C4 carbon fixation

C4 carbon fixation or the Hatch–Slack pathway is one of three

known photosynthetic processes of carbon fixation in plants. It
owes the names to the 1960s discovery by Marshall Davidson Hatch
and Charles Roger Slack[1] that some plants, when supplied with
14CO incorporate the 14C label into four-carbon molecules first.
2,

Leaf anatomy in most C4 plants.

A: Mesophyll cell
B: Chloroplast
C: Vascular tissue
D: Bundle sheath cell
E: Stoma
F: Vascular tissue
1. CO2 is fixed to produce a four-carbon
molecule (malate or aspartate).
2. The molecule exits the cell and enters the
bundle sheath cells.
3. It is then broken down into CO2 and pyruvate.
CO2 enters the Calvin cycle to produce
carbohydrates.
4. Pyruvate reenters the mesophyll cell, where it
is reused to produce malate or aspartate.
C4 fixation is an addition to the ancestral and more common C3
carbon fixation. The main carboxylating enzyme in C3
photosynthesis is called RuBisCO, which catalyses two distinct
reactions using either CO2 (carboxylation) or oxygen (oxygenation)
as a substrate. RuBisCO oxygenation gives rise to phosphoglycolate,
which is toxic and requires the expenditure of energy to recycle
through photorespiration. C4 photosynthesis reduces
photorespiration by concentrating CO2 around RuBisCO.

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 mesophyll cells and
bundle-sheath cells. CO2 is initially fixed in the mesophyll cells in a
reaction catalysed by the enzyme PEP carboxylase in which the
three-carbon phosphoenolpyruvate (PEP) reacts with CO2 to form
the four-carbon oxaloacetic acid (OAA). OAA can then be reduced to
malate or transaminated to aspartate. These intermediates diffuse
to the bundle sheath cells, where they are decarboxylated, creating a
CO2-rich environment around RuBisCO and thereby suppressing
photorespiration. The resulting pyruvate (PYR), together with about
half of the phosphoglycerate (PGA) produced by RuBisCO, diffuses
back to the mesophyll. PGA is then chemically reduced and diffuses
back to the bundle sheath to complete the reductive pentose
phosphate cycle (RPP). This exchange of metabolites is essential
for C4 photosynthesis to work.

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 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 Peter Kortschak and Yuri Karpilov.[5][6] The C4 pathway was
elucidated by Marshall Davidson Hatch and Charles Roger Slack, in
Australia, in 1966.[1] While Hatch and Slack originally referred to the
pathway as the "C4 dicarboxylic acid pathway", it is sometimes
called the Hatch–Slack pathway.[6]

Anatomy

Cross section of a maize leaf, a C4 plant. Kranz

anatomy (rings of cells) shown

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. Mesophyll and
bundle sheath cells are connected through numerous cytoplasmic
sleeves called plasmodesmata whose permeability at leaf level is
called bundle sheath conductance. A layer of suberin[7] is often
deposed at the level of the middle lamella (tangential interface
between mesophyll and bundle sheath) in order to reduce the
apoplastic diffusion of CO2 (called leakage). The carbon
concentration mechanism in C4 plants distinguishes their isotopic
signature from other photosynthetic organisms.

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.[8][9][10][11] 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 are separated from
decarboxylase enzymes and RuBisCO in the chloroplasts. A
diffusive barrier is 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 C4 cycle to operate, it is relatively
inefficient. Much leakage of CO2 from around RuBisCO occurs.

There is also evidence 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.[12]

Biochemistry
In C3 plants, the first step in the light-independent reactions of
photosynthesis is the fixation of CO2 by the enzyme RuBisCO to
form 3-phosphoglycerate. However, RuBisCo has a dual carboxylase
and oxygenase activity. Oxygenation results in part of the substrate
being oxidized rather than carboxylated, resulting in loss of
substrate and consumption of energy, in what is known as
photorespiration. Oxygenation and carboxylation are competitive,
meaning that the rate of the reactions depends on the relative
concentration of oxygen and CO2.

In order to reduce the rate of photorespiration, C4 plants increase

the concentration of CO2 around RuBisCO. To do so two partially
isolated compartments differentiate within leaves, the mesophyll
and the bundle sheath. Instead of direct fixation by RuBisCO, CO2 is
initially incorporated into a four-carbon organic acid (either malate
or aspartate) in the mesophyll. The organic acids then diffuse
through plasmodesmata into the bundle sheath cells. There, they are
decarboxylated creating a CO2-rich environment. The chloroplasts of
the bundle sheath cells convert this CO2 into carbohydrates by the
conventional C3 pathway.
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-
malic enzyme, NADP-ME; NAD-malic enzyme, NAD-ME; and PEP
carboxykinase, PEPCK). Since PEPCK is often recruited atop NADP-
ME or NAD-ME it was proposed to classify the biochemical
variability in two subtypes. For instance, maize and sugarcane use a
combination of NADP-ME and PEPCK, millet uses preferentially
NAD-ME and Megathyrsus maximus, uses preferentially PEPCK.

NADP-ME

NADP-ME subtype

The first step in the NADP-ME type C4 pathway is the conversion of

pyruvate (Pyr) to phosphoenolpyruvate (PEP), by the enzyme
Pyruvate phosphate dikinase (PPDK). This reaction requires
inorganic phosphate and ATP plus pyruvate, producing PEP, AMP,
and inorganic pyrophosphate (PPi). The next step is the
carboxylation of PEP by the PEP carboxylase enzyme (PEPC)
producing oxaloacetate. Both of these steps occur in the mesophyll
cells:
 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 malate (M), which diffuses to

the bundle-sheath cells surrounding a nearby vein. Here, it is
decarboxylated by the NADP-malic enzyme (NADP-ME) to produce
CO2 and pyruvate. The CO2 is fixed by RuBisCo to produce
phosphoglycerate (PGA) while the pyruvate is transported back to
the mesophyll cell, together with about half of the phosphoglycerate
(PGA). This PGA is chemically reduced in the mesophyll and
diffuses back to the bundle sheath where it enters the conversion
phase of the Calvin cycle. For each CO2 molecule exported to the
bundle sheath the malate shuttle transfers two electrons, and
therefore reduces the demand of reducing power in the bundle
sheath.
NAD-ME

NAD-ME subtype

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

PEPCK subtype
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 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.[18]

C4 carbon fixation has evolved in up to 61 independent occasions in

19 different families of plants, making it a prime example of
convergent evolution.[19] 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.[20] C4 plants arose around
35 (https://geoltime.github.io/?Ma=35) million years ago[19] during
the Oligocene (precisely when is difficult to determine) and did not
become ecologically significant until around
6 to 7 (https://geoltime.github.io/?Ma=6%E2%80%937) million years ago
, in the Miocene.[21] C4 metabolism in grasses originated when their
habitat migrated from the shady forest undercanopy to more open
environments,[22] where the high sunlight gave it an advantage over
the C3 pathway.[23] 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.[23]
Today, C4 plants represent about 5% of Earth's plant biomass and 3%
of its known plant species.[18][24] Despite this scarcity, they account
for about 23% of terrestrial carbon fixation.[21][25] 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 degrees) where the high air temperature
increases rates of photorespiration in C3 plants.

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.[25][26] All these 8,100
species are angiosperms. C4 carbon fixation is more common in
monocots compared with dicots, with 40% of monocots using the
C4 pathway, compared with only 4.5% of dicots. Despite this, only
three families of monocots use 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.
46% of grasses are C4 and together account for 61% of C4 species.
C4 has arisen independently in the grass family some twenty or
more times, in various subfamilies, tribes, and genera,[27] including
the Andropogoneae tribe which contains the food crops maize,
sugar cane, and sorghum. Various kinds of millet are also C4.[28][29]
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 1,000 species of the related
Amaranthaceae also use C4.[18][30]

Members of the sedge family Cyperaceae, and members of

numerous families of eudicots – including Asteraceae (the daisy
family), Brassicaceae (the cabbage family), and Euphorbiaceae (the
spurge family) – also use C4.

No large trees (above 15 m in height) use C4,[31] 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.[32]

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 rice, naturally a C3 plant, that uses the C4 pathway by
studying the C4 plants maize and Brachypodium.[33] 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.[34][35][36]

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.[37] 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.[38]

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.[39] In 2021, the UK Government provided £1.2 million
on studying C2 engineering.[40]

See also
C2 photosynthesis
CAM photosynthesis
 C3 photosynthesis

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External links
Khan Academy, video lecture (https://www.khanacademy.org/vide
o/c-4-photosynthesis?playlist=Biology)

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