Download Will C3 crops enhanced with the C4 CO2

Journal of Experimental Botany, Vol. 64, No. 13, pp. 3925–3935, 2013
doi:10.1093/jxb/ert103 Advance Access publication 12 April, 2013
Review paper
Will C3 crops enhanced with the C4 CO2-concentrating
mechanism live up to their full potential (yield)?
Steven M. Driever1,* and Johannes Kromdijk2
1
School of Biological Sciences, University of Essex, Colchester, UK
Wageningen UR Greenhouse Horticulture, Wageningen, The Netherlands
2
* To whom correspondence should be addressed. E-mail: [email protected]
Received 8 January 2013; Revised 8 March 2013; Accepted 12 March 2013
Abstract
Sustainably feeding the world’s growing population in future is a great challenge and can be achieved only by increasing yield per unit land surface. Efficiency of light interception and biomass partitioning into harvestable parts (harvest
index) has been improved substantially via plant breeding in modern crops. The conversion efficiency of intercepted
light into biomass still holds promise for yield increase. This conversion efficiency is to a great extent constrained by
the metabolic capacity of photosynthesis, defined by the characteristics of its components. Genetic manipulations
are increasingly applied to lift these constraints, by improving CO2 or substrate availability for the photosynthetic carbon reduction cycle. Although these manipulations can lead to improved potential growth rates, this increase might
be offset by a decrease in performance under stress conditions. In this review, we assess possible positive or negative
effects of the introduction of a CO2-concentrating mechanism in C3 crop species on crop potential productivity and
yield robustness.
Key words: C4 photosynthesis, CO2-concentrating mechanism, crop productivity, nitrogen metabolism, photorespiration, redox
signalling, yield improvement.
Introduction
As the world population keeps increasing, it is vital for
the global production of food to match this growth. The
most resource-use-efficient way of producing food that is
currently known is the intensive cultivation of plants with
edible parts, which is why the production of arable crops
has been the main focus area to meet future global food
demands. Whereas global resources for new arable land are
becoming increasingly scarce, the approach to simply convert more land to grow crops seems to be a dead end. It
appears, therefore, that future increases in food production
should be obtained by increasing crop productivity per unit
land surface. During the green revolution, various strategies
have already been employed to improve this productivity. As
a result, efficiency of light interception and biomass partitioning into harvestable parts (harvest index) have been
improved substantially via plant breeding in modern crops.
Although these areas still deserve further exploration, the
scientific consensus appears to be that improving the conversion efficiency of intercepted light into biomass holds
most promise for the required substantial increases in crop
yield capacity.
The potential of introducing CO2concentrating mechanisms
Central to plant growth is the required energy from
absorbed photons for the acquisition of inorganic carbon
and subsequent reduction. Under light-limited conditions,
any process that limits the availability of NADPH and
ATP for photosynthesis tends to directly reduce the capacity for carbon assimilation. The photorespiratory cycle is a
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3926 | Driever and Kromdijk
major example of such a competing process, whereby due
to limited discriminating ability of ribulose-bisphosphate
carboxylase-oxygenase (Rubisco) between O2 and CO2, the
substrate ribulose bisphosphate (RuBP) becomes oxygenated instead of carboxylated (for reviews, see, for example,
Leegood et al., 1995; Foyer et al., 2009; Sage et al., 2012).
One of the products of this reaction is phosphoglycolate,
which is toxic when allowed to accumulate. Plants convert
phosphoglycolate to phosphoglycerate via photorespiration, an intricate chain of metabolic conversions that routes
from the chloroplast via the peroxisome to the mitochondria and back. Although the end product phosphoglycerate feeds back into the Calvin–Benson–Bassham (CBB)
cycle, photorespiration reduces the net efficiency of using
intercepted light to produce carbohydrates because of the
release of CO2 during the mitochondrial conversion of
glycine to serine and the overall energetic costs associated
with production of phosphoglycerate via photorespiration,
which are higher compared to the CBB cycle. Additionally,
when light is not limiting, RuBP oxygenation limits Rubisco
carboxylation capacity by directly competing with carboxylation for Rubisco active sites.
Because the rate of RuBP oxygenation relative to carboxylation is linearly dependent on the ratio of [CO2] over
[O2] at the site of Rubisco expression, photorespiration can
be drastically suppressed by increasing [CO2] in the chloroplast stroma. A number of specific selection pressures
(Raven et al., 2008; Sage et al., 2012) has spurred evolution
to give rise to a large variety of CO2-concentrating mechanisms (CCMs), all succeeding in reducing photorespiration
by increasing [CO2]/[O2] around Rubisco. Rather than relying on Rubisco catalytic action for both primary fixation of
inorganic carbon, as well as reduction following the CBB
cycle, CCMs organize the initial capture of inorganic carbon in a different way. Many CCMs in cyanobacteria, algae,
and some higher plants employ active transport and subcellular compartmented conversions of CO2/bicarbonate (catalysed by specifically localized carbonic anhydrase activity) to
concentrate CO2 in subcellular carboxysomes, pyrenoids, or
chloroplast stroma (Raven et al., 2008). Fig. 1A shows an
example of a proposed single-cell CO2-concentrating mechanism (CCM) to be engineered into C3 crops (Price et al.,
2013) based on these principles. In C4 (Hatch and Slack,
1966) and crassulacean acid metabolism (CAM) metabolism
(Nuernbergk, 1961), different types of CCMs which are present primarily in higher plants, organic C4 acids are used as
a temporary carbon store, releasing CO2 around Rubisco by
tissue- or organelle-specific decarboxylase activity (Fig 1B).
Additional to the primary fixation of carbon, refixation of
(photo-)respired CO2 can also be a major source of inorganic carbon. In some species, specific chloroplast arrangements force the diffusion path of respired CO2 through the
chloroplast stroma, to promote high rates of refixation (see,
for example, von Caemmerer and Furbank, 2003). Exclusive
expression of glycine decarboxylase in mitochondria of
bundle sheath cells can aid recapture of photorespired CO2
as well as help raising the stromal [CO2] in bundle sheath
chloroplasts (also referred to as C2 photosynthesis). This
phenomenon is often mentioned as one of the evolutionary events preceding full expression of the C4 syndrome, as
extensively reviewed by Sage et al. (2012).
The presence of a CCM can be beneficial from an agronomical point of view. First, suppressing photorespiration
allows for increases in the maximal rate of CO2 assimilation.
Furthermore, since Rubisco is the major sink for nitrogen in
plant leaves, nitrogen-use efficiency of primary productivity
tends to be improved by the presence of a CCM in carbon
acquisition and reduction: namely, when [CO2] surrounding Rubisco is (close to) saturation, Rubisco’s operating efficiency is higher, so less protein is needed to obtain the same
turnover. When the primary fixation of inorganic carbon is
performed by enzymes with much lower Km for CO2 (or bicarbonate) than Rubisco, intercellular [CO2] can also be kept at
lower levels than C3 photosynthesis, promoting higher instantaneous water-use efficiency (WUE). These beneficial effects
have led to a number of highly productive CCM crop species,
in particular from the C4 grasses (including maize, sorghum,
and millet), which provide a significant proportion of the
global food supply.
It follows naturally from the previous paragraph to
investigate the possible introduction of a CCM into existing C3 crop species as a strategy to improve the conversion
efficiency of absorbed light into harvestable biomass. It is,
therefore, no surprise to find this idea central to a number
of research initiatives with the ultimate aim of improving
crop productivity per unit land surface (Matsuoka et al.,
2001; Hibberd et al., 2008; McCormick et al., 2012; von
Caemmerer et al., 2012). Such an introduction, when successful, would seem to involve a potentially considerable
increase in productivity.
What could be the side-effects of these
yield improvement strategies?
Whereas the potential productivity increases of introducing
a CCM into C3 crop species might be evident, these increases
should be accompanied by (in worst case) neutral effects
on yield robustness, in order to avoid greater uncertainty in
global food production. Whereas under optimal conditions,
increasing photosynthetic CO2 assimilation might lead to a
yield bonus, the side-effects may determine the robustness
of yield under conditions less advantageous. The growth of
plants and harvestable organs leading to crop productivity
is a very complex trait, influenced by a plethora of heavily
entangled processes. It seems unlikely that photosynthesis
can be altered without simultaneously affecting many other
processes. These alterations can positively, but also negatively, affect the applicability of the altered genotypes in the
pursuit of increasing global food supply. In the following
paragraphs, we aim to address these points by highlighting a
number of key processes involved in yield stability that may
be affected by the successful introduction of the C4 CCM
into a C3 crop species.
Effects of introducing CO2-concentrating mechanisms | 3927
Fig. 1. The two types of CO2-concentrating mechanism. (A.) An example of a proposed single-cell CO2-concentrating mechanism
(CCM), to be engineered into higher plants. This type, after Price et al. (2013), depends on the presence of a carboxysome in the
chloroplast, as well as inorganic carbon transporters that transport bicarbonate (HCO3 –) from outside the cell into the chloroplast and
the carboxysome. Carbonic anhydrase (CA) is only present inside the carboxysome, where CO2 is released and Rubisco is located and
the initial step of the Calvin–Benson–Bassham (CBB) cycle takes place. (B.) An example of a two-cell CO2-concentrating mechanism
(CCM), the NADP-malic enzyme (NADP-ME) type of C4 photosynthesis. This mechanism depends on the fixation of CO2 in one cell type
(mesophyll) and the transport to and release in another cell type (bundle sheath). In the mesophyll cytosol, HCO3 – is equilibrated with
CO2 by CA, and oxaloacetate (OAA) is produced from the carboxylation of phosphoenolpyruvate (PEP) mediated by PEP carboxylase
(PEPC). Inside the mesophyll chloroplast, OAA is converted into malate by malate dehydrogenase (MDH), which is transported into
the chloroplast of the bundle sheath cell. Here, malate is decarboxylated into pyruvate and CO2 by NADP-ME and the CO2 is used in
the CBB cycle. Pyruvate is transported back to the mesophyll chloroplast where it is phosphorylated to regenerate PEP in a reaction
mediated by pyruvate orthophosphate dikinase (PPDK).
Will there be enough reducing power left
for N metabolism?
Plants take nitrogen from the root environment, in the shape
of nitrate or ammonium ions. Sufficient supply of nitrogen
is required for the establishment of a productive photosynthetic apparatus. Chlorophyll (Evans, 1989), as well as
various CBB-cycle enzymes, in particular Rubisco (Makino
et al., 1994), comprise major investments of leaf nitrogen.
Leaf nitrogen metabolism can be an important determinant
of rate-limiting processes in C3 photosynthesis (Yamori
et al., 2011), due to the negative correlation between leaf
N and the ratio Jmax/Vcmax (Sage et al., 1990; Makino et al.,
1994).
3928 | Driever and Kromdijk
The photorespiratory pathway is strongly intertwined
with the pathway of nitrate reduction in C3 species (Fig. 2).
Various studies report impaired nitrate metabolism as a
result of increased stromal [CO2] (Bloom et al., 1989, 2002,
2010, 2012; Smart et al., 1998; Searles and Bloom, 2003;
Rachmilevitch et al., 2004). Interactive effects between
N-supply and atmospheric [CO2] were also found for a
range of C3 crop species grown in the free-air CO2 enrichment (FACE) experiments (Ainsworth and Long, 2005);
however, specific effects of nitrate as the source of N were
not evaluated. Interestingly, Bloom et al. (2012) suggest
that C3 capacity for nitrate metabolism could be acclimated
to historical CO2 concentrations (i.e. lower than current)
and might already be reduced under current atmospheric
conditions.
The reasons for the apparent correlation between photorespiration and nitrate metabolism are not completely
clear. A number of underlying mechanisms can be distinguished, although the supporting evidence for their relative
importance remains inconclusive (for a complete discussion,
see Foyer et al., 2009). First, a decrease in the photorespiratory production of malate may lead to diminished reductive
power (NADH) for the cytosolic reduction of NO3– to NO2–
by nitrate reductase, although this effect might be counteracted by the increased export of triose phosphate from the
chloroplast at high CO2 (Kaiser et al., 2000). Additionally,
transport of nitrite from cytosol to chloroplast stroma,
requires co-transport of protons across the chloroplast envelope. As diffusion is considered the main mode of transport,
this can be hampered by acidification of the stroma relative
Fig. 2. Schematic diagram of photorespiration and nitrogen metabolism, illustrating interactions between these processes. In the
process of photorespiration, the oxygenation reaction by Rubisco uses O2 and produces phosphoglycolate (P-Glyco) and glycerate3-phospate (Gly-3-P). The latter is used in the Calvin–Benson–Bassham (CBB) cycle. P-Glyco is hydrolysed into glycolate (Glyco)
and transported into the peroxisome. Glyco is turned into glyoxylate (Glyox), which consumes O2 and produces H2O2. Glyox is then
turned into glycine (Gly) and transported to the mitochondrion, where it is decarboxylated. In the mitochondrion, CO2 and NH3 are
released, as well as serine (Ser). Ser is transported back into the peroxisome, where it is converted into glycerate via hydroxypyruvate
(Hpyr). Glycerate is subsequently returned to the chloroplast where it feeds back into the CCB cycle. Nitrogen metabolism is closely
interlinked with photorespiration. The 2-oxoglutarate (2-OG) from the peroxisome is recycled to glutamate (Glu) and returned back
to the peroxisome, involving malate. However, in the chloroplast this cycle is shared with the conversion of glutamine (Gln) to Glu,
which reassimilates the NH3 released in the mitochondrion. In this reaction, NH3 from other sources can also be used, such as the
photosynthetic electron transport-driven, ferredoxin (Fd)-dependent conversion of nitrite from nitrate.
Effects of introducing CO2-concentrating mechanisms | 3929
to the cytosol by higher [CO2] (Shingles et al., 1996; Bloom
et al., 2002). Finally, chloroplastic reduction of nitrite and
the incorporation of ammonium into amino acids compete
with NADP reduction for reduced ferredoxin supplied by
photosynthetic electron transport. However, the Km of ferredoxin-NADP reductase is much lower compared to nitrite
reductase and glutamate synthase (Knaff, 1996; Bloom et al.,
2010), strongly suppressing nitrate metabolism in the presence of high [NADP+]/[NADPH] in the chloroplast stroma.
Reducing photorespiration decreases the proportional
demand for ATP relative to NADPH by the photosynthetic
dark reactions. As a result, increases in stromal CO2 can lead
to higher [NADP+]/[NADPH], thereby limiting the available
reducing power for nitrate metabolism.
Higher atmospheric CO2 leads to less capacity for nitrate
reduction in C3 plants, but not in crops with a naturally occurring CCM, such as the NADP-ME C4 species Zea mays and
Flaveria bidentis, the C4 NAD-ME species Amaranthus retroflexus, and the CAM species Crassula ovata (Cousins and
Bloom, 2003; Bloom et al., 2012). Bloom et al. (2012) also
surveyed two Flaveria C3–C4 intermediates, which showed
intermediate sensitivity. Although the reasons for these differences are not clear, a hypothesis could be that nitrate
metabolism is tuned to the prevailing chloroplastic stromal
CO2 concentration or availability of reductive power in the
cytosol. If true, this potentially seriously limits the yields
of CCM-enhanced C3 crops when grown with nitrate as the
prime nitrogen source. As nitrate is the predominant form of
the total N-availability to plants (Epstein and Bloom, 2005),
this side-effect could harm the applicability of a CCMenhanced C3 crop (also noted by Rachmilevitch et al., 2004).
Therefore, retuning of the nitrate assimilatory machinery
might be required along with the introduction of a CCM in
current C3 crop species.
A trade-off between water-use efficiency
and drought tolerance?
The exchange of water vapour and CO2 between plants
and the surrounding atmosphere share to a large extent the
same path of diffusion. As a result, water exchange is usually strongly connected to photosynthetic CO2 assimilation.
Loss of leaf water tends to occur via transition from liquid to gaseous phase into intercellular airspaces, followed
by diffusion through the stomata, whereas intake of CO2
moves in the opposite direction. Although the internal
pathway of water movement is not identical to that of CO2,
crop water relations can also significantly affect the internal resistance to CO2 (for review, see Flexas et al., 2012).
Additionally, leaf internal conductance and stomatal conductance can be tightly connected to maintain leaf water
status (Savvides et al., 2012) and, as a result, feedback regulation from leaf water status can also impact photosynthetic
carbon acquisition.
The majority of studies focus on the importance of superior CO2 acquisition under photorespiratory conditions to
explain the evolutionary rise of C4 photosynthesis (Edwards
et al., 2001; Sage, 2004; Sage et al., 2012). However, more
recently, the beneficial effects of the C4 syndrome from
the perspective of plant water relations were highlighted
(Osborne and Sack, 2012), as well as the structural benefits
of a bundle sheath to prevent xylem cavitation in areas with
high evaporative demand (Griffiths et al., 2013). When primary fixation of CO2 is performed by an enzyme with higher
affinity for CO2 than Rubisco, introduction of a CCM into
a C3 crop species could result in higher instantaneous WUE
through reduced stomatal opening, which is commonly found
in most C4 species (Long, 1999). This could allow for more
conservative water supply during irrigation, although this is
also heavily influenced by crop total leaf area and climatic
conditions during the growing period.
As stomata are the main gateways for water as well as CO2
exchange, it is not surprising to find adjustments in plant species with a naturally occurring CCM. For example, in facultative CAM plants, the diurnal rhythmicity in the opening and
closing of stomata during CAM metabolism almost perfectly
opposes the stomatal behaviour observed for the same plant
in C3 mode (Borland et al., 2011). In C4 photosynthesis, development and regulation of stomatal conductance has also
been modified compared to the C3 ancestral form, although
the changes are more subtle. Whereas C3 stomata tend to
respond more directly to a change in light intensity, Huxman
and Monson (2003) found the main mode of response by C4
stomata to be indirect as a result of the corresponding change
in intercellular [CO2] (ci). Taylor et al. (2010) also showed
lower operating stomatal conductance in C4 compared to
C3 in a comparison of phylogenetically closely related species. Taylor et al. (2012) further elaborated on this difference,
demonstrating C4 grasses as having lower maximum stomatal conductance than C3 grasses, due to smaller stomata at a
given stomatal density. They also provided evidence for this
difference to be evolutionarily coupled specifically to the photosynthetic pathway.
Experiments studying the difference in drought-response
of C4 compared to C3 species yield remarkable results, as
reviewed by (Ghannoum, 2009). Under well-watered conditions, C4 species generally tend to have higher instantaneous WUE (per CO2 fixed), as well as WUE per biomass
produced. However, these comparative differences become
substantially reduced, and sometimes even disappear altogether (Ripley et al., 2007), when drought is applied experimentally (Taylor et al., 2011) or when monitored in arid
habitats (Ibrahim et al., 2008; Ripley et al., 2010). Whereas
the decline of C3 photosynthesis under drought primarily reflects a (reversible) reduction in CO2 supply, in C4
photosynthesis the observed reduction is mostly due to a
decrease in biochemical capacity. As a result, after an initial decline in ci at mild drought (e.g. Williams et al., 2001;
Leakey et al., 2004), ci often actually increases in C4 species
when drought is sustained and photosynthetic reductions
become insensitive to high atmospheric [CO2] (Ghannoum
et al., 2003; Ghannoum, 2009). Limited potential for alternative electron sinks has been suggested to explain greater
sensitivity to water stress in C4 (Ghannoum, 2009). Energyuse efficiency of the C4 CCM also tends to be negatively
3930 | Driever and Kromdijk
influenced by drought stress, due to increased overcycling
(Buchmann et al., 1996; Williams et al., 2001). This could
be explained by the biochemical activity of the CCM being
less affected by drought than the activity of the CBB cycle.
However, increased overcycling may also reflect readjustment to balance ATP consumption between photorespiratory losses and excessive phosphoenolpyruvate regeneration
due to leakiness (leak rate of CO2 away from bundle sheath
cells to neighbouring mesophyll cells, divided by rate of primary bicarbonate fixation). At high light intensity, such a
futile cycle may presumably also act as a protective mechanism, when it helps to keep the plastoquinone pool in bundle sheath chloroplasts less reduced. At lower light intensity,
when CO2 released via leakage primarily originates from
mitochondrial respiration, overcycling may actually be energetically less costly than a relative increase in photorespiration (Kromdijk et al., 2010).
Considering the differences between C4 and C3 photosynthesis mentioned in the preceding paragraphs, introduction
of a CO2-concentrating mechanism into C3 crop species may
increase biomass production, as well as WUE, provided that
stomatal regulation can be modified to adjust to the presence of the CO2-concentrating mechanism. However, the
higher sensitivity of the performance of C4 photosynthesis
to drought highlights a potential decrease in yield robustness,
when drought events occur. The quickly reversible nature of
the drought-induced reduction in C3 photosynthesis also promotes higher yield robustness, compared to the slower recovery after rewatering in C4 (Ripley et al., 2010).
An advantage at high temperature, but a
disadvantage at low temperature?
The comparative advantage of a CCM changes markedly
with temperature. The catalytic action of RuBP oxygenation
is favoured over carboxylation when temperature increases.
CO2 solubility in water also decreases relative to O2 at higher
temperatures, leading to potentially higher rates of photorespiration at higher temperatures (Sage and Kubien, 2007).
Since the presence of a CCM suppresses photorespiration,
the comparative advantage increases at higher (physiologically relevant) temperatures (Raven, 1991; Long, 1999; Raven
et al., 2002). However, in CCMs that occur in zooxanthellae, high temperature may actually impair the concentrating
mechanism (Jones et al., 1998).
Early work (Long, 1983; Long et al., 1983) on C4 chilling sensitivity led to the hypothesis that C4 photosynthesis,
although theoretically advantageous even at low temperatures (Long, 1983, 1999), might be inherently incompetent
at sustaining photosynthetic capacity at low temperatures
(below approximately 15 °C). This incompetence was postulated to stem from the lack of cold stability of key C4
proteins, phosphoenolpyruvate carboxylase and pyruvate
orthophosphate dikinase. However, later studies have
confirmed the presence of more stable isoforms of these
proteins in C4 species adapted to cooler climates, such as
Miscanthus × giganteus (Naidu et al., 2003; Wang et al.,
2008). The common chilling sensitivity of these enzymes
in C4 species is therefore more likely to be associated
with ecological adaptation to warmer climates (Sage and
Kubien, 2007).
Since the kinetic properties of Rubisco respond strongly
to temperature (Bernacchi et al., 2001), at low temperatures
the maximum turnover rate of Rubisco can become severely
reduced and be the main factor limiting CO2 assimilation.
Because the presence of a CCM commonly results in lower
leaf nitrogen investment in Rubisco protein (e.g. Makino
et al., 2003), limitation by Rubisco activity in C4 photosynthesis tends to occur at relatively less cool temperatures
compared to C3 photosynthesis (Pittermann and Sage,
2000; Kubien et al., 2003). Together with limited phosphoenolpyruvate regeneration capacity due to declining pyruvate orthophosphate dikinase activity at low temperature
(Naidu et al., 2003; Wang et al., 2008), this results in a severe
reduction of the plateau for CO2 assimilation rate in C4 species below 15 °C. The significance of this reduction is most
obvious at both the start and end of the growing season,
when the combination of high light intensity and low daytime temperatures (early in the day) occurs frequently, creating considerable risk for photoinhibition in C4 crops (Long,
1983; Long et al., 1994).
Sage and McKown (2006) also suggested that acclimation of C4 photosynthesis to low temperatures by increasing
Rubisco content may be constrained by space limitations due
to the relatively small fraction of leaf tissue where Rubisco
is expressed, as well as by generally less phenotypic plasticity
associated with the greater structural and biochemical complexity to maintain functional C4 compared to C3 photosynthesis. However, if any spatial limitations to increase Rubisco
content are caused by specific expression of Rubisco in bundle sheath chloroplasts, these could presumably be overcome
when the introduced CCM can operate within a single cell
(such as the example in Fig. 1A).
It appears that the natural cold tolerance found in a minority fraction of C4 species is associated with greater potential
for cold acclimation. Work by Liu and Osborne (2008) showed
that 20 days chilling pretreatment (15/5 °C day/night) induced
cold acclimation in C3 and C4 grass species (naturally cooccurring on a site with regular low temperatures). Although
maximal CO2 assimilation rates were more reduced in C4 than
C3 species, acclimation to the chilling pretreatment provided
significant protection to subsequent high-light freezing treatments in both photosynthetic types. The extent of protection
was similar in both photosynthetic types and associated with
an upregulation of osmotic potential. Although this mode of
acclimation does only occur in specific cold-tolerant C4 species, it provides evidence for a lack of inherent barriers to
cold acclimation and subsequent freezing injury in C4 grasses
(Liu and Osborne, 2008).
To summarize temperature effects, the introduction of a
CCM into C3 crops is likely to lead to superior maximum
assimilation rates at temperatures ranging between 20 and
25 °C to approximately 38 to 45 °C and reduced temperature sensitivity of the quantum yield of CO2 fixation (Sage
and Kubien, 2007). However, below this temperature range,
Effects of introducing CO2-concentrating mechanisms | 3931
maximum assimilation rates are likely to be lower than the
original C3 crop due to limitations by Rubisco content and
the compromised ability to acclimate. As a result, biomass
production may be boosted when sufficiently high temperatures prevail, but beneficial effects on yield could be counteracted due to a shortened growing period in strongly seasonal
climates. At lower temperatures, presence of a CCM is likely
to lead to increased risk of photoinhibition, and thus the
introduction of a CCM should be accompanied by upregulation of photoprotective mechanisms to avoid problems with
yield robustness due to cold spells.
Does perturbation of photorespiration
affect redox signalling?
The role of photorespiration as a photoprotective mechanism
has been known for some time. The photoprotective role is
realized through NADH production in the mitochondria and
the use of NADH in the peroxisomes, while reducing power
from the chloroplast is exported, which facilitates energy dissipation (Wingler et al., 2000). However, photorespiration
does not only provide photoprotection: it has been shown to
be directly involved in repair of the D1 protein (Takahashi
et al., 2007). Furthermore, photorespiration is a source of
metabolic H2O2, produced in the peroxisome. Through this,
photorespiration is involved in the redox status of the peroxisome and the cell as a whole.
Under the current atmospheric oxygen concentration,
production of reactive oxygen species (ROS) is unavoidable in many different parts of the cell, such as peroxisomes,
mitochondria, and chloroplasts. They are produced by primary processes such as photosynthetic electron transport,
photorespiration, and mitochondrial respiration, as well as
enzymes like glucose oxidase, xanthine oxidase, and several
plant peroxidases (Mittler, 2002). Due to their reactive nature,
ROS are potentially dangerous for cellular processes, causing
oxidative damage to proteins, DNA, and lipids (Halliwell and
Gutteridge, 1999). An extensive array of enzymic and nonenzymic detoxification mechanisms allow for management of
ROS within safe levels and are found in almost every cellular
compartment (Mittler et al., 2004; Torres et al., 2006).
However, when plants are exposed to severe environmental conditions, changes in oxygen metabolism can perturb the
balance between reduction and oxidation reactions in the cell
in favour of the latter and induce oxidative stress. Under oxidative stress, the production of ROS and the subsequent oxidation reactions exceed the rate of scavenging as well as the
rate of repair of oxidative damage to cell components. When
this situation continues, damage may become irreversible and
result in a loss of physiological function of the cell or death.
Production of ROS may be deleterious to the cell under
certain conditions, but under conditions that are within
the adaptive range of the plant, they can also fulfil several
beneficial functions. It has been shown that ROS can be
involved in redox regulation (Buchanan and Balmer, 2005;
Dietz, 2003) and signalling (e.g. Apel and Hirt, 2004; Baier
and Dietz, 2005; Mullineaux and Baker, 2010). It has also
been suggested that ROS production could potentially dissipate excess excitation energy through the water–water cycle
and act as a photoprotective mechanism (Asada, 1999, 2000;
Ort and Baker, 2002). Although it has been shown that there
is production of ROS in chloroplasts at high light intensities in the presence of alternative electron transport, the
low capacity of the water–water cycle makes it unlikely that
this mechanism contributes significantly to photoprotection
(Driever and Baker, 2011). Therefore, it is more likely that
the water–water cycle operates in conjunction with processes
such as photorespiration. Furthermore, ROS produced in
response to high light are expected to contribute to stress signalling in response to changes in environmental conditions.
Particularly H2O2 has been identified as a trigger for retrograde signalling events from the chloroplast to the nucleus
(Galvez-Valdivieso and Mullineaux, 2010; Maruta et al.,
2012). However, not only ROS produced in the chloroplast
can act as a trigger for retrograde signalling events but also
the redox status of the plastoquinone pool itself can act as a
trigger (Pfannschmidt et al., 2009) and both events can even
occur at the same time (Galvez-Valdivieso and Mullineaux,
2010). This illustrates that the photosynthetic function of
chloroplasts acts as an integrator of cues from environmental changes such as increases in light intensity into molecular signals that are vital for adaptation to these changes. As
mentioned already, photorespiration is involved in the overall redox status of the peroxisome and the whole cell, and
as a result is directly linked to the ROS signalling network
(Fujita et al., 2006; Foyer and Noctor, 2009). This highlights
that the prevailing balance between photosynthesis and photorespiration could be vital for redox and ROS signalling
network functioning.
When striving to improve yield through increasing photosynthesis, the role of redox and ROS signalling, the antioxidant capacity, and the involvement of both the chloroplasts
and mitochondria in these should not be overlooked.
Introduction of any CCM and the effects this may have on
ROS metabolism and the redox status of the cell as a whole
can have great impact on both energy flow and ROS signalling networks and may compromise the ability of the plant to
cope with environmental changes.
Combining high-throughput screening and
physiology: phenomics+
A popular strategy to improve crop productivity is phenomics, the high-throughput phenotypic screening of
large numbers of plants to identify outstanding genotypes
(Furbank, 2009). Recently, a number of phenomics centres have been established to apply this approach for yield
improvement. To assess any potential side-effects apart
from the trait selected by the screening condition, the identified genotypes from a phenomics approach need either to
be evaluated mechanistically to explore the physiological
basis for the superior performance or empirically by extensive (and expensive) further performance assessments. With
regards to the potential ­side-effects or pitfalls mentioned
3932 | Driever and Kromdijk
in this review, we suggest that these secondary screens
could be informed by similar mechanistic analyses for the
crop under evaluation. For this purpose, we expect current advances in combining various omics fields (genomics,
transcriptomics, proteomics, metabolomics, phenomics)
and (eco)physiological knowledge to be particularly useful,
by allowing evaluation of G × E at various levels of integration (Leakey and Lau, 2012).
Conclusions and recommendations
The strategy of enhancing crop yield by means of introduction of a CCM in C3 crop species undoubtedly holds great
promise to increase the maximum energy conversion efficiency of intercepted solar irradiance into biomass. However,
to what extent this improvement can be used to increase agricultural production efficiency depends on a range of additional interacting factors. We have tried to define some of
these factors by identifying potential side-effects that could
coincide with the implementation of a CCM. It is difficult to
assess the potential impact of each side-effect, as their real
importance remains to be found, as well as to what extent
they can be overcome by further genetic manipulations. In
the worst case, unwanted side-effects could (1) narrow the
range of climatic conditions under which the implementation
of a CO2-concentrating-mechanism-enhanced could lead
to an actual yield increase or (2) increase the sensitivity of
the CO2-concentrating-mechanism-enhanced crop to abiotic
stress conditions, leading to a decrease in yield robustness.
By providing a summary of the main potential side-effects
that could be expected based on current knowledge, we hope
to provide a list for further targeted testing, whenever the
first CCM-enhanced C3 genotypes become available. We
have focused specifically on side-effects with regards to the
crop response to abiotic stress. To allow any potential yield
increase to be translated into actual yield increases while
preventing an increase in vulnerability, the crop’s response
to biotic stress also needs to remain in good shape. We therefore suggest that a similar analysis should be done to assess
whether any interactive effects may occur with regards to
crop defence reactions or disease tolerance or proneness, as
well as the ability of the CCM-enhanced crop to compete
with weed species.
An important assumption interacting with the issues
mentioned in this paper is the strength of the correlation
between photosynthetic conversion efficiency and actual
biomass production and yield. Although there is a good
case to expect a correlation (Long et al., 2006; Zhu et al.,
2010), this can often be limited to certain phases in the
topology of the crop. The specific conditions during these
topological phases are especially important when determining to what extent improvements in potential yield will
translate into actual yield. Although climatic conditions
are relatively stable for a given geographic region, yearby-year variation in seasonal timing and the occurrence of
extreme weather events can be substantial. This variation
will be reflected in the extent of the improvement of yield
due to the presence of a CCM as well as on the impact of
potential side-effects on yield robustness.
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