Skip to main content

Advertisement

SpringerLink
Log in

Osmotic and elastic adjustments in cold desert shrubs differing in rooting depth: coping with drought and subzero temperatures

  • Physiological ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Physiological adjustments to enhance tolerance or avoidance of summer drought and winter freezing were studied in shallow- to deep-rooted Patagonian cold desert shrubs. We measured leaf water potential (ΨL), osmotic potential, tissue elasticity, stem hydraulic characteristics, and stomatal conductance (g S) across species throughout the year, and assessed tissue damage by subzero temperatures during winter. Species behavior was highly dependent on rooting depth. Substantial osmotic adjustment (up to 1.2 MPa) was observed in deep-rooted species exhibiting relatively small seasonal variations in ΨL and with access to a more stable water source, but having a large difference between predawn and midday ΨL. On the other hand, shallow-rooted species exposed to large seasonal changes in ΨL showed limited osmotic adjustment and incomplete stomatal closure, resulting in turgor loss during periods of drought. The bulk leaf tissue elastic modulus (ε) was lower in species with relatively shallow roots. Daily variation in g S was larger in shallow-rooted species (more than 50 % of its maximum) and was negatively associated with the difference between ΨL at the turgor loss point and minimum ΨL (safety margin for turgor maintenance). All species increased ε by about 10 MPa during winter. Species with rigid tissue walls exhibited low leaf tissue damage at −20 °C. Our results suggest that osmotic adjustment was the main water relationship adaptation to cope with drought during summer and spring, particularly in deep-rooted plants, and that adjustments in cell wall rigidity during the winter helped to enhance freezing tolerance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Abrams MD (1988) Sources of variation in osmotic potentials with special reference to North American tree species. For Sci 34:1030–1046

    Google Scholar 

  • Abrams MD (1990) Adaptations and responses to drought in Quercus species of North America. Tree Physiol 7:227–238

    PubMed  Google Scholar 

  • Abrams MD, Menges ES (1992) Leaf ageing and plateau effect on seasonal pressure–volume relationships in three sclerophyllous Quercus species in south–eastern USA. Funct Ecol 6:353–360

    Google Scholar 

  • Ball MC, Wolfe J, Canny M, Hofmann M, Nicotra AB, Hughes D (2002) Space and time dependence of temperature and freezing in evergreen leaves. Funct Plant Biol 29:1259–1272

    Google Scholar 

  • Barradas VL, Ramos-Vázquez A, Orozco-Segovia A (2004) Stomatal conductance in a tropical xerophilous shrub land at a lava substratum. Int J Biomet 48:119–127

    Google Scholar 

  • Bowman WD, Roberts SW (1985) Seasonal and diurnal water relations adjustments in three chaparral shrubs. Ecology 66:738–742

    Google Scholar 

  • Boyer JS (1982) Plant productivity and environment. Science 218:443–448

    PubMed  CAS  Google Scholar 

  • Brodribb TJ, Holbrook NM (2004) Stomatal protection against hydraulic failure: a comparison of coexisting ferns and angiosperms. New Phytol 162:663–670

    Google Scholar 

  • Bucci SJ, Scholz FG, Goldstein G, Meinzer FC, Hinojosa JA, Hoffmann WA, Franco AC (2004) Processes preventing nocturnal equilibration between leaf and soil water potential in tropical savanna woody species. Tree Physiol 24:1119–1127

    PubMed  Google Scholar 

  • Bucci SJ, Goldstein G, Meinzer FC, Franco AC, Campanello P, Scholz FG (2005) Mechanisms contributing to seasonal homeostasis of minimum leaf water potential and predawn disequilibrium between soil and plants in Neotropical savanna trees. Trees 19:296–304

    Google Scholar 

  • Bucci SJ, Scholz FG, Goldstein G, Meinzer FC, Franco AC, Zhang Y, Hao G-Y (2008) Water relations and hydraulic architecture in Cerrado trees: adjustments to seasonal changes in water availability and evaporative demand. Braz J Plant Physiol 20:233–245

    Google Scholar 

  • Bucci SJ, Scholz FG, Goldstein G, Meinzer FC, Arce ME (2009) Soil water availability and rooting depth as determinants of hydraulic architecture of Patagonian woody species. Oecologia 160:631–641

    PubMed  Google Scholar 

  • Bucci SJ, Scholz FG, Iogna PA, Goldstein G (2011) Economía de agua de especies arbustivas de la Estepa Patagónica. Ecol Austral 21:43–60

    Google Scholar 

  • Callister A, Arndt S, Ades P, Merchant A, Rowell D, Adams M (2008) Leaf osmotic potential of Eucalyptus hybrids respond differently to freezing and drought, with little clonal variation. Tree Physiol 28:1297–1304

    PubMed  Google Scholar 

  • Campanella MV, Bertiller MB (2008) Plant phenology, leaf traits, and leaf litter fall of contrasting life forms in the arid Patagonian Monte, Argentina. J Veg Sci 19:75–78

    Google Scholar 

  • Cavender-Bares J (2005) Impacts of freezing on long distance transport in woody plants. In: Holbrook NM, Zweiniecki MA (eds) Vascular transport in plants. Elsevier, Boston, pp 401–424

    Google Scholar 

  • Corcuera L, Camarero JJ, Gil-Pelegrın E (2002) Functional groups in Quercus species derived from the analysis of pressure–volume curves. Trees 16:465–472

    Google Scholar 

  • Damascos MA, Barthelemy D, Ezcurra C, Martinez AP, Brion AC (2008) Plant phenology, shoot growth, and branching pattern in Mulinum spinosum (Apiaceae), a cushion shrub of the arid Patagonian steppe of Argentina. J Arid Environ 72:1977–1988

    Google Scholar 

  • Douglas DC, Bockheim JG (2006) Soil-forming rates and processes in Quaternary moraines near Lago Buenos Aires, Argentina. Quatern Res 65:293–307

    Google Scholar 

  • Durante M, Maseda PH, Fernández RJ (2011) Xylem efficiency vs. safety: acclimation to drought of seedling root anatomy for six Patagonian shrub species. J Arid Environ 75:397–402

    Google Scholar 

  • Evans RD, Black RA, Link SO (1990) Rehydration-induced changes in pressure–volume relationships of Artemisia tridentata Nutt. ssp. tridentata. Plant Cell Environ 13:455–461

    Google Scholar 

  • Fisher RA, Williams M, Do Vale RL, Da Costa AL, Meir P (2006) Evidence from Amazonian forests is consistent with isohydric control of leaf water potential. Plant Cell Environ 29:151–165

    PubMed  Google Scholar 

  • Franks PJ, Drake PL, Froend RH (2007) Aniso hydric but isohydrodynamic: seasonally constant plant water potential gradient explained by a stomatal control mechanism incorporating variable plant hydraulic conductance. Plant Cell Environ 30:19–30

    PubMed  Google Scholar 

  • Galmes J, Flexas J, Save R, Medrano H (2007) Water relations and stomatal characteristics of Mediterranean plants with different growth forms and leaf habits: responses to water stress and recovery. Plant Soil 290:139–155

    CAS  Google Scholar 

  • Goldstein G, Nobel PS (1991) Changes in osmotic pressure and mucilage during low-temperature acclimation of Opuntia ficus-indica. Plant Physiol 97:954–961

    PubMed  CAS  Google Scholar 

  • Golluscio RA, Oesterheld MR (2007) Water use efficiency of twenty-five co-existing Patagonian species growing under different soil water availability. Oecologia 154:207–217

    PubMed  CAS  Google Scholar 

  • Golluscio RA, Sigal Escalada V, Perez J (2009) Minimal plant responsiveness to summer water pulses: ecophysiological constraints of three species of semiarid Patagonia rangeland. Ecol Manag 62:171–178

    Google Scholar 

  • Graefe S, Leuschner Ch, Coners H, Hertel D (2011) Root functioning in tropical high-elevation forests: environmental vs. biological control of root water absorption. Environ Exp Bot 71:329–336

    Google Scholar 

  • Hao G-Y, Sack L, Wang A-Y, Cao K-F, Goldstein G (2010) Differentiation of leaf water flux and drought tolerance traits in hemiepiphytic and non-hemiepiphytic Ficus tree species. Funct Ecol 24:731–740

    Google Scholar 

  • Iogna PA, Bucci SJ, Scholz FG, Goldstein G (2011) Water relations and hydraulic architecture of two Patagonian steppe shrubs: effect of slope orientation and microclimate. J Arid Environ 75:763–772

    Google Scholar 

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

    Google Scholar 

  • Kosová K, Vitamvas P, Prasil IT (2007) The role of dehydrins in plant response to cold. Biol Plant 51:601–617

    Google Scholar 

  • Kowaljowa E, Fernández RJ (2011) Differential utilization of a shallow-water pulse by six shrub species in the Patagonian steppe. J Arid Environ 75(2):211–214

    Google Scholar 

  • Kubiske ME, Abrams MD (1994) Ecophysiological analysis of temperate woody species on contrasting sites during wet and dry years. Oecologia 98:303–312

    Google Scholar 

  • Levitt J (1980) Responses of plants to environmental stresses, Vol 1, 2nd edn. Academic, New York

  • Loik ME, Nobel PS (1991) Water relations and mucopolysaccharide increases for a winter hardy cactus during acclimation to subzero temperatures. Oecologia 88:340–346

    Google Scholar 

  • Meinzer FC, Rundel PW, Shari MR, Nilsen ET (1986) Turgor and osmotic relations of the desert shrub Larrea tridentata. Plant Cell Environ 9:467–475

    Google Scholar 

  • Mitchell PJ, Veneklaas EJ, Lambers H, Burgess SO (2008) Leaf water relations during summer water deficit: differential responses in turgor maintenance and variation in leaf structure among different plant communities in south–western Australia. Plant Cell Environ 31:1791–1802

    PubMed  Google Scholar 

  • Myers B, Landsberg J (1989) Water stress and seedling growth of eucalyptus species from contrasting habitats. Tree Physiol 5:207–208

    PubMed  Google Scholar 

  • Ngugi M, Doley D, Hunt A, Dart P, Ryan P (2003) Leaf water relations of Eucalyptus cloeziana and Eucalyptus argophloia in response of water deficit. Tree Physiol 23:335–343

    PubMed  Google Scholar 

  • Nilsen ET (1991) The relationships between freezing tolerance and thermotropic leaf movement in five Rhododendron species. Oecologia 87:63–71

    Google Scholar 

  • Paruelo JM, Aguiar MR, Golluscio RA (1988) Soil water availability in the Patagonian arid steppe: gravel content effect. Arid Soil Res Rehabil 7:67–74

    Google Scholar 

  • Patakas A, Noitsakis B (1997) Cell wall elasticity as a mechanism to maintain favorable water relations during leaf ontogeny in grapevines. Am J Enol Vitic 48:352–358

    Google Scholar 

  • Rajashekar CB, Burke MJ (1996) Freezing characteristics of rigid plant tissues. Plant Physiol 111:597–603

    PubMed  CAS  Google Scholar 

  • Sala OE, Golluscio RA, Lauenroth WK, Soriano A (1989) Resource partitioning between shrubs and grasses in the Patagonian steppe. Oecologia 81:501–505

    Google Scholar 

  • Solecka D, Zebrowski J, Kacperska A (2008) Are pectins involved in cold acclimation and de-acclimation of winter oil-seed rape plants? Ann Bot (Lond) 101:521–530

    CAS  Google Scholar 

  • Stefanowska M, Kuras M, Kubacka-zebalska M, Kacperska A (1999) Low temperature affects pattern of leaf growth and structure of cell walls in winter oilseed rape (Brassica napus L., var. oleifera L.). Ann Bot 84:313–319

    Google Scholar 

  • Thomas H, James AR (1993) Freezing tolerance and solute changes in contrasting genotypes of Lolium perenne L. acclimated to cold and drought. Ann Bot 72:249–254

    CAS  Google Scholar 

  • Turner NC, Jones MN (1980) Turgor maintenance by osmotic adjustment: a review and evaluation. In: Turner NC, Kramer PJ (eds) Adaptation of plants to water and high temperature stress. Wiley, New York, pp 84–104

    Google Scholar 

  • Tyree MT, Jarvis PG (1982) Water in tissues and cells, vol 12. Springer, Berlin

    Google Scholar 

  • Tyree MT, Cheung YNS, McGregor ME, Talbot AJB (1978) The characteristic of seasonal and ontogenic changes in the tissue-water relations of Acer, Populus, Tsuga and Picea. Can J Bot 56:635–647

    Google Scholar 

  • Weiser RL, Wallner SJ, Waddell JW (1990) Cell wall and extensin mRNA changes during cold acclimation of pea seedlings. Plant Physiol 93:1021–1026

    Google Scholar 

  • White DA, Beadle CL, Worledge D (1996) Leaf water relations of Eucalyptus globulus ssp. globulus and E. nitens: seasonal, drought and species effects. Tree Physiol 16:469–476

    PubMed  Google Scholar 

  • Wilner J (1960) Relative and absolute electrolytic conductance tests for frost hardiness of apple varieties. Can J Plant Sci 40:630–637

    Google Scholar 

  • Wisniewski M, Davis G, Schaffer K (1991) Mediation of deep supercooling of peach and dogwood by enzymatic modifications in cell-wall structure. Planta 184:254–260

    CAS  Google Scholar 

  • Xin Z, Browse J (2000) Cold comfort farm: the acclimation of plants to freezing temperatures. Plant Cell Environ 23:893–902

    Google Scholar 

  • Yamada T, Kuroda K, Jitsuyama Y, Takezawa D, Arakawa K, Fujikawa S (2002) Roles of the plasma membrane and the cell wall in the responses of plant cells to freezing. Planta 215:770–778

    PubMed  CAS  Google Scholar 

Download references

Acknowledgment

This study was supported by CONICET grant (PIP 112-200801-01703). This work complies with Argentinean Law.

Conflict of interest

The authors have no conflict of interest.

Author information

Authors and Affiliations

  1. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina

    Fabian G. Scholz, Sandra J. Bucci, Nadia Arias & Guillermo Goldstein

  2. Grupo de Estudios Biofísicos y Eco-fisiológicos (GEBEF), Departamento de Biología, Facultad de Ciencias Naturales, Universidad Nacional de la Patagonia San Juan Bosco, Comodoro Rivadavia, Argentina

    Fabian G. Scholz, Sandra J. Bucci & Nadia Arias

  3. USDA Forest Service, Forestry Sciences Laboratory, 3200 SW Jefferson Way, Corvallis, OR, 97331, USA

    Frederick C. Meinzer

  4. Laboratorio de Ecología Funcional (LEF), Departamento de Ecología, Genética y Evolución, FCEyN, Universidad de Buenos Aires, Buenos Aires, Argentina

    Guillermo Goldstein

  5. Department of Biology, University of Miami, P.O. Box 249118, Coral Gables, FL, USA

    Guillermo Goldstein

Authors
  1. Fabian G. Scholz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sandra J. Bucci
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nadia Arias
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Frederick C. Meinzer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Guillermo Goldstein
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fabian G. Scholz.

Additional information

Communicated by Allan Green.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Scholz, F.G., Bucci, S.J., Arias, N. et al. Osmotic and elastic adjustments in cold desert shrubs differing in rooting depth: coping with drought and subzero temperatures. Oecologia 170, 885–897 (2012). https://doi.org/10.1007/s00442-012-2368-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-012-2368-y

Keywords

Search

Navigation