C4 carbon fixation

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Kranz anatomy allows C4 carbon fixation.
A: Mesophyll Cell
B: Chloroplast
C: Vascular Tissue
D: Bundle Sheath Cell
E: Stroma
F: Vascular Tissue: provides continuous source of water
1) Carbon is fixed to produce oxaloacetate by PEP carboxylase.
2) The four carbon molecule then exits the cell and enters the chloroplasts of bundle sheath cells.
3) It is then broken down releasing carbon dioxide and producing pyruvate. Carbon dioxide combines with ribulose bisphosphate and proceeds to the Calvin Cycle.
4) Pyruvate re-enters the mesophyll cell. It then reacts with ATP to produce the beginning compound of the C4 cycle.

C4 carbon fixation is one of three biochemical processes, along with C3 and CAM photosynthesis, used to fix carbon. It is named for the 4-carbon molecule present in the first product of carbon fixation in the small subset of plants that use that process, 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 the process of photorespiration. This is achieved in a more efficient environment for RubisCo by shuttling CO2 via malate or aspartate from mesophyll cells 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. C4 plants use PEP carboxylase to capture more CO2 in the mesophyll cells. PEP Carboxylase (3 carbons) binds to CO2 to make oxaloacetic acid (OAA). Then OAA makes malate (4 carbons). Malate enters bundle sheath cells and releases CO2 inside bundle sheath for RuBisCO to work more efficiently. 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 drought, high temperatures, and limitations of nitrogen or CO2, with the more common C3 pathway being more efficient in the other conditions.

C4 pathway[edit]

NADP-ME type of the C4 pathway
NAD-ME type of the C4 pathway
PEPCK type of the C4 pathway

The first experiments indicating that some plants do not use C3 carbon fixation but instead produce malate and aspartate in the first step of carbon fixation were done in the 1950s and early 1960s by Hugo P. Kortschak[1] and Yuri Karpilov.[2] The C4 pathway was elucidated by Marshall Davidson Hatch and C. R. Slack, in Australia, in 1966; it is sometimes called the Hatch-Slack pathway.[3]

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 and oxygenase activity of RuBisCo, some part 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 oxaloacetate 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 HCO3- — 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[edit]

Cross section of a C4 plant, specifically of a maize leaf. Kranz anatomy shown. Drawing based on microscopic images courtesy of Cambridge University Plant Sciences Department.

The C4 plants often possess a characteristic leaf anatomy called kranz anatomy, from the German word for wreath. Their vascular bundles are surrounded by two rings of cells; the inner ring, called bundle sheath cells, contains starch-rich chloroplasts lacking grana, which differ from those in mesophyll cells present as the outer ring. Hence, the chloroplasts are called dimorphic. 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.[4]

Although most C4 plants exhibit kranz anatomy, there are, however, a few species that operate a limited C4 cycle without any distinct bundle sheath tissue. Suaeda aralocaspica, Bienertia cycloptera, Bienertia sinuspersici and Bienertia kavirense (all chenopods) are terrestrial plants that inhabit dry, salty depressions in the deserts of the Middle East. These plants have been shown to operate single-cell C4 CO2-concentrating mechanisms, which are unique among the known C4 mechanisms.[5][6][7][8] Although the cytology of both genera 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.[9]

The evolution and advantages of the C4 pathway[edit]

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. This increased water use efficiency of C4 grasses means that soil moisture is conserved, allowing them to grow for longer in arid environments.[10]

C4 carbon fixation has evolved on up to 40 independent occasions in different families of plants, making it a prime example of convergent evolution.[11] This convergence may have been facilitated by the fact that many potential evolutionary pathways to a C4 phenotype exist, many of which involve initial evolutionary steps not directly related to photosynthesis.[12] C4 plants arose around 25 to 32 million years ago[11] 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.[11] C4 metabolism originated when grasses migrated from the shady forest undercanopy to more open environments,[13] where the high sunlight gave it an advantage over the C3 pathway.[14] 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.[14]

Today, C4 plants represent about 5% of Earth's plant biomass and 3% of its known plant species.[10][15] Despite this scarcity, they account for about 30% of terrestrial carbon fixation.[11] 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 and subtropics (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[edit]

About 7,600 plant species use C4 carbon fixation, which represents about 3% of all terrestrial species of plants. All these 7,600 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.[16][17] 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 1,400 species using it. About 250 of the 1000 species of the related Amaranthaceae also use C4.[10][18]

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

Converting C3 plants to C4[edit]

Given the advantages of C4, a group of scientists from institutions around the world are working on the C4 Rice Project to turn rice, a C3 plant, into a C4 plant by studying the C4 plants corn and Brachypodium.[19] As rice is the world's most important human food—it is the staple food for more than half the planet—having rice that is more efficient at converting sunlight into grain could have significant global benefits towards improving food security. The team claim C4 rice could produce up to 50% more grain—and be able to do it with less water and nutrients.[20][21][22]

The researchers have already identified genes needed for C4 photosynthesis in rice and are now looking towards developing a prototype C4 rice plant. In 2012, the Government of the United Kingdom along with the Bill & Melinda Gates Foundation provided $14 million over 3 years towards the C4 Rice Project at the International Rice Research Institute.[23]

See also[edit]


  1. ^ Nickell, Louis G. (1993). "A tribute to Hugo P. Kortschak: The man, the scientist and the discoverer of C4 photosynthesis". Photosynthesis Research. 35 (2): 201–204. doi:10.1007/BF00014751. 
  2. ^ Hatch, Marshall D. (2002). "C(4) photosynthesis: Discovery and resolution". Photosynthesis Research. 73 (1–3): 251–6. doi:10.1023/A:1020471718805. PMID 16245128. 
  3. ^ 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. doi:10.1042/bj1030660. PMC 1270465free to read. PMID 4292834. Retrieved 2010-04-08. 
  4. ^ Laetsch (1971) Photosynthesis and Photorespiration, eds Hatch, Osmond and Slatyer
  5. ^ Freitag, H; Stichler, W (2000). "A remarkable new leaf type with unusual photosynthetic tissue in a central Asiatic genus of Chenopodiaceae". Plant Biol. 2: 154–160. doi:10.1055/s-2000-9462. 
  6. ^ Voznesenskaya, Elena; Vincent R. Franceschi; Olavi Kiirats; Elena G. Artyusheva; Helmut Freitag; 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. 
  7. ^ 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): 290–301. doi:10.1600/0363644054223684. 
  8. ^ Akhani, H; Chatrenoor, T; Dehghani, M; Khoshravesh, R; Mahdavi, P.; Matinzadeh, Z. (2012). "A new species of Bienertia (Chenopodiaceae) from Iranian salt deserts: a third species of the genus and discovery of a fourth terrestrial C4 plant without Kranz anatomy". Plant Biosystems. 146: 550–559. doi:10.1080/11263504.2012.662921. 
  9. ^ 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 440321free to read. PMID 16661184. 
  10. ^ a b c Sage, Rowan; Russell Monson (1999). "7". C4 Plant Biology. pp. 228–229. ISBN 0-12-614440-0. 
  11. ^ 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 1626541free to read. PMID 16553316. 
  12. ^ Williams BP, Johnston IG, Covshoff S, Hibberd JM (September 2013). "Phenotypic landscape inference reveals multiple evolutionary paths to C₄ photosynthesis". eLife. 2: e00961. doi:10.7554/eLife.00961. PMID 24082995. 
  13. ^ 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 2823882free to read. PMID 20142480. 
  14. ^ 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 2674487free to read. PMID 19324795. 
  15. ^ 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. 
  16. ^ Sage, Rowan; Russell Monson (1999). "16". C4 Plant Biology. pp. 551–580. ISBN 0-12-614440-0. 
  17. ^ Zhu XG, Long SP, Ort DR (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. 
  18. ^ 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. 
  19. ^ Slewinski. "Scarecrow Plays a Role in Establishing Kranz Anatomy in Maize Leaves" (PDF). 
  20. ^ Gilles van Kote (2012-01-24). "Researchers aim to flick the high-carbon switch on rice". The Guardian. Retrieved 2012-11-10. 
  21. ^ Von Caemmerer, S.; Quick, W. P.; Furbank, R. T. (2012). "The Development of C4 Rice: Current Progress and Future Challenges". Science. 336 (6089): 1671–1672. Bibcode:2012Sci...336.1671V. doi:10.1126/science.1220177. PMID 22745421. 
  22. ^ Hibberd, J. M.; Sheehy, J. E.; Langdale, J. A. (2008). "Using C4 photosynthesis to increase the yield of rice—rationale and feasibility". Current Opinion in Plant Biology. 11 (2): 228–231. doi:10.1016/j.pbi.2007.11.002. PMID 18203653. 
  23. ^ Munawan Hasan (2012-11-06). "C4 rice project gets financial boost". The News. Retrieved 2012-11-10. 

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