Trees

, Volume 28, Issue 5, pp 1323–1331 | Cite as

Role of aquaporin activity in regulating deep and shallow root hydraulic conductance during extreme drought

  • Daniel M. Johnson
  • Mark E. Sherrard
  • Jean-Christophe Domec
  • Robert B. Jackson
Original Paper

Abstract

Key message

Deep root hydraulic conductance is upregulated during severe drought and is associated with upregulation in aquaporin activity.

Abstract

In 2011, Texas experienced the worst single-year drought in its recorded history and, based on tree-ring data, likely its worst in the past millennium. In the Edwards Plateau of Texas, rainfall was 58 % lower and the mean daily maximum temperatures were >5 °C higher than long-term means in June through September, resulting in extensive tree mortality. To better understand the balance of deep and shallow root functioning for water supply, we measured root hydraulic conductance (KR) in deep (~20 m) and shallow (5–10 cm) roots of Quercus fusiformis at four time points in the field in 2011. Deep roots of Q. fusiformis obtained water from a perennial underground (18–20 m) stream that was present even during the drought. As the drought progressed, deep root KR increased 2.6-fold from early season values and shallow root KR decreased by 50 % between April and September. Inhibitor studies revealed that aquaporin contribution to KR increased in deep roots and decreased in shallow roots as the drought progressed. Deep root aquaporin activity was upregulated during peak drought, likely driven by increased summer evaporative demand and the need to compensate for declining shallow root KR. A whole-tree hydraulic transport model predicted that trees with greater proportions of deep roots would have as much as five times greater transpiration during drought periods and could sustain transpiration during droughts without experiencing total hydraulic failure. Our results suggest that trees shift their dependence on deep roots versus shallow roots during drought periods, and that upregulation of aquaporin activity accounts for at least part of this increase.

Keywords

Caves Cavitation Climate change Embolism Water potential 

References

  1. Alder NN, Sperry JS, Pockman WT (1996) Root and stem xylem cavitation, stomatal conductance, and leaf turgor in Acer grandidentatum across a soil moisture gradient. Oecologia 105:293–301CrossRefGoogle Scholar
  2. Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EH, Gonzalez P, Fensham R, Zhang Z, Castro J, Demidova N, Lim J-H, Allard G, Running SW, Semerci A, Cobb N (2009) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecol Manag 259:660–684CrossRefGoogle Scholar
  3. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress and signal transduction. Ann Rev Plant Biol 55:379–399CrossRefGoogle Scholar
  4. Aroca R, Porcel R, Ruiz-Lozano JM (2012) Regulation of root water uptake under abiotic stress conditions. J Exp Bot 63:43–57PubMedCrossRefGoogle Scholar
  5. Bleby TM, McElrone AJ, Jackson RB (2010) Water uptake and hydraulic redistribution across large woody root systems to 20 m depth. Plant Cell Environ 33:2132–2148PubMedCrossRefGoogle Scholar
  6. Bogeat-Triboulot MB, Martin R, Chatelet D, Cochard H (2002) Hydraulic conductance of root and shoot measured with the transient mode of the high-pressure flowmeter. Ann For Sci 59:389–396CrossRefGoogle Scholar
  7. Bréda N, Cochard H, Dreyer E, Granier A (1993) Water transfer in a mature oak stand (Quercus petraea): seasonal evolution and effects of a severe drought. Can J For Res 23:1136–1143CrossRefGoogle Scholar
  8. Burgess SSO, Adams MA, Turner NC, Ong CK (1998) The redistribution of soil water by tree root systems. Oecologia 115:306–311CrossRefGoogle Scholar
  9. Burgess SSO, Pate JS, Adams MA, Dawson TE (2000) Seasonal water acquisition and redistribution in the Austrailian woody phreatophyte, Banksia prionotes. Ann Bot 85:215–224CrossRefGoogle Scholar
  10. Cochard H, Bréda N, Granier A (1996) Whole tree hydraulic conductance and water loss regulation in Quercus during drought: evidence for stomatal control of embolism? Ann For Sci 53:197–206CrossRefGoogle Scholar
  11. Cook ER, Woodhouse CA, Eakin CM, Meko DM, Stahle DW (2004) North American summer PDSI reconstructions. IGBP PAGES/World Data Center for Paleoclimatology. Data contribution series # 2004-045. NOAA/NGDC Paleoclimatology Program, Boulder CO, USAGoogle Scholar
  12. Cruizat P, Cochard H, Améglio T (2002) Hydraulic architecture of trees: main concepts and results. Ann For Sci 59:723–752CrossRefGoogle Scholar
  13. David TS, Henriques MO, Besson CK, Nunes J, Valente F, Vaz M, Pereira JS, Siegwolf R, Chaves MM, Gazarini LC, David JS (2007) Water use strategies in two co-occurring Mediterranean evergreen oaks: surviving the summer drought. Tree Physiol 27:793–803PubMedCrossRefGoogle Scholar
  14. Diffenbaugh NS, Ashfaq M, Scherer M (2011) Transient regional climate change: analysis of the summer climate response in a high-resolution, century-scale ensemble experiment over the continental United States. J Geophys Res 116:D24111Google Scholar
  15. Domec J-C, Warren JM, Meinzer FC, Brooks JR, Coulombe R (2004) Native root xylem embolism and stomatal closure in stands of Douglas-fir and ponderosa pine: mitigation by hydraulic redistribution. Oecologia 141:7–16PubMedCrossRefGoogle Scholar
  16. Domec J-C, Noormets A, King JS, Sun G, McNulty SG, Gavazzi MJ, Boggs JL, Treasure EA (2009a) Decoupling the influence of leaf and root hydraulic conductances on stomatal conductance and its sensitivity to vapor pressure deficit as soil dries in a drained loblolly pine plantation. Plant Cell Environ 32:980–991PubMedCrossRefGoogle Scholar
  17. Domec J-C, Warren JM, Meinzer FC, Lachenbruch B (2009b) Safety factors for xylem failure by implosion and air-seeding within roots, trunks and branches of young and old conifer trees. IAWA J 30:100–120CrossRefGoogle Scholar
  18. Domec J-C, Schafer K, Oren R, Kim H, McCarthy (2010) Variable conductivity and embolism in roots and branches of four contrasting tree species and their impacts on whole-plant hydraulic performance under future atmospheric CO2 concentration. Tree Physiol 30:1001–1015PubMedCrossRefGoogle Scholar
  19. Doody TM, Benyon RG (2010) Direct measurement of groundwater uptake through tree roots in a cave. Ecohydrology 4:644–649CrossRefGoogle Scholar
  20. Eissenstat DM, Yanai RD (1997) The ecology of root lifespan. Adv Ecol Res 27:1–60CrossRefGoogle Scholar
  21. Elliot WR, Veni G (eds) (1994) The caves and karst of Texas. National Speleological Society, Huntsville, AL, USAGoogle Scholar
  22. Henzler T, Ye Q, Steudle E (2004) Oxidative gating of water channels (aquaporins) in Chara by hydroxyl radicals. Plant Cell Environ 27:1184–1195CrossRefGoogle Scholar
  23. Hoffmann WA, Marchin R, 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 Biol 8:2731–2742CrossRefGoogle Scholar
  24. Hubbard RM, Ryan MG, Stiller V, Sperry JS (2001) Stomatal conductance and photosynthesis vary linearly with plant hydraulic conductance in ponderosa pine. Plant Cell Environ 24:113–121CrossRefGoogle Scholar
  25. Jackson RB, Moore LA, Hoffmann WA, Pockman WT, Linder CR (1999) Ecosystem rooting depth determined with caves and DNA. Proc Natl Acad Sci USA 96:11387–11392PubMedCrossRefPubMedCentralGoogle Scholar
  26. Johnson DM, McCulloh KA, Meinzer FC, Woodruff DR, Eissenstat DM (2011) Hydraulic patterns and safety margins, from stem to stomata, in three eastern US tree species. Tree Physiol 31:659–668PubMedCrossRefGoogle Scholar
  27. Laur J, Hacke U (2013) Transpirational demand affects aquaporin expression in poplar roots. J Exp Bot 64:2283–2293PubMedCrossRefPubMedCentralGoogle Scholar
  28. Maurel C, Verdoucq L, Luu DT, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Ann Rev Plant Biol 59:595–624CrossRefGoogle Scholar
  29. McCulley RL, Jobbágy EG, Pockman WT, Jackson RB (2004) Nutrient uptake as a contributing explanation for deep rooting in arid and semi-arid ecosystems. Oecologia 141:620–628PubMedCrossRefGoogle Scholar
  30. McCulloh KA, Johnson DM, Meinzer FC, Woodruff DR (2014) The dynamic pipeline: Hydraulic capacitance and xylem hydraulic safety in four tall conifer species. Plant Cell Environ 37: 1171–1183Google Scholar
  31. McElrone AJ, Pockman WT, Martinez-Vilalta J, Jackson RB (2004) Variation in xylem structure and function in stems and roots of trees to 20 m depth. New Phytol 163:507–517CrossRefGoogle Scholar
  32. McElrone AJ, Bichler J, Pockman WT, Addington RN, Linder CR, Jackson RB (2007) Aquaporin-mediated changes in hydraulic conductivity of deep tree roots accessed via caves. Plant Cell Environ 30:142–1411CrossRefGoogle Scholar
  33. Meinzer FC, Goldstein G, Jackson P, Holbrook NM, Gutierrez MV, Cavelier J (1995) Environmental and physiological regulation of transpiration in tropical forest gap species: the influence of boundary layer and hydraulic properties. Oecologia 101:514–522CrossRefGoogle Scholar
  34. Nardini A, Pitt F (1999) Drought resistance of Quercus pubescens as a function of root hydraulic conductance, xylem embolism and hydraulic architecture. New Phytol 143:485–493CrossRefGoogle Scholar
  35. Nardini A, Battistuzzo M, Savi T (2013) Shoot desiccation and hydraulic failure in temperate woody angiosperms during an extreme summer drought. New Phytol 200:322–329PubMedCrossRefGoogle Scholar
  36. Nepstad DC, Carvalho CD, Davidson EA, Jipp PH, Lefebvre PA, Negreiros GH, da Silva ED, Stone TA, Trumbore SE, Viera S (1994) The role of deep roots in the hydrological and carbon cycles of Amazonian forests and pastures. Nature 372:666–669CrossRefGoogle Scholar
  37. Peñuelas J, Filella I (2003) Deuterium labeling of roots provides evidence of deep water access and hydraulic lift by Pinus nigra in a Mediterranean forest of NE Spain. Env Exp Bot 49:201–208CrossRefGoogle Scholar
  38. Persson H, Fircks YV, Majdi H, Nilsson LO (1995) Root distribution in a Norway spruce (Picea abies (L.) Karst.) stand subjected to drought and ammonium-sulphate application. Plant Soil 168–169:161–165CrossRefGoogle Scholar
  39. Schenk HJ, Jackson RB (2002) Rooting depths, lateral root spreads, and belowground/aboveground allometries of plants in water limited ecosystems. J Ecol 90:480–494CrossRefGoogle Scholar
  40. Seager R, Ting M, Held I, Kushnir Y, Lu J, Vecchi G, Huang HP, Harnik N, Lau NC, Li C, Velez J, Naik N (2007) Model projections on an imminent transition to a more arid climate in southwestern North America. Science 316:1181–1184PubMedCrossRefGoogle Scholar
  41. Sperry JS, Saliendra NZ (1994) Intra- and inter-plant variation in xylem cavitation in Betula occidentalis. Plant Cell Environ 16:279–287CrossRefGoogle Scholar
  42. 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 Environ 21:347–359CrossRefGoogle Scholar
  43. Sperry JS, Hacke UG, Oren R, Comstock JP (2002) Water deficits and hydraulic limits to leaf water supply. Plant Cell Environ 25:251–263PubMedCrossRefGoogle Scholar
  44. Steudle E, Peterson CA (1998) How does water get through roots? J Exp Bot 49:775–788Google Scholar
  45. Texas Forest Service (2012) Texas A&M forest survey shows 301 million trees killed by drought. Online: http://texasforestservice.tamu.edu/main/popup.aspx?id=16509
  46. Tyree MT, Ewers FW (1991) The hydraulic architecture of trees and other woody plants. New Phytol 119:345–360CrossRefGoogle Scholar
  47. Tyree MT, Zimmermann MH (2002) Xylem structure and the ascent of sap, 2nd edn. Springer, New York, NYCrossRefGoogle Scholar
  48. Tyree MT, Patiño S, Bennink J, Alexander J (1995) Dynamic measurements of roots hydraulic conductance using a high-pressure flowmeter in the laboratory and field. J Exp Bot 46:83–94CrossRefGoogle Scholar
  49. Vandeleur RK, Mayo G, Shelden MC, Gilliham M, Kaiser BN, Tyerman S (2009) The role of plasma membrane intrinsic protein aquaporins in water transport through roots: diurnal and drought stress responses reveal different strategies between isohydric and anisohydric cultivars of grapevine. Plant Physiol 149:445–460PubMedCrossRefPubMedCentralGoogle Scholar
  50. Ye Q, Steudle E (2006) Oxidative gating of water channels (aquaporins) in corn roots. Plant Cell Environ 29:459–470PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Daniel M. Johnson
    • 1
    • 5
  • Mark E. Sherrard
    • 2
  • Jean-Christophe Domec
    • 1
    • 3
  • Robert B. Jackson
    • 1
    • 4
  1. 1.Nicholas School of the EnvironmentDuke UniversityDurhamUSA
  2. 2.Department of BiologyUniversity of Northern IowaCedar FallsUSA
  3. 3.Bordeaux Sciences Agro, UMR 1391 INRA-ISPAUniversity of BordeauxGradignan CedexFrance
  4. 4.School of Earth Sciences, Woods Institute for the Environment, and Precourt Institute for EnergyStanford UniversityStanfordUSA
  5. 5.Department of Forest, Ranglend and Fire SciencesUniversity of IdahoMoscowUSA

Personalised recommendations