Yuri Nakajima Munekage* and Yukimi Y. Taniguchi
School of Science and Technology, Kwansei Gakuin University, 2-1 Gakuen, Sanda, Hyogo, 669-1337 Japan
*Corresponding author: E-mail, [email protected]; Fax, +81-79-565-7030.
(Received September 30, 2015; Accepted January 11, 2016)
C4 photosynthesis is present in approximately 7,500 species
classified into 19 families, including monocots and eudicots.
In the majority of documented cases, a two-celled CO2concentrating system that uses a metabolic cycle of
four-carbon compounds is employed. C4 photosynthesis repeatedly evolved from C3 photosynthesis, possibly driven by
the survival advantages it bestows in the hot, often dry, and
nutrient-poor soils of the tropics and subtropics. The development of the C4 metabolic cycle greatly increased the ATP
demand in chloroplasts during the evolution of malic
enzyme-type C4 photosynthesis, and the additional ATP
required for C4 metabolism may be produced by the cyclic
electron transport around PSI. Recent studies have revealed
the nature of cyclic electron transport and the elevation of its
components during C4 evolution. In this review, we discuss
the energy requirements of C3 and C4 photosynthesis, the
current model of cyclic electron transport around PSI and
how cyclic electron transport is promoted during C4 evolution using studies on the genus Flaveria, which contains a
number of closely related C3, C4 and C3–C4 intermediate
species.
Keywords: C4 evolution C4 photosynthesis Cyclic electron transport around photosystem I Genus Flaveria.
Abbreviations: BS, bundle sheath; M, mesophyll; NAD-ME,
NAD-malic enzyme; NADP-ME, NADP-malic enzyme; NDH,
NADH dehydrogenase; PEP-CK, phosphoenolpyruvate carboxykinase; 3-PGA, 3-phosphoglyceric acid; PGR5, PROTON
GRADIENT REGULATION 5; PGRL1, PGR5-like 1; RuBisCO,
ribulose-1.5-bisphosphate carboxylase/oxygenase; triose-P,
triose-phosphate.
Energy Requirements in the C3 and C4
Metabolic Cycle, and Photorespiration
In C3 photosynthesis, the first step of CO2 fixation involves
ribulose-1.5-bisphosphate carboxylase/oxygenase (RuBisCO)
in the C3 cycle in the chloroplasts of mesophyll (M) cells. To
drive the C3 cycle, three ATP and two NADPH molecules are
required per fixed CO2 in the chloroplast (Osmond 1981).
RuBisCO can also fix O2 instead of CO2, resulting in the production of 2-phosphoglycolate, which is metabolized by photorespiration, but it increases energy costs and releases CO2.
At atmospheric levels of CO2, the RuBisCO oxygenation
reaction proceeds at approximately a quarter of the rate of
the RuBisCO carboxylation reaction (Kubein et al. 2008)
where 4.43 ATP and 2.86 NADPH molecules are required per
CO2 fixation. At the CO2 compensation point, the RuBisCO
oxygenation reaction proceeds at twice the rate of the
RuBisCO carboxylation reaction. In this condition, 10 ATP
and 6 NADPH molecules are required for the re-fixation of
each molecule of CO2 evolved in photorespiration and there
is no net CO2 fixation, meaning that energys produced by
photosynthetic electron transport is used only to drive the
metabolic cycle of 2-phosphoglycolate (Osmond 1981).
Therefore, the required ATP/NADPH ratio for C3 photosynthesis in the chloroplast is estimated to fluctuate from 1.55 to 1.67,
depending on the environmental conditions.
In C4 photosynthesis, more ATPs are required per fixed CO2
to concentrate CO2 into bundle sheath (BS) cells by driving the
C4 metabolic cycle in addition to the energy required for the C3
metabolic cycle. In the C4 metabolic cycle, inorganic carbon is
initially fixed in M cells into the four-carbon compound oxaloacetic acid, which is then converted into malate or aspartate.
These compounds are then diffused into BS cells and are decarboxylated to release CO2. Because the bulk of RuBisCO activity is localized to the BS cells, the RuBisCO oxygenation reaction
and subsequent photorespiration are largely suppressed in C4
photosynthesis. Although little energy is required for driving
photorespiration, ATP/NADPH demands are constitutively
increased in either M or BS cells, or in both, in C4 photosynthesis. There are three major C4 metabolic cycles depending on
the different decarboxylation enzyme of the C4 acids, NADPmalic enzyme (NADP-ME), NAD-malic enzyme (NAD-ME) and
phosphoenolpyruvate carboxykinase (PEP-CK). In the NADPME- and NAD-ME-dependent metabolic cycles, two molecules
of ATP are required for phosphorylation of pyruvate in M
chloroplasts per fixed CO2, whereas in the PEP-CK-dependent
metabolic cycle, one molecule of ATP is required per fixed CO2
for PEP-CK reaction in BS cytosol (Kanai and Edwards 1999,
Edward and Voznessenskaya 2011).
Flexible Metabolic Cycle in C4 Photosynthesis
C4 species are traditionally classified into three subtype groups
based on the major C4 metabolic cycle functioning in the
plants, but were also classified into two subtype groups,
NADP-ME and NAD-ME, in a recent study in which the
Plant Cell Physiol. 57(5): 897–903 (2016) doi:10.1093/pcp/pcw012, Advance Access publication on 17 February 2016,
available online at www.pcp.oxfordjournals.org
! The Author 2016. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists.
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Special Focus Issue – Invited Mini Review
Promotion of Cyclic Electron Transport Around Photosystem I
with the Development of C4 Photosynthesis
Y. N. Munekage and Y. Y. Taniguchi | Promotion of CET during C4 evolution
PEP-CK-dependent metabolic cycle was suggested to be supplementary, providing metabolic flexibility (Wang et al. 2014).
PEP-CK-type C4 species are known to have the NAD-ME-dependent metabolic pathway to balance the amino groups of
metabolites (Kanai and Edwards 1999, Voznesenskaya et al.
2006). Furthermore, PEP-CK activity was detected in several
NADP-ME- and NAD-ME-type C4 species. For example, in Zea
mays and Echinochloa frumentacea, which are classified as
NADP-ME type, substantial amounts of PEP-CK are found to
be active (Furumoto et al. 1999, Voznesenskaya et al. 2006). In
Z. mays, approximately 25% of 14CO2 is initially incorporated
into aspartate in M cells (Hatch 1971), which can presumably
be converted to oxaloacetate in BS mitochondria and then
decarboxylated by PEP-CK in BS cytosol (Wingler et al. 1999,
Furbank 2011) (Fig. 1A). Additionally, high PEP-CK activity was
detected in the eudicot C4 species classified in the NAD-ME
subtype group, such as Cleome gynandra and Zaleya pentandra
(Marshall et al. 2007, Sommer et al. 2012, Muhaidat and
McKown 2013). In eudicot NADP-ME-type C4 species Flaveria
bidentis and Flaveria trinervia, 35–40% of 14CO2 is incorporated
into aspartate (Moore and Edwards 1986). This aspartate is
predicted to be transported to the BS chloroplasts, then converted to oxaloacetate and subsequently reduced to malate. In
C4 Flaveria, a relatively high NADP-malate dehydrogenase
(MDH) activity, which is essentially low in other C4 species, is
found in BS cells, as well as high aspartate and alanine aminotransferase activities (Meister et al. 1996) (Fig. 1B). This evidence shows that many C4 plants can use multiple metabolic
pathways that have been selected during the evolutionary process, and suggest that ATP/NADPH demands have been altered,
depending on the flux of the different metabolic pathways.
Estimation of Required ATP/NADPH Ratio in
M and BS Chloroplasts
The estimation of the ATP demand in chloroplasts of M and BS
cells is rather complicated because it also depends on assumptions regarding the flux of 3-phosphoglyceric acid (3-PGA)
export and triose phosphate (triose-P) import in BS cells
(Hatch 1987). Exported 3-PGA is converted to triose-P in M
cells that use ATP and NADPH, then triose-P returns to the BS
cell or is metabolized to sucrose. The exchange of 3-PGA and
triose-P is indicated by the activities of phosphoglycerate kinase
and glyceraldehyde-3-phosphate dehydrogenase, which are
involved in the conversion of 3-PGA to triose-P. Both were
observed in M and BS cells, although the activities and localizations of other C3 cycle enzymes, including RuBisCO, phosphoribulokinase and chloroplastic fructose-1,6-bisphosphatase,
were strongly restricted to the BS cells (Slack et al. 1969. Ku and
Edwards 1975. Majeran et al. 2005). This exchange of 3-PGA and
triose-P may occur in all subtypes of C4 photosynthesis (Ku and
Edwards 1999, Ohnishi et al. 1989), but its flux has not been
evaluated.
In NADP-ME-type C4 photosynthesis, the ATP/NADPH
demand is estimated to be higher in BS cells than in M cells
because the reduction of oxaloacetate uses NADPH in M
898
chloroplasts and malate decarboxylation produces NADPH in
BS chloroplasts. In Z. mays and Sorghum bicolor, grana-free
structures and almost no linear electron transport activity for
NAPDH production were observed in the BS cells (Woo et al.
1970, Andersen et al. 1972). It has therefore been suggested that
only ATP is required in BS cells in these species (Kanai and
Edwards 1999). According to the calculation by Kanai and
Edwards (1999), the energy requirement per fixed CO2 in
chloroplasts is 2 NADPH and 3.25 ATP in M cells and 2.25
ATP in BS cells. In this calculation, 20% of CO2 is assumed to
leak from BS to M cells and 37.5% of 3-PGA is assumed to be
transported to M cells. Without assuming the CO2 leakage, 50%
of 3-PGA is assumed to be transported to M cells to balance the
production and consumption of NADPH in BS chloroplasts,
and the energy requirement per fixed CO2 in chloroplasts is
estimated to be 3 ATP and 2 NADPH (ATP/NADPH = 1.5) in M
cells and 2 ATP in BS cells. If the contribution of the PEP-CKdependent metabolic cycle (25%) is taken into account as
described above in Z. mays, then a higher flux (63%) of 3PGA/triose-P exchange should be considered to balance the
production and consumption of NADPH in BS chloroplasts
(Fig. 1A). In this scheme, ATP for the PEP-CK reaction in the
cytosol is assumed to be provided from chloroplasts, and the
energy requirement per fixed CO2 in chloroplasts is estimated
to be 2.75 ATP and 2 NADPH (ATP/NADPH = 1.4) in M cells
and 2 ATP in BS cells (Fig. 1A).
In C4 Flaveria species, PSII activity in the BS chloroplasts
remains at approximately 20% of that in the M chloroplasts
(Hofer et al. 1992). Because transported aspartate is converted
to oxaloacetate and subsequently reduced to malate using
NADPH in BS chloroplasts, the remaining PSII activity probably
contributes to NADPH production to balance the metabolism
in C4 Flaveria (Meister et al. 1996). Assuming that 40% of CO2 is
incorporated as aspartate, then the energy requirement per
fixed CO2 in chloroplasts is estimated to be 3 ATP and 1.6
NADPH (ATP/NADPH = 1.9) in M cells, and to be 2 ATP and
0.4 NADPH (ATP/NADPH = 5) in BS cells (Fig. 1B). In this
calculation, 50% of 3-PGA is estimated to be transported to
M chloroplasts. In the C4 Flaveria, ATP/NADPH demand may
become higher in both M and BS cells than in M cells in C3
species.
In NAD-ME-type C4 species, the ATP/NADPH demand is
conversely thought to be higher in M cells than in BS cells
because there is no production or consumption of reducing
power in chloroplasts during the NAD-ME-dependent metabolic cycle. Fewer grana stacks were observed in the M cells of
the NAD-ME-type C4 species in the family Chenopodiaceae.
From this evidence, the energy requirement per fixed CO2 in
chloroplasts is estimated to be 2.67 ATP and 0.67 NADPH
(ATP/NADPH = 4) in M cells, and 2.33 ATP and 1.33 NADPH
(ATP/NADPH = 1.75) in BS cells (Edwards and Voznessenskaya
2011). In this calculation, 33% of 3-PGA is assumed to be transported to M cells. However, the ATP/NADPH demand can be
higher in BS cells (>2.5) than in M cells if the transport of 3PGA to M cells is assumed to be >67%. When the contribution
of the PEP-CK-dependent metabolic cycle was taken into
consideration as was suggested in C. gynandra, then the
Plant Cell Physiol. 57(5): 897–903 (2016) doi:10.1093/pcp/pcw012
A
and consumption of ATP and NADPH in M cells (ATP/NADPH
= 1.29–2). Therefore, the ATP/NADPH demand in BS cells is
estimated to be 1.78–1.5. Consistent with the predicted ATP/
NADPH demand, decreases in the grana stacks are not observed
in PEP-CK-type C4 species (Vozneskaya et al. 2006).
Energy Production by Linear and Cyclic
Electron Transport Around PSI
B
Fig. 1 Illustration of metabolic pathways and ATP/NADPH demand
in Zea mays (A) and C4 Flaveria (B). Energy consumed or produced in
the pathways is indicated by red and blue, respectively. Solid lines
indicate the NADP-ME-type metabolic cycle and the C3 cycle.
Dashed lines indicate the supplementary metabolic pathway predicted in each plant. Numbers shown in parentheses indicate the
required ATP or NADPH molecules per fixed CO2. Total requirements
of ATP and NADPH per fixed CO2, and the ratios in each mesophyll
and bundle sheath cell, are shown at the bottom. In the metabolic
pathway in Z. mays, whether pyruvate is converted to alanine in
bundle sheath cytosol and subsequently converted back to pyruvate
in mesophyll cytosol remains unclear. Metabolite abbreviations: PEP,
phosphoenolpyruvate; Pyr, pyruvate; OAA, oxaloacetate; Mal, malate;
Asp, aspartate, Ala, alanine.
ATP/NADPH demand decreases in M cells and increases in BS
cells compared with the demand in plants conducting exclusively the NAD-ME-dependent metabolic cycle.
In the PEP-CK-type C4 photosynthesis, 0.6 ATP and 0.3
NADPH are estimated to be required per fixed CO2 in M cells
during the C4 metabolic cycle. The ATP used for the PEP-CK
reaction is suggested to be provided by the coupled operation
of the mitochondrial NAD-ME reaction, which releases NADH
for ATP production via mitochondrial respiration (Edwards and
Voznessenskaya 2011). Consequently the ATP/NADPH
demand probably does not increase in the PEP-CK-type C4
photosynthesis as it did in the malic enzyme type. Because
the ATP/NADPH production ratio by linear electron transport
is assumed to be 1.29 (Allen 2003), the transport of 3-PGA to M
cells is assumed to be less than 36% to balance the production
Linear electron transport from water to NADP+ is driven by PSII
and PSI. Coupled with electron transport, hydrogen ions accumulate in the lumen as a result of water splitting and the translocation of protons across the thylakoid membrane by the Cyt
b6f complex. This results in the generation of a proton-motive
force across the thylakoid membrane, which drives ATP synthesis. In contrast, cyclic electron transport around PSI is driven
solely by PSI. In this electron transport, electrons are recycled
from reduced ferredoxin and transported to plastoquinone.
Cyclic electron transport around PSI contributes to generation
of the proton-motive force without the accumulation of
NADPH. Because the ATP/NADPH production ratio is fixed
(1.29) in linear electron transport (Allen 2003), the cyclic electron transport is thought to be important for supplying ATP to
fulfill the ATP/NADPH ratio required for metabolism. There are
two pathways of cyclic electron transport, one is the PROTON
GRADIENT REGULATION 5 (PGR5)–PGR5-like 1 (PGRL1)-dependent pathway and the other is the chloroplast NADH dehydrogenase-like (NDH) complex-mediated pathway.
The PGR5–PGRL1-dependent pathway is historically identified as an antimycin A-sensitive pathway (Tagawa et al. 1963).
PGRL1 is an intrinsic membrane protein that anchors PGR5
(Munekage et al. 2002, DalCorso et al. 2008). This PGR5–
PGRL1 complex may form supercomplexes with PSI and the
Cyt b6f complex on the stroma thylakoid, and it is involved in
the electron transport from ferredoxin to plastoquinone
(DalCorso et al. 2008, Munekage et al. 2010, Hertle et al.
2013). In C3 Arabidopsis thaliana, the PGR5–PGRL1-dependent
pathway is shown to be a major pathway of cyclic electron
transport (Munekage et al. 2002, Munekage et al. 2004).
Based on the measurement of net CO2 assimilation and the
electron chromic shift in an Arabidopisis mutant pgr5, the contribution of PGR5–PGRL1-dependent cyclic electron transport
to the proton-motive force driving ATP production is estimated to be approximately 14% under steady-state C3 photosynthesis (Kramer et al. 2004, Munekage et al. 2008).
The chloroplast’s NDH complex is a multiprotein complex
consisting of >29 subunits and is associated with PSI (Ifuku et
al. 2011). This complex was first identified as a homolog of
mitochondrial complex III but it was shown to mediate electron
transport from ferredoxin to plastoquinone in a recent work
(Yamamoto et al. 2011). The complex is formed by five subcomplexes: stroma-exposed subcomplexes A, consisting of
NdhH–NdhO: stroma-exposed subcomplexes B, consisting of
PnsB1–PnsB5:
membrane-embedded
subcomplex
M,
consisting of NdhA–NdhG: lumen subcomplex L, containing
PnsL1–PnsL5; and electron donor-binding subcomplex ED,
899
Y. N. Munekage and Y. Y. Taniguchi | Promotion of CET during C4 evolution
F. palmeri
CET
LET
Fig. 2 Schematic of the evolutionary process of C4 photosynthesis and events promoting cyclic electron transport around PSI (CET) and downregulating linear electron transport (LET).
containing NdhS–NdhU (Ifuku et al. 2011). A newly identified
NdhV subunit is proposed to stabilize NDH subcomplexes A
and ED (Fan et al. 2015). The NDH complex is associated with
PSI via linker proteins Lhca5 and Lhca6 (Peng et al. 2009).
Despite forming a large complex through an intricate assembly
system, the NDH-dependent pathway is considered a minor
pathway in C3 plants because there are no significant defects
in photosynthesis and electron transport, except for under
stress conditions in mutants lacking the NDH complex
(Shikanai 2007).
An increased cyclic electron transport activity compared
with that in C3 plants was detected by the kinetics of P700
oxidation and reduction, and photoacoustic measurement
techniques (Herbert et al. 1990, Asada et al. 1993, Nakamura
et al. 2013). Correlated with the predicted ATP requirements in
different cell types, an increase in the NDH complex level in BS
cells was observed in NADP-ME-type C4 species, including Z.
mays, S. bicolor, C4 Flaveria species and Portulaca grandiflora,
and those in M cells was observed in NAD-ME-type C4 species,
including Amaranthus hybridus and Portulaca oleracea (Kubicki
et al. 1996, Takabayashi et al. 2005, Majeran et al. 2008). Based
on a comparative immunoblot analysis of the NDH-H subunit
among the genus Flaveria, the NDH complex is assumed to be
elevated >10 times compared with its level in C3 species
(Nakamura et al. 2013). The relative abundance of the NDH
complex is very low in C3 species, but it is assumed to increase
4-fold in M chloroplasts and 14-fold in the BS chloroplasts in C4
species of the genus Flaveria when compared with those in M
cells of C3 species (Nakamura et al. 2013). Even though the cellspecific increases in the PGR5 and PGRL1 levels were insignificant, they are three times higher in C4 species compared with
C3 species of the genus Flaveria (Nakamura et al. 2013). Because
the ATP/NADPH demand is estimated to be higher in both M
and BS chloroplasts in C4 Flaveria compared with C3 species,
the increased activity of both NDH and PGR5–PGRL1-dependent cyclic electron transport may contribute to ATP production
in C4 Flaveria (Nakamura et al. 2013).
900
Promotion of Cyclic Electron Transport
During C4 Evolution
The evolution of C4 photosynthesis from C3 photosynthesis
may have progressed stepwise through a C3–C4 intermediate
photosynthesis where a photorespiratory-dependent CO2concentration system, the C2 cycle, operated (Sage 2012). In
this cycle, glycine produced as a result of the RuBisCO oxygenase reaction in M cells is transferred to the BS cells and then is
decarboxylated in BS mitochondria, producing serine that returns to the M cells. There are 21 lineages containing C3–C4
intermediate species, and 10 are considered to share common
ancestors with C4 species (Sage et al. 2011). The genus Flaveria
contains nine C3–C4 intermediate and two C4-like species, and
some of them are recognized as evolutionary intermediates
between C3 and C4 species (Monson and Moore 1989,
McKown et al. 2005). We summarized the evolutionary
model of C4 photosynthesis, and a phase for the promotion
of cyclic electron transport and down-regulation of linear electron transport, based on protein expression levels and the ultrastructure of chloroplasts in BS cells from studies using the
following eight species of the genus Flaveria: C3 F. robusta
and F. pringlei, classified as the basal group; C3–C4 intermediate
F. ramosissima, C4-like F. palmeri, C4 F. bidentis and C4 F. trinervia, classified into clade A; and C3–C4 intermediate Flaveria
anomala and C4-like Flaveria brownii, classified into clade B
(McKown et al. 2005) (Fig. 2).
C4 evolution is considered to progress broadly via three
phases as follows. Phase 1: the transition from C3 to C3–C4
intermediate photosynthesis. The C2 cycle was developed
by restricting glycine decarboxylase activity to the BS cells
(Bauwe 2011). Phase 2: the transition from C3–C4 intermediate
to C4-like photosynthesis. The C4 cycle developed in the background of the C2 cycle. Because RuBisCO is not completely
compartmentalized into the BS cells, direct CO2 fixation by
RuBisCO in M cells occurs in C4-like photosynthesis (Cheng
et al. 1988, Moore et al. 1989, Dai et al. 1996). Phase 3: the
Plant Cell Physiol. 57(5): 897–903 (2016) doi:10.1093/pcp/pcw012
transition from C4-like photosynthesis to C4 photosynthesis.
With the restriction of RuBisCO expression to the BS cells,
the C3 cycle is also restricted to the BS cells.
In the C2 cycle, there is no obvious change in the ATP/
NADPH requirements in both M and BS chloroplasts compared
with those in C3 photosynthesis. In C3–C4 intermediate species
such as F. anomala and F. ramosissima, CO2 compensation
points were decreased by the operation of the C2 cycle (Ku et
al. 1991). Although there are higher expression levels of C4
metabolic enzymes compared with in C3 species, and the incorporation of 14CO2 into aspartate and malate suggests the
partial operation of the C4 cycle, the integration of the C4 cycle
into the C3 cycle is not fully developed in C3–C4 intermediates
species (Monson et al. 1986, Monson et al. 1988). This partial
operation of the C4 cycle in intermediate species, possibly providing carbon skeletons for re-assimilation of the ammonium
released during the C2 cycle in BS cells (Mallmann et al. 2014),
will slightly increase ATP/NADPH demands in chloroplasts.
Correlated with this, a slight promotion of cyclic electron transport was observed in C3–C4 intermediate species (Nakamura et
al. 2013). In contrast to the C3–C4 intermediate species, a C4
cycle fully integrated with the C3 cycle operates in C4-like
F. brownii and F. palmeri, where the ATP/NADPH demand is
considered to be increased. Here, we estimated the energy requirement in C4-like species based on the metabolism in
F. brownii, in which 20% of CO2 is directly fixed by the C3
cycle and 50% of the C4 acids are transported to BS cells as
aspartate (Cheng et al. 1988). This aspartate is subsequently
reduced to malate in BS chloroplasts. The energy requirement
per fixed CO2 is estimated to be 3 ATP and 1.6 NADPH, including the energy for direct CO2 fixation by the C3 cycle, whereas it
is estimated to be 1.6 ATP and 0.4 NADPH in BS chloroplasts.
Consequently, the ATP/NADPH demand is estimated to be 1.9
in M cells and to be 4 in BS cells in C4-like photosynthesis
(Fig. 2). In C4 Flaveria, the ATP/NADPH demand is estimated
to be 1.8–1.9 in M chloroplasts and it is estimated to be 5.0–5.7
in BS chloroplasts because there is no direct CO2 fixation by the
C3 cycle in M cells and 35–40% of the C4 acids are transported
to BS cells as aspartate as described above (Figs. 1, 2). In this
calculation, the transport of 3-PGA to M cells is assumed to be
50% and CO2 leakage is neglected in both C4-like and C4
photosynthesis.
The elevation of the NDH complex is initially induced (in
phase 2) to promote cyclic electron transport for ATP production during the C4 evolution in the genus Flaveria. It was
observed in the C3–C4 intermediate F. ramossisima (twice as
high as in C3 species) and C4-like F. brownii (seven times
higher than in C3 species), where neither the elevation of
PGR5 and PGRL1 levels nor the decrease in grana stacks of BS
chloroplasts was observed (Nakamura et al. 2013). The additional
ATP required for the C4 cycle in F. brownii is probably supplied
mainly by the elevated NDH activity. The elevation of the
PGR5–PGRL1 complex and the decrease in grana stacks of
BS chloroplasts were induced in phase 3. Decreases in the
grana stacks are associated with a reduction in PSII activity,
leading to the suppression of linear electron transport activity
(Sheen et al. 1987, Oswald et al. 1990). Therefore, it will change
the rate of linear and cyclic electron transport. Interestingly,
more grana stacks in thylakoid membranes were observed in
the BS chloroplasts in F. palmeri compared with the BS
chloroplasts in C4 species (Nakamura et al. 2013). This evidence
indicates that decreases in grana stacks are also induced in a
stepwise fashion in the last phase of C4 evolution. This change
may contribute to the reorganization of electron transport to
adjust the ATP/NADPH production for specific types of
metabolism.
Concluding Remarks
C4 photosynthesis has been developed in various plant families
during the evolutionary process from C3 photosynthesis. These
C4 plants show large variations in their C4 metabolic cycles. The
promotion of cyclic electron transport is observed with the
development of the C4 metabolic cycle in the genus Flaveria
and also in other species using NADP-ME-type or NAD-MEtype C4 metabolic cycles, and this may be required to regulate
ATP/NADPH production, which fulfills the energy required for
C4 metabolism. Although an estimation of the ATP/NADPH
demand still makes assumptions regarding unknown fluxes in
metabolism, they are consistent with the organization of the
electron transport chain that determines the ratio of linear and
cyclic electron transport activity levels. Further studies using
reverse genetics to knock down genes involved in cyclic electron transport around PSI will provide a better model for
understanding the contributions of cyclic electron transport
around PSI to C4 photosynthesis.
Funding
This work was supported by the the Japan Society for
the Promotion of Science [Funding Program for Next
Generation World-Leading Researchers (grant No. GS019) and
Grants-in-Aid for Scientific Research (KAKENHI) (grant No.
22770039)].
Disclosures
The authors have no conflicts of interest to declare.
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