The Physiological Ecology of C₄ Photosynthesis

Abstract

C₄ photosynthesis is an evolutionary syndrome that concentrates CO₂ around Rubisco and in so doing reduces photorespiratory inhibition of photosynthesis to negligible levels. It is not a single pathway, but a syndrome of functionally similar modifications that utilize phosphoenolpyruvate carboxylation in mesophyll cells, and transport of four-carbon acids to an enlarged bundle sheath tissue where Rubisco is localized. At least 14 distinct types of C₄ photosynthesis have been recognized, reflecting the use of one of three decarboxylating enzymes and one to two cell layers around the periphery of the vascular bundle. Despite substantial variation in how C₄ plants accomplish CO₂ concentration, the net effect on photosynthesis is similar in all forms. Relative to C₃ plants, C₄ plants have enhanced photosynthesis at CO₂ levels below the current atmospheric level of 360 μmol mol⁻¹. Increases in temperature above 25 °C favor C₄ relative to C₃ photosynthesis because photorespiration increases in C₃ species as temperatures rise while in C₄ species it remains minimal. Thus, in the current atmosphere, C₄ species have higher temperature optima relative to C₃ species of similar life form and higher CO₂ assimilation capacity at the temperature optimum. Because rising CO₂ inhibits photorespiration, the photosynthetic advantage of C₄ plants at warmer temperature is reduced or eliminated in high CO₂ conditions. C₄ plants have higher water and nitrogen use efficiencies than C₃ plants. This occurs because the capacity of C₄ systems to saturate Rubisco with CO₂ at low atmospheric CO₂ levels enables C₄ species to operate at lower stomatal conductances and Rubisco contents than C₃ species of equivalent CO₂ assimilation capacity. However, light use efficiency (quantum yield) differences between C₃ and C₄ depend on temperature. At current atmospheric CO₂ levels, C₃ species have higher quantum yields than C₄ plants below about 25 °C but lower above 30 °C. In C₄ plants, quantum yields do not change with temperature and CO₂ variation as they do in C₃ species, but do show differences between the biochemical subtypes. Species using NADP-malic enzyme generally have higher quantum yields than NAD-malic enzyme types for reasons that remain unclear. Differences in CO₂ leak rates had been suggested as a possible cause but recent permeability estimates do not show consistent variation between subtypes.

Ecologically, the C₄ pathway promotes fitness in warm environments receiving greater than approximately 30% of full sunlight intensities. C₄ species are generally absent in environments where average growing season temperatures are less than 15 to 18 °C, yet potentially dominate environments where the growing seasons are on average warmer than 22 °C. In warm climates, the dominance of C₄ species is largely dependent upon the availability of summer precipitation and conditions that inhibit establishment and dominance of woody vegetation. Where soil conditions (arid or infertile) and ecological disturbances such as fire restrict woody vegetation, C₄ species are abundant if not dominant. In general, however, moisture, salinity or low soil fertility have a subordinate role over C₄ abundance in that the dominant factors of temperature and light must be favorable or else C₄ species will not be competitive. Where intermediate temperatures favor neither photosynthetic pathway, however, drought, high salinity and nitrogen deficiency are important secondary controls, and appear to promote C₄ success in environments that otherwise would support C₄ dominance.

In the future, the distribution and abundance of C₄ species may become restricted because C₄ species generally respond more to rising atmospheric CO₂ than C₄ plants. Paleoecology studies indicate that the direct consequences of rising CO₂ will be mostimportant in the tropics, with woodland ecosystems potentially spreading into C₄ grasslands. In temperate zones, paleoecological studies indicate that rising CO₂ and temperature could offset each other. If this occurs, other key ecological controls could become paramount; in particular, changes in the seasonality of precipitation could be important. Everywhere, human land use practices will have to be considered, given that people can radically alter vegetation characteristics depending upon their needs and desires.