Predicting stomatal responses to the environment from the optimization of photosynthetic gain and hydraulic cost.

Stomatal regulation presumably evolved to optimize CO2 for H2 O exchange in response to changing conditions. If the optimization criterion can be readily measured or calculated, then stomatal responses can be efficiently modelled without recourse to empirical models or underlying mechanism. Previous efforts have been challenged by the lack of a transparent index for the cost of losing water. Yet it is accepted that stomata control water loss to avoid excessive loss of hydraulic conductance from cavitation and soil drying. Proximity to hydraulic failure and desiccation can represent the cost of water loss. If at any given instant, the stomatal aperture adjusts to maximize the instantaneous difference between photosynthetic gain and hydraulic cost, then a model can predict the trajectory of stomatal responses to changes in environment across time. Results of this optimization model are consistent with the widely used Ball-Berry-Leuning empirical model (r2  > 0.99) across a wide range of vapour pressure deficits and ambient CO2 concentrations for wet soil. The advantage of the optimization approach is the absence of empirical coefficients, applicability to dry as well as wet soil and prediction of plant hydraulic status along with gas exchange.

[1]  F. Meinzer,et al.  Relationships between hydraulic architecture and leaf photosynthetic capacity in nitrogen-fertilized Eucalyptus grandis trees. , 2001, Tree physiology.

[2]  A. E. Hall,et al.  Stomatal Responses, Water Loss and CO2 Assimilation Rates of Plants in Contrasting Environments , 1982 .

[3]  G. Goldstein,et al.  Genotypic variability in vulnerability of leaf xylem to cavitation in water-stressed and well-irrigated sugarcane. , 1992, Plant physiology.

[4]  Brendan Choat,et al.  Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe , 2016, Proceedings of the National Academy of Sciences.

[5]  N. McDowell,et al.  Pragmatic hydraulic theory predicts stomatal responses to climatic water deficits. , 2016, The New phytologist.

[6]  Stephen W Pacala,et al.  Optimal stomatal behavior with competition for water and risk of hydraulic impairment , 2016, Proceedings of the National Academy of Sciences.

[7]  N. Holbrook,et al.  Leaf hydraulic capacity in ferns, conifers and angiosperms: impacts on photosynthetic maxima. , 2004, The New phytologist.

[8]  I. C. Prentice,et al.  Balancing the costs of carbon gain and water transport: testing a new theoretical framework for plant functional ecology. , 2014, Ecology letters.

[9]  Y. Malhi,et al.  Death from drought in tropical forests is triggered by hydraulics not carbon starvation , 2015, Nature.

[10]  J. Morison,et al.  Intercellular CO_2 Concentration and Stomatal Response to CO_2 , 1987 .

[11]  N. McDowell,et al.  Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? , 2008, The New phytologist.

[12]  R. Leuning A critical appraisal of a combined stomatal‐photosynthesis model for C3 plants , 1995 .

[13]  Amilcare Porporato,et al.  Optimizing stomatal conductance for maximum carbon gain under water stress: a meta-analysis across plant functional types and climates , 2011 .

[14]  M. Tyree,et al.  Leaf Hydraulics and Its Implications in Plant Structure and Function , 2005 .

[15]  T. Givnish Optimal stomatal conductance, allocation of energy between leaves and roots, and the marginal cost of transpiration , 1986 .

[16]  F. Woodward,et al.  The role of stomata in sensing and driving environmental change , 2003, Nature.

[17]  I. R. Cowan Regulation of Water Use in Relation to Carbon Gain in Higher Plants , 1982 .

[18]  G. Katul,et al.  A stomatal optimization theory to describe the effects of atmospheric CO2 on leaf photosynthesis and transpiration. , 2010, Annals of botany.

[19]  D. Hodáňová An introduction to environmental biophysics , 1979, Biologia Plantarum.

[20]  Frederick R. Adler,et al.  Limitation of plant water use by rhizosphere and xylem conductance: results from a model , 1998 .

[21]  Christopher B. Field,et al.  Tree mortality predicted from drought-induced vascular damage , 2015 .

[22]  S. Schwinning,et al.  Hydraulic responses to extreme drought conditions in three co-dominant tree species in shallow soil over bedrock , 2013, Oecologia.

[23]  G. Katul,et al.  Relationship between plant hydraulic and biochemical properties derived from a steady‐state coupled water and carbon transport model , 2003 .

[24]  Van Genuchten,et al.  A closed-form equation for predicting the hydraulic conductivity of unsaturated soils , 1980 .

[25]  T. Brodribb Xylem hydraulic physiology: the functional backbone of terrestrial plant productivity. , 2009 .

[26]  Yadvinder Malhi,et al.  Confronting model predictions of carbon fluxes with measurements of Amazon forests subjected to experimental drought. , 2013, The New phytologist.

[27]  Contrasting whole-tree water use, hydraulics, and growth in a co-dominant diffuse-porous vs. ring-porous species pair , 2015, Trees.

[28]  Carl J. Bernacchi,et al.  Improved temperature response functions for models of Rubisco‐limited photosynthesis , 2001 .

[29]  Denis Loustau,et al.  Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data , 2002 .

[30]  J. Sparks,et al.  Regulation of water loss in populations of Populus trichocarpa: the role of stomatal control in preventing xylem cavitation. , 1999, Tree physiology.

[31]  T. Brodribb,et al.  Leaf Maximum Photosynthetic Rate and Venation Are Linked by Hydraulics1[W][OA] , 2007, Plant Physiology.

[32]  G. Collatz,et al.  Coupled Photosynthesis-Stomatal Conductance Model for Leaves of C4 Plants , 1992 .

[33]  J. Sperry,et al.  Do woody plants operate near the point of catastrophic xylem dysfunction caused by dynamic water stress? : answers from a model. , 1988, Plant physiology.

[34]  Graham D. Farquhar,et al.  Responses to Humidity by Stomata of Nicotiana glauca L. And Corylus avellana L. Are Consistent With the Optimization of Carbon Dioxide Uptake With Respect to Water Loss , 1980 .

[35]  M. Paul,et al.  Sink regulation of photosynthesis. , 2001, Journal of experimental botany.

[36]  D. Eamus,et al.  Optimization Theory Of Stomatal Behaviour - Ii. Stomatal Responses Of Several Tree Species Of North Australia To Changes In Light, Soil And Atmospheric Water Content And Temperature , 1999 .

[37]  I. R. Cowan,et al.  Stomatal function in relation to leaf metabolism and environment. , 1977, Symposia of the Society for Experimental Biology.

[38]  Sylvain Delzon,et al.  Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world's woody plant species. , 2016, The New phytologist.

[39]  P. Campanello,et al.  Coordination between water-transport efficiency and photosynthetic capacity in canopy tree species at different growth irradiances. , 2008, Tree physiology.

[40]  J. Sperry,et al.  What plant hydraulics can tell us about responses to climate-change droughts. , 2015, The New phytologist.

[41]  Ray Leuning,et al.  Temperature dependence of two parameters in a photosynthesis model , 2002 .

[42]  Patrick J. Hudson,et al.  Regulation and acclimation of leaf gas exchange in a piñon-juniper woodland exposed to three different precipitation regimes. , 2013, Plant, cell & environment.

[43]  I. R. Cowan,et al.  Stomatal conductance correlates with photosynthetic capacity , 1979, Nature.

[44]  S. Wofsy,et al.  Modelling the soil-plant-atmosphere continuum in a Quercus-Acer stand at Harvard Forest : the regulation of stomatal conductance by light, nitrogen and soil/plant hydraulic properties , 1996 .

[45]  M. G. Ryan,et al.  Evaluating theories of drought-induced vegetation mortality using a multimodel-experiment framework. , 2013, The New phytologist.

[46]  Amilcare Porporato,et al.  Optimization of stomatal conductance for maximum carbon gain under dynamic soil moisture , 2013 .

[47]  Paolo De Angelis,et al.  Reconciling the optimal and empirical approaches to modelling stomatal conductance , 2011 .

[48]  C. Field,et al.  Catastrophic xylem failure: Tree life at the brink , 1989 .

[49]  P. Jarvis The Interpretation of the Variations in Leaf Water Potential and Stomatal Conductance Found in Canopies in the Field , 1976 .

[50]  A. Mäkelä,et al.  Optimal Control of Gas Exchange during Drought: Theoretical Analysis , 1996 .

[51]  N. Holbrook,et al.  Hydraulic and photosynthetic co‐ordination in seasonally dry tropical forest trees , 2002 .

[52]  J. Vose,et al.  Drought limitations to leaf-level gas exchange: results from a model linking stomatal optimization and cohesion-tension theory. , 2016, Plant, cell & environment.

[53]  N. McDowell,et al.  Interdependence of chronic hydraulic dysfunction and canopy processes can improve integrated models of tree response to drought , 2015 .

[54]  T. Brodribb,et al.  Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification. , 2010, Ecology letters.

[55]  K. Oleson,et al.  Modeling stomatal conductance in the earth system: linking leaf water-use efficiency and water transport along the soil–plant–atmosphere continuum , 2014 .

[56]  A. Nardini,et al.  Stomatal closure is induced by hydraulic signals and maintained by ABA in drought-stressed grapevine , 2015, Scientific Reports.

[57]  Lawren Sack,et al.  Optimal plant water economy. , 2017, Plant, cell & environment.

[58]  G. Collatz,et al.  Physiological and environmental regulation of stomatal conductance, photosynthesis and transpiration: a model that includes a laminar boundary layer , 1991 .

[59]  Hervé Cochard,et al.  An overview of models of stomatal conductance at the leaf level. , 2010, Plant, cell & environment.