Advertisement

Plant and Soil

, Volume 366, Issue 1–2, pp 305–320 | Cite as

Drought affects tracheid structure, dehydrin expression, and above- and belowground growth in 5-year-old Norway spruce

  • Toril Drabløs Eldhuset
  • Nina Elisabeth Nagy
  • Daniel Volařík
  • Isabella Børja
  • Roman Gebauer
  • Igor A. Yakovlev
  • Paal KrokeneEmail author
Regular Article

Abstract

Purpose

Drought-induced tree susceptibility is a major risk associated with climate change. Here we report how an 11-week drought affected tracheid structure, gene expression, and above- and belowground growth in 5-year-old Norway spruce trees (Picea abies) under controlled conditions.

Results

The canopy of trees subjected to severe drought had significantly less current-year needle biomass, and fewer tracheids and tracheid rows in current-year shoots compared to fully watered control trees. Belowground tissues were more strongly affected by drought than aboveground tissues. In fine roots (<2 mm diameter) severe drought significantly reduced root biomass, root diameter, root length density and root surface area per soil volume compared to the control. Tracheid diameter and hydraulic conductivity in fine roots were significantly lower and tracheid flatness higher in trees subjected to severe drought than in control trees, both for long and short roots. Transcripts of the drought-related dehydrins PaDhn1 and PaDhn6 were strongly upregulated in stem bark and current-year needles in response to drought, whereas PaDhn4.5 was down-regulated.

Conclusions

This study demonstrates that drought reduces biomass and hydraulic conductivity in fine roots and needles. We suggest that the ratio between PaDhn6 and PaDhn4.5 may be a sensitive marker of drought stress in Norway spruce.

Keywords

Dehydrin Fine roots Needles Norway spruce Picea abies Tracheid structure 

Abbreviations

qRT-PCR

Quantitative reverse transcription-polymerase chain reaction

PaDhn

Picea abies dehydrin

PaCAP

Picea abies cold acclimation protein

Notes

Acknowledgement

We thank A. E. Nilsen and G. Østreng for taking care of the plants, C. Kierulf for assistance with harvesting, M. Kjos for dehydrin analysis and Dr. S. Eich-Greatorex for allowing us to use the WinRhizo equipment. The project was financed by the Czech Ministry of Education (grant no. 6215648902), the EEA Financial Mechanism funded by Iceland, Liechtenstein and Norway, the Norwegian Financial Mechanism (grant no. A/CZ0046/2/0009), the Mendel University in Brno (grant IGA 12/2010), and the Norwegian Forest and Landscape Institute.

References

  1. Abe H, Nakai T (1999) Effect of the water status within a tree on tracheid morphogenesis in Cryptomeria japonica D. Don. Trees 14:124–129Google Scholar
  2. Adams HD, Guardiola-Claramonte M, Barron-Gafford GA, Villegas JC, Breshears DD, Zou CB, Troch PA, Huxman TE (2009) Temperature sensitivity of drought-induced tree mortality portends increased regional die-off under global-change-type drought. Proc Nat Acad Sci USA 106:7063–7066PubMedCrossRefGoogle Scholar
  3. Alder NN, Sperry JS, Pockman WT (1996) Root and stem xylem embolism, stomatal conductance and leaf turgor in Acer grandidentatum populations along a soil moisture gradient. Oecologia 105:293–301CrossRefGoogle Scholar
  4. Allen CD, Macalady AK, Chenchouni H et al (2010) A global overview of drought- and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manage 259:660–684CrossRefGoogle Scholar
  5. Andreassen K, Solberg S, Tveito OE, Lystad SL (2006) Regional differences in climatic responses of Norway spruce (Picea abies L. Karst) growth in Norway. For Ecol Manage 222:211–221CrossRefGoogle Scholar
  6. Artlip T, Wisniewski M (1997) Tissue-specific expression of a dehydrin gene in one-year-old ‘Rio Oso Gem’ peach trees. J Am Soc Hortic Sci 122:784–787Google Scholar
  7. Blödner C, Skrøppa T, Johnsen Ø, Polle A (2005) Freezing tolerance in two Norway spruce (Picea abies (L.) Karst.) progenies is physiologically correlated with drought tolerance. J Plant Physiol 162:549–558PubMedCrossRefGoogle Scholar
  8. Bréda N, Huc R, Granier A, Dreyer E (2006) Temperate forest trees and stands under severe drought: a review of ecophysiological responses, adaptation processes and long-term consequences. Ann Forest Sci 63:625–644CrossRefGoogle Scholar
  9. Campbell SA, Close TJ (1997) Dehydrins: genes, proteins and associationswith phenotypic traits. New Phytol 137:61–74CrossRefGoogle Scholar
  10. Charra-Vaskou K, Mayr S (2011) The hydraulic conductivity of the xylem in conifer needles (Picea abies and Pinus mugo). J Exp Bot 62:4383–4390PubMedCrossRefGoogle Scholar
  11. Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought – from genes to the whole plant. Funct Plant Biol 30:239–264CrossRefGoogle Scholar
  12. Christensen JH, Christensen OB (2003) Climate modelling: severe summertime flooding in Europe. Nature 421:805–806PubMedCrossRefGoogle Scholar
  13. Close TJ (1997) Dehydrins: a commonality in the response of plants to dehydration and low temperature. Physiol Plantarum 100:291–296CrossRefGoogle Scholar
  14. Cochard H (1992) Vulnerability of several conifers to air embolism. Tree Physiol 11:73–83PubMedCrossRefGoogle Scholar
  15. Craine JM (2006) Competition for nutrients and optimal root allocation. Plant Soil 285:171–185CrossRefGoogle Scholar
  16. Davies WJ, Bacon MA (2003) Adaptation of roots to drought. In: De Kroon H, Visser EJW (eds) Root ecology. Ecological Studies 168. Springer-Verlag, Berlin, pp 173–192Google Scholar
  17. Davis SD, Sperry JS, Hacke UG (1999) The relationship between xylem conduit diameter and cavitation caused by freezing. Am J Bot 86:1367–1372PubMedCrossRefGoogle Scholar
  18. Denne MP (1988) Definition of latewood according to Mork (1928). IAWA Bull 10:59–62Google Scholar
  19. R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org
  20. Ditmarová L, Kurjak D, Palmroth S, Kmet J, Střelcová K (2010) Physiological responses of Norway spruce (Picea abies) seedlings to drought stress. Tree Physiol 30:205–213PubMedCrossRefGoogle Scholar
  21. Eissenstat DM, Wells CE, Yanai RD, Whitbeck JL (2000) Building roots in a changing environment: implications for root longevity. New Phytol 147:33–42CrossRefGoogle Scholar
  22. Ericsson A (1979) Effects of fertilization and irrigation on the seasonal changes of carbohydrate reserves in different age-classes of needle on 20-year-old Scots pine (Pinus sylvestris). Physiol Plantarum 45:270–280CrossRefGoogle Scholar
  23. Feil W, Kottke I, Oberwinkler F (1988) The effect of drought on mycorrhizal production and very fine root system development of Norway spruce under natural and experimental conditions. Plant Soil 108:221–231CrossRefGoogle Scholar
  24. Gebauer R, Volařík D, Martinková M (2011) Impact of soil pressure and compaction on tracheids in Norway spruce seedlings. New forests 41:75–88CrossRefGoogle Scholar
  25. Gebauer R, Volařík D, Urban J, BØrja I, Nagy NE, Eldhuset TD, Krokene P (2012) Effects of different light conditions on the xylem structure of Norway spruce needles. Trees. 26:1079–1089Google Scholar
  26. Gryc V, Vavrčík H (2006) Effect of the position in a stem on the variability of tracheids in spruce with the occurrence the compression wood. In: Wood Structure and Properties, Arbora Publishers, Zvolen, pp 43–49Google Scholar
  27. Hejnowicz Z (1997) Graviresponses in herbs and tree: a major role for the redistribution of tissue and growth stresses. Planta 203:136–146CrossRefGoogle Scholar
  28. Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211CrossRefGoogle Scholar
  29. Jinxing L (1989) Distribution, size and effective aperture area of the inter-tracheid pits in the radial wall of Pinus radiata tracheids. IAWA Bull 10:53–58Google Scholar
  30. Joslin JD, Wolfe MH (2003) Fine root growth response. In: Hanson PJ, Wullschleger SD (eds) North American temperate deciduous forest response to changing precipitation regimes. Ecological Studies166. Springer, New York, pp 274–302CrossRefGoogle Scholar
  31. Jyske T, Hölttä T, Mäkinen H, Nöjd P, Lumme I, Spiecker H (2010) The effect of artificially induced drought on radial increment and wood properties of Norway spruce. Tree Physiol 30:103–15PubMedCrossRefGoogle Scholar
  32. Kalberer SR, Wisniewski M, Arora R (2006) Deacclimation and reacclimation of cold-hardy plants: current understanding and emerging concepts. Plant Sci 171:3–16CrossRefGoogle Scholar
  33. Karlson DT, Zeng Y, Stirm VE, Joly RJ, Ashworth EN (2003) Photoperiodic regulation of a 24-kD dehydrin-like protein in red-osierdogwood (Cornus sericea L.) in relation to freeze-tolerance. Plant Cell Physiol 44:25–34PubMedCrossRefGoogle Scholar
  34. Karlsson PE, Medin EL, Wallin G, Selldén G, Skärby L (1997) Effects of ozone and drought stress on the physiology and growth of two clones of Norway spruce. New Phytol 136:265–275CrossRefGoogle Scholar
  35. Krasowski MJ, Owens JN (1999) Tracheids in white spruce seedling’s long lateral roots in response to nitrogen availability. Plant Soil 217:215–228CrossRefGoogle Scholar
  36. 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 25:1109–1117PubMedCrossRefGoogle Scholar
  37. Le Thiec D, Dixon M, Garrec JP (1994) The effects of slightly elevated ozone concentrations and mild drought stress on the physiology and growth of Norway spruce, Picea abies (L.) Karst. and beech, Fagus sylvatica L., in open-top chambers. New Phytol 128:671–678CrossRefGoogle Scholar
  38. Leuschner C, Backes K, Hertel D, Schipka F, Schmitt U, Terborg O, Runge M (2001) Drought responses at leaf, stem and fine root levels of competitive Fagus sylvatica L. and Quercus petraea (Matt) Liebl. trees in dry and wet years. Forest Ecol Manage 149:33–46CrossRefGoogle Scholar
  39. Lippert M, Häberle K, Steiner K, Payer H, Rehfuess K (1996) Interactive effects of elevated CO2 and O3 on photosynthesis and biomass production of clonal 5-year-old Norway spruce [Picea abies (L.) Karst.] under different nitrogen nutrition and irrigation treatments. Trees 10:382–392Google Scholar
  40. Lopez CG, Banowetz G, Peterson CJ, Kronstad WE (2001) Differential accumulation of a 24-kd dehydrin protein in wheat seedlings correlates with drought stress tolerance at grain filling. Hereditas 135:175–181PubMedCrossRefGoogle Scholar
  41. Lu P, Biron P, Granier A, Cochard H (1996) Water relations of adult Norway spruce (Picea abies (L.) Karst) under soil drought in the Vosges mountains: whole-tree hydraulic conductance, xylem embolism and water loss regulation. Ann Sci For 53:113–121CrossRefGoogle Scholar
  42. Mandre M, Tullus H, Kõšeiko J (2002) Partitioning of carbohydrates and biomass of needles in Scots pine canopy. Z Naturforsch 57c:296–302Google Scholar
  43. McDowell N, Pockman WT, Allen CD et al (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739PubMedCrossRefGoogle Scholar
  44. McElrone AJ, Pockaman 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
  45. Meier IC, Leuschner C (2008) Genotypic variation and phenotypic plasticity in the drought response of fine roots of European beech. Tree Physiol 28:297–309PubMedCrossRefGoogle Scholar
  46. Mork E (1928) Die Qualität des Fichtenholzes unter besonderer Rücksichtnahme auf Schleif- und Papierholz. Der Papier-Fabrikant 26:741–747Google Scholar
  47. Nobel PS (2005) Physicochemical and environmental plant physiology. Elssevier Academic Press, USA, pp 446–454Google Scholar
  48. Palátová E (2002) Effect of increased nitrogen deposition and drought stress on the development of Scots pine (Pinus sylvestris L.) – II. Root system response. J For Sci 48:237–247Google Scholar
  49. Parker J, Patton RL (1975) Effects of drought and defoliation on some metabolites in roots of black oak seedlings. Can J For Res 5:457–463CrossRefGoogle Scholar
  50. Pittermann J, Sperry JS (2003) Tracheid diameter is the key trait determining the extent of freezing-induced embolism in conifers. Tree Physiol 23:907–914PubMedCrossRefGoogle Scholar
  51. Rinne PL, Kaikuranta PL, van der Plas LH, van der Schoot C (1999) Dehydrins in cold-acclimated apices of birch (Betula pubescens Ehrh.): production, localization and potential role in rescuing enzyme function during dehydration. Planta 209:377–388PubMedCrossRefGoogle Scholar
  52. Rowell DP, Jones RG (2006) Causes and uncertainty of future summer drying over Europe. Clim Dyn 27:281–299CrossRefGoogle Scholar
  53. Rowland LJ, Arora R (1997) Proteins related to endodormancy (rest) in woody perennials. Plant Sci 126:119–144CrossRefGoogle Scholar
  54. Schume H, Grabner M, Eckmüllner O (2004) The influence of an altered groundwater regime on vessel properties of hybrid poplar. Trees 18:184–194CrossRefGoogle Scholar
  55. Solberg S (2004) Summer drought – a driver for crown condition and mortality of Norway spruce in Norway. Forest Pathol 34:93–104CrossRefGoogle Scholar
  56. Sperry JS, Meinzer FC, McCulloh KA (2008) Safety and efficiency conflicts in hydraulic architecture: scaling from tissues to trees. Plant Cell Environ 31:632–645PubMedCrossRefGoogle Scholar
  57. Turtola S, Manninen A, Rikala R, Kainulainen P (2003) Drought stress alters the concentration of wood terpenoids in Scots pine and Norway spruce seedlings. J Chem Ecol 29:1981–1995PubMedCrossRefGoogle Scholar
  58. Tyree MT, Zimmermann MH (2002) Xylem structure and the ascent of sap. Springer, BerlinCrossRefGoogle Scholar
  59. Velasco-Conde T, Yakovlev I, Majada J, Aranda I, Johnsen Ø (2012) Dehydrins in maritime pine (Pinus pinaster) and their expression related to drought stress response. Tree Genet Genomes. (in press) (doi:  10.1007/s11295-012-0476-9).
  60. Wallin G, Karlsson PE, Selldén G, Ottosson S, Medin E-L, Pleijel H, Skärby L (2002) Impact of four years exposure to different levels of ozone, phosphorus and drought on chlorophyll, mineral nutrients, and stem volume of Norway spruce, Picea abies. Physiol Plantarum 114:192–2006CrossRefGoogle Scholar
  61. Wilkins O, Waldron L, Nahal H, Provart NJ, Campbell MM (2009) Genotype and time of day shape the Populus drought response. Plant J 60:703–715PubMedCrossRefGoogle Scholar
  62. Yakovlev I, Asante D, Fossdal C, Partanen J, Junttila O, Johnsen Ø (2008) Dehydrins expression related to timing of bud burst in Norway spruce. Planta 228:459–472PubMedCrossRefGoogle Scholar
  63. Zimmermann MH (1983) Xylem structure and the ascent of sap. Springer, New YorkGoogle Scholar
  64. Zwieniecki MA, Melcher PJ, Holbrook MN (2001) Hydraulic properties of individual xylem vessels of Fraxinus americana. J Exp Bot 52:257–264PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Toril Drabløs Eldhuset
    • 1
  • Nina Elisabeth Nagy
    • 1
  • Daniel Volařík
    • 2
  • Isabella Børja
    • 1
  • Roman Gebauer
    • 2
  • Igor A. Yakovlev
    • 1
  • Paal Krokene
    • 1
    Email author
  1. 1.Norwegian Forest and Landscape InstituteÅsNorway
  2. 2.Department of Forest Botany, Dendrology and GeobiocoenologyMendel University in BrnoBrnoCzech Republic

Personalised recommendations