation of either transfusion or xylem tracheids did not contribute to declines in Kleaf in the reversible range. Moreover, the deformation of transfusion tracheids was quickly reversible, thus acting as a circuit breaker regulating the flux of water through the leaf vasculature. As transfusion tissue is present in all gymnosperms, the reversible collapse of transfusion tracheids may be a general mechanism in this group for the protection of leaf xylem from excessive loads generated in the living leaf tissue.

Tracheid

10.1104/pp.114.243105

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Citations (41)

Appendix A. A figure showing correlations between stem hydraulic conductivity and wood density in Ficus species.

Figshare (2016)

Guang‐You Hao Guillermo Goldstein Lawren Sack N. Michèle Holbrook Zhihui Liu

A figure showing correlations between stem hydraulic conductivity and wood density in Ficus species.

Ficus

10.6084/m9.figshare.3552147

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Water Stress Deforms Tracheids Peripheral to the Leaf Vein of a Tropical Conifer

PLANT PHYSIOLOGY (2005)

Timothy J. Brodribb N. Michèle Holbrook

Abstract Just as a soggy paper straw is prone to yielding under the applied suction of a thirsty drinker, the xylem tracheids in leaves seem prone to collapse as water potential declines, impeding their function. Here we describe the collapse, under tension, of lignified cells peripheral to the leaf vein of a broad-leaved rainforest conifer, Podocarpus grayi de Laub. Leaves of Podocarpus are characterized by an array of cylindrical tracheids aligned perpendicular to the leaf vein, apparently involved in the distribution of water radially through the mesophyll. During leaf desiccation the majority of these tracheids collapsed from circular to flat over the water potential range −1.5 to −2.8 MPa. An increase in the percentage of tracheids collapsed during imposed water stress was mirrored by declining leaf hydraulic conductivity (K leaf), implying a direct effect on water transport efficiency. Stomata responded to water stress by closing at −2.0 MPa when 45% of cells were collapsed and K leaf had declined by 25%. This was still substantially before the initial indications of cavitation-induced loss of hydraulic conductance in the leaf vein, at −3 MPa. Plants droughted until 49% of tracheids had collapsed were found to fully recover tracheid shape and leaf function 1 week after rewatering. A simple mechanical model of tracheid collapse, derived from the theoretical buckling pressure for pipes, accurately predicted the collapse dynamics observed in P. grayi, substantiating estimates of cell wall elasticity and measured leaf water potential. The possible adaptive advantages of collapsible vascular tissue are discussed.

Tracheid

Water Transport

Podocarpus

Water Stress

10.1104/pp.104.058156

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Citations (174)

Faculty Opinions recommendation of Freeze/thaw-induced embolism depends on nadir temperature: the heterogeneous hydration hypothesis.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature (2006)

N. Michèle Holbrook

Nadir

10.3410/f.1032354.373032

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Faculty Opinions recommendation of Physical limits and design principles for plant and fungal movements.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature (2005)

N. Michèle Holbrook

10.3410/f.1009911.323300

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Freeze/Thaw-Induced Embolism: Probability of Critical Bubble Formation Depends on Speed of Ice Formation

Frontiers in Plant Science (2012)

Sanna Sevanto N. Michèle Holbrook Marilyn C. Ball

ORIGINAL RESEARCH article Front. Plant Sci., 06 June 2012Sec. Plant Biophysics and Modeling Volume 3 - 2012 | https://doi.org/10.3389/fpls.2012.00107

Electrical conduit

Ice formation

Ice nucleus

Liquid bubble

10.3389/fpls.2012.00107

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Citations (66)

Leaf Hydraulic Architecture and Stomatal Conductance: A Functional Perspective

PLANT PHYSIOLOGY (2017)

Fulton E. Rockwell N. Michèle Holbrook

Mechanistic modeling of water transport from petiole to stomata provides new perspectives on optimality in vascular and mesophyll transport properties.

Petiole (insect anatomy)

Stomatal Conductance

Water Transport

10.1104/pp.17.00303

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Citations (38)

Changes In Ploidy Affect Vascular Allometry And Hydraulic Function In Trees

bioRxiv (Cold Spring Harbor Laboratory) (2021)

Miguel Barceló‐Anguiano N. Michèle Holbrook JI Hormaza Juan M. Losada

Summary The enucleated vascular elements of the xylem and the phloem offer an excellent system to test the effect of ploidy on plant function because variation in vascular geometry has a direct influence on transport efficiency. However, evaluations of conduit sizes in polyploid plants have remained elusive, most remarkably in woody species. We used a combination of molecular, physiological, and microscopy techniques to model the hydraulic resistance between source and sinks in tetraploid and diploid mango trees. Tetraploids exhibited larger chloroplasts, mesophyll cells, and stomatal guard cells, resulting in higher leaf elastic modulus and lower dehydration rates despite the high water potentials of both ploidies in the field. Both the xylem and the phloem displayed a scaling of conduits with ploidy, revealing attenuated hydraulic resistance in tetraploids. Conspicuous wall hygroscopic moieties in the cells involved in processes of transpiration and transport advocates a role in volumetric adjustments due to turgor change in polyploids, which, together with the enlargement of organelles, cells, and tissues that are critical for water and photo assimilate transport at long distances, imply major physiological novelties of polyploidy.

Plasmodesma

Allometry

Water Transport

Polyploid

10.1101/2021.06.10.447312

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Faculty Opinions recommendation of The transpiration of water at negative pressures in a synthetic tree.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature (2008)

N. Michèle Holbrook

Plant scientists believe that transpiration-the motion of water from the soil, through a vascular plant, and into the air-occurs by a passive, wicking mechanism. This mechanism is described by the cohesion-tension theory: loss of water by evaporation reduces the pressure of the liquid water within the leaf relative to atmospheric pressure; this reduced pressure pulls liquid water out of the soil and up the xylem to maintain hydration. Strikingly, the absolute pressure of the water within the xylem is often negative, such that the liquid is under tension and is thermodynamically metastable with respect to the vapour phase. Qualitatively, this mechanism is the same as that which drives fluid through the synthetic wicks that are key elements in technologies for heat transfer, fuel cells and portable chemical systems. Quantitatively, the differences in pressure generated in plants to drive flow can be more than a hundredfold larger than those generated in synthetic wicks. Here we present the design and operation of a microfluidic system formed in a synthetic hydrogel. This synthetic 'tree' captures the main attributes of transpiration in plants: transduction of subsaturation in the vapour phase of water into negative pressures in the liquid phase, stabilization and flow of liquid water at large negative pressures (-1.0 MPa or lower), continuous heat transfer with the evaporation of liquid water at negative pressure, and continuous extraction of liquid water from subsaturated sources. This development opens the opportunity for technological uses of water under tension and for new experimental studies of the liquid state of water. PMID: 18784721

Water Transport

Transpiration stream

10.3410/f.1120859.577124

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