Trends in Plant Science
Volume 9, Issue 8, August 2004, Pages 399-405
Journal home page for Trends in Plant Science

Abiotic stress series
Antifreeze proteins in overwintering plants: a tale of two activities

https://doi.org/10.1016/j.tplants.2004.06.007Get rights and content

Antifreeze proteins are found in a wide range of overwintering plants where they inhibit the growth and recrystallization of ice that forms in intercellular spaces. Unlike antifreeze proteins found in fish and insects, plant antifreeze proteins have multiple, hydrophilic ice-binding domains. Surprisingly, antifreeze proteins from plants are homologous to pathogenesis-related proteins and also provide protection against psychrophilic pathogens. In winter rye (Secale cereale), antifreeze proteins accumulate in response to cold, short daylength, dehydration and ethylene, but not pathogens. Transferring single genes encoding antifreeze proteins to freezing-sensitive plants lowered their freezing temperatures by ∼1°C. Genes encoding dual-function plant antifreeze proteins are excellent models for use in evolutionary studies to determine how genes acquire new expression patterns and how proteins acquire new activities.

Section snippets

Interaction between antifreeze proteins and ice

Unlike most solutes that are simply pushed ahead of the ice face during freezing, AFPs bind irreversibly to the surface of ice and are incorporated into the ice crystal lattice [5]. Although it seems counterintuitive, the ice-binding domains of fish and insect AFPs are flat and relatively hydrophobic and their adsorption onto ice is a hydrophobic interaction driven by the increase in entropy gained by releasing hydration water from the ice and protein surfaces. Binding to ice is stabilized by a

Antifreeze activity in plants

Antifreeze activity was first reported in plants in 1992 12, 13 and has since been found in many more overwintering vascular plants, including ferns, gymnosperms, and monocotyledonous and dicotyledonous angiosperms (see Supplementary material) 11, 13, 18, 19. Antifreeze activity is present in overwintering plants only after they have been exposed to low temperatures and only in plants that tolerate the presence of ice in their tissues. Antifreeze activity has been observed in different parts of

Plant antifreeze proteins are also pathogenesis-related proteins

AFPs have been isolated from six plants and full-length nucleotide sequences are available for genes encoding five AFPs (Table 1). The surprising result of sequencing plant AFPs, or their corresponding genes, is that most of them are homologous to pathogenesis-related (PR) proteins [20]. Normally, PR proteins are released into the apoplast in response to pathogen infection and act together to degrade fungal cell walls enzymatically and inhibit fungal enzymes. Secreted PR proteins with

Regulation of antifreeze proteins

To date, no plant has been reported to have constitutive antifreeze activity; rather all studies have shown that transcripts and translation products of AFP genes accumulate during cold acclimation 12, 13, 20, 21, 28. The conditions used for cold acclimation mimic autumn when days become shorter and colder. Therefore, low temperature and daylength are important environmental cues for AFP production. For example, winter rye plants grown at low temperatures accumulate more apoplastic protein

Role of antifreeze proteins in freezing in planta

The lower limit of freezing tolerance of a plant population is measured as LT50, the lethal temperature for 50% of the individuals. In single plants, LT50 is often determined as the loss of 50% of the electrolytes from plant tissues after freezing. As plants acclimate to low temperatures in autumn, they acquire freezing tolerance and the LT50 becomes progressively lower. In breeding programs, plants are often selected for increased freezing tolerance based on changes in LT50; however, any

Plant transformation with genes encoding antifreeze proteins

Agricultural production in many areas is limited by freezing temperatures. Higher yields could be achieved either by improving the freezing tolerance of an overwintering crop or by increasing the survival of freezing-sensitive crop plants following light frosts. Moreover, AFPs could increase the shelf life and improve the quality of frozen foods by inhibiting the recrystallization of ice if the AFPs are targeted to accumulate in fruits and vegetables before harvest [41]. Therefore, it is not

Conclusions

Plant AFPs are unusual proteins: they have multiple, hydrophilic ice-binding domains that appear to function as inhibitors of ice recrystallization and ice nucleation. AFPs have little effect on LT50 but could enhance winter survival by slowing freezing processes. Moreover, most AFPs from plants are modified PR proteins that retain high sequence identify and even the antifungal activities of the progenitor PR proteins. Therefore, genes encoding plant AFPs are excellent models for use in

Acknowledgements

We thank Maja Stressmann and André Peters, University of Waterloo, and Alejandra M. Regand and Alejandro G. Marangoni, University of Guelph, for assistance with Figure 2. Our work is supported by the Natural Science and Engineering Research Council of Canada. M.G. is a Killam Research Fellow.

References (50)

  • J.G. Duman et al.

    Thermal hysteresis protein activity in bacteria, fungi, and phylogenetically diverse plants

    Cryobiology

    (1993)
  • K. Meyer

    A leucine-rich repeat protein of carrot that exhibits antifreeze activity

    FEBS Lett.

    (1999)
  • J.G. Duman

    Purification and characterization of a thermal hysteresis protein from a plant, the bittersweet nightshade Solanum dulcamara

    Biochim. Biophys. Acta

    (1994)
  • P.D.A. Pudney

    The physico-chemical characterization of a boiling stable antifreeze protein from a perennial grass (Lolium perenne)

    Arch. Biochem. Biophys.

    (2003)
  • A.J. Cutler

    Winter flounder antifreeze protein improves the cold hardiness of plant tissues

    J. Plant Physiol.

    (1989)
  • N. Holmberg

    Targeted expression of a synthetic codon optimized gene, encoding the spruce budworm antifreeze protein, leads to accumulation of antifreeze activity in the apoplasts of transgenic tobacco

    Gene

    (2001)
  • C.S. Snider

    Role of ice nucleation and antifreeze activities in pathogenesis and growth of snow molds

    Phytopathology

    (2000)
  • A.L. DeVries

    Antifreeze glycopeptides and peptides: interactions with ice and water

    Methods Enzymol.

    (1986)
  • M. Stressmann

    Calcium interacts with antifreeze proteins and chitinases from cold-acclimated winter rye

    Plant Physiol.

    (2004)
  • M. Smallwood

    Isolation and characterization of a novel antifreeze protein from carrot (Daucus carota)

    Biochem. J.

    (1999)
  • M. Griffith

    Antifreeze protein produced endogenously in winter rye leaves

    Plant Physiol.

    (1992)
  • X.M. Yu et al.

    Antifreeze proteins in winter rye leaves form oligomeric complexes

    Plant Physiol.

    (1999)
  • N. Li

    Enhancement of insect antifreeze protein activity by solutes of low molecular mass

    J. Exp. Biol.

    (1998)
  • A. Zamani

    Endochitinase and antifreeze activity in the apoplastic fluid of Douglas-fir in response to Phellinus weirii infection

    For. Pathol.

    (2003)
  • W-C. Hon

    Antifreeze proteins in winter rye are similar to pathogenesis-related proteins

    Plant Physiol.

    (1995)
  • Cited by (0)

    View full text