C4 carbon fixation

C₄ carbon fixation is one of three biochemical mechanisms, along with C₃ and CAM photosynthesis, used in carbon fixation. It is named for the 4-carbon molecule present in the first product of carbon fixation in these plants, in contrast to the 3-carbon molecule products in C₃ plants.

C₄ fixation is an elaboration of the more common C₃ carbon fixation and is believed to have evolved more recently. C₄ and CAM overcome the tendency of the enzyme RuBisCO to wastefully fix oxygen rather than carbon dioxide in what is called photorespiration. This is achieved by using a more efficient enzyme to fix CO₂ in mesophyll cells and shuttling this fixed carbon via malate or asparate to bundle-sheath cells. In these bundle-sheath cells, RuBisCO is isolated from atmospheric oxygen and saturated with the CO₂ released by decarboxylation of the malate or oxaloacetate. These additional steps, however, require more energy in the form of ATP. Because of this extra energy requirement, C₄ plants are able to more efficiently fix carbon in only certain conditions, with the more common C₃ pathway being more efficient in other conditions.

C₄ pathway

NADP-ME type of the C4 pathway

NAD-ME type of the C4 pathway

PEPCK type of the C4 pathway

The C₄ pathway was discovered by Dr. Marshall Davidson Hatch and C. R. Slack, in Australia, in 1966, so it is sometimes called the Hatch-Slack pathway.^[1]

In C₃ plants, the first step in the light-independent reactions of photosynthesis involves the fixation of CO₂ by the enzyme RuBisCO into 3-phosphoglycerate. However, due to the dual carboxylase / oxygenase activity of RuBisCo, an amount of the substrate is oxidized rather than carboxylated, resulting in loss of substrate and consumption of energy, in what is known as photorespiration. In order to bypass the photorespiration pathway, C₄ plants have developed a mechanism to efficiently deliver CO₂ to the RuBisCO enzyme. They utilize their specific leaf anatomy where chloroplasts exist not only in the mesophyll cells in the outer part of their leaves but in the bundle sheath cells as well. Instead of direct fixation to RuBisCO in the Calvin cycle, CO₂ is incorporated into a 4-carbon organic acid, which has the ability to regenerate CO₂ in the chloroplasts of the bundle sheath cells. Bundle sheath cells can then utilize this CO₂ to generate carbohydrates by the conventional C₃ pathway.

The first step in the pathway is the conversion of pyruvate to phosphoenolpyruvate (PEP), by the enzyme pyruvate orthophosphate dikinase. This reaction requires inorganic phosphate and ATP plus pyruvate, producing phosphoenolpyruvate, AMP, and inorganic pyrophosphate (PPi). The next step is the fixation of CO₂ into PEP by the enzyme PEP carboxylase. Both of these steps occur in the mesophyll cells:

pyruvate + Pi + ATP → PEP + AMP + PPi

PEP + CO₂ → oxaloacetate

PEP carboxylase has a lower Km for CO₂ — and, hence, higher affinity — than RuBisCO. Furthermore, O₂ is a very poor substrate for this enzyme. Thus, at relatively low concentrations of CO₂, most CO₂ will be fixed by this pathway.

The product is usually converted to malate, a simple organic compound, which is transported to the bundle-sheath cells surrounding a nearby vein. Here, it is decarboxylated to produce CO₂ and pyruvate. The CO₂ now enters the Calvin cycle and the pyruvate is transported back to the mesophyll cell.

Since every CO₂ molecule has to be fixed twice, first by 4-carbon organic acid and second by RuBisCO, the C₄ pathway uses more energy than the C₃ pathway. The C₃ pathway requires 18 molecules of ATP for the synthesis of one molecule of glucose, whereas the C₄ pathway requires 30 molecules of ATP. This energy debt is more than paid for by avoiding losing more than half of photosynthetic carbon in photorespiration as occurs in some tropical plants,^{[citation needed]} making it an adaptive mechanism for minimizing the loss.

There are several variants of this pathway:

1. The 4-carbon acid transported from mesophyll cells may be malate, as above, or aspartate
2. The 3-carbon acid transported back from bundle-sheath cells may be pyruvate, as above, or alanine
3. The enzyme that catalyses decarboxylation in bundle-sheath cells differs. In maize and sugarcane, the enzyme is NADP-malic enzyme; in millet, it is NAD-malic enzyme; and, in Panicum maximum, it is PEP carboxykinase.

C₄ leaf anatomy

The C₄ plants often possess a characteristic leaf anatomy. Their vascular bundles are surrounded by two rings of cells, the inner ring, called bundle sheath cells, contain starch-rich chloroplasts lacking grana, which differ from those in mesophyll cells present as the outer ring. Hence, the chloroplasts are called dimorphic. This peculiar anatomy is called kranz anatomy, from the German word for wreath. The primary function of kranz anatomy is to provide a site in which CO₂ can be concentrated around RuBisCO, thereby avoiding photorespiration. In order to maintain a significantly higher CO₂ concentration in the bundle sheath compared to the mesophyll, the boundary layer of the kranz has a low conductance to CO₂, a property that may be enhanced by the presence of suberin.^[2]

Although most C₄ plants exhibit kranz anatomy, there are many species that operate a limited C₄ cycle without any distinct bundle sheath tissue. Suaeda aralocaspica, Bienertia cycloptera and Bienertia sinuspersici (all chenopods) are terrestrial plants that inhabit dry, salty depressions in the deserts of south-east Asia. These plants have been shown to operate single-cell C₄ CO₂-concentrating mechanisms, which are unique among the known C₄ mechanisms.^[3][4][5] Although the cytology of both species differs slightly, the basic principle is that fluid-filled vacuoles are employed to divide the cell into two separate areas. Carboxylation enzymes in the cytosol can, therefore, be kept separate from decarboxylase enzymes and RuBisCO in the chloroplasts, and a diffusive barrier can be established between the chloroplasts (which contain RuBisCO) and the cytosol. This enables a bundle-sheath-type area and a mesophyll-type area to be established within a single cell. Although this does allow a limited C₃ cycle to operate, it is relatively inefficient, with the occurrence of much leakage of CO₂ from around RuBisCO. There is also evidence for the exhibiting of inducible C₄ photosynthesis by non-kranz aquatic macrophyte Hydrilla verticillata under warm conditions, although the mechanism by which CO₂ leakage from around RuBisCO is minimised is currently uncertain.^[6]

The evolution and advantages of the C₄ pathway

Further information: Evolutionary history of plants#Advances in metabolism

C₄ plants have a competitive advantage over plants possessing the more common C₃ carbon fixation pathway under conditions of drought, high temperatures, and nitrogen or CO₂ limitation. When grown in the same environment, at 30°C, C₃ grasses lose approximately 833 molecules of water per CO₂ molecule that is fixed, whereas C₄ grasses lose only 277 water molecules per CO₂ molecule fixed. This increased water use efficiency of C₄ grasses means that soil moisture is conserved, allowing them to grow for longer in arid environments.^[7]

C₄ carbon fixation has evolved on up to 40 independent occasions in different families of plants, making it a prime example of convergent evolution.^[8] C₄ plants arose around 25 to 32 million years ago^[8] during the Oligocene (precisely when is difficult to determine) and did not become ecologically significant until around 6 to 7 million years ago, in the Miocene Period.^[8] C₄ metabolism originated when grasses migrated from the shady forest undercanopy to more open environments,^[9] where the high sunlight gave it an advantage over the C₃ pathway.^[10] Drought was not necessary for its innovation; rather, the increased resistance to water stress was a by-product of the pathway and allowed C₄ plants to more readily colonise arid environments.^[10]

Today, C₄ plants represent about 5% of Earth's plant biomass and 1% of its known plant species.^[11] Despite this scarcity, they account for about 30% of terrestrial carbon fixation.^[8] Increasing the proportion of C4 plants on earth could assist biosequestration of CO₂ and represent an important climate change avoidance strategy. Present-day C₄ plants are concentrated in the tropics (below latitudes of 45°) where the high air temperature contributes to higher possible levels of oxygenase activity by RuBisCO, which increases rates of photorespiration in C₃ plants.

Plants that use C₄ carbon fixation

About 7600 species of plants use C₄ carbon fixation, which represents about 3% of all terrestrial species of plants. All these 7600 species are angiosperms. C₄ carbon fixation is less common in dicots than in monocots, with only 4.5% of dicots using the C₄ pathway, compared to 40% of monocots. Despite this, only three families of monocots utilise C₄ carbon fixation compared to 15 dicot families. Of the monocot clades containing C₄ plants, the grass (Poaceae) species use the C₄ photosynthetic pathway most. Forty-six percent of grasses are C₄ and together account for 61% of C₄ species. These include the food crops maize, sugar cane, millet, and sorghum.^[7][12] Of the dicot clades containing C₄ species, the order, Caryophyllales contains the most species. Of the families in the Caryophyllales, the Chenopodiaceae use C₄ carbon fixation the most, with 550 out of 1400 species using it. About 250 of the 1000 species of the related Amaranthaceae also use C₄.^[7][13]

Members of the sedge family Cyperaceae, and numerous families of Eudicots, including the daisies Asteraceae, cabbages Brassicaceae, and spurges Euphorbiaceae also use C₄.

See also

• C₃ carbon fixation
• CAM Photosynthesis

External links

• Khan Academy, video lecture

References

1. ^ Slack, CR; Hatch, MD (1967). "Comparative studies on the activity of carboxylases and other enzymes in relation to the new pathway of photosynthetic carbon dioxide fixation in tropical grasses" (PDF). The Biochemical journal 103 (3): 660–5. PMC 1270465. PMID 4292834. http://www.biochemj.org/bj/103/0660/1030660.pdf. Retrieved 2010-04-08. 
2. ^ Laetsch (1971) Photosynthesis and Photorespiration, eds Hatch, Osmond and Slatyer
3. ^ Wang, L.; Huang, Z.; Baskin, C. C.; Baskin, J. M.; Dong, M. (2008). "Germination of Dimorphic Seeds of the Desert Annual Halophyte Suaeda aralocaspica (Chenopodiaceae), a C4 Plant without Kranz Anatomy". Annals of Botany 102 (5): 757–69. doi:10.1093/aob/mcn158. PMC 2712381. PMID 18772148. http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pmcentrez&artid=2712381. 
4. ^ Voznesenskaya, Elena; Vincent R. Franceschi, Olavi Kiirats, Elena G. Artyusheva, Helmut Freitag and Gerald E. Edwards (2002). "Proof of C4 photosynthesis without Kranz anatomy in Bienertia cycloptera (Chenopodiaceae)". The Plant Journal 31 (5): 649–662. doi:10.1046/j.1365-313X.2002.01385.x. PMID 12207654. 
5. ^ Akhani, Hossein; Barroca, João; Koteeva, Nuria; Voznesenskaya, Elena; Franceschi, Vincent; Edwards, Gerald; Ghaffari, Seyed Mahmood; Ziegler, Hubert (2005). "Bienertia sinuspersici (Chenopodiaceae): A New Species from Southwest Asia and Discovery of a Third Terrestrial C₄ Plant Without Kranz Anatomy". Systematic Botany 30 (2): 290. doi:10.1600/0363644054223684. 
6. ^ Holaday, A. S.; Bowes, G. (1980). "C4 Acid Metabolism and Dark CO2 Fixation in a Submersed Aquatic Macrophyte (Hydrilla verticillata)". Plant Physiology 65 (2): 331–5. doi:10.1104/pp.65.2.331. PMC 440321. PMID 16661184. http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pmcentrez&artid=440321. 
7. ^ ^{a b c} Sage, Rowan; Russell Monson (1999). "7". C4 Plant Biology. pp. 228–229. ISBN 0126144400. http://books.google.com/?id=H7Wv9ZImW-QC&pg=PA228. 
8. ^ ^{a b c d} Osborne, C.P.; Beerling, D.J. (2006). "Nature's green revolution: the remarkable evolutionary rise of C4 plants". Philosophical Transactions of the Royal Society B: Biological Sciences 361 (1465): 173–194. doi:10.1098/rstb.2005.1737. PMC 1626541. PMID 16553316. http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pmcentrez&artid=1626541. 
9. ^ Edwards, E. J.; Smith, S. A. (2010). "Phylogenetic analyses reveal the shady history of C4 grasses". Proceedings of the National Academy of Sciences 107 (6): 2532–7. Bibcode 2010PNAS..107.2532E. doi:10.1073/pnas.0909672107. PMC 2823882. PMID 20142480. http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pmcentrez&artid=2823882. 
10. ^ ^{a b} Osborne, C. P.; Freckleton, R. P. (2009). "Ecological selection pressures for C4 photosynthesis in the grasses". Proceedings of the Royal Society B: Biological Sciences 276 (1663): 1753–60. doi:10.1098/rspb.2008.1762. PMC 2674487. PMID 19324795. http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pmcentrez&artid=2674487. 
11. ^ Bond, W.J.; Woodward, F.I.; Midgley, G.F. (2005). "The global distribution of ecosystems in a world without fire". New Phytologist 165 (2): 525–538. doi:10.1111/j.1469-8137.2004.01252.x. PMID 15720663. 
12. ^ Zhu, Xin-Guang,Long, Stephen P;Ort, R Donald (2008). "What is the maximum efficiency with which photosynthesis can convert solar energy into biomass?". Current Opinion in Biotechnology 19 (2): 153–159. doi:10.1016/j.copbio.2008.02.004. PMID 18374559. 
13. ^ Kadereit, G; Borsch,T; Weising,K; Freitag, H (2003). "Phylogeny of Amaranthaceae and Chenopodiaceae and the Evolution of C4 Photosynthesis". International Journal of Plant Sciences 164 (6): 959–86. doi:10.1086/378649.