Embolism spread in the primary xylem of Polystichum munitum : implications for water transport during seasonal drought

Brodersen, Craig R.; Rico, Christopher; Guenni, Orlando; Pittermann, Jarmila

doi:10.1111/pce.12618

Title: Embolism spread in the primary xylem of Polystichum munitum : implications for water transport during seasonal drought

Journal Article · Sat Nov 14 00:00:00 EST 2015 · Plant, Cell and Environment

DOI:https://doi.org/10.1111/pce.12618· OSTI ID:1401393

Brodersen, Craig R. ^[1]; Rico, Christopher ^[2]; Guenni, Orlando ^[3]; Pittermann, Jarmila ^[4]

School of Forestry and Environmental Studies Yale University New Haven CT 06511 USA
Pioneer Hi‐Bred International Inc. Woodland CA 95695 USA
Universidad Central de Venezuela Facultad de Agronomía, Instituto de Botánica Agrícola Maracay 2101 Venezuela
Department of Ecology and Evolutionary Biology University of California Santa Cruz CA 95064 USA

Abstract Xylem network structure and function have been characterized for many woody plants, but less is known about fern xylem, particularly in species endemic to climates where water is a limiting resource for months at a time. We characterized seasonal variability in soil moisture and frond water status in a common perennial fern in the redwood understory of a costal California, and then investigated the consequences of drought‐induced embolism on vascular function. Seasonal variability in air temperature and soil water content was minimal, and frond water potential declined slowly over the observational period. Our data show that Polystichum munitum was protected from significant drought‐induced hydraulic dysfunction during this growing season because of a combination of cavitation resistant conduits (Air‐seeding threshold (ASP) = −1.53 MPa; xylem pressure inducing 50% loss of hydraulic conductivity ( P ₅₀ ) = −3.02 MPa) and a soil with low moisture variability. High resolution micro‐computed tomography (MicroCT) imaging revealed patterns of embolism formation in vivo for the first time in ferns providing insight into the functional status of the xylem network under drought conditions. Together with stomatal conductance measurements, these data suggest that P . munitum is adapted to tolerate drier conditions than what was observed during the growing season.

View Accepted Manuscript (Publisher)

Cite

Export

Save

Sponsoring Organization:: USDOE

Grant/Contract Number:: DE‐AC02‐05CH11231

OSTI ID:: 1401393

Journal Information:: Plant, Cell and Environment, Journal Name: Plant, Cell and Environment Vol. 39 Journal Issue: 2; ISSN 0140-7791

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

Citation Metrics:

Cited by: 8 works

Citation information provided by
Web of Science

References (35)

Patterns and consequences of differential vascular sectoriality in 18 temperate tree and shrub species Zanne, A. E.; Sweeney, K.; Sharma, M. Functional Ecology, Vol. 20, Issue 2 https://doi.org/10.1111/j.1365-2435.2006.01101.x	journal	April 2006
Consequences of widespread tree mortality triggered by drought and temperature stress Anderegg, William R. L.; Kane, Jeffrey M.; Anderegg, Leander D. L. Nature Climate Change, Vol. 3, Issue 1 https://doi.org/10.1038/nclimate1635	journal	September 2012
Genotypic Variability in Vulnerability of Leaf Xylem to Cavitation in Water-Stressed and Well-Irrigated Sugarcane Neufeld, Howard S.; Grantz, David A.; Meinzer, Frederick C. Plant Physiology, Vol. 100, Issue 2 https://doi.org/10.1104/pp.100.2.1020	journal	October 1992
Hydraulic properties of fern sporophytes: Consequences for ecological and evolutionary diversification Watkins, James E.; Holbrook, N. Michele; Zwieniecki, Maciej A. American Journal of Botany, Vol. 97, Issue 12 https://doi.org/10.3732/ajb.1000124	journal	December 2010
Global convergence in the vulnerability of forests to drought Choat, Brendan; Jansen, Steven; Brodribb, Tim J. Nature, Vol. 491, Issue 7426 https://doi.org/10.1038/nature11688	journal	November 2012
Tree die-off in response to global change-type drought: mortality insights from a decade of plant water potential measurements Breshears, David D.; Myers, Orrin B.; Meyer, Clifton W. Frontiers in Ecology and the Environment, Vol. 7, Issue 4 https://doi.org/10.1890/080016	journal	May 2009
Automated analysis of three-dimensional xylem networks using high-resolution computed tomography Brodersen, Craig R.; Lee, Eric F.; Choat, Brendan New Phytologist, Vol. 191, Issue 4 https://doi.org/10.1111/j.1469-8137.2011.03754.x	journal	May 2011
Rare pits, large vessels and extreme vulnerability to cavitation in a ring-porous tree species Christman, Mairgareth A.; Sperry, John S.; Smith, Duncan D. New Phytologist, Vol. 193, Issue 3 https://doi.org/10.1111/j.1469-8137.2011.03984.x	journal	December 2011
How do trees die? A test of the hydraulic failure and carbon starvation hypotheses: How do trees die? Sevanto, Sanna; Mcdowell, Nate G.; Dickman, L. Turin Plant, Cell & Environment, Vol. 37, Issue 1 https://doi.org/10.1111/pce.12141	journal	June 2013
Fog in the California redwood forest: ecosystem inputs and use by plants Dawson, T. E. Oecologia, Vol. 117, Issue 4 https://doi.org/10.1007/s004420050683	journal	December 1998
Polystichum munitum (Dryopteridaceae) varies geographically in its capacity to absorb fog water by foliar uptake within the redwood forest ecosystem Limm, Emily B.; Dawson, Todd E. American Journal of Botany, Vol. 97, Issue 7 https://doi.org/10.3732/ajb.1000081	journal	July 2010
Structure and function of bordered pits: new discoveries and impacts on whole-plant hydraulic function Choat, Brendan; Cobb, Alexander R.; Jansen, Steven New Phytologist, Vol. 177, Issue 3 https://doi.org/10.1111/j.1469-8137.2007.02317.x	journal	February 2008
The Structure and Function of Xylem in Seed-Free Vascular Plants: An Evolutionary Perspective Pittermann, Jarmila; Watkins, James E.; Cary, Katharine L. Functional and Ecological Xylem Anatomy https://doi.org/10.1007/978-3-319-15783-2_1	book	January 2015
Xylem Transport Safety and Efficiency Differ among Fynbos Shrub Life History Types and between Two Sites Differing in Mean Rainfall Pratt, Robert B.; Jacobsen, Anna L.; Jacobs, Shayne M. International Journal of Plant Sciences, Vol. 173, Issue 5 https://doi.org/10.1086/665267	journal	June 2012
Mechanism of Water Stress-Induced Xylem Embolism Sperry, John S.; Tyree, Melvin T. Plant Physiology, Vol. 88, Issue 3 https://doi.org/10.1104/pp.88.3.581	journal	November 1988
Differential summer water use by Pinus edulis and Juniperus osteosperma reflects contrasting hydraulic characteristics West, A. G.; Hultine, K. R.; Jackson, T. L. Tree Physiology, Vol. 27, Issue 12 https://doi.org/10.1093/treephys/27.12.1711	journal	December 2007
The Dynamics of Embolism Repair in Xylem: In Vivo Visualizations Using High-Resolution Computed Tomography Brodersen, Craig R.; McElrone, Andrew J.; Choat, Brendan Plant Physiology, Vol. 154, Issue 3 https://doi.org/10.1104/pp.110.162396	journal	September 2010
Cavitation Resistance in Seedless Vascular Plants: The Structure and Function of Interconduit Pit Membranes Brodersen, Craig; Jansen, Steven; Choat, Brendan Plant Physiology, Vol. 165, Issue 2 https://doi.org/10.1104/pp.113.226522	journal	April 2014
Leaf hydraulic architecture and water relations of three ferns from contrasting light habitats Lo Gullo, Maria A.; Raimondo, Fabio; Crisafulli, Alessandro Functional Plant Biology, Vol. 37, Issue 6 https://doi.org/10.1071/FP09303	journal	January 2010
Fog Water and Ecosystem Function: Heterogeneity in a California Redwood Forest Ewing, Holly A.; Weathers, Kathleen C.; Templer, Pamela H. Ecosystems, Vol. 12, Issue 3 https://doi.org/10.1007/s10021-009-9232-x	journal	February 2009
Use of centrifugal force in the study of xylem cavitation Alder, N. N.; Pockman, W. T.; Sperry, J. S. Journal of Experimental Botany, Vol. 48, Issue 3 https://doi.org/10.1093/jxb/48.3.665	journal	March 1997
The physiological implications of primary xylem organization in two ferns: Fern xylem and physiology Brodersen, Craig R.; Roark, Lindsey C.; Pittermann, Jarmila Plant, Cell & Environment, Vol. 35, Issue 11 https://doi.org/10.1111/j.1365-3040.2012.02524.x	journal	May 2012
A method for measuring hydraulic conductivity and embolism in xylem Sperry, J. S.; Donnelly, J. R.; Tyree, M. T. Plant, Cell and Environment, Vol. 11, Issue 1 https://doi.org/10.1111/j.1365-3040.1988.tb01774.x	journal	January 1988
In Vivo Visualizations of Drought-Induced Embolism Spread in Vitis vinifera Brodersen, Craig Robert; McElrone, Andrew Joseph; Choat, Brendan Plant Physiology, Vol. 161, Issue 4 https://doi.org/10.1104/pp.112.212712	journal	March 2013
Hydraulic integration and shrub growth form linked across continental aridity gradients Schenk, H. J.; Espino, S.; Goedhart, C. M. Proceedings of the National Academy of Sciences, Vol. 105, Issue 32 https://doi.org/10.1073/pnas.0804294105	journal	August 2008
The physiological resilience of fern sporophytes and gametophytes: advances in water relations offer new insights into an old lineage Pittermann, Jarmila; Brodersen, Craig; Watkins, James E. Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00285	journal	January 2013
Origin and evolution of the Mediterranean vegetation and climate in Europe Suc, J. -P. Nature, Vol. 307, Issue 5950 https://doi.org/10.1038/307429a0	journal	February 1984
Phenotypic Plasticity and Interactions Among Plants Callaway, Ragan M.; Pennings, Steven C.; Richards, Christina L. Ecology, Vol. 84, Issue 5 https://doi.org/10.1890/0012-9658(2003)084[1115:PPAIAP]2.0.CO;2	journal	May 2003
Xylem water potentials and hydraulic conductances in eight species of ferns Calkin, Howard W.; Gibson, Arthur C.; Nobel, Park S. Canadian Journal of Botany, Vol. 63, Issue 3 https://doi.org/10.1139/b85-079	journal	March 1985
Drought resistance in early and late secondary successional species from a tropical dry forest: the interplay between xylem resistance to embolism, sapwood water storage and leaf shedding: Drought resistance of tropical dry forest species Pineda-GarcÍA, Fernando; Paz, Horacio; Meinzer, Frederick C. Plant, Cell & Environment, Vol. 36, Issue 2 https://doi.org/10.1111/j.1365-3040.2012.02582.x	journal	August 2012
Ferns in an Angiosperm World: Cretaceous Radiation into the Epiphytic Niche and Diversification on the Forest Floor Watkins, J. E.; Cardelús, Catherine L. International Journal of Plant Sciences, Vol. 173, Issue 6 https://doi.org/10.1086/665974	journal	July 2012
Evolution, origin and age of lineages in the Californian and Mediterranean floras Ackerly, David D. Journal of Biogeography, Vol. 36, Issue 7 https://doi.org/10.1111/j.1365-2699.2009.02097.x	journal	July 2009
Structure-function constraints of tracheid-based xylem: a comparison of conifers and ferns Pittermann, Jarmila; Limm, Emily; Rico, Christopher New Phytologist, Vol. 192, Issue 2 https://doi.org/10.1111/j.1469-8137.2011.03817.x	journal	July 2011
Constraints and trade-offs in Mediterranean plant communities: The case of holm oak-Aleppo pine forests Zavala, M. A.; Espelta, J. M.; Retana, Javier The Botanical Review, Vol. 66, Issue 1 https://doi.org/10.1007/BF02857785	journal	January 2000
Sustained and significant negative water pressure in xylem Pockman, William T.; Sperry, John S.; O'Leary, James W. Nature, Vol. 378, Issue 6558 https://doi.org/10.1038/378715a0	journal	December 1995

Similar Records

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

Journal Article · Fri Feb 12 00:00:00 EST 2021 · Plant Physiology (Bethesda) · OSTI ID:1401393

Wason, Jay; Bouda, Martin; Lee, Eric F.; +5 more

Distinct xylem responses to acute vs prolonged drought in pine trees

Journal Article · Fri Jan 24 00:00:00 EST 2020 · Tree Physiology (Online) · OSTI ID:1401393

Guérin, Marceau; von Arx, Georg; Martin-Benito, Dario; +5 more

Differences in xylem and leaf hydraulic traits explain differences in drought tolerance among mature Amazon rainforest trees

Journal Article · Thu Apr 20 00:00:00 EDT 2017 · Global Change Biology · OSTI ID:1401393

Powell, Thomas L.; Wheeler, James K.; de Oliveira, Alex A. R.; +4 more

Title: Embolism spread in the primary xylem of Polystichum munitum : implications for water transport during seasonal drought

Citation Formats

References (35)

Similar Records

Related Subjects