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Thylakoid Membranes -- Summary
Nearly all of earth's plants respond positively to increases in the air's CO2 content by exhibiting enhanced rates of photosynthesis, partly as a consequence of decreases in photorespiration and increases in the operating efficiency of the primary carboxylating enzyme rubisco.  Little research, however, has addressed the direct effects of elevated CO2 on thylakoid membranes, i.e., the membranes within chloroplasts that contain chlorophyll and other pigments that absorb sunlight, together with the specialized protein complexes of photosystem II that play an integral role in the light-dependent reactions of photosynthesis that convert sunlight into usable cellular energy.  In this summary, we review the findings of some papers that have broached this subject in attempting to determine how elevated CO2 may impact thylakoid membranes and thereby influence the overall process of carbon fixation in plants.

After growing alfalfa in open-top chambers at ambient (340 ppm) and enriched (600 ppm) atmospheric CO2 concentrations with ample soil moisture for twenty-five days, followed by inadequate levels of soil moisture for five additional days, Sgherri et al. (1998) determined that the plants grown in the elevated CO2 treatment maintained greater leaf chlorophyll contents and lipid-to-protein ratios in their thylakoid membranes, especially under conditions of water stress.  When water was withheld, for example, leaf chlorophyll content dropped by a mere 6% at 600 ppm CO2, while it plummeted by approximately 30% at 340 ppm.  Moreover, leaf lipid contents in the plants grown in the CO2-enriched air were about 22 and 83% higher than those measured in the plants grown in the ambient air treatment during the periods of ample and insufficient soil moisture, respectively.  In addition, in the high CO2 treatment the average degree of unsaturation of the two most important thylakoid membrane lipids was approximately 20 and 37% greater than what it was in the plants grown at 340 ppm CO2 during times of adequate and inadequate soil moisture, respectively.

What are some of the implications of these observations?  It is generally believed that the greater concentrations of thylakoid lipids that are typically observed at elevated atmospheric CO2 concentrations, plus their enhanced degree of unsaturation, may allow thylakoid membranes to maintain a more fluid and stable environment, which is critical during periods of water stress in enabling plants to continue photosynthetic carbon uptake.  These effects are so important, in fact, that some researchers have suggested that adaptive plant responses such as these may allow plants to better cope with any altered environmental condition that produces stress.

A good example of this phenomenon as it pertains to extreme water stress is provided by the study of Tuba et al. (1998), wherein detached leaves of Xerophyta scabrida (a woody shrub that grows in arid regions of east Africa) were re-hydrated and re-greened in air of 350 and 700 ppm CO2, after which they were allowed to desiccate.  The elevated CO2 in this case did not affect the amount of chlorophyll, the functioning of the thylakoid membranes, or the time to complete drying during desiccation.  However, it allowed positive photosynthetic carbon gains in the shrub's leaves to continue three times longer than it did in leaves exposed to ambient air, which phenomenon resulted in the CO2-enriched leaves gaining more than ten times the amount of carbon over the period of desiccation than was gained by the leaves exposed to normal air.

Tuba et al. additionally studied the effects of desiccation on the carbon balance of a moss and a lichen under the same two atmospheric CO2 concentrations, observing similar response patterns in both plants.  Positive photosynthetic carbon gains were maintained 14% longer with atmospheric CO2 enrichment; and total assimilation during the dry-down in elevated CO2 was increased by 52 and 69% in the lichen and moss, respectively.

Shifting to the stress of chilling, in our Editorial of 13 Nov 2002 we discuss some of the impacts of enhanced thylakoid lipid unsaturation on the stress produced by plant exposure to ordinarily hurtful low temperatures, beginning with the study of Hugly and Somerville (1992), who worked with wild-type Arabidopsis thaliana and two mutants deficient in thylakoid lipid unsaturation.  They 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, for 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 15C (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 (Wallace, 2000; Tilman et al., 2001).

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 20C (Graham and Patterson, 1982); and with the 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, significantly increasing ecosystem biodiversity along the way (see our Editorial of 25 September 2002).

Turning to the other end of the biologically-tolerable temperature spectrum, we encounter heat stress.  With respect to this debilitating phenomenon, Taub et al. (2000) note that electron transport through photosystem II is the most heat-sensitive component of the entire photosynthetic process, and that any reductions in electron transport through this thylakoid membrane-bound protein complex invariably lead to reductions in photosynthetic carbon uptake and reduced growth potential.  Hence, they conducted several experiments on herbaceous, woody, monocot and dicot species (to assess the degree of universality of any response that might be detected) in controlled environment chambers, greenhouses and FACE plots to examine the photosynthetic responses of this wide array of plants to acute heat stress under ambient and elevated CO2 concentrations ranging from 550 to 1000 ppm.

Of the sixteen plant species studied, all but one displayed greater photochemical efficiencies of photosystem II when growing in CO2-enriched air as opposed to ambient air when exposed to high air temperatures.  In fact, the air temperatures that caused a 50% reduction in the maximum efficiency of photosystem II were nearly one degree Celsius higher for plants grown in elevated CO2 air than for plants grown in ambient air.  In other words, elevated CO2 almost universally allowed more electrons to flow through photosystem II, thereby laying the foundation for greater photosynthetic rates; and in an extended experiment, rates of net photosynthesis measured at 40C in CO2-enriched cucumbers were 3.2 times greater than those exhibited by plants grown in ambient air and exposed to the same air temperature.

Another stress to which many plants are routinely exposed is that produced by elevated atmospheric ozone concentrations.  In a study of this phenomenon, Oksanen et al. (2001) grew aspen clones with varying degrees of ozone tolerance together with sugar maple and paper birch trees for three years in 30-m diameter FACE plots maintained at atmospheric CO2 concentrations of 360 and 560 ppm with and without exposure to elevated ozone concentrations (1.5 times ambient) to study the interactive effects of these two trace gases on leaf ultrastructure.  In the birch trees, the negative effects of ozone on leaf ultrastructure were minor, and injuries to thylakoid membranes were partially ameliorated by exposure to elevated CO2.  In the aspen clones, ozone exposure caused more significant structural injuries to thylakoid membranes and the stromal compartment within chloroplasts; but these injuries were also largely ameliorated by atmospheric CO2 enrichment.  Likewise, leaf thickness, mesophyll tissue thickness, the amount of chloroplasts per unit cell area, and the amount of starch in chloroplasts were all decreased in the high ozone treatment; but in the case of these leaf properties, simultaneous exposure of the ozone-stressed trees to elevated CO2 more than compensated for the ozone-induced problems.  As tropospheric ozone concentrations continue to rise, therefore, they will likely pose a problem for regenerating aspen and birch trees by negatively affecting chloroplast ultrastructure at the site of carbon fixation, which will likely decrease their productivity and growth.  However, if the atmospheric CO2 concentration also continues to rise, these negative effects will be either partly, completely, or more than completely ameliorated, thus stimulating productivity and growth to varying degrees within these species.

Considered in their entirety, the results of the studies reviewed above suggest that atmospheric CO2 enrichment may be a powerful "treatment" for all sorts of environmental ailments that afflict earth's plants and have their origin in stress-induced problems associated with the thylakoid membranes of chloroplasts.

References
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.

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.

Oksanen, E., Sober, J. and Karnosky, D.F.  2001.  Impacts of elevated CO2 and/or O3 on leaf ultrastructure of aspen (Populus tremuloides) and birch (Betula papyrifera) in the Aspen FACE experiment.  Environmental Pollution 115: 437-446.

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.

Taub, D.R., Seeman, J.R. and Coleman, J.S.  2000.  Growth in elevated CO2 protects photosynthesis against high-temperature damage.  Plant, Cell and Environment 23: 649-656.

Tilman, D., Fargione, J., Wolff, B., D'Antonio, C., Dobson, A., Howarth, R., Schindler, D., Schlesinger, W.H., Simberloff, D. and Swackhamer, D.  2001.  Forecasting agriculturally driven global environmental change.  Science 292: 281-284.

Tuba, Z., Csintalan, Z., Szente, K., Nagy, Z. and Grace, J.  1998.  Carbon gains by desiccation-tolerant plants at elevated CO2Functional Ecology 12: 39-44.

Wallace, J.S.  2000.  Increasing agricultural water use efficiency to meet future food production.  Agriculture, Ecosystems & Environment 82: 105-119.

Last updated 4 May 2005