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Published on April 30, 2004; 10.1104/pp.103.038158

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Received December 19, 2003
Returned for revision February 9, 2004
Accepted February 9, 2004

Calcium Interacts with Antifreeze Proteins and Chitinase from Cold-Acclimated Winter Rye

Maja Stressmann , Satoshi Kitao , Marilyn Griffith *, Christine Moresoli , León A. Bravo , and Alejandro G. Marangoni

Departments of Biology (S.K., M.G., C.M., L.A.B.) and Chemical Engineering (M.S., C.M.), University of Waterloo, Waterloo, Ontario N2L 3G1, Canada; and Department of Food Science, University of Guelph, Guelph, Ontario N1G 2W1, Canada (A.G.M.)

* Corresponding author; email: griffith{at}uwaterloo.ca.

During cold acclimation, winter rye (Secale cereale) plants accumulate pathogenesis-related proteins that are also antifreeze proteins (AFPs) because they adsorb onto ice and inhibit its growth. Although they promote winter survival in planta, these dual-function AFPs proteins lose activity when stored at subzero temperatures in vitro, so we examined their stability in solutions containing CaCl2, MgCl2, or NaCl. Antifreeze activity was unaffected by salts before freezing, but decreased after freezing and thawing in CaCl2 and was recovered by adding a chelator. Ca2+ enhanced chitinase activity 3- to 5-fold in unfrozen samples, although hydrolytic activity also decreased after freezing and thawing in CaCl2. Native PAGE, circular dichroism, and Trp fluorescence experiments showed that the AFPs partially unfold after freezing and thawing, but they fold more compactly or aggregate in CaCl2. Ruthenium red, which binds to Ca2+-binding sites, readily stained AFPs in the absence of Ca2+, but less stain was visible after freezing and thawing AFPs in CaCl2. We conclude that the structure of AFPs changes during freezing and thawing, creating new Ca2+-binding sites. Once Ca2+ binds to those sites, antifreeze activity, chitinase activity and ruthenium red binding are all inhibited. Because free Ca2+ concentrations are typically low in the apoplast, antifreeze activity is probably stable to freezing and thawing in planta. Ca2+ may regulate chitinase activity if concentrations are increased locally by release from pectin or interaction with Ca2+-binding proteins. Furthermore, antifreeze activity can be easily maintained in vitro by including a chelator during frozen storage.




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