Plant and Soil

, Volume 360, Issue 1–2, pp 175–185 | Cite as

N uptake and growth responses to sub-lethal freezing in the grass Poa pratensis L.

  • Andrey V. Malyshev
  • Hugh A. L. HenryEmail author
Regular Article


Background and aims

Climate warming has the potential to increase both the exposure and vulnerability of grass roots to frost in temperate regions by reducing snow cover and altering the timing of cold acclimation. Despite a strong research focus on the direct effects of freezing on grass mortality, the direct sub-lethal effects of freezing on grass performance have not been well-characterized. We examined sub-lethal responses of the grass Poa pratensis to variation in the timing, severity, rate and length of freezing.


We assessed short term root functional responses (15N uptake) and longer term plant growth responses to freezing administered both under controlled conditions in a refrigerated incubator, and in the field by manipulating snow and litter cover.


In fall and spring, 15N uptake declined in response to 1 day of freezing down to −10 °C or to 3 days of freezing at −5 °C, whereas in winter, 15N uptake was insensitive to freezing. Long term growth responses were similar, with reduced growth only occurring for grasses frozen for 3 days at −5 °C in spring, but not for grasses frozen in fall or winter. Snow and litter removal intensified soil freezing over winter, but did not significantly affect plant growth.


Our results demonstrate that while P. pratensis is relatively tolerant to frost damage over winter, it may be vulnerable to sub-lethal frost effects in fall, and particularly in spring. These sub-lethal effects occur at temperatures approximately 15–20 °C warmer than the published LT50 values for this species.


Cold acclimation Grass 15N uptake Root Winter 



This research was supported by a Natural Sciences and Engineering Research Council of Canada Discovery Grant to HALH and an Ontario Graduate Scholarship to AVM.


  1. Andresen LC, Michelsen A (2005) Off-season uptake of nitrogen in temperate heath vegetation. Oecologia 144:585–597PubMedCrossRefGoogle Scholar
  2. Belanger G, Rochette P, Castonguay Y, Bootsma A, Mongrain D, Ryan DAJ (2002) Climate change and winter survival of perennial forage crops in eastern Canada. Agron J 94:1120–1130CrossRefGoogle Scholar
  3. Bigras FJ, Dumais D (2005) Root-freezing damage in the containerized nursery: impact on plantation sites—a review. New For 30:167–184CrossRefGoogle Scholar
  4. Bilbrough CJ, Welker JM, Bowman WD (2000) Early spring nitrogen uptake by snow-covered plants: a comparison of arctic and alpine plant function under the snowpack. Arct Antarct Alp Res 32:404–411CrossRefGoogle Scholar
  5. Bokhorst S, Bjerke JW, Street LE, Callaghan TV, Phoenix GK (2011) Impacts of multiple extreme winter warming events on sub-Arctic heathland: phenology, reproduction, growth, and CO2 flux responses. Global Change Biol 17:2817–2830CrossRefGoogle Scholar
  6. Campbell JL, Mitchell MJ, Groffman PM, Christenson LM, Hardy JP (2005) Winter in northeastern North America: a critical period for ecological processes. Front Ecol Environ 3:314–322CrossRefGoogle Scholar
  7. Dionne J, Castonguay Y, Nadeau P, Desjardins Y (2001) Freezing tolerance and carbohydrate changes during cold acclimation of green-type annual bluegrass (Poa annua L.) ecotypes. Crop Sci 41:443–451CrossRefGoogle Scholar
  8. Eagles CF, Williams J, Louis DV (1993) Recovery after freezing in Avena sativa L., Lolium perenne L. and L. multiflorum Lam. New Phytol 123:477–483Google Scholar
  9. Elliott AC, Henry HAL (2009) Freeze-thaw cycle amplitude and freezing rate effects on extractable nitrogen in a temperate old field soil. Biol Fertil Soils 45:469–476CrossRefGoogle Scholar
  10. Engels C, Marschner H (1992) Root to shoot translocation of macronutiens in relation to shoot demand in maize (Zea mays L.) grown at different root zone temperatures. J Plant Nutr Soil Sci 155:121–128CrossRefGoogle Scholar
  11. Epstein E, Schmid WE, Rains DW (1963) Significance and technique of short-term experiments on solute absorption by plant tissue. Plant Cell Physiol 4:79–84Google Scholar
  12. Finkle BJ, Pereira ESB, Brown MS (1974) Freezing of non-woody plant tissues; effect of rate of cooling on damage to frozen beet root sections. Plant Physiol 53:705–708PubMedCrossRefGoogle Scholar
  13. Gaul D, Hertel D, Leuschner C (2008) Effects of experimental soil frost on the fine-root system of mature Norway spruce. J Plant Nutr Soil Sci 171:690–698CrossRefGoogle Scholar
  14. Groffman PM, Driscoll CT, Fahey TJ, Hardy JP, Fitzhugh RD, Tierney GL (2001) Colder soils in a warmer world: a snow manipulation study in a northern hardwood forest ecosystem. Biogeochemistry 56:135–150CrossRefGoogle Scholar
  15. Grogan P, Michelsen A, Ambus P, Jonasson S (2004) Freeze-thaw regime effects on carbon and nitrogen dynamics in sub-arctic heath tundra mesocosms. Soil Biol Biochem 36:641–654CrossRefGoogle Scholar
  16. Gu L, Hanson PJ, MacPost W, Kaiser DP, Yang B, Nemani R, Pallardy SG, Meyers T (2008) The 2007 eastern US spring freezes: increased cold damage in a warming world? Bioscience 58:253–262CrossRefGoogle Scholar
  17. Gudleifsson BE, Andrews CJ, Bjornsson H (1986) Cold hardiness and ice tolerance of pasture grasses grown and tested in controlled environments. Can J Plant Sci 66:601–608Google Scholar
  18. Hänninen H (1991) Does climatic warming increase the risk of frost damage in northern trees. Plant Cell Environ 14:449–454CrossRefGoogle Scholar
  19. Hanslin HM, Hoglind M (2009) Differences in winter-hardening between phenotypes of Lolium perenne with contrasting water-soluble carbohydrate concentrations. Grass Forage Sci 64:187–195CrossRefGoogle Scholar
  20. Henry HAL (2007) Soil freeze-thaw cycle experiments: trends, methodological weaknesses and suggested improvements. Soil Biol Biochem 39:977–986CrossRefGoogle Scholar
  21. Henry HAL (2008) Climate change and soil freezing dynamics: historical trends and projected changes. Clim Change 87:421–434CrossRefGoogle Scholar
  22. Hulke BS, Watkins E, Wyse DL, Ehlke NJ (2008) Freezing tolerance of selected perennial ryegrass (Lolium perenne L.) accessions and its association with field winterhardiness and turf traits. Euphytica 163:131–141CrossRefGoogle Scholar
  23. Hutchison JS, Henry HAL (2010) Additive effects of warming and increased nitrogen deposition in a temperate old field: plant productivity and the importance of winter. Ecosystems 13:661–672CrossRefGoogle Scholar
  24. IPCC (2007) Climate change 2007: the physical science basis. contribution of working group I to the fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, p 940Google Scholar
  25. Jacobsen SE, Monteros C, Christiansen JL, Bravo LA, Corcuera LJ, Mujica A (2005) Plant responses of quinoa (Chenopodium quinoa Willd.) to frost at various phenological stages. Eur J Agron 22:131–139CrossRefGoogle Scholar
  26. 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
  27. Kreyling J (2010) Winter climate change: a critical factor for temperate vegetation performance. Ecology 91:1939–1948PubMedCrossRefGoogle Scholar
  28. Kreyling J, Beierkuhnlein C, Pritsch K, Schloter M, Jentsch A (2008) Recurrent soil freeze-thaw cycles enhance grassland productivity. New Phytol 177:938–945PubMedCrossRefGoogle Scholar
  29. Laine P, Bigot J, Ourry A, Boucaud J (1994) Effects of low temperature on nitrate uptake, and xylem and phloem flows of nitrogen, in Secale cereale L. and Brassica napus L. New Phytol 127:675–683CrossRefGoogle Scholar
  30. Livingston DP, Tallury SP (2009) Freezing in non-acclimated oats. II: thermal response and histology of recovery in gradual and rapidly frozen plants. Thermochim Acta 481:20–27CrossRefGoogle Scholar
  31. Lloyd DT, Soldat DJ, Stier JC (2011) Low-temperature nitrogen uptake and use of three cool-season turfgrasses under controlled environments. Hortscience 46:1545–1549Google Scholar
  32. Man RZ, Kayahara GJ, Dang QL, Rice JA (2009) A case of severe frost damage prior to budbreak in young conifers in Northeastern Ontario: consequence of climate change? For Chron 85:453–462Google Scholar
  33. Meehl GA, Karl T, Easterling DR, Changnon S, Pielke R, Changnon D, Evans J, Groisman PY, Knutson TR, Kunkel KE, Mearns LO, Parmesan C, Pulwarty R, Root T, Sylves RT, Whetton P, Zwiers F (2000) An introduction to trends in extreme weather and climate events: observations, socioeconomic impacts, terrestrial ecological impacts, and model projections. Bull Am Meteorol Soc 81:413–416CrossRefGoogle Scholar
  34. Miltner ED, Stahnke GK, Johnston WJ, Golob CT (2004) Late fall and winter nitrogen fertilization of turfgrass in two pacific northwest climates. Hortscience 39:1745–1749Google Scholar
  35. Ostrem L, Rapacz M, Jorgensen M, Hoglind M (2010) Impact of frost and plant age on compensatory growth in timothy and perennial ryegrass during winter. Grass Forage Sci 65:15–22CrossRefGoogle Scholar
  36. Ouellet CE (1976) Winter hardiness and survival of forage crops in Canada. Can J Plant Sci 56:679–689CrossRefGoogle Scholar
  37. Pilon CE, Cote B, Fyles JW (1994) Effect of snow removal on leaf water potential, soil moisture, leaf and soil nutrient status and leaf peroxidase activity of sugar maple. Plant Soil 162:81–88CrossRefGoogle Scholar
  38. Rapacz M (2002) Cold-deacclimation of oilseed rape (Brassica napus var. oleifera) in response to fluctuating temperatures and photoperiod. Ann Bot 89:543–549PubMedCrossRefGoogle Scholar
  39. Repo T, Ryyppo A (2008) The electrolyte leakage method can be misleading for assessing the frost hardiness of roots. Plant Biosyst 142:298–301CrossRefGoogle Scholar
  40. Rigby JR, Porporato A (2008) Spring frost risk in a changing climate. Geophys Res Lett 35:L12703CrossRefGoogle Scholar
  41. Robitaille G, Boutin R, Lachance D (1995) Effects of soil freezing stress on sap flow and sugar content of mature sugar maples (Acer saccharum). Can J For Res 25:577–587CrossRefGoogle Scholar
  42. Sandve SR, Kosmala A, Rudi H, Fjellheim S, Rapacz M, Yamada T, Rognli OA (2011) Molecular mechanisms underlying frost tolerance in perennial grasses adapted to cold climates. Plant Sci 180:69–77PubMedCrossRefGoogle Scholar
  43. Schaberg PG, Hennon PE, D’Amore DV, Hawley GJ (2008) Influence of simulated snow cover on the cold tolerance and freezing injury of yellow-cedar seedlings. Global Change Biol 14:1282–1293CrossRefGoogle Scholar
  44. Souther S, McGraw JB (2011) Vulnerability of wild American ginseng to an extreme early spring temperature fluctuation. Popul Ecol 53:119–129CrossRefGoogle Scholar
  45. Taulavuori K, Laine K, Taulavuori E, Pakonen T, Saari E (1997) Accelerated dehardening in bilberry (Vaccinium myrtillus L.) induced by a small elevation in air temperature. Environ Pollut 98:91–95PubMedCrossRefGoogle Scholar
  46. Taulavuori KMJ, Taulavuori EB, Skre O, Nilsen J, Igeland B, Laine KM (2004) Dehardening of mountain birch (Betula pubescens ssp czerepanovii) ecotypes at elevated winter temperatures. New Phytol 162:427–436CrossRefGoogle Scholar
  47. Thorsen SM, Hoglind M (2010a) Assessing winter survival of forage grasses in Norway under future climate scenarios by simulating potential frost tolerance in combination with simple agroclimatic indices. Agric For Meteorol 150:1272–1282CrossRefGoogle Scholar
  48. Thorsen SM, Hoglind M (2010b) Modelling cold hardening and dehardening in timothy. Sensitivity analysis and Bayesian model comparison. Agric For Meteorol 150:1529–1542CrossRefGoogle Scholar
  49. Tierney GL, Fahey TJ, Groffman PM, Hardy JP, Fitzhugh RD, Driscoll CT (2001) Soil freezing alters fine root dynamics in a northern hardwood forest. Biogeochemistry 56:175–190CrossRefGoogle Scholar
  50. Viti R, Bartolini S, Andreini L (2010) Flower bud frost tolerance of several Italian apricot genotypes. Eur J Hortic Sci 75:185–192Google Scholar
  51. Walsh JE, Anisimov O, Hagen JO, Jakobsson T, Oerelemans J, Prowse T, Romanovsky VE, Savelieva NI, Serreze M, Shiklomanov A, Shiklomanov I, Solomon S (2005) Cryosphere and hydrology. In: Symon C, Arris L, Heal B (eds) Arctic climate impact assessment. Cambridge University Press, Cambridge, pp 183–242Google Scholar
  52. Weih M, Karlsson PS (2002) Low winter soil temperature affects summertime nutrient uptake capacity and growth rate of mountain birch seedlings in the subarctic, Swedish Lapland. Arct Antarct Alp Res 34:434–439CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Department of BiologyUniversity of Western OntarioLondonCanada

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