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The Physiological Ecology of C4 Photosynthesis

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Part of the Advances in Photosynthesis and Respiration book series (AIPH,volume 9)

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.

Keywords

  • Bundle Sheath
  • Carbon Isotope Ratio
  • Photosynthetic Pathway
  • Chenopodium Album
  • Physiological Ecology

These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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Abbreviations

Ca:

ambient partial pressure of CO2

Ci:

intercellular partial pressure of CO2

N:

nitrogen

NAD(P)-ME:

malic enzyme

NUE:

nitrogen use efficiency

PCK:

PEP carboxykinase

PEP:

phosphoenolpyruvate

PEPCase:

PEP carboxylase

PG:

phosphoglycollate

PPDK:

pyruvatephosphate dikinase

WUE:

water use efficiency

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Sage, R.F., Pearcy, R.W. (2000). The Physiological Ecology of C4 Photosynthesis. In: Leegood, R.C., Sharkey, T.D., von Caemmerer, S. (eds) Photosynthesis. Advances in Photosynthesis and Respiration, vol 9. Springer, Dordrecht. https://doi.org/10.1007/0-306-48137-5_21

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