Advertisement

Life at 0 °C: the biology of the alpine snowbed plant Soldanella pusilla

Abstract

All plant species reach a low temperature range limit when either low temperature extremes exceed their freezing tolerance or when their metabolism becomes too restricted. In this study, we explore the ultimate thermal limit of plant tissue formation exemplified by a plant species that seemingly grows through snow. By a combination of studies in alpine snowbeds and under controlled environmental conditions, we demonstrate and quantify that the clonal herb Soldanella pusilla (Primulaceae) does indeed grow its entire flowering shoot at 0 °C. We show that plants resume growth under 2–3 m of snow in mid-winter, following an internal clock, with the remaining period under snow until snow melt (mostly in July) sufficient to produce a flowering shoot that is ready for pollination. When snow pack gets thin, the flowering shoot intercepts and re-radiates long-wave solar radiation, so that snow and ice gently melt around the fragile shoot and the flowers emerge without any mechanical interaction. We evidence bud preformation in the previous season and enormous non-structural carbohydrate reserves in tissues (mainly below ground) in the form of soluble sugars (largely stachyose) that would support basic metabolism for more than 2 entire years under snow. However, cell-wall formation at 0 °C appears to lack unknown strengthening factors, including lignification (assessed by confocal Raman spectroscopy imaging) that require between a few hours or a day of warmth after snow melt to complete tissue strengthening. Complemented with a suite of anatomical data, the work opens a window towards understanding low temperature limits of plant growth in general, with potential relevance for winter crops and trees at the natural climatic treeline.

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

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

References

  1. Abdrakhamanova A, Wang QY, Khokhlova L, Nick P (2003) Is microtubule disassembly a trigger for cold acclimation? Plant Cell Phys 44:676–686

  2. Alvarez-Uria P, Körner C (2007) Low temperature limits of root growth in deciduous and evergreen temperate tree species. Funct Ecol 21:211–218

  3. Benkeblia N, Ueno K, Onodera S, Shiomi N (2005) Variation of fructooligosaccharides and their metabolizing enzymes in onion bulb (Allium cepa L. cv. Tenshin) during long-term storage. J Food Sci 70:208–214

  4. Billings WD, Bliss LC (1959) An alpine snowbank environment and its effects on vegetation, plant development, and productivity. Ecology 40:388–397

  5. Billings WD, Shaver GR, Trent AW (1976) Measurement of root growth in simulated and natural temperature gradients over permafrost. Arctic Alp Res 8:247–250

  6. Chope GA, Cools K, Hammond JP, Thompson AJ, Terry LA (2012) Physiological, biochemical and transcriptional analysis of onion bulbs during storage. Ann Bot 109:819–831

  7. De Witte LC, Armbruster GFJ, Gielly L, Taberlet P, Stocklin J (2012) AFLP markers reveal high clonal diversity and extreme longevity in four key arctic-alpine species. Mol Ecol 21:1081–1097

  8. Dey PM, Haborne JB (1997) Plant biochemistry. Academic Press, London, p 554

  9. Donaldson LA (2001) Lignification and lignin topochemistry—an ultrastructural view. Phytochemistry 57:859–873

  10. Fenner M (1985) Seed ecology. Chapman and Hall, London

  11. Ferreira BG, Falcioni R, Guedes LM, Avritzer SC, Antunes WC, Souza LA, Isaias MS (2017) Preventing false negatives for histochemical detection of phenolics and lignines in PEG-embedded plant tissues. J Histochem Cytochem 65:105–116

  12. Gierlinger N, Keplinger T, Harrington M (2012) Imaging of plant cell walls by confocal Raman microscopy. Nat Protoc 7:1694–1708

  13. Green K, Pickering C (2009) Vegetation, microclimate and soils associated with the latest-lying snowpatches in Australia. Plant Ecol Divers 2:289–300

  14. Grime JP, Mowforth MA (1982) Variation in genome size—an ecological interpretation. Nature 299:151–153

  15. Hartmann H (1957) Studien über die vegetative Fortpflanzung in den Hochalpen. Jahresber Naturf Ges Graubündens 86:3–168

  16. Hoch G, Popp M, Körner C (2002) Altitudinal increase of mobile carbon pools in Pinus cembra suggests sink limitation of growth at the Swiss treeline. Oikos 98:361–374

  17. Inauen N, Körner C, Hiltbrunner E (2012) No growth stimulation by CO2 enrichment in alpine glacier forefield plants. Glob Change Biol 18:985–999

  18. Inoue K, Araki T, Endo M (2018) Circadian clock during plant development. J Plant Res 131:59–66

  19. Körner C (2003) Alpine plant life, 2nd edn. Springer, Berlin

  20. Körner C (2006) Significance of temperature in plant life. In: Morison JIL, Morecroft MD (eds) Plant growth and climate change. Blackwell Publishing Ltd, Oxford, pp 48–69

  21. Körner C (2008) Winter crop growth at low temperature may hold the answer for alpine treeline formation. Plant Ecol Divers 1:3–11

  22. Körner C (2011) Coldest places on earth with angiosperm plant life. Alp Bot 121:11–22

  23. Körner C, Diemer M (1987) In situ photosynthetic responses to light, temperature and carbon dioxide in herbaceous plants from low and high altitude. Funct Ecol 1:179–194

  24. Körner C, Hiltbrunner E (2018) The 90 ways to describe plant temperature. Persp Plant Ecol Evol Syst 30:16–21

  25. Körner C, Pelaez Menendez-Riedl S (1989) The significance of developmental aspects in plant growth analysis. In: Lambers H, Cambridge ML, Konings H, Pons TL (eds) Causes and consequences of variation in growth rate and productivity of higher plants. SPB Acad Publ, The Hague, pp 141–157

  26. Körner C, Woodward FI (1987) The dynamics of leaf extension in plants with diverse altitudinal ranges. 2. Field studies in Poa species between 600 and 3200 m altitude. Oecologia 72:279–283

  27. Körner C, Leuzinger S, Riedl S, Siegwolf RT, Streule L (2016) Carbon and nitrogen stable isotope signals for an entire alpine flora, based on herbarium samples. Alp Bot 126:153–166

  28. Ladinig U, Hacker J, Neuner G, Wagner J (2013) How endangered is sexual reproduction of high-mountain plants by summer frosts? Frost resistance, frequency of frost events and risk assessment. Oecologia 171:743–760

  29. Larcher W, Kainmüller C, Wagner J (2010) Survival types of high mountain plants under extreme temperatures. Flora 205:3–18

  30. Larigauderie A, Körner C (1995) Acclimation of leaf dark respiration to temperature in alpine and lowland plant species. Ann Bot 76:245–252

  31. Li X, Rossi S, Liang E, Camarero JJ (2016) Temperature thresholds for the onset of xylogenesis in alpine shrubs on the Tibetan Plateau. Trees 30:2091–2099

  32. Ligrone R, Carafa A, Duckett JG, Renzaglia KS, Ruel K (2008) Immunocytochemical detection of lignin-related epitopes in cell walls in bryophytes and the charalean alga Nitella. Plant Syst Evol 270:257–272

  33. Lovejoy C, Vincent WF, Bonilla S, Roy S, Martineau M-J, Terrado R, Potvin M, Massana R, Pedros-Alio C (2007) Distribution, phylogeny, and growth of cold adapted Picoprasinophytes in Arctic seas. J Phycol 43:78–89

  34. Luterbacher J, Pfister C (2015) The year without a summer. Nat Geosci 8:246–248

  35. Merchant A, Richter A, Popp M, Adams M (2006) Targeted metabolite profiling provides a functional link among eucalypt taxonomy, physiology and evolution. Phytochemistry 67:402–408

  36. Molau U (1993) Relationships between flowering phenology and life history strategies in tundra plants. Arctic Alp Res 25:391–402

  37. Müller T, Leya T, Fuhr G (2001) Persistent snow algal fields in Spitsbergen: field observations and a hypothesis about the annual cell circulation. Arct Antarct Alp Res 33:42–51

  38. Nagelmüller S, Hiltbrunner E, Körner C (2016) Critically low soil temperatures for root growth and root morphology in three alpine plant species. Alpine Bot 126:11–21

  39. Nagelmüller S, Hiltbrunner E, Körner C (2017) Low temperature limits for root growth in alpine species are set by cell differentiation. AoB Plants 9:plx054. https://doi.org/10.1093/aobpla/plx054

  40. Onipchenko VG, Makarov MI, van Logtestijn RSP, Ivanov VB, Akhmetzhanova AA, Tekeev DK, Ermak AA, Salpagarova FS, Kozhevnikova AD, Cornelissen JHC (2009) New nitrogen uptake strategy: specialized snow roots. Ecol Lett 12:758–764

  41. Onipchenko VG, Kipkeev AM, Makarov MI, Kozhevnikova AD, Ivanov VB, Soudzilovskaia NA, Tekeev DK, Salpagarova FS, Werger MJA, Cornelissen JHC (2014) Digging deep to open the white black box of snow root phenology. Ecol Res 29:529–534

  42. Penfield S (2008) Temperature perception and signal transduction in plants. New Phytol 179:615–628

  43. Pesquet E, Zhang B, Gorzsas A, Puhakainen T, Serk H, Escamez S, Barbier O, Gerber L, Courtois-Moreau C, Alatalo E, Paulin L, Kangasjarvi J, Sundberg B, Goffner D, Tuominen H (2013) Non-cell-autonomous postmortem lignification of tracheary elements in Zinnia elegans. Plant Cell 25:1314–1328

  44. Plohovska SG, Yemets AI, Blume YB (2016) Influence of cold on organization of actin filaments of different types of root cells in Arabidopsis thaliana. Cytol Genet 50:318–323

  45. Quentin AG, Pinkard EA, Ryan MG, Tissue DT et al (2015) Non-structural carbohydrates in woody plants compared among laboratories. Tree Physiol 35:1146–1165

  46. Richardson SG, Salisbury FB (1977) Plant responses to the light penetrating snow. Ecology 58:1152–1158

  47. Schäppi B, Körner C (1996) Growth responses of an alpine grassland to elevated CO2. Oecologia 105:43–52

  48. Schenker G, Lenz A, Körner C, Hoch G (2014) Physiological minimum temperatures for root growth in seven common European broad-leaved tree species. Tree Physiol 34:302–313

  49. Scherrer D, Körner C (2009) Infra-red thermometry of alpine landscapes challenges climatic warming projections. Glob Change Biol 16:2602–2613

  50. Scherrer D, Körner C (2011) Topographically controlled thermal-habitat differentiation buffers alpine plant diversity against climate warming. J Biogeogr 38:406–416

  51. Steffen S, Kadereit JW (2014) Parallel evolution of flower reduction in two alpine Soldanella species (Primulaceae). Bot J Linn Soc 175:409–422

  52. Steinacher G, Wagner J (2012) Effect of temperature on the progamic phase in high-mountain plants. Plant Biol 14:295–305

  53. Steinacher G, Wagner J (2013) The progamic phase in high-mountain plants: from pollination to fertilization in the cold. Plants 2:354–370

  54. Wright JC (2001) Cryptobiosis 300 years on from van Leuwenhoek: what have we learned about tardigrades? Zool Anzeig/J Comp Zool 240:563–582

  55. Yang Y, Siegwolf RTW, Körner C (2015) Species specific and environment induced variation of δ13C and δ15N in alpine plants. Front Plant Sci 6:Article 423

  56. YouTube (2019) Movie: ‘Pollination of Soldanella’. https://www.youtube.com/watch?v=deEbgFkMVoE&feature=youtu.be

  57. Zhang L-B, Kadereit JW (2003) The systematics of Soldanella (Primulaceae) based on morphological and molecular (ITS, AFLPs) evidence. Nord J Bot 22:129–169

Download references

Acknowledgements

We thank Sandra Schmid for carbohydrate (NSC) analysis in the lab, Patrick Möhl and Sven Trecco for field assistance and Rolf Siegwolf (PSI, Brugg, Switzerland) for mass-spectrometer data. The Alpine Research and Education Station (ALPFOR) on Furka Pass provided the essential local infrastructure.

Author information

CK designed the study, conducted the field- and phytotron-work, and wrote the manuscript. EH helped with field work, provided macro-photographs, and contributed to the manuscript. SR conducted the light microscopy work and contributed the artwork. TK provided Raman spectroscopy scans, which would not have been possible unless FS managed to obtain microtome cuts of unembedded stem tissue and he verified lignification histochemically. AR and JW provided chromatography data for Table 3.

Correspondence to Christian Körner.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

The work for this paper meets all ethical standards.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 46052 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Körner, C., Riedl, S., Keplinger, T. et al. Life at 0 °C: the biology of the alpine snowbed plant Soldanella pusilla. Alp Botany 129, 63–80 (2019) doi:10.1007/s00035-019-00220-8

Download citation

Keywords

  • Anatomy
  • Development
  • Growth
  • Low temperature
  • Non-structural carbohydrates
  • Phenology
  • Tissue formation