Loik et al. (2000) grew three Yucca species (brevifolia, schidigera, and whipplei) in pots placed within glasshouses maintained at atmospheric CO2 concentrations of 360 and 700 ppm and day/night air temperatures of 40/24°C for seven months, after which some of the plants were subjected to a two-week day/night air temperature treatment of 20/5°C.  In addition, leaves from each Yucca species were removed and placed in a freezer that was cooled at a rate of 3°C per hour until a minimum temperature of -15°C was reached.  These manipulations indicated that elevated CO2 lowered the air temperature at which 50% low-temperature-induced cell mortality occurred by 1.6, 1.4 and 0.8°C in brevifolia, schidigera and whipplei, respectively.  And on the basis of the result obtained for Y. brevifolia, Dole et al. (2003) estimated that "the increase in freezing tolerance caused by doubled CO2 would increase the potential habitat of this species by 14%."

In contrast to these positive results, Obrist et al. (2001) observed just the opposite response.  In an open-top chamber study of a temperate grass ecosystem growing on a nutrient-poor calcareous soil in northwest Switzerland, portions of which had been exposed to atmospheric CO2 concentrations of 360 and 600 ppm for a period of six years, they determined that the average temperature at which 50% low-temperature-induced leaf mortality occurred in five prominent species actually rose by an average of 0.7°C in response to the extra 240 ppm of CO2 employed in their experiment.

Most relevant investigations, however, have produced evidence of positive CO2 effects on plant low temperature tolerance.  Sigurdsson (2001), for example, grew black cottonwood seedlings near Gunnarsholt, Iceland within closed-top chambers maintained at ambient and twice-ambient atmospheric CO2 concentrations for a period of three years, finding that elevated CO2 tended to hasten the end of the growing season.  This effect was interpreted as enabling the seedlings to better avoid the severe cold-induced dieback of newly-produced tissues that often occurs with the approach of winter in this region.  Likewise, Wayne et al. (1998) found that yellow birch seedlings grown at an atmospheric CO2 concentration of 800 ppm exhibited greater dormant bud survivorship at low air temperatures than did seedlings grown at 400 ppm CO2.

Schwanz and Polle (2001) investigated the effects of elevated CO2 on chilling stress in micropropagated hybrid poplar clones that were subsequently potted and transferred to growth chambers maintained at either ambient (360 ppm) or elevated (700 ppm) CO2 for a period of three months.  They determined that "photosynthesis was less diminished and electrolyte leakage was lower in stressed leaves from poplar trees grown under elevated CO2 as compared with those from ambient CO2."  Although severe chilling did cause pigment and protein degradation in all stressed leaves, the damage was expressed to a lower extent in leaves from the elevated CO2 treatment.  This CO2-induced chilling protection was determined to be accompanied by a rapid induction of superoxide dismutase activity, as well as by slightly higher stabilities of other antioxidative enzymes.

Another means by which chilling-induced injury may be reduced in CO2-enriched air is suggested by the study of Sgherri et al. (1998), who reported that raising the air's CO2 concentration from 340 to 600 ppm increased lipid concentrations in alfalfa thylakoid membranes while simultaneously inducing a higher degree of unsaturation in the most prominent of those lipids.  Under well-watered conditions, for example, the 76% increase in atmospheric CO2 enhanced overall thylakoid lipid concentration by about 25%, while it increased the degree of unsaturation of the two main lipids by approximately 17% and 24%.  Under conditions of water stress, these responses were found to be even greater, as thylakoid lipid concentration rose by approximately 92%, while the degree of unsaturation of the two main lipids rose by about 22% and 53%.

What do these observations have to do with a plant's susceptibility to chilling injury?  According to a number of studies conducted over the past decade, a lot.

Working with wild-type Arabidopsis thaliana and two mutants deficient in thylakoid lipid unsaturation, Hugly and Somerville (1992) found that "chloroplast membrane lipid polyunsaturation contributes to the low-temperature fitness of the organism," and that it "is required for some aspect of chloroplast biogenesis."  When lipid polyunsaturation was low, for example, they observed "dramatic reductions in chloroplast size, membrane content, and organization in developing leaves."  Furthermore, there was a positive correlation "between the severity of chlorosis in the two mutants at low temperatures and the degree of reduction in polyunsaturated chloroplast lipid composition."

Working with tobacco, Kodama et al. (1994) demonstrated that the low-temperature-induced suppression of leaf growth and concomitant induction of chlorosis observed in wild-type plants was much less evident in transgenic plants containing a gene that allowed for greater expression of unsaturation in the fatty acids of leaf lipids.  This observation and others led them to conclude that substantially unsaturated fatty acids "are undoubtedly an important factor contributing to cold tolerance."

In a closely related study, Moon et al. (1995) found that heightened unsaturation of the membrane lipids of chloroplasts stabilized the photosynthetic machinery of transgenic tobacco plaints against low-temperature photoinibition "by accelerating the recovery of the photosystem II protein complex."  Likewise, Kodama et al. (1995), also working with transgenic tobacco plants, showed that increased fatty acid desaturation is one of the prerequisites for normal leaf development at low, nonfreezing temperatures; and Ishizaki-Nishizawa et al. (1996) demonstrated that transgenic tobacco plants with a reduced level of saturated fatty acids in most membrane lipids "exhibited a significant increase in chilling resistance."

These observations are laden with significance for earth's agro-ecosystems.  Many economically important crops, such as rice, maize and soybeans, are classified as chilling-sensitive; and they experience injury or death at temperatures between 0 and 15°C (Lyons, 1973).  If atmospheric CO2 enrichment enhances their production and degree-of-unsaturation of thylakoid lipids, as it does in alfalfa, a continuation of the ongoing rise in the air's CO2 content could increase the abilities of these critically important agricultural species to withstand periodic exposure to debilitating low temperatures; and this phenomenon could provide the extra boost in food production that will be needed to sustain our increasing numbers in the years and decades ahead.

Earth's natural ecosystems would also benefit from a CO2-induced increase in thylakoid lipids containing more-highly-unsaturated fatty acids.  Many plants of tropical origin, for example, suffer cold damage when temperatures fall below 20°C (Graham and Patterson, 1982); and with improved lipid characteristics provided by the ongoing rise in the air's CO2 content, such plants would be able to expand their ranges both poleward and upward in a higher-CO2 world.

Clearly, more research remains to be done before we can accurately assess the extent of these potential biological benefits.  In particular, we must conduct more studies of the effects of atmospheric CO2 enrichment on the properties of thylakoid lipids in a greater variety of plants; and, in the same experiments, we must assess the efficacy of these lipid property changes in enhancing plant tolerance of low temperatures.  Such studies should rank high on the to-do list of relevant funding agencies.

References
Dole, K.P., Loik, M.E. and Sloan, L.C.  2003.  The relative importance of climate change and the physiological effects of CO2 on freezing tolerance for the future distribution of Yucca brevifolia.  Global and Planetary Change 36: 137-146.

Graham, D. and Patterson, B.D.  1982.  Responses of plants to low, non-freezing temperatures: proteins, metabolism, and acclimation.  Annual Review of Plant Physiology 33: 347-372.

Hugly, S. and Somerville, C.  1992.  A role for membrane lipid polyunsaturation in chloroplast biogenesis at low temperature.  Plant Physiology 99: 197-202.

Ishizaki-Nishizawa, O., Fujii, T., Azuma, M., Sekiguchi, K., Murata, N., Ohtani, T. and Toguri T.  1996.  Low-temperature resistance of higher plants is significantly enhanced by a nonspecific cyanobacterial desaturase.  Nature Biotechnology 14: 1003-1006.

Kodama, H., Hamada, T., Horiguchi, G., Nishimura, M. and Iba, K.  1994.  Genetic enhancement of cold tolerance by expression of a gene for chloroplast w-3 fatty acid desaturase in transgenic tobacco.  Plant Physiology 105: 601-605.

Kodama, H., Horiguchi, G., Nishiuchi, T., Nishimura, M. and Iba, K.  1995.  Fatty acid desaturation during chilling acclimation is one of the factors involved in conferring low-temperature tolerance to young tobacco leaves.  Plant Physiology 107: 1177-1185.

Loik, M.E., Huxman, T.E., Hamerlynck, E.P. and Smith, S.D.  2000.  Low temperature tolerance and cold acclimation for seedlings of three Mojave Desert Yucca species exposed to elevated CO2.  Journal of Arid Environments 46: 43-56.

Lyons, J.M.  1973.  Chilling injury in plants.  Annual Review of Plant Physiology 24: 445-466.

Moon, B.Y., Higashi, S.-I., Gombos, Z. and Murata, N.  1995.  Unsaturation of the membrane lipids of chloroplasts stabilizes the photosynthetic machinery against low-temperature photoinhibition in transgenic tobacco plants.  Proceedings of the National Academy of Sciences, USA 92: 6219-6223.

Obrist, D., Arnone III, J.A. and Korner, C.  2001.  In situ effects of elevated atmospheric CO2 on leaf freezing resistance and carbohydrates in a native temperate grassland.  Annals of Botany 87: 839-844.

Schwanz, P. and Polle, A.  2001.  Growth under elevated CO2 ameliorates defenses against photo-oxidative stress in poplar (Populus alba x tremula).  Environmental and Experimental Botany 45: 43-53.

Sgherri, C.L.M., Quartacci, M.F., Menconi, M., Raschi, A. and Navari-Izzo, F.  1998.  Interactions between drought and elevated CO2 on alfalfa plants.  Journal of Plant Physiology 152: 118-124.

Sigurdsson, B.D.  2001.  Elevated [CO2] and nutrient status modified leaf phenology and growth rhythm of young Populus trichocarpa trees in a 3-year field study.  Trees 15: 403-413.

Wayne, P.M., Reekie, E.G. and Bazzaz, F.A.  1998.  Elevated CO2 ameliorates birch response to high temperature and frost stress: implications for modeling climate-induced geographic range shifts.  Oecologia 114: 335-342.