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Title: Growth and physiological responses of isohydric and anisohydric poplars to drought

Abstract

Understanding how different plants prioritize carbon gain and drought vulnerability under a variable water supply is important for predicting which trees will maximize woody biomass production under different environmental conditions. Here, Populus balsamifera (BS, isohydric genotype), P. simonii (SI, previously uncharacterized stomatal behaviour), and their cross, P. balsamifera x simonii (BSxSI, anisohydric genotype) were studied to assess the physiological basis for biomass accumulation and water-use efficiency across a range of water availabilities. Under ample water, whole plant stomatal conductance (gs), transpiration (E), and growth rates were higher in anisohydric genotypes (SI and BSxSI) than in isohydric poplars (BS). Under drought, all genotypes regulated the leaf to stem water potential gradient via changes in gs, synchronizing leaf hydraulic conductance (Kleaf) and E: isohydric plants reduced Kleaf, gs, and E, whereas anisohydric genotypes maintained high Kleaf and E, which reduced both leaf and stem water potentials. Nevertheless, SI poplars reduced their plant hydraulic conductance (Kplant) during water stress and, unlike, BSxSI plants, recovered rapidly from drought. Low gs of the isohydric BS under drought reduced CO2 assimilation rates and biomass potential under moderate water stress. While anisohydric genotypes had the fastest growth under ample water and higher photosynthetic rates under increasing watermore » stress, isohydric poplars had higher water-use efficiency. Overall, the results indicate three strategies for how closely related biomass species deal with water stress: survival-isohydric (BS), sensitive-anisohydric (BSxSI), and resilience-anisohydric (SI). Lastly, we discuss implications for woody biomass growth, water-use efficiency, and survival under variable environmental conditions.« less

Authors:
 [1];  [2];  [3];  [4];  [5]
  1. Hebrew Univ. of Jerusalem (Israel). Inst. of Plant Sciences and Genetics in Agriculture
  2. Bordeaux Sciences Agro UMR INRA-ISPA, Gradignan (France); North Carolina State Univ., Raleigh, NC (United States); Duke Univ., Durham, NC (United States)
  3. Duke Univ., Durham, NC (United States); Swedish University of Agricultural Sciences (SLU), Umea (Sweden)
  4. Duke Univ., Durham, NC (United States); Univ. of Western Ontario, London, ON (Canada)
  5. Hebrew Univ. of Jerusalem (Israel). Inst. of Plant Sciences and Genetics in Agricultur
Publication Date:
Research Org.:
Duke Univ., Durham, NC (United States)
Sponsoring Org.:
USDOE; US–Israeli Bi-national Science Foundation; National Science Foundation (NSF); Natural Sciences and Engineering Research Council of Canada (NSERC); USDA
OSTI Identifier:
1343100
Grant/Contract Number:  
SC0006967
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Experimental Botany
Additional Journal Information:
Journal Volume: 66; Journal Issue: 14; Journal ID: ISSN 0022-0957
Publisher:
Oxford University Press
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; 59 BASIC BIOLOGICAL SCIENCES; Bioenergy; biomass; carbon; hydraulic conductance; stomata; transpiration

Citation Formats

Attia, Ziv, Domec, Jean-Christophe, Oren, Ram, Way, Danielle A., and Moshelion, Menachem. Growth and physiological responses of isohydric and anisohydric poplars to drought. United States: N. p., 2015. Web. doi:10.1093/jxb/erv195.
Attia, Ziv, Domec, Jean-Christophe, Oren, Ram, Way, Danielle A., & Moshelion, Menachem. Growth and physiological responses of isohydric and anisohydric poplars to drought. United States. https://doi.org/10.1093/jxb/erv195
Attia, Ziv, Domec, Jean-Christophe, Oren, Ram, Way, Danielle A., and Moshelion, Menachem. Thu . "Growth and physiological responses of isohydric and anisohydric poplars to drought". United States. https://doi.org/10.1093/jxb/erv195. https://www.osti.gov/servlets/purl/1343100.
@article{osti_1343100,
title = {Growth and physiological responses of isohydric and anisohydric poplars to drought},
author = {Attia, Ziv and Domec, Jean-Christophe and Oren, Ram and Way, Danielle A. and Moshelion, Menachem},
abstractNote = {Understanding how different plants prioritize carbon gain and drought vulnerability under a variable water supply is important for predicting which trees will maximize woody biomass production under different environmental conditions. Here, Populus balsamifera (BS, isohydric genotype), P. simonii (SI, previously uncharacterized stomatal behaviour), and their cross, P. balsamifera x simonii (BSxSI, anisohydric genotype) were studied to assess the physiological basis for biomass accumulation and water-use efficiency across a range of water availabilities. Under ample water, whole plant stomatal conductance (gs), transpiration (E), and growth rates were higher in anisohydric genotypes (SI and BSxSI) than in isohydric poplars (BS). Under drought, all genotypes regulated the leaf to stem water potential gradient via changes in gs, synchronizing leaf hydraulic conductance (Kleaf) and E: isohydric plants reduced Kleaf, gs, and E, whereas anisohydric genotypes maintained high Kleaf and E, which reduced both leaf and stem water potentials. Nevertheless, SI poplars reduced their plant hydraulic conductance (Kplant) during water stress and, unlike, BSxSI plants, recovered rapidly from drought. Low gs of the isohydric BS under drought reduced CO2 assimilation rates and biomass potential under moderate water stress. While anisohydric genotypes had the fastest growth under ample water and higher photosynthetic rates under increasing water stress, isohydric poplars had higher water-use efficiency. Overall, the results indicate three strategies for how closely related biomass species deal with water stress: survival-isohydric (BS), sensitive-anisohydric (BSxSI), and resilience-anisohydric (SI). Lastly, we discuss implications for woody biomass growth, water-use efficiency, and survival under variable environmental conditions.},
doi = {10.1093/jxb/erv195},
journal = {Journal of Experimental Botany},
number = 14,
volume = 66,
place = {United States},
year = {Thu May 07 00:00:00 EDT 2015},
month = {Thu May 07 00:00:00 EDT 2015}
}

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Works referenced in this record:

Adaptation, Niche Conservatism, and Convergence: Comparative Studies of Leaf Evolution in the California Chaparral
journal, May 2004

  • Ackerly, David D.
  • The American Naturalist, Vol. 163, Issue 5
  • DOI: 10.1086/383062

Functional characterization of drought-responsive aquaporins in Populus balsamifera and Populus simonii×balsamifera clones with different drought resistance strategies
journal, November 2010


Stomatal factors and vulnerability of stem xylem to cavitation in poplars
journal, June 2011


Water Potential Gradients in Field Tobacco
journal, August 1970


Drought resistance, water-use efficiency, and yield potential—are they compatible, dissonant, or mutually exclusive?
journal, January 2005

  • Blum, A.
  • Australian Journal of Agricultural Research, Vol. 56, Issue 11
  • DOI: 10.1071/AR05069

Plant genome sequencing — applications for crop improvement
journal, April 2014


Temperate forest trees and stands under severe drought: a review of ecophysiological responses, adaptation processes and long-term consequences
journal, September 2006

  • Bréda, Nathalie; Huc, Roland; Granier, André
  • Annals of Forest Science, Vol. 63, Issue 6
  • DOI: 10.1051/forest:2006042

Nucleotide diversity among natural populations of a North American poplar ( Populus balsamifera , Salicaceae)
journal, April 2009


Hydraulic Failure Defines the Recovery and Point of Death in Water-Stressed Conifers
journal, November 2008


Stomatal Closure during Leaf Dehydration, Correlation with Other Leaf Physiological Traits
journal, July 2003


Linking root traits to potential growth rate in six temperate tree species
journal, June 2002


Influence of nutrient versus water supply on hydraulic architecture and water balance in Pinus taeda
journal, October 2000


A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species
journal, June 1980

  • Farquhar, G. D.; von Caemmerer, S.; Berry, J. A.
  • Planta, Vol. 149, Issue 1
  • DOI: 10.1007/BF00386231

Vulnerability to drought-induced cavitation in poplars: synthesis and future opportunities: Drought-induced cavitation in poplars: a review
journal, January 2015

  • Fichot, RÉGis; Brignolas, Franck; Cochard, HervÉ
  • Plant, Cell & Environment, Vol. 38, Issue 7
  • DOI: 10.1111/pce.12491

Diffusional conductances to CO2 as a target for increasing photosynthesis and photosynthetic water-use efficiency
journal, May 2013

  • Flexas, Jaume; Niinemets, Ülo; Gallé, Alexander
  • Photosynthesis Research, Vol. 117, Issue 1-3
  • DOI: 10.1007/s11120-013-9844-z

Variable timing of developmental progression in the stomatal pathway in Arabidopsis cotyledons
journal, March 2002


Photosynthetic Organs of Desert Plants
journal, November 1998


The new competition for land: Food, energy, and climate change
journal, January 2011


The impact of water and nutrient deficiencies on the growth, gas exchange and water relations of red oak and chestnut oak
journal, October 1992


How does drought tolerance compare between two improved hybrids of balsam poplar and an unimproved native species?
journal, March 2011


Investigation on water consumption characteristics and water use efficiency of poplar under soil water deficits on the Loess Plateau
journal, November 2006


A new look at water transport regulation in plants
journal, July 2014

  • Martínez-Vilalta, Jordi; Poyatos, Rafael; Aguadé, David
  • New Phytologist, Vol. 204, Issue 1
  • DOI: 10.1111/nph.12912

Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought?
journal, June 2008


Decoding Leaf Hydraulics with a Spatially Explicit Model: Principles of Venation Architecture and Implications for Its Evolution
journal, April 2010

  • McKown, Athena D.; Cochard, Hervé; Sack, Lawren
  • The American Naturalist, Vol. 175, Issue 4
  • DOI: 10.1086/650721

Xylem recovery from drought-induced embolism: where is the hydraulic point of no return?
journal, April 2013


Global developments in the competition for land from biofuels
journal, January 2011


Limitation of stomatal conductance by hydraulic traits: sensing or preventing xylem cavitation?
journal, October 2000


Leaf Hydraulics
journal, June 2006


Risk-taking plants: Anisohydric behavior as a stress-resistance trait
journal, July 2012

  • Sade, Nir; Gebremedhin, Alem; Moshelion, Menachem
  • Plant Signaling & Behavior, Vol. 7, Issue 7
  • DOI: 10.4161/psb.20505

The dynamic isohydric-anisohydric behavior of plants upon fruit development: taking a risk for the next generation
journal, September 2014


Poplar as a feedstock for biofuels: A review of compositional characteristics
journal, March 2010

  • Sannigrahi, Poulomi; Ragauskas, Arthur J.; Tuskan, Gerald A.
  • Biofuels, Bioproducts and Biorefining, Vol. 4, Issue 2
  • DOI: 10.1002/bbb.206

Decline of Leaf Hydraulic Conductance with Dehydration: Relationship to Leaf Size and Venation Architecture
journal, April 2011

  • Scoffoni, Christine; Rawls, Michael; McKown, Athena
  • Plant Physiology, Vol. 156, Issue 2
  • DOI: 10.1104/pp.111.173856

Enhanced assimilation rate and water use efficiency with latitude through increased photosynthetic capacity and internal conductance in balsam poplar ( Populus balsamifera L.)
journal, December 2009


Higher US crop prices trigger little area expansion so marginal land for biofuel crops is limited
journal, September 2011


The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)
journal, September 2006


Differences in drought resistance among 3 deciduous oak species grown in large boxes
journal, January 1993

  • Vivin, P.; Aussenac, G.; Levy, G.
  • Annales des Sciences Forestières, Vol. 50, Issue 3
  • DOI: 10.1051/forest:19930301

The Biology of Transpiration. From Guard Cells to Globe
journal, January 2007


The kinetics of ribulose-1,5-bisphosphate carboxylase/oxygenase in vivo inferred from measurements of photosynthesis in leaves of transgenic tobacco
journal, November 1994

  • von Caemmerer, Susanne; Evans, John R.; Hudson, Graham S.
  • Planta, Vol. 195, Issue 1
  • DOI: 10.1007/BF00206296

Interrelationships between water use and growth traits in biomass-producing willows
journal, January 2004


Impacts of tree height on leaf hydraulic architecture and stomatal control in Douglas-fir
journal, May 2007


Poplar as a feedstock for biofuels: A review of compositional characteristics
journal, March 2010

  • Sannigrahi, Poulomi; Ragauskas, Arthur J.; Tuskan, Gerald A.
  • Biofuels, Bioproducts and Biorefining, Vol. 4, Issue 2
  • DOI: 10.1002/bbb.206

Linking root traits to potential growth rate in six temperate tree species
journal, June 2002


Diffusional conductances to CO2 as a target for increasing photosynthesis and photosynthetic water-use efficiency
journal, May 2013

  • Flexas, Jaume; Niinemets, Ülo; Gallé, Alexander
  • Photosynthesis Research, Vol. 117, Issue 1-3
  • DOI: 10.1007/s11120-013-9844-z

A review of biomass quality research relevant to the use of poplar and willow for energy conversion
journal, January 1990


Hydraulic constraints on plant gas exchange
journal, July 2000


Early effects of water deficit on two parental clones of Populus nigra grown under different environmental conditions
journal, January 2010

  • Cocozza, Claudia; Cherubini, Paolo; Regier, Nicole
  • Functional Plant Biology, Vol. 37, Issue 3
  • DOI: 10.1071/fp09156

Adaptation, Niche Conservatism, and Convergence: Comparative Studies of Leaf Evolution in the California Chaparral
journal, May 2004

  • Ackerly, David D.
  • The American Naturalist, Vol. 163, Issue 5
  • DOI: 10.1086/383062

Decoding Leaf Hydraulics with a Spatially Explicit Model: Principles of Venation Architecture and Implications for Its Evolution
journal, April 2010

  • McKown, Athena D.; Cochard, Hervé; Sack, Lawren
  • The American Naturalist, Vol. 175, Issue 4
  • DOI: 10.1086/650721

The impact of water and nutrient deficiencies on the growth, gas exchange and water relations of red oak and chestnut oak
journal, October 1992


Tree responses to drought
journal, March 2011


Xylem recovery from drought-induced embolism: where is the hydraulic point of no return?
journal, April 2013


The dynamic isohydric-anisohydric behavior of plants upon fruit development: taking a risk for the next generation
journal, September 2014


Stomatal Closure during Leaf Dehydration, Correlation with Other Leaf Physiological Traits
journal, July 2003


The Biology of Transpiration. From Guard Cells to Globe
journal, January 2007


Decline of Leaf Hydraulic Conductance with Dehydration: Relationship to Leaf Size and Venation Architecture
journal, April 2011

  • Scoffoni, Christine; Rawls, Michael; McKown, Athena
  • Plant Physiology, Vol. 156, Issue 2
  • DOI: 10.1104/pp.111.173856

Water Potential Gradients in Field Tobacco
journal, August 1970


Enhanced assimilation rate and water use efficiency with latitude through increased photosynthetic capacity and internal conductance in balsam poplar ( Populus balsamifera L.)
journal, December 2009


Functional characterization of drought-responsive aquaporins in Populus balsamifera and Populus simonii×balsamifera clones with different drought resistance strategies
journal, November 2010


Stomatal factors and vulnerability of stem xylem to cavitation in poplars
journal, June 2011


Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought?
journal, June 2008


Nucleotide diversity among natural populations of a North American poplar ( Populus balsamifera , Salicaceae)
journal, April 2009


A new look at water transport regulation in plants
journal, July 2014

  • Martínez-Vilalta, Jordi; Poyatos, Rafael; Aguadé, David
  • New Phytologist, Vol. 204, Issue 1
  • DOI: 10.1111/nph.12912

Risk-taking plants: Anisohydric behavior as a stress-resistance trait
journal, July 2012

  • Sade, Nir; Gebremedhin, Alem; Moshelion, Menachem
  • Plant Signaling & Behavior, Vol. 7, Issue 7
  • DOI: 10.4161/psb.20505

Works referencing / citing this record:

Rainfall seasonality and drought performance shape the distribution of tropical tree species in Ghana
journal, July 2018

  • Amissah, Lucy; Mohren, Godefridus M. J.; Kyereh, Boateng
  • Ecology and Evolution, Vol. 8, Issue 16
  • DOI: 10.1002/ece3.4384

Contrasting strategies of hydraulic control in two codominant temperate tree species
journal, December 2016

  • Matheny, Ashley M.; Fiorella, Richard P.; Bohrer, Gil
  • Ecohydrology, Vol. 10, Issue 3, Article No. e1815
  • DOI: 10.1002/eco.1815

Structural and anatomical responses of Pinus sylvestris and Tilia platyphyllos seedlings exposed to water shortage
journal, May 2018


Vapour pressure deficit control in relation to water transport and water productivity in greenhouse tomato production during summer
journal, March 2017

  • Zhang, Dalong; Du, Qingjie; Zhang, Zhi
  • Scientific Reports, Vol. 7, Issue 1
  • DOI: 10.1038/srep43461

The advantages of functional phenotyping in pre-field screening for drought-tolerant crops
journal, January 2017

  • Negin, Boaz; Moshelion, Menachem
  • Functional Plant Biology, Vol. 44, Issue 1
  • DOI: 10.1071/fp16156

Can sugar metabolism in the cambial region explain the water deficit tolerance in poplar?
journal, May 2018

  • Traversari, Silvia; Francini, Alessandra; Traversi, Maria Laura
  • Journal of Experimental Botany, Vol. 69, Issue 16
  • DOI: 10.1093/jxb/ery195

Transcriptome analysis of Pinus halepensis under drought stress and during recovery
journal, November 2017


Differences in isoprenoid-mediated energy dissipation pathways between coastal and interior Douglas-fir seedlings in response to drought
journal, October 2019

  • Junker-Frohn, Laura Verena; Kleiber, Anita; Jansen, Kirstin
  • Tree Physiology, Vol. 39, Issue 10
  • DOI: 10.1093/treephys/tpz075

More than iso/anisohydry: Hydroscapes integrate plant water use and drought tolerance traits in 10 eucalypt species from contrasting climates
journal, April 2019

  • Li, Ximeng; Blackman, Chris J.; Peters, Jennifer M. R.
  • Functional Ecology, Vol. 33, Issue 6
  • DOI: 10.1111/1365-2435.13320

Global variations in ecosystem-scale isohydricity
journal, July 2016

  • Konings, Alexandra G.; Gentine, Pierre
  • Global Change Biology, Vol. 23, Issue 2
  • DOI: 10.1111/gcb.13389

Genotypic variation in transpiration of coppiced poplar during the third rotation of a short-rotation bio-energy culture
journal, June 2018

  • Navarro, Alejandra; Portillo-Estrada, Miguel; Arriga, Nicola
  • GCB Bioenergy, Vol. 10, Issue 8
  • DOI: 10.1111/gcbb.12526

Linking variation in intrinsic water-use efficiency to isohydricity: a comparison at multiple spatiotemporal scales
journal, August 2018

  • Yi, Koong; Maxwell, Justin T.; Wenzel, Matthew K.
  • New Phytologist, Vol. 221, Issue 1
  • DOI: 10.1111/nph.15384

Beyond soil water potential: An expanded view on isohydricity including land–atmosphere interactions and phenology
journal, February 2019

  • Novick, Kimberly A.; Konings, Alexandra G.; Gentine, Pierre
  • Plant, Cell & Environment, Vol. 42, Issue 6
  • DOI: 10.1111/pce.13517

Chemical and isotopic markers detect water deficit and its influence on nutrient allocation in Phaseolus vulgaris
journal, February 2019

  • Smith, Millicent R.; Fuentes, David; Merchant, Andrew
  • Physiologia Plantarum, Vol. 167, Issue 3
  • DOI: 10.1111/ppl.12899

Improving water use efficiency by changing hydraulic and stomatal characteristics in soybean exposed to drought: the involvement of nitric oxide
journal, June 2019

  • Sousa, Letícia F.; Menezes‐Silva, Paulo E.; Lourenço, Lucas L.
  • Physiologia Plantarum, Vol. 168, Issue 3
  • DOI: 10.1111/ppl.12983

Variation in Ecophysiological Traits and Drought Tolerance of Beech (Fagus sylvatica L.) Seedlings from Different Populations
journal, June 2016

  • Cocozza, Claudia; de Miguel, Marina; Pšidová, Eva
  • Frontiers in Plant Science, Vol. 7
  • DOI: 10.3389/fpls.2016.00886

UAV-Based Thermal Imaging for High-Throughput Field Phenotyping of Black Poplar Response to Drought
journal, September 2017

  • Ludovisi, Riccardo; Tauro, Flavia; Salvati, Riccardo
  • Frontiers in Plant Science, Vol. 8
  • DOI: 10.3389/fpls.2017.01681

Temporal network analysis identifies early physiological and transcriptomic indicators of mild drought in Brassica rapa
journal, August 2017

  • Greenham, Kathleen; Guadagno, Carmela Rosaria; Gehan, Malia A.
  • eLife, Vol. 6
  • DOI: 10.7554/elife.29655

Vapour pressure deficit control in relation to water transport and water productivity in greenhouse tomato production during summer
journal, March 2017

  • Zhang, Dalong; Du, Qingjie; Zhang, Zhi
  • Scientific Reports, Vol. 7, Issue 1
  • DOI: 10.1038/srep43461

Can sugar metabolism in the cambial region explain the water deficit tolerance in poplar?
journal, May 2018

  • Traversari, Silvia; Francini, Alessandra; Traversi, Maria Laura
  • Journal of Experimental Botany, Vol. 69, Issue 16
  • DOI: 10.1093/jxb/ery195

Transcriptome analysis of Pinus halepensis under drought stress and during recovery
journal, November 2017


Genotypic variation in transpiration of coppiced poplar during the third rotation of a short-rotation bio-energy culture
journal, June 2018

  • Navarro, Alejandra; Portillo-Estrada, Miguel; Arriga, Nicola
  • GCB Bioenergy, Vol. 10, Issue 8
  • DOI: 10.1111/gcbb.12526

Variation in Ecophysiological Traits and Drought Tolerance of Beech (Fagus sylvatica L.) Seedlings from Different Populations
journal, June 2016

  • Cocozza, Claudia; de Miguel, Marina; Pšidová, Eva
  • Frontiers in Plant Science, Vol. 7
  • DOI: 10.3389/fpls.2016.00886

UAV-Based Thermal Imaging for High-Throughput Field Phenotyping of Black Poplar Response to Drought
journal, September 2017

  • Ludovisi, Riccardo; Tauro, Flavia; Salvati, Riccardo
  • Frontiers in Plant Science, Vol. 8
  • DOI: 10.3389/fpls.2017.01681

Transpiration Response of Cotton to Vapor Pressure Deficit and Its Relationship With Stomatal Traits
journal, October 2018