C4 Photosynthesis

C4 plants are plants that undergo a specialised extrametabolic pathway, the C4 cycle, in which CO2 is transferred from mesophyll cells to a special ring of bundle sheath cells by a pump. CO2 gets dissolved by carbonic anhydrase, forming bicarbonate, which is then fixed with phosphoenolpyruvate carboxylase into C4 oxaloacetic acid (hence the name), which is then converted to malate. This diffuses to the bundle sheath ring through plasmodesmata, where the CO2 is set free by decarboxylases, including the all-important RuBisCo (Hatch, 1987). Regular C3 photosynthesis occurs, but under the locally very high CO2 concentrations 3-8x higher than other area of the leaf.

The net result is a minimisation of CO2 loss through photorespiration, a reduction in use of stomata leading to less water loss through transpiration, and a much higher rate of photosynthesis, at the cost of substantial energy needed to drive the CO2 pump, energy acquired from sunlight. C4 plants are also more efficient in using nitrogen, since they need to use less enzymes to maintain their higher photosynthetic rates (Pearcy & Ehleringer, 1984).

In practical ecological terms, what those advantages bring is either an ability to grow faster than C3 plants, or an ability to grow in more challenging environments than C3 plants (Hatch, 1987).

The reason why C4 photosynthesis works is the evolutionary history of C3 enzymes, especially the main one, RuBisCo. RuBisCo evolved back in the times when the atmosphere contained very little oxygen and 100x more CO2 than today (Rye et al., 1995). Therefore, all that C4 photosynthesis does is recreate that atmosphere very locally around the enzyme so that it acts in the environment it evolved to be optimal in, namely an atmosphere with very high CO2 and low O2, so that the competitive inhibition of RuBisCo by O2 is eliminated. For those with engineering experience, C4 photosynthesis works just like a supercharged combustion engine.

Although only 3% of vascular plant species undergo C4 photosynthesis, those plants are responsible for almost a quarter of the photosynthesis that happens on land (Lloyd & Farquhar, 1994). Its evolution is therefore quite an important development not only from a physiological perspective, but also from an ecological one.

C4 metabolism evolved convergently from regular C3 photosynthesis in over 45 land plant families, both monocot and dicot (Sage, 2004), as a result of the steady depletion atmospheric CO2 levels between 40-15 Ma (Edwards & Smith, 2010). This reduction in CO2 levels led to inefficiency in carbon uptake in land plants, especially those in warm and arid landscapes (most C4 plants are grasses), providing a strong selective pressure to reduce photorespiration, and by the Pliocene, C4 grasslands had displaced C3 grasslands in lower latitudes. Tropical grasslands and savannahs are dominated by C4 plants, as are many breakfast tables (Sorghum, maize, and sugarcane are all C4). At higher latitudes, the cost of driving the CO2 pump outweighs the gains: the C4 vs. C3 biogeographical dominance has a threshold defined by temperature (Ehleringer et al., 1997), with C4 plants dominating in warm temperatures and C3s in cold temperatures (the distinction also applies with altitudinal gradients). Other important factors influencing distribution are moisture/precipitation and light intensity.

Water plays a large role in the distributional patterns of C4 and C3 plants. C3 plants dominate in low latitude rainforests because of the abundance of water: C4 plants may be very efficient, but that doesn’t hold a candle to the high growth rates achieveable by C3 plants when environmental variables are ideal, e.g. when there is an overabundance of water. (THanks to Don Strong in the comments for pointing this out!)

There are no novel enzymes involved in C4 photosynthesis, it is all achieved using cooption of pre-existing enzymes and changes in their expression patterns causing the enzymes to accumulate to various levels in the mesophyll and bundle sheath cells. These changes are pretty complicated considering that they involve 20-30 unlinked genes (Wyrich et al., 1998) – it’s remarkable that this all evolved convergently so many times. We know of some intermediate species exhibiting some “proto-C4” characteristics, e.g. several species in the Neurachne, Flaveria, Parthenium, Mollugo, and Alternanthera genera (list just random examples I dug up, there are definitely more!). Xu et al. (2012) show that both C3 and C4 pathways work at the same time in the alga Ulva prolifera.

It’s also worth noting that some unique lineages have managed to make a C4 mechanism that takes place within individual cells rather than in different tissues, see Keeley (1998) for examples.

References:

Edwards EJ & Smith SA. 2010. Phylogenetic analyses reveal the shady history of C4 grasses. PNAS 107, 2532-2537.

Ehleringer JR, Cerling TE & Helliker BR. 1997. C4 photosynthesis, atmospheric CO2, and climate. Oecologia 112, 285-299.

Hatch MD. 1987. C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochimica et Biophysica Acta 895, 81-106.

Keeley JE. 1998. C4 photosynthetic modifications in the evolutionary transition from land to water in aquatic grasses. Oecologia 116, 85-97.

Lloyd J & Farquhar GD. 1994. 13C discrimination during CO2 assimilation by the terrestrial biosphere. Oecologia 99, 201-215.

Pearcy RW & Ehleringer J. 1984. Comparative ecophysiology of C3 and C4 plants. Plant, Cell & Environment 7, 1-13.

Rye R, Kuo PH & Holland HD. 1995. Atmospheric carbon dioxide concentrations before 2.2 billion years ago. Nature 378, 603-605.

Sage RF. 2004. The evolution of C4 photosynthesis. New Phytologist 161, 341-370.

Wyrich R, Dressen U, Brockmann S, Streubel M, Chang C, Qiang D, Paterson AH & Westhoff P. 1998. The molecular basis of C4 photosynthesis in sorghum: isolation, characterization and RFLP mapping of mesophyll- and bundle-sheath-specific cDNAs obtained by differential screening. Plant Molecular Biology 37, 319-335.

Xu J, Fan X, Zhang X, Xu D, Mou S, Cao S, Zheng Z, Miao J & Ye N. 2012. Evidence of Coexistence of C3 and C4 Photosynthetic Pathways in a Green-Tide-Forming Alga, Ulva prolifera. PLoS ONE 7, e37438.

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