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Mechanisms of frost resistance in Arabidopsis thaliana

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Abstract

Main conclusion

Freezing resistance strategies vary in Arabidopsis depending on origin. Southern accessions may avoid or tolerate freezing, while northern ones are always tolerant and reduce the proportion of freezable tissue water during acclimation.

Survival of sub-zero temperatures can be achieved by either avoiding or tolerating extracellular ice formation. Conflicting evidence has been presented showing that detached leaves of Arabidopsis thaliana are either freeze avoiding or tolerant. Here, we used three different natural Arabidopsis accessions from different habitats to investigate the frost resistance strategy of whole plants in soil. Plants were cooled to fixed temperatures or just held at their individual ice nucleation temperature for different time intervals. Tissue damage of whole plants was compared to the standard lethal temperature determined for detached leaves with external ice nucleation. While all detached leaves survived freezing when ice nucleation was externally initiated at mild sub-zero temperatures, whole plants of the southern accession behaved as freeze avoiding in the non-acclimated state. The northern accessions and all cold acclimated plants were freezing tolerant, but the duration of the freezing event affected tissue damage. Because this pointed to cell dehydration as mechanism of damage, the proportion of freezable water in leaves and osmolality of cell sap was determined. Indeed, the freezing tolerant accession Rsch had a lower proportion of freezable water and higher cell sap osmolality compared to the sensitive accession C24 in the cold acclimated state.

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Abbreviations

AC:

Cold acclimated

INT:

Ice nucleation temperature

LT50 :

Lethal temperature for 50%

NA:

Non-acclimated

References

  • Arias NS, Bucci SJ, Scholz FG, Goldstein G (2015) Freezing avoidance by super-cooling in Olea europaea cultivars: the role of apoplastic water, solute content and cell wall rigidity. Plant, Cell Environ 38:2061–2070

    Article  CAS  Google Scholar 

  • Armstrong JJ, Takebayashi N, Sformo T, Wolf DE (2015) Cold tolerance in Arabidopsis kamchatica. Am J Bot 102:439–448

    Article  PubMed  Google Scholar 

  • Block W (2002) Interactions of water, ice nucleators and desiccation in invertebrate cold survival. Eur J Entomol 99:259–266

    Article  Google Scholar 

  • Burke MJ, Gusta LV, Quamme HA, Weiser CJ, Li PH (1976) Freezing and injury in plants. Annu Rev Plant Physiol 27:507–528

    Article  Google Scholar 

  • Costanzo JP, do Amaral MCF, Rosendale AJ, Lee RE (2013) Hibernation physiology, freezing adaptation and extreme freeze tolerance in a northern population of the wood frog. J Exp Biol 216:3461–3473

    Article  CAS  PubMed  Google Scholar 

  • Crowe J, Oliver A, Hoekstra F, Crowe L (1997) Stabilization of dry membranes by mixtures of hydroxyethyl starch and glucose—the role of vitrification. Cryobiology 35:20–30

    Article  CAS  PubMed  Google Scholar 

  • de Mendiburu F (2016) agricolae: Statistical procedures for agricultural research. R package version 1.2-4. https://CRAN.R-project.org/package=agricolae

  • Des Marais DL, McKay JK, Richards JH, Sen S, Wayne T, Juenger TE (2012) Physiological genomics of response to soil drying in diverse Arabidopsis accessions. Plant Cell 24:893–914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldstein G, Rada F, Azocar A (1985) Cold hardiness and supercooling along an altitudinal gradient in andean giant rosette species. Oecologia 68:147–152

    Article  CAS  PubMed  Google Scholar 

  • Gusta LV, Wisniewski M (2013) Understanding plant cold hardiness: an opinion. Physiol Plant 147:4–14

    Article  CAS  PubMed  Google Scholar 

  • Gusta L, Wisniewski M, Nesbitt N, Gusta M (2004) The effect of water, sugars, and proteins on the pattern of ice nucleation and propagation in acclimated and nonacclimated canola leaves. Plant Physiol 135:1642–1653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hacker J, Neuner G (2008) Ice propagation in dehardened alpine plant species studied by infrared differential thermal analysis (IDTA). Arc Antarct Alp Res 40:660–670

    Article  Google Scholar 

  • Hacker J, Ladinig U, Wagner J, Neuner G (2011) Inflorescences of alpine cushion plants freeze autonomously and may survive subzero temperatures by supercooling. Plant Sci 180:149–156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hincha D, Zuther E, Hellwege E, Heyer A (2002) Specific effects of fructo- and gluco-oligosaccharides in the preservation of liposomes during drying. Glycobiology 12:103–110

    Article  CAS  PubMed  Google Scholar 

  • Hoermiller II, Naegele T, Augustin H, Stutz S, Weckwerth W, Heyer AG (2016) Subcellular reprogramming of metabolism during cold acclimation in Arabidopsis thaliana. Plant Cell Environ 40:602–610

    Article  CAS  PubMed  Google Scholar 

  • Jacobsen AL, Pratt RB, Ewers FW, Davis SD (2007) Cavitation resistance among 26 chaparral species of Southern California. Ecol Monogr 77:99–115

    Article  Google Scholar 

  • Kasuga J, Arakawa K, Fujikawa S (2007) High accumulation of soluble sugars in deep supercooling Japanese white birch xylem parenchyma cells. New Phytol 174:569–579

    Article  CAS  PubMed  Google Scholar 

  • Knaupp M, Mishra KB, Nedbal L, Heyer AG (2011) Evidence for a role of raffinose in stabilizing photosystem II during freeze-thaw cycles. Planta 234:477–486

    Article  CAS  PubMed  Google Scholar 

  • Levitt J (1980) Responses of plants to environmental stresses. Academic Press, New York, London

    Google Scholar 

  • Lipp CC, Goldstein G, Meinzer FC, Niemczura W (1994) Freezing tolerance and avoidance in high-elevation Hawaiian plants. Plant Cell Environ 17:1035–1044

    Article  Google Scholar 

  • Nagao M, Arakawa K, Takezawa D, Fujikawa S (2008) Long- and short-term freezing induce different types of injury in Arabidopsis thaliana leaf cells. Planta 227:477–489

    Article  CAS  PubMed  Google Scholar 

  • Nägele T, Heyer AG (2013) Approximating subcellular organisation of carbohydrate metabolism during cold acclimation in different natural accessions of Arabidopsis thaliana. New Phytol 198:777–787

    Article  CAS  PubMed  Google Scholar 

  • Nannos N, Bersimis S, Georgakellos D (2013) Evaluating climate change in Greece through the insurance compensations of the rural production damages. Global Planet Change 102:51–66

    Article  Google Scholar 

  • Papagiannakis K, Lagouvardos K, Kotroni V, Papagiannakis G (2014) Agricultural losses related to frost events: use of the 850 hPa level temperature as an explanatory variable of the damage cost. Nat Hazards Earth Syst Sci 14:2375–2386

    Article  Google Scholar 

  • Pearce RS (2001) Plant freezing and damage. Ann Bot 87:417–424

    Article  CAS  Google Scholar 

  • R Core Team (2016) R: A language and environment for statistical computing. https://www.R-project.org/

  • Reyes-Diaz M, Ulloa N, Zuniga-Feest A, Gutierrez A, Gidekel M, Alberdi M, Corcuera LJ, Bravo LA (2006) Arabidopsis thaliana avoids freezing by supercooling. J Exp Bot 57:3687–3696

    Article  CAS  PubMed  Google Scholar 

  • Ritz C, Baty F, Streibig JC, Gerhard D (2015) Dose-response analysis using R. PLoS One 10:e0146021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakai A, Larcher W (1987) Frost survival of plants: responses and adaptation to freezing stress. Springer, Berlin, Heidelberg

    Book  Google Scholar 

  • Schulze E-D, Beck E, Müller-Hohenstein K (2005) Plant ecology. Springer, Heidelberg

    Google Scholar 

  • Snyder RL, de Melo-Abreu JP (2005) Frost protection: fundamentals, practice, and economics. In: Environment and natural resources series, Food and Agriculture Organization of the United Nations, Rome, no. 10, vol 1

  • Vertucci CW, Stushnoff C (1992) The state of water in acclimating vegetative buds from Malus and Amelanchier and its relationship to winter hardiness. Physiol Plant 86:503–511

    Article  Google Scholar 

  • White GF, Haas JE (1975) Assessment of research on natural hazards. MIT Press, Cambridge, Mass

    Google Scholar 

  • Wilson P, Heneghan A, Haymet A (2003) Ice nucleation in nature: supercooling point (SCP) measurements and the role of heterogeneous nucleation. Cryobiology 46:88–98

    Article  CAS  PubMed  Google Scholar 

  • Wisniewski M, Gusta L, Neuner G (2014) Adaptive mechanisms of freeze avoidance in plants: a brief update. Environ Exp Bot 99:133–140

    Article  CAS  Google Scholar 

  • Xie G, Timasheff SN (1997) The thermodynamic mechanism of protein stabilization by trehalose. Biophys Chem 64:25–43

    Article  CAS  PubMed  Google Scholar 

  • Yoshida M, Abe J, Moriyama M, Shimokawa S, Nakamura Y (1997) Seasonal changes in the physical state of crown water associated with freezing tolerance in winter wheat. Physiol Plant 99:363–370

    Article  CAS  Google Scholar 

  • Zhen Y, Ungerer M (2008) Clinal variation in freezing tolerance among natural accessions of Arabidopsis thaliana. New Phytol 177:419–427

    PubMed  Google Scholar 

  • Zuther E, Schulz E, Childs LH, Hincha DK (2012) Clinal variation in the non-acclimated and cold-acclimated freezing tolerance of Arabidopsis thaliana accessions. Plant Cell Environ 35:1860–1878

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by a Grant from the Deutsche Forschungsgemeinschaft (DFG), Grant Nr. HE-3087/10-2 to AGH. We would like to thank Diether Gotthardt and Marvin Müller for plant cultivation and the members of the Department of Plant Biotechnology for fruitful discussions.

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Authors and Affiliations

  1. Department of Plant Biotechnology, Institute of Biomaterials and Biomolecular Systems, University of Stuttgart, Pfaffenwaldring 57, 70569, Stuttgart, Germany

    Imke I. Hoermiller & Arnd G. Heyer

  2. Department of Botany, Science Center Weihenstephan, Technical University Munich, Emil-Ramann-Straße 4, 85354, Freising, Germany

    Moritz Ruschhaupt

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  1. Imke I. Hoermiller
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  2. Moritz Ruschhaupt
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  3. Arnd G. Heyer
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Correspondence to Arnd G. Heyer.

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Hoermiller, I.I., Ruschhaupt, M. & Heyer, A.G. Mechanisms of frost resistance in Arabidopsis thaliana. Planta 248, 827–835 (2018). https://doi.org/10.1007/s00425-018-2939-1

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