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ENVIRONMENTAL STRESS AND ADAPTATION

Antifreeze Proteins Modify the Freezing Process In Planta^1,2

Department of Biology, University of Waterloo, Waterloo, Ontario, Canada N2L 3G1 (M.G., C.L., S.B.W., R.W.J.); U. S. Department of Agriculture, Agricultural Research Service, Kearneysville, West Virginia 25430 (M.W.); and Department of Food Science, University of Guelph, Guelph, Ontario, Canada N1G 2W1 (A.G.M.)

During cold acclimation, winter rye (Secale cereale L. cv Musketeer) plants accumulate antifreeze proteins (AFPs) in the apoplast of leaves and crowns. The goal of this study was to determine whether these AFPs influence survival at subzero temperatures by modifying the freezing process or by acting as cryoprotectants. In order to inhibit the growth of ice, AFPs must be mobile so that they can bind to specific sites on the ice crystal lattice. Guttate obtained from cold-acclimated winter rye leaves exhibited antifreeze activity, indicating that the AFPs are free in solution. Infrared video thermography was used to observe freezing in winter rye leaves. In the absence of an ice nucleator, AFPs had no effect on the supercooling temperature of the leaves. However, in the presence of an ice nucleator, AFPs lowered the temperature at which the leaves froze by 0.3°C to 1.2°C. In vitro studies showed that apoplastic proteins extracted from cold-acclimated winter rye leaves inhibited the recrystallization of ice and also slowed the rate of migration of ice through solution-saturated filter paper. When we examined the possible role of winter rye AFPs in cryoprotection, we found that lactate dehydrogenase activity was higher after freezing in the presence of AFPs compared with buffer, but the same effect was obtained by adding bovine serum albumin. AFPs had no effect on unstacked thylakoid volume after freezing, but did inhibit stacking of the thylakoids, thus indicating a loss of thylakoid function. We conclude that rye AFPs have no specific cryoprotective activity; rather, they interact directly with ice in planta and reduce freezing injury by slowing the growth and recrystallization of ice.

² In memory of Prof. Marilyn Griffith, her endless energy, her openness, and her dedication to the pursuit of scientific excellence.

Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.058628.

^* Corresponding author; e-mail amarango{at}uoguelph.ca; fax 519–824–6631.

Received December 23, 2004; returned for revision February 3, 2005; accepted February 8, 2005.

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