We review the current understanding of the temperature responses of C3 and C4 photosynthesis across thermal ranges that do not harm the photosynthetic apparatus. In C3 species, photosynthesis is classically considered to be limited by the capacities of ribulose 1·5-bisphosphate carboxylase/oxygenase (Rubisco), ribulose bisphosphate (RuBP) regeneration or Pi regeneration. Using both theoretical and empirical evidence, we describe the temperature response of instantaneous net CO2 assimilation rate (A) in terms of these limitations, and evaluate possible limitations on A at elevated temperatures arising from heat-induced lability of Rubisco activase. In C3 plants, Rubisco capacity is the predominant limitation on A across a wide range of temperatures at low CO2 (<300 mbar), while at elevated CO2, the limitation shifts to Pi regeneration capacity at suboptimal temperatures, and either electron transport capacity or Rubisco activase capacity at supraoptimal temperatures. In C4 plants, Rubisco capacity limits A below 20°C in chilling-tolerant species, but the control over A at elevated temperature remains uncertain. Acclimation of C3 photosynthesis to suboptimal growth temperature is commonly associated with a disproportional enhancement of the Pi regeneration capacity. Above the thermal optimum, acclimation of A to increasing growth temperature is associated with increased electron transport capacity and/or greater heat stability of Rubisco activase. In many C4 species from warm habitats, acclimation to cooler growth conditions increases levels of Rubisco and C4 cycle enzymes which then enhance A below the thermal optimum. By contrast, few C4 species adapted to cooler habitats increase Rubisco content during acclimation to reduced growth temperature; as a result, A changes little at suboptimal temperatures. Global change is likely to cause a widespread shift in patterns of photosynthetic limitation in higher plants. Limitations in electron transport and Rubisco activase capacity should be more common in the warmer, high CO2 conditions expected by the end of the century.

Global warming and the rise in atmospheric CO(2) will increase the operating temperature of leaves in coming decades, often well above the thermal optimum for photosynthesis. Presently, there is controversy over the limiting processes controlling photosynthesis at elevated temperature. Leading models propose that the reduction in photosynthesis at elevated temperature is a function of either declining capacity of electron transport to regenerate RuBP, or reductions in the capacity of Rubisco activase to maintain Rubisco in an active configuration. Identifying which of these processes is the principal limitation at elevated temperature is complicated because each may be regulated in response to a limitation in the other. Biochemical and gas exchange assessments can disentangle these photosynthetic limitations; however, comprehensive assessments are often difficult and, for many species, virtually impossible. It is proposed that measurement of the initial slope of the CO(2) response of photosynthesis (the A/C(i) response) can be a useful means to screen for Rubisco activase limitations. This is because a reduction in the Rubisco activation state should be most apparent at low CO(2) when Rubisco capacity is generally limiting. In sweet potato, spinach, and tobacco, the initial slope of the A/C(i) response shows no evidence of activase limitations at high temperature, as the slope can be accurately modelled using the kinetic parameters of fully activated Rubisco. In black spruce (Picea mariana), a reduction in the initial slope above 30 degrees C cannot be explained by the known kinetics of fully activated Rubisco, indicating that activase may be limiting at high temperatures. Because black spruce is the dominant species in the boreal forest of North America, Rubisco activase may be an unusually important factor determining the response of the boreal biome to climate change.

C(4) plants are directly affected by all major global change parameters, often in a manner that is distinct from that of C(3) plants. Rising CO(2) generally stimulates C(3) photosynthesis more than C(4), but C(4) species still exhibit positive responses, particularly at elevated temperature and arid conditions where they are currently common. Acclimation of photosynthesis to high CO(2) occurs in both C(3) and C(4) plants, most notably in nutrient-limited situations. High CO(2) aggravates nitrogen limitations and in doing so may favor C(4) species, which have greater photosynthetic nitrogen use efficiency. C(4) photosynthesis is favored by high temperature, but global warming will not necessarily favor C(4) over C(3) plants because the timing of warming could be more critical than the warming itself. C(3) species will likely be favored where harsh winter climates are moderated, particularly where hot summers also become drier and less favorable to C(4) plant growth. Eutrophication of soils by nitrogen deposition generally favors C(3) species by offsetting the superior nitrogen use efficiency of C(4) species; this should allow C(3) species to expand at the expense of C(4) plants. Land-use change and biotic invasions are also important global change factors that affect the future of C(4) plants. Human exploitation of forested landscapes favors C(4) species at low latitude by removing woody competitors and opening gaps in which C(4) grasses can establish. Invasive C(4) grasses are causing widespread forest loss in Asia, the Americas and Oceania by accelerating fire cycles and reducing soil nutrient status. Once established, weedy C(4) grasses can prevent woodland establishment, and thus arrest ecological succession. In sum, in the future, certain C(4) plants will prosper at the expense of C(3) species, and should be able to adjust to the changes the future brings.

Rubisco, the primary photosynthetic carboxylase, evolved 3-4 billion years ago in an anaerobic, high CO(2) atmosphere. The combined effect of low CO(2) and high O(2) levels in the modern atmosphere, and the inability of Rubisco to distinguish completely between CO(2) and O(2), leads to the occurrence of an oxygenation reaction that reduces the efficiency of photosynthesis. Among land plants, C(4) photosynthesis largely solves this problem by facilitating a high CO(2)/O(2) ratio at the site of Rubisco that resembles the atmosphere in which the ancestral enzyme evolved. The prediction that such conditions favor Rubiscos with higher kcat(CO2) and lower CO(2)/O(2) specificity (S(C/O)) is well supported, but the structural basis for the differences between C(3) and C(4) Rubiscos is not clear. Flaveria (Asteraceae) includes C(3), C(3)-C(4) intermediate, and C(4) species with kinetically distinct Rubiscos, providing a powerful system in which to study the biochemical transition of Rubisco during the evolution from C(3) to C(4) photosynthesis. We analyzed the molecular evolution of chloroplast rbcL and nuclear rbcS genes encoding the large subunit (LSu) and small subunit (SSu) of Rubisco from 15 Flaveria species. We demonstrate positive selection on both subunits, although selection is much stronger on the LSu. In Flaveria, two positively selected LSu amino acid substitutions, M309I and D149A, distinguish C(4) Rubiscos from the ancestral C(3) species and statistically account for much of the kinetic difference between the two groups. However, although Flaveria lacks a characteristic "C(4)" SSu, our data suggest that specific residue substitutions in the SSu are correlated with the kinetic properties of Rubisco in this genus.

C(4) plants have been reported to have Rubiscos with higher maximum carboxylation rates (kcat(CO(2))) and Michaelis-Menten constants (K(m)) for CO(2) (K(c)) than the enzyme from C(3) species, but variation in other kinetic parameters between the two photosynthetic pathways has not been extensively examined. The CO(2)/O(2) specificity (S(C/O)), kcat(CO(2)), K(c), and the K(m) for O(2) (K(o)) and RuBP (K(m-RuBP)), were measured at 25 degrees C, in Rubisco purified from 16 species of Flaveria (Asteraceae). Our analysis included two C(3) species of Flaveria, four C(4) species, and ten C(3)-C(4) or C(4)-like species, in addition to other C(4) (Zea mays and Amaranthus edulis) and C(3) (Spinacea oleracea and Chenopodium album) plants. The S(C/O) of the C(4) Flaveria species was about 77 mol mol(-1), which was approximately 5% lower than the corresponding value in the C(3) species. For Rubisco from the C(4) Flaverias kcat(CO(2)) and K(c) were 23% and 45% higher, respectively, than for Rubisco from the C(3) plants. Interestingly, it was found that the K(o) for Rubisco from the C(4) species F. bidentis and F. trinervia were similar to the C(3) Flaveria Rubiscos (approximately 650 microM) while the K(o) for Rubisco in the C(4) species F. kochiana, F. australasica, Z. mays, and A. edulis was reduced more than 2-fold. There were no pathway-related differences in K(m-RuBP). In the C(3)-C(4) species kcat(CO(2)) and K(c) were generally similar to the C(3) Rubiscos, but the K(o) values were more variable. The typical negative relationships were observed between S(C/O) and both kcat(CO(2)) and K(c), and a strongly positive relationship was observed between kcat(CO(2)) and Kc. However, the statistical significance of these relationships was influenced by the phylogenetic relatedness of the species.