Photosynthesis in a Changing World

Oxygenic photosynthesis has sustained life on Earth since its appearance about 3.5 Gyr ago ([Nisbet and Sleep, 2001]). This ancient process has adapted in the past to an enormous range of life conditions and to massive environmental changes, yet has remained unchanged in its essential characteristics. Nowadays, the world is undergoing a series of rapid environmental changes, often referred to as global change, predominantly caused by anthropogenic activities, that may positively or negatively affect photosynthesis, triggering the onset of a variety of adaptive responses. The effects of global changes on photosynthesis can be extremely complex, reflecting natural plant biodiversity and also microclimate diversity. There are several reasons to specifically and urgently study the interaction between current global change and photosynthesis.

First, the unprecedented rapidity of global changes ([IPCC, 2001]) makes it difficult to predict whether and how photosynthesis will adapt to the new or changing environments, and how this will in turn influence important parameters for ecosystem stability such as species-specific distribution, length of photosynthetically-active season, and ecosystem composition. Rapidly increasing CO₂ and temperature are key factors in this respect.

Second, some of the factors contributing to global change are “new” to plants. Water, soil, and air pollution seriously affect urban, peri-urban, and industrial areas, where plants are exposed to chronic or acute levels of pollutants. Even remote areas are not immune to pollution, as air-borne pollutants may be transported from their sources by atmospheric circulation, and may be deposited or may initiate photochemical reactions far away from the place of origin. Coping with man-made pollutants is certainly possible, as many plants can survive in heavily polluted areas, but the cost of this, in terms of integrity and functionality of the photosynthetic apparatus, is unknown or insufficiently documented.

Third, mechanistic studies have often addressed the impact of single stress factors on photosynthesis, but the combined impact of factors which are changing together is more difficult to assess and needs to be explored with ad hoc field experiments and with manipulation/simulation experiments. Let us return to the most striking and rapid effect of climate change, the concurrent increase of CO₂ levels and temperature. Increasing levels of CO₂ alone would overwhelmingly increase photosynthesis and, probably to a lesser extent, plant productivity. In fact, CO₂ would also influence transpiration and respiration, the two other processes by which CO₂ is directly sensed by plants ([Drake et al., 1997]). However, rising temperatures will have contrasting influences on these primary processes, and will be responsible for a series of secondary alterations in ecosystem structure and productivity (plant growth rates, litter quantity and quality, canopy structure and architecture, shading, rooting depth). When considering the short-term biochemical response of photosynthesis and respiration to rising CO₂ levels and temperature (namely, the exponential increase in respiration at CO₂ and temperature levels saturating or inhibiting photosynthesis), a decline in ecosystem productivity could be envisaged (Fig. [1]). However, there is still considerable uncertainty about the long-term balance of these processes and the extent and direction of acclimation of primary processes to global change factors. This knowledge is essential to be able to make predictions on the sustainability of agriculture and forestry in a rapidly changing world.

Fig. 1 Scenarios of net carbon uptake by terrestrial ecosystems, determined by carbon assimilation (photosynthesis) and carbon loss (respiration) changes, for increasing temperature and CO₂ concentration. With the current use of fossil fuels, it is estimated that CO₂ concentration is increasing by 1,8 µmol mol^-1 per year, while the surface temperature of the Earth will increase on average by 0.4 - 0.6 °C per decade throughout the 21st century. Predicted changes in atmospheric CO₂ concentration are expected to increase photosynthetic rates in C₃ plants, both by increasing the rate of carbon fixation and by reducing photorespiratory loss of carbon. Because the form of the response is a saturating curve, increasing CO₂ concentration will have an ever-smaller effect on photosynthesis as it rises over time (green line). However, both photosynthesis and respiration respond directly and in contrasting ways to the increase in air temperature, but the pattern of their acclimatory responses to rising temperature is highly uncertain, as outlined by the three possible scenarios shown by blue lines, and is still a matter of much debate. Ultimately, the form of the response function of net carbon uptake over time will be determined by the acclimatory responses of photosynthesis and respiration to global change. (Modified from [Norby [2003].])

Fourth, virtually each changing environmental factor acting on primary processes feeds back on other factors, thus constituting a secondary, indirect, source of instability for the photosynthetic apparatus. [Sellers et al. (1996]) have reasoned that the reduction in transpiration caused by rising CO₂ levels will result in a decline in the ratio of latent to sensible heat transfer from canopies, in turn resulting in continental warming of 1 - 2 °C. Field experiments have shown a similar daytime temperature increase in wheat plots subjected to free air CO₂ enrichment ([Kimball et al., 1995]). Much less is known about feedback effects on photosynthesis determined by the interaction between increasing temperature and CO₂ and environmental stresses (e.g., water and saline stress or pollutants).

Fifth, photosynthesis is the only natural process actively sequestering a massive amount of CO₂ from the atmosphere. This sink effect is of extraordinary importance because it can counteract the present trend toward a rise in atmospheric CO₂ ([Janssens et al., 2003]). Utilization of forest photosynthesis to mitigate CO₂ increase is recommended by the Kyoto Protocol (1997). Similar sink effects may be present for other greenhouse gases and for anthropogenic pollutants, thus making plants, in principle, powerful and natural elements for mitigation of global change.

Participants in the High Level Scientific Conference “Photosynthesis in a changing world” (Chania, Crete, May 2003) received a thorough overview of current knowledge on the photosynthetic response to environmental factors affected by global changes. They developed and shared original and innovative knowledge of the adaptive mechanisms and ideas on how to mitigate the negative consequences of global change in fragile environments. During the thematic sessions of the conference, focused on the main factors involved in global change, many issues were tackled and a number of them emerged because of their relevant interaction with photosynthesis. Some of these topics are reviewed in this special issue, which also contains original papers investigating specific aspects of global change and their influence on photosynthesis.

Drought and salinity, which plague large areas of the world, notably the Mediterranean area, and increases in planetary CO₂ that are predicted to reach 700 µmol mol^-1 during the second half of this century in a “business-as-usual” scenario ([IPCC, 2001]), were focal points of the conference. As reported by Flexas et al. in their review paper on the impact of drought and salinity on photosynthesis, compelling evidence shows that photosynthesis is generally limited by diffusive (stomatal and mesophyll) resistances until the leaf water content drops to values close to wilting. Sharkey et al., in their review addressing photosynthesis under rising CO₂ levels, pointed out the importance of efficient end product synthesis to optimize photosynthesis in the future atmosphere, and presented novel experiments on sugar synthesis/degradation, focused on understanding future possible end product limitations to photosynthesis.

The influence of thermal regimes on photosynthesis has rarely received the same attention as is given to other environmental parameters, such as CO₂ and water. This is, in our opinion, an oversight. Of course, temperature increase is relatively small and may not have a large impact on photosynthesis, and temperature change cannot be definitively attributed to the concurrent rise in greenhouse gases. But Europe is warming at a steady rate of about 0.3 - 0.6 °C per decade ([IPCC, 2001]). This leads to increases in evapotranspiration by vegetation and is one of the main factors contributing to desertification of fragile, dry areas, such as large areas of southern Europe. Kirschbaum has demonstrated the importance of temperature interactions with other environmental factors, and their role in controlling photosynthetic rates and plant distribution.

Progress in characterising photosynthesis in vivo has been impressive, and new equipment allowing precise and unambiguous interpretation of photosynthetic constraints in laboratory and field experiments is now available. Eichelmann et al. presented practical applications of new techniques to study the impact of changing environmental factors on photosynthesis. Technical advances have also helped in refining parameterization and modelling of photosynthesis in response to the environment, as clearly indicated by the contributions of Kirschbaum and of Niinemets and Valladares.

The impact of pollution on photosynthesis probably requires the most attention. Pollution sources are not fully itemized and are even less controlled. In fact, political (economic) reasons have inhibited implementation of precise and world-wide policies to control pollutants, as exemplified by the lack of consensus or agreement on the Kyoto Protocol with regard to the most recognized anthropogenic pollutant: CO₂. There is still much uncertainty over the interaction between pollutants and vegetation. Plants may take up contaminants from soil, water, and air, but the effectiveness and cost of phytoremediation has yet to be studied carefully. Indices of vegetation damage (e.g., AOT40, in the case of ozone, [Fuhrer et al., 1997]) are often ineffective or imprecise because exposure to pollutants does not necessarily result in their uptake, and uptake mechanisms have not been investigated in detail. Several contributions in this issue address the impact of pollutants per se or indirectly, as for instance through the eutrophication and over-fertilization of fresh-water, in turn affecting light use and photochemical properties of vegetation, as described by Bartak et al. and Masojidek et al.

We hope that the special issue that we are introducing here will convey to the readers the same challenging and provocative ideas that were so lively discussed by lecturers and young researchers at the conference. Our aim was to facilitate convergence of perceptions about the addressed themes, thus emphasising the need for further studies in the field of plant-environment interactions.

References

• 1 Drake B. G., Gonzàlez-Meler M. A., Long S. P.. More efficient plants: a consequence of rising atmospheric CO₂?.  Annual Review of Plant Physiology and Molecular Biology. (1997);  48 607-637
• 2 Fuhrer J., Skarby L., Ashmore M. R.. Critical levels for ozone effects on vegetation in Europe.  Environmental Pollution. (1997);  97 91-106
• 3 IPCC .Climate change 2001: IPCC third assessment report. Intergovernamental Panel on Climate Change. On-line at http://www.grida.no/climate/ipcc_tar/ . Cambridge; Cambridge University Press (2001)
• 4 Janssens  et al. I. A.. Europe's terrestrial biosphere absorbs 7 to 12 % of European anthropogenic CO₂ emissions.  Science. (2003);  300 1538-1542
• 5 Kimball B. A., Pinter P. J., Garcia R. L., LaMorte R. L., Wall G. W., Hunsaker D. J., Wechsung G., Wechsung F., Kartschall T.. Productivity and water use of wheat under free-air carbon dioxide enrichment.  Global Change Biology. (1995);  1 429-442
• 6 Nisbet E. G., Sleep N. H.. The habitat and nature of early life.  Nature. (2001);  409 1083-1091
• 7 Norby R. J.. Interactions between increasing CO₂ and temperature in terrestrial ecosystems: a conceptual framework. TERACC workshop, “Interactions Between Increasing CO₂ and Temperature in Terrestrial Ecosystems”. Lake Tahoe, CA, April, 2003 (http://www.esd.ornl.gov/facilities/ORNL-FACE/pubs.html). (2003)
• 8 Sellers P. J., Bounoua L., Collatz G. J., Randall D. A., Dazlich D. A., Los S. O., Berry J. A., Fung I., Tucker C. J., Field C. B., Jensen T. G.. Comparison of radiative and physiological effects of doubled CO₂ on climate.  Science. (1996);  271 1402-1406