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 discovery by Marshall Davidson
Hatch and Charles Roger Slack[1] that
some plants, when supplied with 14CO2 ,
incorporate the 14C label into four-carbon
molecules first.
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
 . y u ate ee te s t e esop y ce , ee t s
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, and
catalyses two distinct reactions, with CO2
(carboxylation), and with oxygen
(oxygenation), which gives rise to the
wasteful process of photorespiration. C4
photosythesis reduces photorespiration
by concentrating CO2 around RuBisCO.
To ensure that RuBisCO works in an
environment where there is a lot of
carbon dioxide and very little oxygen, C4
leaves generally differentiate two
partially isolated compartments called
mesophyll cells and bundle-sheath cells.
CO2 is initially fixed in the mesophyll cells
by the enzyme PEP carboxylase which
reacts the three carbon
phosphoenolpyruvate (PEP) with CO2 to
form the four carbon oxaloacetic acid
(OAA). OAA can be chemically reduced to
malate or transaminated to aspartate.
These 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 diffuse 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.

On the one hand, these additional steps

require more energy in the form of ATP
used to regenerate PEP. On the other,
concentrating CO2 allows to overcome
the reduction of gas solubility with
temperatures (Henry's law) allowing high
rates of photosynthesis at high
temperatures. The CO2 concentrating
mechanism also allows to maintain high
gradients of CO2 concentration across
the stomatal pores. This means that C4
plants have generally lower stomatal
conductance, reduce water losses and
have generally higher water use
efficiency.[2] C4 plants are also more
efficient in using nitrogen, since PEP
carboxylase is much 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, like, 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] it is sometimes called the
Hatch–Slack pathway.

Anatomy

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

Cross section of a maize leaf, a C4 plant. Kranz
anatomy (rings of cells) shown

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.
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
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 C4
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.[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 acid is produced then diffuses
through plasmodesmata into the bundle
sheath cells, where 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
fixation of CO2 into oxaloacetate by the
PEP carboxylase enzyme (PEPC). 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, diffucing to the mesophyll.
Alanine is finally transaminated to
pyruvate (PYR) which can be regenerated
to PEP by PPDK in the bundle sheath
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
PEPC. 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 retrodiffsion 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.[14] The
apportioning of excitation energy
between the two cell types will influence
the availability of ATP and NADPH in the
mesohyll 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.[15] 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 limit the amount of light that can be
harvested.[16]

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 retrodiffusion
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[17] 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.[18]

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.[19]

C4 carbon fixation has evolved on up to

61 independent occasions in 19 different
families of plants, making it a prime
example of convergent evolution.[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 did not become
ecologically significant until around
6 to 7 million years ago, in the
Miocene.[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.[19][25] Despite this
scarcity, they account for about 23% of
terrestrial carbon fixation.[22][26]
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.[26][27] 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,[28]
including the Andropogoneae tribe which
contains the food crops maize, sugar
cane, and sorghum. Various kinds of
millet are also C4.[29][30] 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.[19][31]
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.

There are very few trees which use C4.

Only a handful are known: Paulownia,
seven Hawaiian Euphorbia species and a
few desert shrubs that reach the size and
shape of trees with age.[32][33]

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.[34] 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.[35][36][37]

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.[38]

See also
C2 photosynthesis
CAM photosynthesis
C3 photosynthesis

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External links
Khan Academy, video lecture

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