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Xylem plasticity allows rapid hydraulic adjustment to annual climatic variability

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Abstract

Thanks to acclimation, trees overcome environmental changes and endure for centuries. The anatomy of water conducting cells is an important factor determining plant success. Forming cells are coupled with the environment and their properties are naturally archived in the wood. Its variability across tree rings can thus provide a retrospective of plant’s hydraulic adjustments. In this work, we measured lumen and wall thickness of tracheids along tree-rings to explore how trees regulate their conducting system under variable plant-water conditions. Tracheids were measured along 51 dated rings of five mature Larix decidua and Picea abies trees from a low elevation site. Anatomical-based chronologies of annual growth performance, hydraulic conductance and safety, and construction costs were built. Similarities among chronologies and the relation to monthly climate data were analyzed. Most parameters displayed high annual plasticity which was partly coherent among trees and mostly associated with radial growth. In general, summer drought reduced growth and potential hydraulic conductivity of the forming ring, and increased hydraulic safety and construction costs. To evaluate the functional relevance of the annual acclimation, the conductivity of the forming ring relative to the entire sapwood needs to be assessed.

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References

  • Anfodillo T, Carraro V, Carrer M, Fior C, Rossi S (2006) Convergent tapering of xylem conduits in different woody species. New Phytol 169:279–290

    Article  PubMed  Google Scholar 

  • Awad H, Barigah T, Badel E, Cochard H, Herbette S (2010) Poplar vulnerability to xylem cavitation acclimates to drier soil conditions. Physiol Plant 139:280–288

    PubMed  CAS  Google Scholar 

  • Barnard DM, Meinzer FC, Lachenbruch B, McCulloh KA, Johnson DM, Woodruff DR (2011) Climate-related trends in sapwood biophysical properties in two conifers: avoidance of hydraulic dysfunction through coordinated adjustments in xylem efficiency, safety and capacitance. Plant Cell Environ 34:643–654

    Article  PubMed  Google Scholar 

  • Beikircher B, Mayr S (2009) Intraspecific differences in drought tolerance and acclimation in hydraulics of Ligustrum vulgare and Viburnum lantana. Tree Physiol 29:765–775

    Article  PubMed  Google Scholar 

  • Cermak J, Kucera J, Bauerle WL, Phillips N, Hinckley TM (2007) Tree water storage and its diurnal dynamics related to sap flow and changes in stem volume in old-growth Douglas-fir trees. Tree Physiol 27:181–198

    Article  PubMed  Google Scholar 

  • Chave J, Muller-Landau HC, Baker TR, Easdale TA, ter Steege H, Webb CO (2006) Regional and phylogenetic variation of wood density across 2456 Neotropical tree species. Ecol Appl 16:2356–2367

    Article  PubMed  Google Scholar 

  • Choat B, Cobb AR, Jansen S (2008) Structure and function of bordered pits: new discoveries and impacts on whole-plant hydraulic function. New Phytol 177:608–625

    Article  PubMed  Google Scholar 

  • Cook ER, Kairiukstis LA (1990) Methods of dendrochronology applications in the environmental sciences. Kluwer, Dordrecht

    Google Scholar 

  • DeSoto L, De la Cruz M, Fonti P (2011) Intra-annual patterns of tracheid size in the Mediterranean tree Juniperus thurifera as an indicator of seasonal water stress. Can J For Res 41:1280–1294

    Article  Google Scholar 

  • Dobbertin M, Eilmann B, Bleuler P, Giuggiola A, Pannatier EG, Landolt W, Schleppi P, Rigling A (2010) Effect of irrigation on needle morphology, shoot and stem growth in a drought-exposed Pinus sylvestris forest. Tree Physiol 30:346–360

    Article  PubMed  Google Scholar 

  • Eilmann B, Zweifel R, Buchmann N, Fonti P, Rigling A (2009) Drought-induced adaptation of the xylem in Scots pine and pubescent oak. Tree Physiol 29:1011–1020

    Article  PubMed  Google Scholar 

  • Fonti P, Garcìa-Gonzàlez I (2004) Suitability of chestnut earlywood vessel chronologies for ecological studies. New Phytol 163:77–86

    Article  Google Scholar 

  • Fonti P, Garcìa-Gonzàlez I (2008) Earlywood vessel size of oak as a potential proxy for spring precipitation in mesic sites. J Biogeogr 35:2249–2257

    Article  Google Scholar 

  • Fonti P, von Arx G, Garcia-Gonzalez I, Eilmann B, Sass-Klaassen U, Gartner H, Eckstein D (2010) Studying global change through investigation of the plastic responses of xylem anatomy in tree rings. New Phytol 185:42–53

    Article  PubMed  Google Scholar 

  • Fritts HC (1976) Tree rings and climate. Academic Press, London

    Google Scholar 

  • Garcia-Gonzalez I, Eckstein D (2003) Climatic signal of earlywood vessels of oak on a maritime site. Tree Physiol 23:497–504

    Article  Google Scholar 

  • Garcìa-Gonzàlez I, Fonti P (2006) Selecting earlywood vessels to maximize their environmental signal. Tree Physiol 26:1289–1296

    Article  PubMed  Google Scholar 

  • Garcìa-Gonzàlez I, Fonti P (2008) Ensuring a representative sample of earlywood vessels for dendroecological studies: an example from two ring-porous species. Trees-Struct Funct 22:237–244

    Article  Google Scholar 

  • Hacke UG, Jansen S (2009) Embolism resistance of three boreal conifer species varies with pit structure. New Phytol 182:675–686

    Article  PubMed  Google Scholar 

  • Hacke UG, Sperry JS (2001) Functional and ecological xylem anatomy. Perspect Plant Ecol 4:97–115

    Article  Google Scholar 

  • Hacke UG, Sperry JS, Pockman WT, Davis SD, McCulloch KA (2001) Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 126:457–461

    Article  Google Scholar 

  • Holbrook NM, Zwieniecki MA (2005) Vascular transport in plants. Elsevier, Amsterdam

    Google Scholar 

  • Horn JL (1965) A rationale and test for the number of factors in factor analysis. Psychometrika 30:179–185

    Article  PubMed  CAS  Google Scholar 

  • Klein T, Cohen S, Yakir D (2011) Hydraulic adjustments underlying drought resistance of Pinus halepensis. Tree Physiol 31:637–648

    Article  PubMed  Google Scholar 

  • Ladjal M, Huc R, Ducrey M (2005) Drought effects on hydraulic conductivity and xylem vulnerability to embolism in diverse species and provenances of Mediterranean cedars. Tree Physiol 25:1109–1117

    Article  PubMed  Google Scholar 

  • Maherali H, Pockman WT, Jackson RB (2004) Adaptive variation in the vulnerability of woody plants to xylem cavitation. Ecology 85:2184–2199

    Article  Google Scholar 

  • Makinen H, Jyske T, Saranpää P (2008) Variation of tracheid length within annual rings of Scots pine and Norway spruce. Holzforschung 62:123–128

    Article  CAS  Google Scholar 

  • Markesteijn L, Poorter L (2009) Seedling root morphology and biomass allocation of 62 tropical tree species in relation to drought- and shade-tolerance. J Ecol 97:311–325

    Article  Google Scholar 

  • Martin JA, Esteban LG, de Palacios P, Fernandez FG (2010) Variation in wood anatomical traits of Pinus sylvestris L. between Spanish regions of provenance. Trees-Struct Funct 24:1017–1028

    Article  Google Scholar 

  • Martinez-Cabrera HI, Jones CS, Espino S, Schenk HJ (2009) Wood anatomy and wood density in shrubs: responses to varying aridity along transcontinental transects. Am J Bot 96:1388–1398

    Article  PubMed  Google Scholar 

  • McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739

    Article  PubMed  Google Scholar 

  • Meier IC, Leuschner C (2008) Belowground drought response of European beech: fine root biomass and carbon partitioning in 14 mature stands across a precipitation gradient. Global Change Biol 14:2081–2095

    Article  Google Scholar 

  • Meinzer FC (2011) Size-and age-related changes in tree structure and function. Springer, Dordrecht

    Book  Google Scholar 

  • Meinzer FC, Johnson DM, Lachenbruch B, McCulloh KA, Woodruff DR (2009) Xylem hydraulic safety margins in woody plants: coordination of stomatal control of xylem tension with hydraulic capacitance. Funct Ecol 23:922–930

    Article  Google Scholar 

  • Panyushkina IP, Hughes MK, Vaganov EA, Munro MAR (2003) Summer temperature in northeastern Siberia since 1642 reconstructed from tracheid dimensions and cell numbers of Larix cajanderi. Can J Forest Res 33:1905–1914

    Article  Google Scholar 

  • Pittermann J, Sperry JS, Hacke UG, Wheeler JK, Sikkema EH (2006a) Inter-tracheid pitting and the hydraulic efficiency of conifer wood: the role of tracheid allometry and cavitation protection. Am J Bot 93:1265–1273

    Article  PubMed  Google Scholar 

  • Pittermann J, Sperry JS, Wheeler JK, Hacke UG, Sikkema EH (2006b) Mechanical reinforcement of tracheids compromises the hydraulic efficiency of conifer xylem. Plant Cell Environ 29:1618–1628

    Article  PubMed  Google Scholar 

  • Salleo S, Trifilo P, Esposito S, Nardini A, Lo Gullo MA (2009) Starch-to-sugar conversion in wood parenchyma of field-growing Laurus nobilis plants: a component of the signal pathway for embolism repair? Funct Plant Biol 36:815–825

    Article  Google Scholar 

  • Schenk HJ, Espino S, Goedhart CM, Nordenstahl M, Cabrera HIM, Jones CS (2008) Hydraulic integration and shrub growth form linked across continental aridity gradients. Proc Natl Acad Sci USA 105:11248–11253

    Article  PubMed  CAS  Google Scholar 

  • Schoonmaker AL, Hacke UG, Landhausser SM, Lieffers VJ, Tyree MT (2010) Hydraulic acclimation to shading in boreal conifers of varying shade tolerance. Plant Cell Environ 33:382–393

    Article  PubMed  Google Scholar 

  • Spicer R, Gartner BL (2001) The effects of cambial age and position within the stem on specific conductivity in Douglas-fir (Pseudotsuga menziesii) sapwood. Trees-Struct Funct 15:222–229

    Article  Google Scholar 

  • Tyree MT, Zimmermann MH (2002) Xylem structure and the ascent of sap, 2nd edn. Springer, Berlin

    Book  Google Scholar 

  • Weber P, Bugmann H, Rigling A (2007) Radial growth responses to drought of Pinus sylvestris and Quercus pubescens in an inner-Alpine dry valley. J Veg Sci 18:777–792

    Article  Google Scholar 

  • Yasue K, Funada R, Kobayashi O, Ohtani J (2000) The effects of tracheid dimensions on variations in maximum density of Picea glehnii and relationships to climatic factors. Trees-Struct Funct 14:223–229

    Article  Google Scholar 

  • Zobel BJ, van Buijtenen JP (1989) Wood variation: its causes and control. Springer, Berlin

    Book  Google Scholar 

Download references

Acknowledgments

This study was supported by Swiss National Foundation through an International short visit (Grant number: #131408) and through the cooperation on the project INTEGRAL (#121859). We would like to thank David Frank and Georg von Arx for their assistance and critical discussion of an earlier version of the manuscript, and Kathlene English and Gregory King for the English review.

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Correspondence to Patrick Fonti.

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Communicated by Y. Sano.

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Bryukhanova, M., Fonti, P. Xylem plasticity allows rapid hydraulic adjustment to annual climatic variability. Trees 27, 485–496 (2013). https://doi.org/10.1007/s00468-012-0802-8

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  • DOI: https://doi.org/10.1007/s00468-012-0802-8

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