C4 carbon fixation
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Carbon cycle |
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C4 carbon fixation or the Hatch–Slack pathway is one of three known
C4 fixation is an addition to the ancestral and more common
To enable RuBisCO to work in an environment where there is a lot of carbon dioxide and very little oxygen, C4 leaves generally contain two partially isolated compartments called
Additional biochemical steps require more energy in the form of ATP to regenerate PEP, but concentrating CO2 allows high rates of photosynthesis at higher temperatures. Higher CO2 concentration overcomes the reduction of gas solubility with temperature (Henry's law). The CO2 concentrating mechanism also maintains high gradients of CO2 concentration across the stomatal pores. This means that C4 plants have generally lower stomatal conductance, reduced water losses and have generally higher water-use efficiency.[2] C4 plants are also more efficient in using nitrogen, since PEP carboxylase is cheaper to make than RuBisCO.[3] However, since the C3 pathway does not require extra energy for the regeneration of PEP, it is more efficient in conditions where photorespiration is limited, typically at low temperatures and in the shade.[4]
Discovery
The first experiments indicating that some plants do not use
Anatomy
C4 plants often possess a characteristic
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.
There is also evidence of inducible C4 photosynthesis by non-kranz aquatic
Biochemistry
In
In order to reduce the rate of
There is large variability in the biochemical features of C4 assimilation, and it is generally grouped in three subtypes, differentiated by the main enzyme used for decarboxylation (
NADP-ME
- pyruvate + Pi + ATP → PEP + AMP + PPi
- PEP + CO2 → oxaloacetate
PEPC has a low KM for HCO−
3 — and, hence, high affinity, and is not confounded by O2 thus it will work even at low concentrations of CO2.
The product is usually converted to
NAD-ME
Here, the OAA produced by PEPC is transaminated by aspartate aminotransferase to aspartate (ASP) which is the metabolite diffusing to the bundle sheath. In the bundle sheath ASP is transaminated again to OAA and then undergoes a futile reduction and oxidative decarboxylation to release CO2. The resulting Pyruvate is transaminated to alanine, diffusing to the mesophyll. Alanine is finally transaminated to pyruvate (PYR) which can be regenerated to PEP by PPDK in the mesophyll chloroplasts. This cycle bypasses the reaction of malate dehydrogenase in the mesophyll and therefore does not transfer reducing equivalents to the bundle sheath.
PEPCK
In this variant the OAA produced by aspartate aminotransferase in the bundle sheath is decarboxylated to PEP by PEPCK. The fate of PEP is still debated. The simplest explanation is that PEP would diffuse back to the mesophyll to serve as a substrate for PEPC. Because PEPCK uses only one ATP molecule, the regeneration of PEP through PEPCK would theoretically increase photosynthetic efficiency of this subtype, however this has never been measured. An increase in relative expression of PEPCK has been observed under low light, and it has been proposed to play a role in facilitating balancing energy requirements between mesophyll and bundle sheath.
Metabolite exchange
While in C3 photosynthesis each chloroplast is capable of completing light reactions and dark reactions, C4 chloroplasts differentiate in two populations, contained in the mesophyll and bundle sheath cells. The division of the photosynthetic work between two types of chloroplasts results inevitably in a prolific exchange of intermediates between them. The fluxes are large and can be up to ten times the rate of gross assimilation.[13] The type of metabolite exchanged and the overall rate will depend on the subtype. To reduce product inhibition of photosynthetic enzymes (for instance PECP) concentration gradients need to be as low as possible. This requires increasing the conductance of metabolites between mesophyll and bundle sheath, but this would also increase the retro-diffusion of CO2 out of the bundle sheath, resulting in an inherent and inevitable trade off in the optimisation of the CO2 concentrating mechanism.
Light harvesting and light reactions
To meet the NADPH and ATP demands in the mesophyll and bundle sheath, light needs to be harvested and shared between two distinct electron transfer chains. ATP may be produced in the bundle sheath mainly through cyclic electron flow around Photosystem I, or in the M mainly through linear electron flow depending on the light available in the bundle sheath or in the mesophyll. The relative requirement of ATP and NADPH in each type of cells will depend on the photosynthetic subtype.[13] The apportioning of excitation energy between the two cell types will influence the availability of ATP and NADPH in the mesophyll and bundle sheath. For instance, green light is not strongly adsorbed by mesophyll cells and can preferentially excite bundle sheath cells, or vice versa for blue light.[14] Because bundle sheaths are surrounded by mesophyll, light harvesting in the mesophyll will reduce the light available to reach BS cells. Also, the bundle sheath size limits the amount of light that can be harvested.[15]
Efficiency
Different formulations of efficiency are possible depending on which outputs and inputs are considered. For instance, average quantum efficiency is the ratio between gross assimilation and either absorbed or incident light intensity. Large variability of measured quantum efficiency is reported in the literature between plants grown in different conditions and classified in different subtypes but the underpinnings are still unclear. One of the components of quantum efficiency is the efficiency of dark reactions, biochemical efficiency, which is generally expressed in reciprocal terms as ATP cost of gross assimilation (ATP/GA).
In C3 photosynthesis ATP/GA depends mainly on CO2 and O2 concentration at the carboxylating sites of RuBisCO. When CO2 concentration is high and O2 concentration is low photorespiration is suppressed and C3 assimilation is fast and efficient, with ATP/GA approaching the theoretical minimum of 3.
In C4 photosynthesis CO2 concentration at the RuBisCO carboxylating sites is mainly the result of the operation of the CO2 concentrating mechanisms, which cost circa an additional 2 ATP/GA but makes efficiency relatively insensitive of external CO2 concentration in a broad range of conditions.
Biochemical efficiency depends mainly on the speed of CO2 delivery to the bundle sheath, and will generally decrease under low light when PEP carboxylation rate decreases, lowering the ratio of CO2/O2 concentration at the carboxylating sites of RuBisCO. The key parameter defining how much efficiency will decrease under low light is bundle sheath conductance. Plants with higher bundle sheath conductance will be facilitated in the exchange of metabolites between the mesophyll and bundle sheath and will be capable of high rates of assimilation under high light. However, they will also have high rates of CO2 retro-diffusion from the bundle sheath (called leakage) which will increase photorespiration and decrease biochemical efficiency under dim light. This represents an inherent and inevitable trade off in the operation of C4 photosynthesis. C4 plants have an outstanding capacity to attune bundle sheath conductance. Interestingly, bundle sheath conductance is downregulated in plants grown under low light[16] and in plants grown under high light subsequently transferred to low light as it occurs in crop canopies where older leaves are shaded by new growth.[17]
Evolution and advantages
C4 plants have a competitive advantage over plants possessing the more common
C4 carbon fixation has evolved in at least 62 independent occasions in 19 different families of plants, making it a prime example of convergent evolution.[19][20] 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.[21] C4 plants arose around 35 million years ago[20] during the Oligocene (precisely when is difficult to determine) and were becoming ecologically significant in the early Miocene around 21 million years ago.[22] C4 metabolism in grasses originated when their habitat migrated from the shady forest undercanopy to more open environments,[23] where the high sunlight gave it an advantage over the C3 pathway.[24] Drought was not necessary for its innovation; rather, the increased parsimony in water use was a byproduct of the pathway and allowed C4 plants to more readily colonize arid environments.[24]
Today, C4 plants represent about 5% of Earth's plant biomass and 3% of its known plant species.
Plants that use C4 carbon fixation
About 8,100 plant species use C4 carbon fixation, which represents about 3% of all terrestrial species of plants.
Members of the sedge family
No large trees (above 15 m in height) use C4,[33] however a number of small trees or shrubs smaller than 10 m exist which do: six species of Euphorbiaceae all native to Hawaii and two species of Amaranthaceae growing in deserts of the Middle-East and Asia.[34]
Converting C3 plants to C4
Given the advantages of C4, a group of scientists from institutions around the world are working on the C4 Rice Project to produce a strain of
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 US$14 million over three years towards the C4 Rice Project at the International Rice Research Institute.[39] In 2019, the Bill & Melinda Gates Foundation granted another US$15 million to the Oxford-University-led C4 Rice Project. The goal of the 5-year project is to have experimental field plots up and running in Taiwan by 2024.[40]
C2 photosynthesis, an intermediate step between C3 and Kranz C4, may be preferred over C4 for rice conversion. The simpler system is less optimized for high light and high temperature conditions than C4, but has the advantage of requiring fewer steps of genetic engineering and performing better than C3 under all temperatures and light levels.[41] In 2021, the UK Government provided £1.2 million on studying C2 engineering.[42]
See also
- C2 photosynthesis
- CAM photosynthesis
- C3 photosynthesis
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