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Repeated freeze–thaw cycles induce embolism in drought stressed conifers (Norway spruce, stone pine)

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Abstract

Freezing and thawing lead to xylem embolism when gas bubbles caused by ice formation expand during the thaw process. However, previous experimental studies indicated that conifers are resistant to freezing-induced embolism, unless xylem pressure becomes very negative during the freezing. In this study, we show that conifers experienced freezing-induced embolism when exposed to repeated freeze–thaw cycles and simultaneously to drought. Simulating conditions at the alpine timberline (128 days with freeze–thaw events and thawing rates of up to 9.5 K h−1 in the xylem of exposed twigs during winter), young trees of Norway spruce [Picea abies (L.) Karst.] and stone pine (Pinus cembra L.) were exposed to 50 and 100 freeze–thaw cycles. This treatment caused a significant increase in embolism rates in drought-stressed samples. Upon 100 freeze–thaw cycles, vulnerability thresholds (50% loss of conductivity) were shifted 1.8 MPa (Norway spruce) and 0.8 MPa (stone pine) towards less negative water potentials. The results demonstrate that freeze–thaw cycles are a possible reason for winter-embolism in conifers observed in several field studies. Freezing-induced embolism may contribute to the altitudinal limits of conifers.

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Abbreviations

ψ:

xylem water potential

References

  • Borghetti M, Edwards WRN, Grace J, Jarvis PG, Raschi A (1991) The refilling of embolized xylem in Pinus sylvestris L.. Plant Cell Environ 14:357–369

    Google Scholar 

  • Chiu S, Ewers FW (1993) The effect of segment length on conductance measurements in Lonicera fragrantissima. J Exp Bot 44:175–181

    Google Scholar 

  • Cochard H, Tyree MT (1990) Xylem dysfunction in Quercus: vessel sizes, tyloses, cavitation and seasonal changes in embolism. Tree Physiol 6:393–407

    Google Scholar 

  • Davis SD, Sperry JS, Hacke UG (1999) The relationship between xylem conduit diameter and cavitation caused by freezing. Am J Bot 86:1367–1372

    PubMed  Google Scholar 

  • Edwards WRN, Jarvis PG, Grace J, Moncrieff JB (1994) Reversing cavitation in tracheids of Pinus sylvestris L. under negative water potentials. Plant Cell Environ 17:389–397

    Google Scholar 

  • Ewers FW (1985) Xylem structure and water conduction in conifer trees, dicot trees and lianas. Int Assoc Wood Anat Bull 6:309–317

    Google Scholar 

  • Feild TS, Brodribb T (2001) Stem water transport and freeze–thaw xylem embolism in conifers and angiosperms in a Tasmanian treeline heath. Oecologia 127:314–320

    Article  Google Scholar 

  • Groß M, Rainer I, Tranquillini W (1991) Über die Frostresistenz der Fichte mit besonderer Berücksichtigung der Zahl der Gefrierzyklen und der Geschwindigkeit der Temperaturänderung beim Frieren und Auftauen. Forstwiss Centralbl 110:207–217

    Google Scholar 

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

    Google Scholar 

  • Hammel HT (1967) Freezing of xylem sap without cavitation. Plant Physiol 42:55–66

    Google Scholar 

  • Just J, Sauter JJ (1991) Changes in hydraulic conductivity upon freezing of the xylem of Populus × canadiensis Moench "robusta". Trees 5:117–121

    Google Scholar 

  • Kolb KJ, Sperry JS (1999) Differences in drought adaptation between subspecies of sagebrush (Artemisia tridentata). Ecology 80:2373–2384

    Google Scholar 

  • Langan SJ, Ewers FW, Davis SD (1997) Xylem dysfunction caused by water stress and freezing in two species of co-occurring chaparral shrubs. Plant Cell Environ 20:425–437

    Google Scholar 

  • Lemoine D, Granier A, Cochard H (1999) Mechanism of freeze-induced embolism in Fagus sylvatica L.. Trees 13:206–210

    Article  Google Scholar 

  • Lipp CC, Nilsen ET (1997) The impact of subcanopy light environment on the hydraulic vulnerability of Rhododendron maximum to freeze–thaw cycles and drought. Plant Cell Environ 20:1264–1272

    Google Scholar 

  • Lo Gullo MA, Salleo S (1993) Different vulnerabilities of Quercus ilex L. to freeze- and summer drought-induced xylem embolism: an ecological interpretation. Plant Cell Environ 16:511–519

    Google Scholar 

  • Mayr S, Wolfschwenger M, Bauer H (2002) Winter-drought induced embolism in Norway spruce (Picea abies) at the Alpine timberline. Physiol Plant 115:74–80

    Article  CAS  PubMed  Google Scholar 

  • Mayr S, Schwienbacher F, Bauer H (2003) Winter at the Alpine timberline: Why does embolism occur in Norway spruce but not in stone pine? Plant Physiol 131:780–792

    Article  PubMed  Google Scholar 

  • Nardini A, Salleo S, LoGullo MA, Pitt F (2000) Different responses to drought and freeze stress of Quercus ilex L. growing along a latitudinal gradient. Plant Ecol 148:139–147

    Article  Google Scholar 

  • Pammenter NW, Vander Willigen C (1998) A mathematical and statistical analysis of the curves illustrating vulnerability of xylem to cavitation. Tree Physiol 18:589–593

    Google Scholar 

  • Robson DJ, Petty JA (1987) Freezing in conifer xylem I. Pressure changes and growth velocity of ice. J Exp Bot 38:1901–1908

    Google Scholar 

  • Robson DJ, McHardy WJ, Petty JA (1988) Freezing in conifer xylem II. Pit aspiration and bubble formation. J Exp Bot 39:1617–1621

    Google Scholar 

  • Sobrado MA, Grace J, Jarvis PG (1992) The limits to xylem embolism recovery in Pinus sylvestris L.. J Exp Bot 43:831–836

    Google Scholar 

  • Sparks JP, Campbell GS, Black RA (2001) Water content, hydraulic conductivity, and ice formation in winter stems of Pinus contorta: a TDR case study. Oecologia 127:468–475

    Article  Google Scholar 

  • Sperry JS, Robson DJ (2001) Xylem cavitation and freezing in conifers. In: Bigras FJ, Colombo SJ (ed) Conifer cold hardiness. Kluwer, Dordrecht, pp 121–136

  • Sperry JS, Sullivan JEM (1992) Xylem embolism in response to freeze–thaw cycles and water stress in ring-porous, diffuse-porous and conifer species. Plant Physiol 100:605–613

    Google Scholar 

  • Sperry JS, Donnelly JR, Tyree MT (1988) A method for measuring hydraulic conductivity and embolism in xylem. Plant Cell Environ 11:35–40

    Google Scholar 

  • Sperry JS, Nichols KL, Sullivan JEM, Eastlack SE (1994) Xylem embolism in ring-porous, diffuse-porous, and coniferous trees of northern Utah and interior Alaska. Ecology 75:1736–1752

    Google Scholar 

  • Sucoff E (1969) Freezing of conifer xylem and the cohesion-tension theory. Physiol Plant 22:424–431

    Google Scholar 

  • Tyree MT, Davis SD, Cochard H (1994) Biophysical perspectives of xylem evolution: Is there a tradeoff of hydraulic efficiency for vulnerability to dysfunction? IAWA J 15:335–360

    Google Scholar 

  • Utsumi Y, Sano Y, Fujikawa S, Funada R, Ohtani J (1998) Visualization of cavitated vessels in winter and refilled vessels in spring in diffuse-porous trees by cryo-scanning electron microscopy. Plant Physiol 117:1463–1471

    Article  CAS  PubMed  Google Scholar 

  • Vogt UK (2001) Hydraulic vulnerability, vessel refilling, and seasonal courses of stem water potential of Sorbus aucuparia L. and Sambucus nigra L.. J Exp Bot 52:1527–1536

    Article  CAS  PubMed  Google Scholar 

  • Zhu XB, Cox RM, Meng FR, Arp PA (2001) Responses of xylem cavitation, freezing injury and shoot dieback to a simulated winter thaw in yellow birch seedlings growing in different nursery culture regimes. For Ecol Manag 145:243–253

    Article  Google Scholar 

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Acknowledgements

This study was supported by the Austrian "Fonds zur Förderung der wissenschaftlichen Forschung", Project-No. P13782-BIO. We thank Hanno Richter and Silvia Kikuta (University of agricultural sciences Vienna) for critical discussion of data, Gilbert Neuner an Johanna Wagner (University Innsbruck) for providing the climate chamber and the equipment for anatomical measurements and Birgit Dämon (University Innsbruck) for helpful assistance.

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Correspondence to Stefan Mayr.

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Mayr, S., Gruber, A. & Bauer, H. Repeated freeze–thaw cycles induce embolism in drought stressed conifers (Norway spruce, stone pine). Planta 217, 436–441 (2003). https://doi.org/10.1007/s00425-003-0997-4

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  • DOI: https://doi.org/10.1007/s00425-003-0997-4

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