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Title: Xylem network connectivity and embolism spread in grapevine( Vitis vinifera L.)

Journal Article · · Plant Physiology (Bethesda)
ORCiD logo [1]; ORCiD logo [2];  [3];  [4];  [5];  [6]; ORCiD logo [7]; ORCiD logo [8]
  1. School of Forest Resources, University of Maine, Orono, Maine 04469, School of the Environment, Yale University, New Haven, CT 06520
  2. Institute of Botany, Czech Academy of Sciences, Průhonice, Czechia
  3. Department of Engineering Sciences, Clackamas Community College, Oregon City, Oregon 97045
  4. Department of Viticulture and Enology, University of California Davis, Davis, California, Crops Pathology and Genetics Research Unit, USDA-ARS, Davis, California
  5. Department of Chemical Engineering, University of California Davis, Davis, California
  6. Department of Plant Science, University of California Davis, Davis, California
  7. Department of Viticulture and Enology, University of California Davis, Davis, California
  8. School of the Environment, Yale University, New Haven, CT 06520

Abstract Xylem networks are vulnerable to the formation and spread of gas embolisms that reduce water transport. Embolisms spread through interconduit pits, but the three-dimensional (3D) complexity and scale of xylem networks means that the functional implications of intervessel connections are not well understood. Here, xylem networks of grapevine (Vitis vinifera L.) were reconstructed from 3D high-resolution X-ray micro-computed tomography (microCT) images. Xylem network performance was then modeled to simulate loss of hydraulic conductivity under increasingly negative xylem sap pressure simulating drought stress conditions. We also considered the sensitivity of xylem network performance to changes in key network parameters. We found that the mean pit area per intervessel connection was constant across 10 networks from three, 1.5-m stem segments, but short (0.5 cm) segments fail to capture complete network connectivity. Simulations showed that network organization imparted additional resistance to embolism spread beyond the air-seeding threshold of pit membranes. Xylem network vulnerability to embolism spread was most sensitive to variation in the number and location of vessels that were initially embolized and pit membrane vulnerability. Our results show that xylem network organization can increase stem resistance to embolism spread by 40% (0.66 MPa) and challenge the notion that a single embolism can spread rapidly throughout an entire xylem network.

Sponsoring Organization:
USDOE
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1784825
Journal Information:
Plant Physiology (Bethesda), Journal Name: Plant Physiology (Bethesda) Journal Issue: 1 Vol. 186; ISSN 0032-0889
Publisher:
Oxford University PressCopyright Statement
Country of Publication:
United States
Language:
English

References (45)

An Introduction to Statistical Modeling of Extreme Values book January 2001
Xylem Structure and the Ascent of Sap book January 2002
Use of X-ray computed microtomography for non-invasive determination of wood anatomical characteristics journal October 2004
The relevance of xylem network structure for plant hydraulic efficiency and safety journal August 2007
Analysis of HRCT-derived xylem network reveals reverse flow in some vessels journal September 2013
Nanobubbles: a new paradigm for air-seeding in xylem journal April 2015
Global convergence in the vulnerability of forests to drought journal November 2012
In vivo pressure gradient heterogeneity increases flow contribution of small diameter vessels in grapevine journal December 2019
Xylem Structure and Connectivity in Grapevine (Vitis vinifera) Shoots Provides a Passive Mechanism for the Spread of Bacteria in Grape Plants journal June 2006
Quantitative Analysis of the Phenotypic Variability of Shoot Architecture in Two Grapevine ( Vitis vinifera ) Cultivars journal January 2007
A broad survey of hydraulic and mechanical safety in the xylem of conifers journal June 2014
Physical analysis of the process of cavitation in xylem sap journal June 2002
Patterns of drought-induced embolism formation and spread in living walnut saplings visualized using X-ray microtomography journal June 2015
In Vivo Visualizations of Drought-Induced Embolism Spread in Vitis vinifera journal March 2013
Noninvasive Measurement of Vulnerability to Drought-Induced Embolism by X-Ray Microtomography journal November 2015
Xylem Surfactants Introduce a New Element to the Cohesion-Tension Theory journal December 2016
Xylem Embolism Spreads by Single-Conduit Events in Three Dry Forest Angiosperm Stems journal June 2020
TRY - a global database of plant traits: TRY - A GLOBAL DATABASE OF PLANT TRAITS journal June 2011
Comparative analysis of end wall resistivity in xylem conduits journal April 2005
Inter-vessel pitting and cavitation in woody Rosaceae and other vesselled plants: a basis for a safety versus efficiency trade-off in xylem transport journal June 2005
The spatial pattern of air seeding thresholds in mature sugar maple trees journal September 2005
Wood Fibres with Living Protoplasts journal April 1963
Testing the ‘rare pit’ hypothesis for xylem cavitation resistance in three species of Acer journal April 2009
Automated analysis of three-dimensional xylem networks using high-resolution computed tomography journal May 2011
Rare pits, large vessels and extreme vulnerability to cavitation in a ring-porous tree species journal December 2011
Inflorescence and bunch architecture development in Vitis vinifera L. journal July 2004
Measurements of stem xylem hydraulic conductivity in the laboratory and field: Measurements of stem xylem hydraulic conductivity journal April 2012
Synchrotron X-ray microtomography of xylem embolism in Sequoia sempervirens saplings during cycles of drought and recovery journal November 2014
Hydraulic safety margins and air-seeding thresholds in roots, trunks, branches and petioles of four northern hardwood trees journal April 2018
X-ray microtomography (micro-CT): a reference technology for high-resolution quantification of xylem embolism in trees: A reference method for xylem embolism journal July 2014
A network model links wood anatomy to xylem tissue hydraulic behaviour and vulnerability to cavitation: Model links wood anatomy to plant hydraulics journal September 2018
High porosity with tiny pore constrictions and unbending pathways characterize the 3D structure of intervessel pit membranes in angiosperm xylem journal August 2019
Vessel-length distribution in stems of some American woody plants journal October 1981
Functional Status of Xylem Through Time journal April 2019
Function and three-dimensional structure of intervessel pit membranes in angiosperms: a review journal November 2019
Visualizing water-filled versus embolized status of xylem conduits by desktop x-ray microtomography journal January 2013
fitplc - an R package to fit hydraulic vulnerability curves journal January 2017
How to quantify conduits in wood? journal January 2013
A quantitative and statistically robust method for the determination of xylem conduit spatial distribution journal August 2010
Spatial distribution and packing of xylem conduits journal June 2012
Xylem vessel relays contribute to radial connectivity in grapevine stems ( Vitis vinifera and V. arizonica ; Vitaceae) journal February 2013
New frontiers in the three-dimensional visualization of plant structure and function journal February 2016
MicroCT imaging as a tool to study vessel endings in situ journal September 2017
Analysis of circular bordered pit function I. Angiosperm vessels with homogenous pit membranes journal March 2004
Vegetative Anatomy of Cultivated Grapes--A Review journal January 1974