A Dynamic Optimality Principle for Water Use Strategies Explains Isohydric to Anisohydric Plant Responses to Drought
Abstract
Optimality principles that underlie models of stomatal kinetics require identifying and formulating the gain and the costs involved in opening stomata. While the gain has been linked to larger carbon acquisition, there is still a debate as to the costs that limit stomatal opening. This work presents an Euler-Lagrange framework that accommodates water use strategy and various costs through the formulation of constraints. The reduction in plant hydraulic conductance due to cavitation is added as a new constraint above and beyond the soil hydrological balance and is analyzed for three different types of whole-plant vulnerability curves. Model results show that differences in vulnerability curves alone lead to relatively iso- and aniso-hydric stomatal behavior. Moreover, this framework explains how the presence of competition (biotic or abiotic) for water alters stomatal response to declining soil water content. This contribution corroborates previous research that predicts that a plant's environment (e.g., competition, soil processes) significantly affects its response to drought and supplies the required mathematical machinery to represent this complexity. The method adopted here disentangles cause and effect of the opening and closure of stomata and complements recent mechanistic models of stomatal response to drought.
- Authors:
-
- Duke Univ., Durham, NC (United States)
- Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
- Duke Univ., Durham, NC (United States); UMR INRA-ISPA 1391, Gradignan (France)
- Publication Date:
- Research Org.:
- Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
- Sponsoring Org.:
- USDOE Laboratory Directed Research and Development (LDRD) Program
- OSTI Identifier:
- 1579698
- Report Number(s):
- LA-UR-19-22773
Journal ID: ISSN 2624-893X
- Grant/Contract Number:
- 89233218CNA000001; NSF-EAR-1344703; NSF-AGS-1644382; NSF-IOS-1754893
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Forests and Global Change
- Additional Journal Information:
- Journal Volume: 2; Journal ID: ISSN 2624-893X
- Publisher:
- Frontiers Media S.A.
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES; biological science; Earth sciences; drought; dynamic optimality; isohydricity and anisohydricity; photosynthesis; plant hydraulics; stomata; transpiration; water use strategy
Citation Formats
Mrad, Assaad, Sevanto, Sanna Annika, Domec, Jean -Christophe, Liu, Yanlan, Nakad, Mazen, and Katul, Gabriel. A Dynamic Optimality Principle for Water Use Strategies Explains Isohydric to Anisohydric Plant Responses to Drought. United States: N. p., 2019.
Web. doi:10.3389/ffgc.2019.00049.
Mrad, Assaad, Sevanto, Sanna Annika, Domec, Jean -Christophe, Liu, Yanlan, Nakad, Mazen, & Katul, Gabriel. A Dynamic Optimality Principle for Water Use Strategies Explains Isohydric to Anisohydric Plant Responses to Drought. United States. doi:10.3389/ffgc.2019.00049.
Mrad, Assaad, Sevanto, Sanna Annika, Domec, Jean -Christophe, Liu, Yanlan, Nakad, Mazen, and Katul, Gabriel. Wed .
"A Dynamic Optimality Principle for Water Use Strategies Explains Isohydric to Anisohydric Plant Responses to Drought". United States. doi:10.3389/ffgc.2019.00049. https://www.osti.gov/servlets/purl/1579698.
@article{osti_1579698,
title = {A Dynamic Optimality Principle for Water Use Strategies Explains Isohydric to Anisohydric Plant Responses to Drought},
author = {Mrad, Assaad and Sevanto, Sanna Annika and Domec, Jean -Christophe and Liu, Yanlan and Nakad, Mazen and Katul, Gabriel},
abstractNote = {Optimality principles that underlie models of stomatal kinetics require identifying and formulating the gain and the costs involved in opening stomata. While the gain has been linked to larger carbon acquisition, there is still a debate as to the costs that limit stomatal opening. This work presents an Euler-Lagrange framework that accommodates water use strategy and various costs through the formulation of constraints. The reduction in plant hydraulic conductance due to cavitation is added as a new constraint above and beyond the soil hydrological balance and is analyzed for three different types of whole-plant vulnerability curves. Model results show that differences in vulnerability curves alone lead to relatively iso- and aniso-hydric stomatal behavior. Moreover, this framework explains how the presence of competition (biotic or abiotic) for water alters stomatal response to declining soil water content. This contribution corroborates previous research that predicts that a plant's environment (e.g., competition, soil processes) significantly affects its response to drought and supplies the required mathematical machinery to represent this complexity. The method adopted here disentangles cause and effect of the opening and closure of stomata and complements recent mechanistic models of stomatal response to drought.},
doi = {10.3389/ffgc.2019.00049},
journal = {Frontiers in Forests and Global Change},
number = ,
volume = 2,
place = {United States},
year = {2019},
month = {8}
}
Works referenced in this record:
Stomatal responses to humidity in air and helox
journal, June 1991
- Mott, K. A.; Parkhurst, D. F.
- Plant, Cell and Environment, Vol. 14, Issue 5
Anisohydric but isohydrodynamic: seasonally constant plant water potential gradient explained by a stomatal control mechanism incorporating variable plant hydraulic conductance
journal, January 2007
- Franks, Peter J.; Drake, Paul L.; Froend, Ray H.
- Plant, Cell and Environment, Vol. 30, Issue 1
Optimizing the statistical estimation of the parameters of the Farquhar–von Caemmerer–Berry model of photosynthesis
journal, October 2007
- Dubois, Jean-Jacques B.; Fiscus, Edwin L.; Booker, Fitzgerald L.
- New Phytologist, Vol. 176, Issue 2
Ozone Damage to Plants
journal, September 1964
- Rich, S.
- Annual Review of Phytopathology, Vol. 2, Issue 1
A critical review and analysis of the use of exposure- and flux-based ozone indices for predicting vegetation effects
journal, March 2006
- Musselman, R.; Lefohn, A.; Massman, W.
- Atmospheric Environment, Vol. 40, Issue 10
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
Ozone uptake, water loss and carbon exchange dynamics in annually drought-stressed Pinus ponderosa forests: measured trends and parameters for uptake modeling
journal, March 2004
- Panek, J. A.
- Tree Physiology, Vol. 24, Issue 3
Simple scaling of photosynthesis from leaves to canopies without the errors of big-leaf models
journal, May 1997
- De Pury, D. G. G.; Farquhar, G. D.
- Plant, Cell and Environment, Vol. 20, Issue 5
New insights into the covariation of stomatal, mesophyll and hydraulic conductances from optimization models incorporating nonstomatal limitations to photosynthesis
journal, October 2017
- Dewar, Roderick; Mauranen, Aleksanteri; Mäkelä, Annikki
- New Phytologist, Vol. 217, Issue 2
Sizes and Shapes of Liane Leaves
journal, September 1976
- Givnish, Thomas J.; Vermeij, Geerat J.
- The American Naturalist, Vol. 110, Issue 975
Root to Shoot Communication in Maize Plants of the Effects of Soil Drying
journal, January 1985
- Blackman, P. G.; Davies, W. J.
- Journal of Experimental Botany, Vol. 36, Issue 1
Rare pits, large vessels and extreme vulnerability to cavitation in a ring-porous tree species
journal, December 2011
- Christman, Mairgareth A.; Sperry, John S.; Smith, Duncan D.
- New Phytologist, Vol. 193, Issue 3
How do trees die? A test of the hydraulic failure and carbon starvation hypotheses: How do trees die?
journal, June 2013
- Sevanto, Sanna; Mcdowell, Nate G.; Dickman, L. Turin
- Plant, Cell & Environment, Vol. 37, Issue 1
Pragmatic hydraulic theory predicts stomatal responses to climatic water deficits
journal, June 2016
- Sperry, John S.; Wang, Yujie; Wolfe, Brett T.
- New Phytologist, Vol. 212, Issue 3
Stomatal movement: Its regulation and regulatory rÔle a review
journal, May 1927
- Scarth, G. W.
- Protoplasma, Vol. 2, Issue 1
Projected increase in continental runoff due to plant responses to increasing carbon dioxide
journal, August 2007
- Betts, Richard A.; Boucher, Olivier; Collins, Matthew
- Nature, Vol. 448, Issue 7157
Reliable estimation of biochemical parameters from C3 leaf photosynthesis-intercellular carbon dioxide response curves: Estimating FvCB model parameters
journal, June 2010
- Gu, Lianhong; Pallardy, Stephen G.; Tu, Kevin
- Plant, Cell & Environment, Vol. 33, Issue 11
Optimal plant water economy: Optimal plant water economy
journal, October 2016
- Buckley, Thomas N.; Sack, Lawren; Farquhar, Graham D.
- Plant, Cell & Environment, Vol. 40, Issue 6
Responses of two semiarid conifer tree species to reduced precipitation and warming reveal new perspectives for stomatal regulation: Stomatal regulation in piñon and juniper trees
journal, August 2015
- Garcia-Forner, NúRia; Adams, Henry D.; Sevanto, Sanna
- Plant, Cell & Environment, Vol. 39, Issue 1
Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model
journal, November 2000
- Cox, Peter M.; Betts, Richard A.; Jones, Chris D.
- Nature, Vol. 408, Issue 6809
Sap flow and sugar transport in plants
journal, September 2016
- Jensen, K. H.; Berg-Sørensen, K.; Bruus, H.
- Reviews of Modern Physics, Vol. 88, Issue 3
Optimal control of gas exchange
journal, December 1986
- Hari, P.; Makela, A.; Korpilahti, E.
- Tree Physiology, Vol. 2, Issue 1-2-3
Leaf stomatal responses to vapour pressure deficit under current and CO 2 -enriched atmosphere explained by the economics of gas exchange
journal, August 2009
- Katul, Gabriel G.; Palmroth, Sari; Oren, Ram
- Plant, Cell & Environment, Vol. 32, Issue 8
A stomatal control model based on optimization of carbon gain versus hydraulic risk predicts aspen sapling responses to drought
journal, July 2018
- Venturas, Martin D.; Sperry, John S.; Love, David M.
- New Phytologist, Vol. 220, Issue 3
Carbon Dioxide and Water Vapor Exchange in Response to Drought in the Atmosphere and in the Soil
journal, January 1986
- Schulze, E-D
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 37, Issue 1
How well do stomatal conductance models perform on closing plant carbon budgets? A test using seedlings grown under current and elevated air temperatures
journal, January 2011
- Way, Danielle A.; Oren, Ram; Kim, Hyun-Seok
- Journal of Geophysical Research, Vol. 116, Issue G4
Relations between stomatal closure, leaf turgor and xylem vulnerability in eight tropical dry forest trees
journal, March 2003
- Brodribb, T. J.; Holbrook, N. M.; Edwards, E. J.
- Plant, Cell and Environment, Vol. 26, Issue 3
Iso/Anisohydry: A Plant–Environment Interaction Rather Than a Simple Hydraulic Trait
journal, February 2018
- Hochberg, Uri; Rockwell, Fulton E.; Holbrook, N. Michele
- Trends in Plant Science, Vol. 23, Issue 2
Reconciling the optimal and empirical approaches to modelling stomatal conductance: RECONCILING OPTIMAL AND EMPIRICAL STOMATAL MODELS
journal, January 2011
- Medlyn, Belinda E.; Duursma, Remko A.; Eamus, Derek
- Global Change Biology, Vol. 17, Issue 6
Beyond isohydricity: The role of environmental variability in determining plant drought responses
journal, December 2018
- Feng, Xue; Ackerly, David D.; Dawson, Todd E.
- Plant, Cell & Environment, Vol. 42, Issue 4
Ecohydrology of Agroecosystems: Quantitative Approaches Towards Sustainable Irrigation
journal, August 2014
- Vico, Giulia; Porporato, Amilcare
- Bulletin of Mathematical Biology, Vol. 77, Issue 2
What plant hydraulics can tell us about responses to climate-change droughts
journal, March 2015
- Sperry, John S.; Love, David M.
- New Phytologist, Vol. 207, Issue 1
Soil Moisture Feedbacks on Convection Triggers: The Role of Soil–Plant Hydrodynamics
journal, February 2009
- Siqueira, Mario; Katul, Gabriel; Porporato, Amilcare
- Journal of Hydrometeorology, Vol. 10, Issue 1
The role of stomata in sensing and driving environmental change
journal, August 2003
- Hetherington, Alistair M.; Woodward, F. Ian
- Nature, Vol. 424, Issue 6951
Observations on Stomata
journal, January 1898
- Darwin, F.
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 190, Issue 0
A critical appraisal of a combined stomatal-photosynthesis model for C3 plants
journal, April 1995
- Leuning, R.
- Plant, Cell and Environment, Vol. 18, Issue 4
Transpiration and Hydraulic Strategies in a PiñOn–Juniper Woodland
journal, June 2008
- West, A. G.; Hultine, K. R.; Sperry, J. S.
- Ecological Applications, Vol. 18, Issue 4
Transport in a coordinated soil-root-xylem-phloem leaf system
journal, September 2018
- Huang, Cheng-Wei; Domec, Jean-Christophe; Palmroth, Sari
- Advances in Water Resources, Vol. 119
Balancing the costs of carbon gain and water transport: testing a new theoretical framework for plant functional ecology
journal, November 2013
- Prentice, I. Colin; Dong, Ning; Gleason, Sean M.
- Ecology Letters, Vol. 17, Issue 1
Fossil leaf traits as archives for the past — and lessons for the future?
journal, May 2019
- Roth-Nebelsick, Anita; Konrad, Wilfried
- Flora, Vol. 254
Optimal stomatal behaviour under stochastic rainfall
journal, April 2016
- Lu, Yaojie; Duursma, Remko A.; Medlyn, Belinda E.
- Journal of Theoretical Biology, Vol. 394
Physiological and environmental regulation of stomatal conductance, photosynthesis and transpiration: a model that includes a laminar boundary layer
journal, April 1991
- Collatz, G. James; Ball, J. Timothy; Grivet, Cyril
- Agricultural and Forest Meteorology, Vol. 54, Issue 2-4
Stomatal conductance and photosynthesis vary linearly with plant hydraulic conductance in ponderosa pine
journal, January 2001
- Hubbard, R. M.; Ryan, M. G.; Stiller, V.
- Plant, Cell & Environment, Vol. 24, Issue 1
Water potential regulation, stomatal behaviour and hydraulic transport under drought: deconstructing the iso/anisohydric concept: Deconstructing the iso/anisohydric concept
journal, December 2016
- Martínez-Vilalta, Jordi; Garcia-Forner, Núria
- Plant, Cell & Environment, Vol. 40, Issue 6
CO 2 and water vapor exchange of Pinus taeda in relation to stomatal behavior: test of an optimization hypothesis
journal, February 1988
- Fites, J. A.; Teskey, R. O.
- Canadian Journal of Forest Research, Vol. 18, Issue 2
Hydraulic constraints on plant gas exchange
journal, July 2000
- Sperry, John S.
- Agricultural and Forest Meteorology, Vol. 104, Issue 1
Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought?
journal, June 2008
- McDowell, Nate; Pockman, William T.; Allen, Craig D.
- New Phytologist, Vol. 178, Issue 4
A perspective on optimal leaf stomatal conductance under CO2 and light co-limitations
journal, December 2013
- Vico, Giulia; Manzoni, Stefano; Palmroth, Sari
- Agricultural and Forest Meteorology, Vol. 182-183
Sunflecks And Photosynthesis In Plant Canopies
journal, January 1990
- Pearcy, R.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 41, Issue 1
Stand growth model based on carbon uptake and allocation in individual trees
journal, October 1986
- Mäkelä, Annikki; Hari, Pertti
- Ecological Modelling, Vol. 33, Issue 2-4
The Interpretation of the Variations in Leaf Water Potential and Stomatal Conductance Found in Canopies in the Field
journal, February 1976
- Jarvis, P. G.
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 273, Issue 927
The effect of plant water storage on water fluxes within the coupled soil-plant system
journal, November 2016
- Huang, Cheng-Wei; Domec, Jean-Christophe; Ward, Eric J.
- New Phytologist, Vol. 213, Issue 3
Hydraulic limits preceding mortality in a piñon-juniper woodland under experimental drought: Hydraulic limits in a piñon-juniper woodland
journal, April 2012
- Plaut, Jennifer A.; Yepez, Enrico A.; Hill, Judson
- Plant, Cell & Environment, Vol. 35, Issue 9
Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data
journal, September 2002
- Medlyn, B. E.; Dreyer, E.; Ellsworth, D.
- Plant, Cell and Environment, Vol. 25, Issue 9
Optimization of stomatal conductance for maximum carbon gain under dynamic soil moisture
journal, December 2013
- Manzoni, Stefano; Vico, Giulia; Palmroth, Sari
- Advances in Water Resources, Vol. 62
Dynamics of leaf water relations components in co-occurring iso- and anisohydric conifer species: Dynamics of leaf water relations components
journal, April 2014
- Meinzer, Frederick C.; Woodruff, David R.; Marias, Danielle E.
- Plant, Cell & Environment, Vol. 37, Issue 11
A stomatal optimization theory to describe the effects of atmospheric CO2 on leaf photosynthesis and transpiration
journal, December 2009
- Katul, Gabriel; Manzoni, Stefano; Palmroth, Sari
- Annals of Botany, Vol. 105, Issue 3
Assimilate transport in phloem sets conditions for leaf gas exchange: Transport stoma
journal, October 2012
- Nikinmaa, Eero; HÖLttÄ, Teemu; Hari, Pertti
- Plant, Cell & Environment, Vol. 36, Issue 3
Flash flood warning at ungauged locations using radar rainfall and antecedent soil moisture estimations
journal, November 2010
- Javelle, Pierre; Fouchier, Catherine; Arnaud, Patrick
- Journal of Hydrology, Vol. 394, Issue 1-2
Evapotranspiration: A process driving mass transport and energy exchange in the soil-plant-atmosphere-climate system: EVAPOTRANSPIRATION AND CLIMATE
journal, July 2012
- Katul, Gabriel G.; Oren, Ram; Manzoni, Stefano
- Reviews of Geophysics, Vol. 50, Issue 3
Soil-plant-atmosphere conditions regulating convective cloud formation above southeastern US pine plantations
journal, March 2016
- Manoli, Gabriele; Domec, Jean-Christophe; Novick, Kimberly
- Global Change Biology, Vol. 22, Issue 6
Increased resin flow in mature pine trees growing under elevated CO2 and moderate soil fertility
journal, January 2012
- Novick, K. A.; Katul, G. G.; McCarthy, H. R.
- Tree Physiology, Vol. 32, Issue 6
The responses of stomata and leaf gas exchange to vapour pressure deficits and soil water content: II. In the mesophytic herbaceous species Helianthus annuus
journal, February 1985
- Turner, Neil C.; Schulze, E. -D.; Gollan, T.
- Oecologia, Vol. 65, Issue 3
Optimal Control of Gas Exchange during Drought: Theoretical Analysis
journal, May 1996
- MÄKelÄ, A.
- Annals of Botany, Vol. 77, Issue 5
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
The relative role of stomata in transpiration and assimilation
journal, January 1971
- Cowan, I. R.; Troughton, J. H.
- Planta, Vol. 97, Issue 4
Maximum entropy production and plant optimization theories
journal, May 2010
- Dewar, Roderick C.
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 365, Issue 1545
Modelling of stomatal density response to atmospheric
journal, August 2008
- Konrad, W.; Roth-Nebelsick, A.; Grein, M.
- Journal of Theoretical Biology, Vol. 253, Issue 4
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
Solutions of the Flow Equation for the Drying of Soils and Other Porous Media1
journal, January 1959
- Gardner, W. R.
- Soil Science Society of America Journal, Vol. 23, Issue 3
An overview of models of stomatal conductance at the leaf level: Models of stomatal conductance
journal, July 2010
- Damour, GaËLle; Simonneau, Thierry; Cochard, HervÉ
- Plant, Cell & Environment
Xylem functioning, dysfunction and repair: a physical perspective and implications for phloem transport
journal, October 2018
- Konrad, Wilfried; Katul, Gabriel; Roth-Nebelsick, Anita
- Tree Physiology, Vol. 39, Issue 2
Improved temperature response functions for models of Rubisco-limited photosynthesis
journal, February 2001
- Bernacchi, C. J.; Singsaas, E. L.; Pimentel, C.
- Plant, Cell and Environment, Vol. 24, Issue 2
Control of Stomatal Behaviour by Abscisic Acid which Apparently Originates in the Roots
journal, January 1987
- Zhang, Jianhua; Schurr, U.; Davies, W. J.
- Journal of Experimental Botany, Vol. 38, Issue 7
Mapping ‘hydroscapes’ along the iso- to anisohydric continuum of stomatal regulation of plant water status
journal, September 2016
- Meinzer, Frederick C.; Woodruff, David R.; Marias, Danielle E.
- Ecology Letters, Vol. 19, Issue 11
Predicting stomatal responses to the environment from the optimization of photosynthetic gain and hydraulic cost: A stomatal optimization model
journal, December 2016
- Sperry, John S.; Venturas, Martin D.; Anderegg, William R. L.
- Plant, Cell & Environment, Vol. 40, Issue 6
Empirical equations for some soil hydraulic properties
journal, August 1978
- Clapp, Roger B.; Hornberger, George M.
- Water Resources Research, Vol. 14, Issue 4
Optimizing stomatal conductance for maximum carbon gain under water stress: a meta-analysis across plant functional types and climates: Optimal leaf gas exchange under water stress
journal, January 2011
- Manzoni, Stefano; Vico, Giulia; Katul, Gabriel
- Functional Ecology, Vol. 25, Issue 3
Works referencing / citing this record:
Optimal stomatal drought response shaped by competition for water and hydraulic risk can explain plant trait covariation
journal, October 2019
- Lu, Yaojie; Duursma, Remko A.; Farrior, Caroline E.
- New Phytologist, Vol. 225, Issue 3