Pragmatic hydraulic theory predicts stomatal responses to climatic water deficits

New Phytologist

Volumn 212, Issue 3, 2016, Pages 577-589

  Sperry, John S ^a   Wang, Yujie ^a   Wolfe, Brett T ^b   Mackay, D Scott ^c   Anderegg, William R L ^a   McDowell, Nate G ^d   Pockman, William T ^e  

^a UNIVERSITY OF UTAH   (United States)

^b SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

^c UNIVERSITY AT BUFFALO   (United States)

^d LOS ALAMOS NATIONAL LABORATORY   (United States)

^e UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

climate change drought; hydraulic limitation; modeling climate change impacts; plant drought responses; plant water transport; stomatal regulation; xylem cavitation; xylem transport

Indexed keywords

ATMOSPHERE-BIOSPHERE INTERACTION; CLIMATE CHANGE; DROUGHT; ECOSYSTEM MODELING; HYDRAULICS; PARAMETERIZATION; PLANT WATER RELATIONS; SEASONAL VARIATION; SOIL-VEGETATION INTERACTION; STOMATAL CONDUCTANCE; TROPICAL FOREST; WATER DEMAND; XYLEM;

JUNIPERUS;

WATER;

BIOLOGICAL MODEL; CHEMISTRY; CLIMATE; DIFFUSION; DROUGHT; EVAPOTRANSPIRATION; HUMIDITY; PHYSIOLOGY; PLANT STOMA; SOIL; XYLEM;

CLIMATE; DIFFUSION; DROUGHTS; HUMIDITY; MODELS, BIOLOGICAL; PLANT STOMATA; PLANT TRANSPIRATION; SOIL; WATER; XYLEM;

EID: 84977594303     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.14059     Document Type: Article

References (67)

1. Allen C, Macalady A, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears D, Hogg EH et al. 2010. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecology and Management 259: 660–684.
2. Anderegg WRL. 2014. Spatial and temporal variation in plant hydraulic traits and their relevance for climate change impacts on vegetation. New Phytologist 205: 1008–1014.
3. Anderegg WRL, Anderegg LDL, Berry JA, Field CB. 2014. Loss of whole-tree hydraulic conductance during severe drought and multi-year forest die-off. Oecologia 175: 11–23.
4. Anderegg WRL, Berry JA, Smith DD, Sperry JS, Anderegg LDL, Field CB. 2012. The roles of hydraulic and carbon stress in a widespread climate-induced forest die-off. Proceedings of the National Academy of Sciences, USA 109: 233–237.
5. Anderegg WRL, Placova L, Anderegg LDL, Hacke UG, Berry JA, Field CB. 2013. Drought's legacy: hydraulic deterioration underlies widespread aspen die-off and portends increased future vulnerability. Global Change Biology 19: 1188–1196.
6. Anderegg WRL, Schwalm C, Biondi F, Camarero JJ, Koch G, Litvak M, Ogle K, Shaw JD, Shevliakova E, Williams AP et al. 2015. Pervasive drought legacies in forest ecosystems and their implications for carbon cycle models. Science 349: 528–532.
7. Ball JT, Woodrow IE, Berry JA. 1987. A model predicting stomatal conductance and its contribution to the control of photosynthesis under different environmental conditions. In: Biggins J, ed. Progress in photosynthesis research, vol 4. Leiden, the Netherlands: Martinus Nijhoff, 221–224.
8. Bristow KL, Campbell GS, Calissendorff C. 1984. The effects of texture on the resistance to water movement within the rhizosphere. Soil Science Society of America Journal 48: 266–270.
9. Brodribb TJ, Cochard H. 2009. Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiology 149: 575–584.
10. Brooks PD, Troch PA, Durcik M, Gallo E, Schlegel M. 2011. Quantifying regional-scale ecosystem responses to changes in precipitation: not all rain is created equal. Water Resources Research 47: W00J08.
11. Brown HR. 2013. The theory of the rise of sap in trees: some historical and conceptual remarks. Physics in Perspective 15: 320–358.
12. Buckley TN, Mott KA. 2013. Modelling stomatal conductance in response to environmental factors. Plant, Cell & Environment 36: 1691–1699.
13. Chen L, Wang L, Ma Y, Liu P. 2015. Overview of ecohydrological models and systems at the watershed scale. IEEE Systems Journal 9: 1091–1099.
14. Comstock JP, Sperry JS. 2000. Theoretical considerations of optimal conduit length for water transport in vascular plants. New Phytologist 148: 195–218.
15. Cosgrove DJ. 1997. Relaxation in a high-stress environment: the molecular bases of extensible cell walls and cell enlargement. Plant Cell 9: 1031–1041.
16. Cowan IR. 1977. Stomatal behaviour and the environment. Advances in Botanical Research 4: 117–228.
17. Dai A. 2011. Drought under global warming: q review. WIREs Climate Change 2: 45–65.
18. Farquhar GD, Caemmerer SV. 1982. Modelling of photosynthetic response to environmental conditions. In: Lange OL, Nobel PS, Osmond CB, Ziegler H, eds. Physiological plant ecology II: water relations and carbon assimilation. Berlin, Germany: Springer-Verlag, 549–587.
19. Field CB, Holbrook NM. 1989. Catastrophic xylem failure: life at the brink. Trends in Ecology and Evolution 4: 124–126.
20. Franks PJ. 2013. Passive and active stomatal control: either or both? New Phytologist 198: 325–327.
21. Franks PJ, Drake PL, Froend RH. 2007. Anisohydric but isohydrodynamic: seasonally constant plant water potential gradient explained by a stomatal control mechanism incorporating variable plant hydraulic conductance. Plant, Cell & Environment 30: 19–30.
22. van Genuchten MT. 1980. A closed form equation for predicting the hydraulic conductivity of unsaturated soils. Soil Science Society of American Journal 44: 892–898.
23. Hacke UG, Sperry JS, Ewers BE, Ellsworth DS, Schäfer KVR, Oren R. 2000. Influence of soil porosity on water use in Pinus taeda. Oecologia 124: 495–505.
24. Hao GY, Hoffmann W, Scholz FG, Bucci SJ, Meinzer FC, Franco AC. 2008. Stem and leaf hydraulics of congeneric tree species from adjacent tropical savanna and forest ecosystems. Oecologia 155: 405–415.
25. Hoffmann WA, Marchin RM, Abit P, Lau OL. 2011. Hydraulic failure and tree dieback are associated with high wood density in a temperate forest under extreme drought. Global Change Biology 17: 2731–2742.
26. Jackson RB, Canadell J, Ehleringer JR, Mooney HA, Sala OE, Schulze ED. 1996. A global analysis of root distributions for terrestrial biomes. Oecologia 108: 389–411.
27. Jacobson AL, Pratt RB, Ewers FW, Davis SD. 2007. Cavitation resistance among 26 chaparral species of southern California. Ecological Monographs 77: 99–115.
28. Jarvis PG. 1976. The interpretation of the variations in leaf water potential and stomatal conductance found in canopies in the field. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences 273: 593–610.
29. Jones HG, Sutherland R. 1991. Stomatal control of xylem embolism. Plant, Cell & Environment 14: 607–612.
30. Kolb KJ, Sperry JS, Lamont BB. 1996. A method for measuring xylem hydraulic conductance and embolism in entire root and shoot systems. Journal of Experimental Botany 47: 1805–1810.
31. Kukowski K, Schwinning S, Schwartz B. 2013. Hydraulic responses to extreme drought conditions in three co-dominant tree species in shallow soil over bedrock. Oecologia 171: 819–830.
32. Le Roux X, Lacointe A, Escobar-Gutiérrez A, Le Dizès S. 2001. Carbon-based models of individual tree growth: a critical appraisal. Annals of Forest Science 58: 469–506.
33. Leij FJ, Alves WJ, Van Genuchten MT, Williams JR. 1996. Unsaturated soil hydraulic database UNSODA 1.0 User's Manual., v. EPA Report 600/R-96/095. Ada, OK, USA: USEPA.
34. 3 plants. Plant, Cell & Environment 18: 339–357.
35. Li S, Assmann SM, Albert R. 2006. Predicting essential components of signal transduction networks: a dynamic model of guard cell abscisic acid signaling. PLoS Biology 4: e312.
36. Lloyd J. 1991. Modeling stomatal responses to environment in Macadamia integrifolia. Australian Journal of Plant Physiology 18: 649–660.
37. Mackay DS, Roberts DE, Ewers BE, Sperry JS, McDowell N, Pockman W. 2015. Interdependence of chronic hydraulic dysfunction and canopy processes can improve integrated models of tree response to drought. Water Resources Research 51: 6156–6176.
38. Martínez-Vilalta J, Poyatos R, Aguadé D, Retana J, Mencuccini M. 2014. A new look at water transport regulation in plants. New Phytologist 204: 105–115.
39. McDowell NG, Fisher RA, Xu C, Domec JC, Hölttä T, Mackay DS, Sperry JS, Boutz A, Diskman L, Geheres N et al. 2013. Evaluating theories of drought-induced vegetation mortality using a multimodel-experimental framework. New Phytologist 200: 304–321.
40. Medlyn BE, Duursma RA, Eamus D, Ellsworth DS, Prentice IC, Barton CVM, Crous KY, de Angelis P, Freeman M, Wingate L. 2011. Reconciling the optimal and empirical approaches to modelling stomatal conductance. Global Change Biology 17: 2134–2144.
41. Milburn JA. 1973. Cavitation in Ricinus by acoustic detection: induction in excised leaves by various factors. Planta 110: 253–265.
42. Milburn JA. 1979. Water flow in plants. London, UK: Longman.
43. Monteith JL. 1995. A reinterpretation of stomatal response to humidity. Plant, Cell & Environment 18: 357–364.
44. Nelder JA, Mead R. 1965. A simplex method for function minimization. Computer Journal 7: 308–313.
45. Oren R, Sperry JS, Katul GG, Pataki DE, Ewers BE, Phillips N, Schafer KVR. 1999. Survey and synthesis of intra- and interspecific variation in stomatal sensitivity to vapour pressure deficit. Plant, Cell & Environment 22: 1515–1526.
46. Pickard WF. 1981. The ascent of sap in plants. Progress in Biophysics and Molecular Biology 37: 181–229.
47. Pieruschka R, Huber G, Berry JA. 2010. Control of transpiration by radiation. Proceedings of the National Academy of Sciences, USA 107: 13372–13377.
48. Powell TL, Galbraith DR, Christoffersen BO, Harper A, Imbuzeiro HMA, Rowland L, Almeida S, Brando PM, da Costa ACL, Costa MH et al. 2013. Confronting model predictions of carbon fluxes with measurements of Amazon forests subjected to experimental drought. New Phytologist 200: 350–365.
49. Press WH, Flannery BP, Teukolsky SA, Vetterling WT. 1989. Numerical recipes in Pascal. Cambridge, UK: Cambridge University Press.
50. Rice KJ, Matzner SL, Byer W, Brown JR. 2004. Patterns of tree dieback in Queensland, Australia: the importance of drought stress and the role of resistance to cavitation. Oecologia 139: 190–198.
51. Saliendra NZ, Sperry JS, Comstock JP. 1995. Influence of leaf water status on stomatal response to humidity, hydraulic conductance, and soil drought in Betula occidentalis. Planta 196: 357–366.
52. Scoffoni C, Rawls M, McKown A, Cochard H, Sack L. 2011. Decline of leaf hydraulic conductance with dehydration: relationship to leaf size and venation architecture. Plant Physiology 156: 832–843.
53. Sevanto S. 2014. Phloem transport and drought. Journal of Experimental Botany 65: 1751–1759.
54. Sparks JP, Black RA. 1999. Regulation of water loss in populations of Populus trichocarpa: the role of stomatal control in preventing xylem cavitation. Tree Physiology 19: 453–459.
55. Sperry JS, Adler FR, Campbell GS, Comstock JP. 1998. Limitation of plant water use by rhizosphere and xylem conductance: results from a model. Plant, Cell & Environment 21: 347–359.
56. Sperry JS, Hacke UG, Oren R, Comstock JP. 2002a. Water deficits and hydraulic limits to leaf water supply. Plant, Cell & Environment 25: 251–263.
57. Sperry JS, Love DM. 2015. What plant hydraulics can tell us about plant responses to climate-change droughts. New Phytologist 207: 14–27.
58. Sperry JS, Stiller V, Hacke UG. 2002b. Soil water uptake and water transport through root systems. In: Waisel Y, Eshel A, Kafkafi U, eds. Plant roots: the hidden half. New York, NY, USA: Marcel Dekker, 663–681.
59. Stewart JB. 1988. Modelling surface conductance of pine forest. Agricultural and Forest Meteorology 43: 16–35.
60. Tardieu F, Davies WJ. 1993. Root-shoot communication and whole-plant regulation of water flux. In: Davies WJ, ed. Water deficits: plant responses from cell to community. Lancaster, UK: BIOS Scientific Publishers, 147–162.
61. Tombesi S, Nardini A, Frioni T, Soccolini M, Zadra C, Farinelli D, Poni S, Palliotti A. 2015. Stomatal closure is induced by hydraulic signals and maintained by ABA in drought-stressed grapevine. Scientific Reports 5: 12449.
62. Tyree MT, Cochard H, Cruiziat P, Sinclair B, Ameglio T. 1993. Drought-induced leaf shedding in walnut – evidence for vulnerability segmentation. Plant, Cell & Environment 16: 879–882.
63. Tyree MT, Hammel HT. 1972. The measurement of the turgor pressure and the water relations of plants by the pressure-bomb technique. Journal of Experimental Botany 23: 267–282.
64. Tyree MT, Sperry JS. 1988. Do woody plants operate near the point of catastrophic xylem dysfunction caused by dynamic water stress? Answers from a model. Plant Physiology 88: 574–580.
65. Urli M, Porte AJ, Cochard H, Guengant Y, Burlett R, Delson S. 2013. Xylem embolism threshold for catastrophic hydraulic failure in angiosperm trees. Tree Physiology 33: 672–688.
66. Williams M, Rastetter EB, Fernandes DN, Goulden ML, Wofsy SC, Shaver GR, Melillo JM, Munger JW, Fan SM, Nadelhoffer KJ. 1996. Modelling the soil–atmosphere continuum in a Quercus-Acer stand at Harvard Forest: the regulation of stomatal conductance by light, nitrogen and soil/plant hydraulic properties. Plant, Cell & Environment 19: 911–927.
67. Wolfe BT, Sperry JS, Kursar TA. 2016. Does leaf shedding protect stems from cavitation during seasonal droughts? A test of the hydraulic fuse hypothesis. New Phytologist (In Press). doi: 10.1111/nph.14087.