Journal of Experimental Botany, Vol. 59, No. 7, pp. 1647–1661, 2008
doi:10.1093/jxb/ern029 Advance Access publication 20 March, 2008
SPECIAL ISSUE REVIEW PAPER
Quantum yield variation across the three pathways of
photosynthesis: not yet out of the dark
John B. Skillman*
Department of Biology, California State University, San Bernardino, CA 92407, USA
Received 28 September 2007; Revised 6 January 2008; Accepted 21 January 2008
Abstract
The convergent quantum yield hypothesis (CQY)
assumes that thermodynamics and natural selection
jointly limit variation in the maximum energetic efficiency of photosynthesis in low light under otherwise
specified conditions (e.g. temperature and CO2 concentration). A literature survey of photosynthetic quantum yield (f) studies in terrestrial plants from C3, C4,
and CAM photosynthetic types was conducted to test
the CQY hypothesis. Broad variation in f values from
C3 plants could partially be explained by accounting
for whether the measuring conditions were permissive
or restrictive for photorespiration. Assimilatory quotients (AQ), calculated from the CO2 f:O2 f ratios,
indicated that 49% and 29% of absorbed light energy
was allocated to carbon fixation and photorespiration
in C3 plants, respectively. The unexplained remainder
(22%) may represent diversion to various other energy-demanding processes (e.g. starch synthesis,
nitrogen assimilation). Individual and cumulative
effects of these other processes on photosynthetic
efficiency are poorly quantified. In C4 plants, little
variation in f values was observed, consistent with
the fact that C4 plants exhibit little photorespiration. As
before, AQ values indicate that 22% of absorbed light
energy cannot be accounted for by carbon fixation in
C4 plants. Among all three photosynthetic types, the f
of photosynthesis in CAM plants is the least studied,
appears to be highly variable, and may present the
greatest challenge to the CQY hypothesis. The high
amount of energy diverted to processes other than
carbon fixation in C3 and C4 plants and the poor
characterization of photosynthetic efficiency in CAM
plants are significant deficiencies in our otherwise
robust understanding of the energetics of terrestrial
photoautotrophy.
Key words: C3 photosynthesis, C4 photosynthesis, Crassulacean acid metabolism (CAM), photosynthetic quantum
yield.
Introduction
The quantum yield of photosynthesis (/) is a definitive
measure of the energetic efficiency of photoautotrophy. The
quantum yield for any defined light-dependent process is
the rate at which that defined event occurs relative to the
rate of photon absorption by the system. As such, the
quantum yield is a measure of the efficiency with which
absorbed light produces a particular effect. Figure 1 shows
the results of simultaneous assessments of net carbon
fixation, the instantaneous quantum yield of photosystem
II electron transport, and the non-productive dissipation of
absorbed light as heat (non-photochemical quenching;
NPQ) from an intact C3 leaf over a range of absorbed
photon flux densities. The dashed line in Fig. 1A is fit to
the linear portion of the light response of carbon
assimilation. This line describes the rate of net carbon
gain as a function of absorbed light for a leaf operating at
maximum realized photosynthetic efficiency. The slope of
this line is the conventional measure of the maximum / of
photosynthesis. This simple measure of maximum photosynthetic efficiency should not to be confused with
‘instantaneous’ measures of photosynthetic efficiency
such as the quantum yield of photosystem II (PSII)
activity (Fig. 1B) derived from chlorophyll fluorescence
measurements (Maxwell and Johnson, 2000; Lichtenthaler
et al., 2007). In low-light, where carbon fixation operates
more or less at maximum photosynthetic efficiency, Fig. 1
shows that the instantaneous quantum yield of PSII activity remains high and the non-productive dissipation of
absorbed light is modest. However, as carbon fixation
becomes increasingly light-saturated, the instantaneous
* E-mail: [email protected]
ª The Author [2008]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved.
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1648 Skillman
Fig. 1. Light response of (A) net carbon assimilation (filled diamonds)
and (B) the quantum yield of photosystem II electron transport (open
diamonds) and NPQ (non-photochemical quenching; filled circles) in an
intact leaf of a shade-grown Heuchera sanguinea plant. A modified
Li-Cor 6400 gas exchange system and a Hansatech FMS2 chlorophyll
fluorometer were used to make simultaneous gas exchange and
chlorophyll fluorescence measurements. Dark adapted Fv/Fm was 0.83.
Leaf absorptance was assumed to be 92% after Skillman and Osmond
(1998). The maximum quantum yield of net carbon assimilation (/)
calculated from the slope of the linear portion of the light response
curve (dashed line in A) was 0.05 mol CO2 fixed mol1 absorbed
photons.
quantum yield of PSII activity declines linearly and heat
dissipation (NPQ) increases linearly with increasing light
availability. Thus, instantaneous measures of photosynthetic efficiency vary with light availability, whereas the
maximum / is an intrinsic characteristic of the photosynthetic tissue of interest. The use of the term ‘quantum
yield’ here will be reserved for this maximum / as
derived from the initial slope of the light response curve
of leaf photosynthesis.
As recently as half a century ago, the actual value of the
maximum / was unresolved and proposed estimates for
the uppermost efficiency of photosynthesis were a source
of contention (Emerson and Lewis, 1941; Warburg, 1958;
reviewed in Govindjee, 1999). Today it is known that for
each O2 produced and each CO2 fixed into triose
phosphates, the minimum assimilatory power requirement
is 3 ATP and 2 NADPH (Hill and Bendall, 1960;
Jagendorf and Uribe, 1996; Edwards and Walker, 1983;
Seelert et al., 2000; Blankenship, 2002). If this alone was
all that mattered it would translate into a maximum / of
approximately 0.111 mol CO2 fixed (or O2 produced) per
mol absorbed photons for C3 photosynthesis. This value
serves as an important ‘upper limit’ on photosynthetic
efficiency. However, as of 25 years ago it was clear that
this potential / value could only be achieved in intact C3
photosynthetic tissues under a restricted set of artificial
laboratory conditions and that realized / values under
ambient conditions in C3 plants fell well below this upper
limit (Ehleringer and Björkman, 1977; Bjorkman and
Demmig, 1987). The discrepancy between the potential
and the realized maximum / indicates that other processes, such as photorespiration or starch synthesis or
nitrogen assimilation, substantially reduce the maximum
energetic efficiency of carbon gain.
With the upper ceiling on photosynthetic efficiency
firmly set by fundamental physiochemical limitations, one
may wonder if a lower threshold on photosynthetic
efficiency also exists. It is axiomatic that plant survival
and productivity depend absolutely upon light-driven
carbon gain. To the extent that the green tissues on an
individual plant operate under light-limited conditions,
knowing about / can inform us about ultimate restrictions
on plant productivity, and ecological and evolutionary
success (Monteith, 1972; Ort and Baker, 1988; Long
et al., 2006). The assumption that most green cells in most
plants are light-limited much of the time predicts that
natural selection will continually and decisively maintain
plant populations with foliar photosynthetic efficiencies at
or near the maximum achievable / for any given
environmental setting. Being sandwiched between fitness
and physics, we have come to expect that the realized /
values in different C3 species under non-stressful conditions should be maximal and invariant. This expectation
may be referred to as the ‘convergent quantum yield’
(CQY) hypothesis. Indeed, it is the fact that this simple
trait is believed to be invariant and serves as a clear
interface between fundamental physiochemical and evolutionary constraints on plant performance that has made /
an important target of research in plant ecophysiology
(Osmond et al., 1999). Similarly, although de-emphasized
here, the ample literature on photoinhibition may be
interpreted as a search for causes and consequences of
reductions in / (Ewart, 1894; Skillman and Osmond,
1998; Demmig-Adams et al., 2006).
Interestingly, an earlier literature survey demonstrated
that there was surprisingly broad scatter in this putatively
Quantum yield variation across the three pathways of photosynthesis 1649
conserved trait in terrestrial C3 plants even under nonstressful conditions (Singsaas et al., 2001). This comparative literature survey approach provided an opening for
Singsaas et al. (2001) to demonstrate how measurement
methods and data analysis methods can make a large
difference in the calculated / estimates for C3 photosynthesis. For example, not accounting for light effects on
mitochondrial respiration (i.e. the Kok effect) leads to
erroneous overestimates of the / of photosynthesis (Sharp
et al., 1984; Singaas et al., 2001). Reassuringly, these
authors found that, in many cases, the observed spread in
measured C3 / values is attributable to analytical errors
and is not a result of biological variation for this trait.
In this review, the literature survey approach used by
Singass et al. (2001) is employed to examine the range of
variation in / values in terrestrial plants in toto and
broken down by mode of photosynthesis [C3, C4, and
Crassulacean acid metabolism (CAM)]. This approach is
used as a means of identifying areas where our understanding of photosynthetic quantum yield biology is
sound and areas where our knowledge is still incomplete.
The surveyed literature was restricted to a large set of
authoritative studies where an accurate determination of /
from leaves of one or more terrestrial plant species was
a central objective of the study and where the described
methods and analysis techniques were judged to be sound,
thus presumably avoiding the sources of error identified
by Singsaas et al. (2001). Although the selected set of
studies analysed here is undoubtedly not exhaustive, it
does include many of the important / studies made on
intact leaf tissue and is large enough to allow informative
generalizations to be made. It will become evident that
most ecophysiological studies on / variation have
concentrated only on C3 and C4 plants and that much
of the observed variation can be understood in terms of
trade-offs between these two well-studied modes of
photosynthesis. By contrast, a consensus on the causes
and range of variation in / among CAM plants has not
been achieved. In addition, there is little quantitative data
available on how other metabolic processes (e.g. nitrogen
assimilation) affect the efficiency of photosynthetic carbon
gain. The high amount of energy diverted to processes
other than carbon fixation in C3 and C4 plants and the
poor characterization of photosynthetic efficiency in CAM
plants are significant deficiencies in our understanding of
the energetics of terrestrial photoautotrophy.
Observed photosynthetic quantum yield values
for terrestrial C3 plants
The distribution of values from a set of authoritative /
studies on various terrestrial plants, including representatives of all three photosynthetic pathways, is presented in
Fig. 2. These data were collected on healthy, non-stressed
Fig. 2. Distribution of photosynthetic / values (absorbed-light basis) of
C3, C4, and CAM terrestrial species from selected publications.
Summarized data were, in most cases, collected at temperatures
between 25 C and 30 C and were made under both photorespiratory
and non-photorespiratory atmospheric conditions. Sources: Ehleringer
and Björkman, 1977; Nobel, 1977; Ku and Edwards, 1978; Nobel and
Hartsock, 1978; Robichaux and Pearcy, 1980; Spalding et al., 1980;
Monson et al., 1982; Nobel, 1982; Ehleringer and Pearcy, 1983; Nobel
and Hartsock, 1983; Osborne and Garrett, 1983; Adams et al., 1986;
Monson et al., 1986; Björkman and Demmig, 1987; Monson et al.,
1987; Long et al., 1993; Singaas et al., 2001.
plants over, in most cases, a narrow range of temperatures
(25–30 C). This plot for 218 observations exhibits broad
and bimodally distributed variation (coefficient of variation (CV)¼33%). Both the high variance and bimodality
may, on first consideration, appear to be at odds with the
CQY hypothesis. The broad scatter is not simply
a consequence of lumping the three different photosynthetic types into a common dataset. These data, when
pared down to include only C3 species (Fig. 3), gives
essentially the same result (N¼127, CV¼33%). However,
there are other important factors besides photosynthetic
pathway differences that are subsumed within Fig. 2 that
can affect measured / values and can explain much of the
variation among the C3 plants shown in Fig. 3.
The effect of photorespiration on quantum yield in
C3 plants
About half of the C3 / data summarized in Fig. 3 were
measured with leaves under artificial atmospheres that
were either enriched in CO2 or depleted in O2 down to
about 2%. These data constitute the right side of the
histogram in Fig. 3 (i.e. both white and hatched bars). The
remaining data on the left side of the histogram (black
bars) are from leaves in ambient atmospheres (21% O2
and ;0.03% CO2). The relative concentrations of O2 and
1650 Skillman
Fig. 3. Distribution of photosynthetic / values (absorbed-light basis) of
terrestrial C3 species from selected publications. Data summarized are
only for measurements made at temperatures between 25 C and 30 C.
Measurements were made under both ambient atmospheric conditions
(i.e. photorespiratory conditions; black bars) and non-photorespiratory
conditions (i.e. either reduced O2 or elevated CO2; white bars and
hatched bars, respectively). Measurements under non-photorespiratory
conditions were made either via IRGA-based CO2 uptake (white bars)
or via Clark-type O2 electrode oxygen production (hatched bars).
Sources: Ehleringer and Björkman, 1977; Ku and Edwards, 1978;
Robichaux and Pearcy, 1980; Monson et al., 1982; Ehleringer and
Pearcy, 1983; Osborne and Garrett, 1983; Monson et al., 1986;
Björkman and Demmig, 1987; Monson et al., 1987; Long et al., 1993;
Singaas et al., 2001.
CO2 affect the maximum measurable efficiency of C3
photosynthesis because Rubisco, the key enzyme of
global photoautotrophy, possesses both a carboxylase and
an oxygenase activity (Bowes et al., 1971). The carboxylation and oxygenation activities of Rubisco are competitive and so depend upon the relative concentrations of
these gases as well as the active site specificity for CO2
relative to O2 (Sc/o). Carboxylation of RuBP by Rubisco
leads to the productive gain of carbon via the photosynthetic carbon reduction (PCR) cycle which is used to
support plant growth. Oxygenation of RuBP by Rubisco
yields a two-carbon compound (phosphoglycolate) which
can only be partially utilized for growth and only after
first being diverted through an alternate and extensive
series of reactions distributed across several cellular
organelles (chloroplast, peroxisome, and mitochondria).
This extensive and energetically costly series of reactions
is referred to as the photorespiratory carbon oxidation
(PCO) cycle (Fig. 4).
The co-ordinated regulation of organelle numbers and
their positions, the synthesis and regulation of PCO
metabolic machinery, the overall flux of photosynthetic
products through this additional cycle, and the actual
photorespiratory oxidation of previously reduced carbon
increases the total energetic requirements of carbon
fixation in C3 plants under ambient atmospheres (Heldt,
2004). This reduced energetic efficiency is clearly illustrated when comparing C3 / values measured under
ambient conditions against those under so-called nonphotorespiratory conditions (Fig. 3). The average / of C3
photosynthesis under ambient atmospheres at moderate
temperatures is 0.052 mol mol1 (N¼61, CV¼6%; black
bars in Fig. 3; see also Table 1). The average C3 /
measured under conditions that inhibit PCO cycle activity
(i.e. reduced O2 or elevated CO2), extracted from the data
in Fig. 3, is 0.096 mol mol1 (N¼66, CV¼15%; white
and hatched bars in Fig. 3). This approaches the
theoretical maximum / value of 0.111 mol mol1
assumed for C3 photosynthesis. Distinguishing between
photosynthetic efficiencies measured with and without
photorespiration largely explains the bimodal distribution
of C3 / values in Fig. 3.
Observed variation in C3 / under ambient atmospheres
would be even greater if measurements over a broader
range of temperatures were included in this analysis.
This is because photorespiration in C3 plants varies
with temperature (Ehleringer and Björkman, 1977).
Temperature-dependent changes in the kinetic properties
of Rubisco result in a drop in Sc/o with rising temperatures, favouring increased RuBP oxygenation at higher
temperatures (Jordan and Ogren, 1984). In addition, the
solubility of CO2 in water decreases more than the
solubility of O2 in water for each incremental increase in
temperature. Consequently, the relative concentration of
CO2 to O2 in the vicinity of the active site of Rubisco
changes with temperature, favouring RuBP oxygenation
more at increasing temperatures (Ku and Edwards, 1978).
Together these factors explain the marked drop in the
C3 / under warm compared with cool temperatures
(Ehleringer and Björkman, 1977). The effect of temperature on the relative RuBP oxygenation and carboxylation
rates, which is reflected in the temperature effect on the C3
/, appears to have far-reaching ecological and evolutionary implications (Ehleringer et al., 1997; Sage and
Kubien, 2003).
Over the narrow range of temperatures used in the
studies summarized in this review, the Sc/o of Rubisco in
C3 plants is typically quite high (>80) with little variation
observed among different C3 species (Jordan and Ogren,
1983; Tcherkez et al., 2006). A high Sc/o value indicates
that the competitive interaction between CO2 and O2 at
the Rubisco active site is strongly biased in favour of
carboxylation. This suggests that there has been selection
to minimize Rubisco oxygenase activity in C3 plants as
might be predicted from the CQY hypothesis. The strong
kinetic bias for carboxylation notwithstanding, in the
contemporary atmosphere (21% O2 and 0.04% CO2),
Quantum yield variation across the three pathways of photosynthesis 1651
Fig. 4. A simplified scheme for photosynthesis and other associated light-dependent reactions in C3 plants. The light-harvesting chlorophyll proteins
(LHCP) for photosystem I and II are drawn here as a single common unit shared between both photosystems to emphasize the co-ordinated diversion
of absorbed light energy to both photosystems. The multi-step photosynthetic carbon reduction (PCR) cycle (localized in the chloroplast) and the
multi-step photorespiratory carbon oxygenation (PCO) cycle (distributed across the chloroplast, peroxisome, and the mitochondria) have been drawn
as a single cycle to emphasize the strict co-functioning of the two cycles. Beginning with light absorption, a small but variable fraction of light
absorbed by the photosynthetic pigment bed is re-emitted either as heat or as light (fluorescence). Excitation energy channelled through the two
photosystems is used to oxidize water and drive coupled transport of electrons (ETC) and protons (DpH) at the thylakoid membrane in the
chloroplast. Thylakoid-based electron and proton transport may be used to generate assimilatory power in the form of NADPH and ATP which, in
turn, may be used to fuel the carboxylation of ribulose-1,5-bisphosphate (RuBP) in the PCR cycle in the chloroplast stroma. This cycle provisions the
plant with carbohydrates (CH2O) for growth and reproduction. Each hexose used in carbohydrate synthesis (chloroplast starch or cytosolic sucrose)
requires one ATP equivalent which may be derived from the thylakoid reactions in the light. Alternatively, the products of the thylakoid reactions
may be diverted into other processes including (a) the multi-step reduction of O2 to superoxide (O
2 ) and then back to water and/or (b) nitrite (NO2 )
reduction and/or ammonia (NH3) assimilation, or to drive the PCO cycle associated with RuBP oxygenation. Each of these other processes
(carbohydrate synthesis, N assimilation, O2 reduction, and PCO cycle) can lower the quantum yield of carbon gain by diverting photogenerated
assimilatory power away from carbon fixation. Abbreviations: LHCP, light-harvesting chlorophyll protein; PSII and PSI, photosystems II and I,
respectively; ETC, electron transport chain; DpH, thylakoidal proton gradient formed from light-driven proton membrane transport; Gln and Glu,
glutamine and glutamate, respectively; CH2O, starch and/or sucrose; PCR and PCO, photosynthetic carbon reduction and photorespiratory carbon
oxygenation cycles, respectively; RuBP, ribulose-1,5-bisphosphate.
Table 1. Summary of mean values of the quantum yield of net carbon gain (absorbed light basis) for plants of different
photosynthetic pathways measured under ambient atmospheric conditions from referenced studies
All measurements included in this summary were made under ambient concentrations of atmospheric CO2 and O2 (i.e. photorespiratory conditions) in
non-stressed photosynthetic tissues and, in most cases, at temperatures between 25 C and 30 C.
Photosynthetic pathway
Number of observations
Quantum yield
(mol mol1)
Coefficient of variation (%)
Referencesa
C3
C4
CAM
61
56
6
0.05260.003
0.05760.006
0.03360.017
6
11
52
1, 3, 5, 7, 9, 11, 12, 13, 14, 15
1, 3, 5, 7, 9, 11, 12, 13
2, 4, 6, 8, 10
a
(1) Ehleringer and Björkman, 1977; (2) Nobel, 1977; (3) Ku and Edwards, 1978; (4) Nobel and Hartsock, 1978; (5) Robichaux and Pearcy, 1980;
(6) Spalding et al. 1980; (7) Monson et al. 1982; (8) Nobel, 1982; (9) Ehleringer and Pearcy, 1983; (10) Nobel and Hartsock, 1983; (11) Osborne and
Garret, 1983; (12) Monson et al., 1986; (13) Monson et al., 1987; (14) Long et al., 1993; (15) Singaas et al., 2001.
photorespiration remains as an unavoidable drain on
photosynthetic efficiency in C3 plants.
Given the inevitability of photorespiration, it is not
surprising that plants exhibit various means by which they
minimize and/or exploit PCO activity for other essential
metabolic processes such as avoiding photo-oxidative
damage (Powles and Osmond, 1978) or facilitating foliar
nitrate assimilation (Rachmilevitch et al., 2004). Despite
1652 Skillman
the fact that plants are able to make the best of a bad
reaction, RuBP oxygenation imposes a substantial penalty
on the overall efficiency of carbon gain in C3 plants. But
ultimately, it is the realized / in C3 plants (i.e. the
maximum efficiency under ambient atmospheric conditions) that is relevant to the discussion of their ecological
and evolutionary success in the field. Accordingly, the
variation in / among C3 plants, when measured over
a narrow temperature range under ambient atmospheric
conditions, turns out to be quite narrow and unimodal
(Table 1; black bars in Fig. 3). This is consistent with the
CQY hypothesis.
Other sinks for assimilatory power
Some examples of chloroplast reactions that can divert
assimilatory power away from the PCR/PCO cycles are
shown in Fig. 4. These include the synthesis of carbohydrates (starch and/or sucrose) from photosynthetically
derived triose phosphates, the photoassimilation of inorganic nitrogen (e.g. chloroplastic nitrite reduction and
ammonia assimilation) and the water–water cycle [i.e.
photoreduction of O2 (the Mehler reaction) and the
subsequent reductive scavenging of reactive oxygen
species]. Additional cellular processes not shown that
may also depend upon photogenerated ATP and reductant
[collectively, reduced Ferredoxin (Fd) and NADPH]
include inorganic sulphur assimilation, cytosolic nitrate
reduction, reductive poising of redox metabolites (e.g.
thioredioxin, ascorbic acid, glutathione, tocopherol), and
fatty acid synthesis (Harwood and Russell, 1984; Noctor
and Foyer, 1998; Saito, 2004; Noctor, 2006). Furthermore, differential engagement of photosynthetic processes
that regulate the ATP:reductant production ratio can also
affect the efficiency of photosynthesis. For example,
photosystem I can use absorbed light to drive cyclicphotophosphorylation without the involvement of photosystem II activity, thereby contributing to ATP synthesis
without producing either O2 or NADPH. Increased diversion of absorbed light to cyclic-photophosphorylation
and away from linear electron transport will lower the /
of O2 evolution while increasing the ATP:NADP production ratio (Allen, 2003). Clearly many metabolic
processes can alter the availability of assimilatory power
for joint PCR/PCO activities and so may be expected to
lower the overall efficiency of photosynthesis below the
theoretical maximum /. These other reactions will be
referred to en masse as ancillary processes. Evidence for
the proposal that a substantial portion of assimilatory
power is directed to these ancillary processes emerges
upon consideration of whether the summarized / values
were measured as CO2 uptake or O2 production. This
distinction was subsumed within Fig. 2. However, as
Fig. 3 indicates, this methodological distinction clearly
explains some of the observed variation in / among C3
plants.
The relative engagement of these various ancillary
processes compared to carbon assimilation will affect the
assimilatory quotient (AQ, the ratio of net CO2 uptake to
net O2 evolution) when photorespiration is controlled for
(Rachmilevitch et al., 2004). Under conditions where all
the assimilatory power is being used for carbon fixation,
AQ¼1.0. Under conditions where assimilatory power is
diverted to processes other than carbon fixation, AQ <1.0.
As shown in Fig. 3, / measurements made in the absence
of photorespiration used two different methods which,
when viewed together, suggest an AQ <1.0. Nonphotorespiratory C3 / observations using closed Clarktype oxygen electrode (CTOE) systems to analyse leaf O2
production in atmospheres containing ;5% CO2 and 21%
O2 had an average / of 0.106 mol mol1 (N¼39,
CV¼6%, hatched bars in Fig. 3). This is remarkably close
to the theoretical maximum / value of 0.111 mol mol1.
Conversely, non-photorespiratory C3 / observations made
using open-flow infrared gas analysis (IRGA) systems to
quantify leaf CO2 uptake in atmospheres containing
ambient CO2 and ;2% O2 had an average / of 0.083
mol mol1 (N¼28, CV¼12%, white bars in Fig. 3). This
is well below the predicted / value of 0.111 mol mol1.
From these data it is not possible to determine whether the
discrepancy between the two photorespiration-free /
datasets is due to different methodologies or due to real
biological phenomena. But, if it is assumed that this
difference is not a methodological artefact, these data give
an AQ of 0.78. Unfortunately, no simultaneous quantum
yield measurements of CO2 and O2 fluxes are available to
confirm this estimate. However, consistent with this value
of 0.78, AQ values of approximately 0.80 were reported
for tomato leaves under non-photorespiratory conditions
(2% O2) over a broad range of brighter light levels
(Searles and Bloom, 2003). An AQ of 0.78 measured
under non-photorespiratory conditions suggests that, at
maximum photosynthetic efficiency, about 22% of assimilatory power is allocated to these various ancillary
processes. Comparing the / of CO2 fixation under
ambient conditions (0.052) to the / of O2 production
under non-photorespiratory conditions (0.106) gives an
AQ of 0.49. This suggests that the maximum efficiency of
net CO2 fixation, after diverting assimilatory power to
these ancillary processes and photorespiration, is only
about 49% of the maximum efficiency of net O2
evolution. The remaining 29% (after accounting for the
22% diverted to ancillary processes and the 49% dedicated to carbon fixation) may be taken as an estimate of
the energetic costs of the PCO cycle. This latter estimate
agrees well with numerous other published estimates of
the relative energy requirement of photorespiration
(Edwards and Walker, 1983; Ogren, 1994; Heldt, 2004).
Terrestrial plants are strict autotrophs and photosynthetic carbon acquisition is an absolute prerequisite to
carbon allocation to all other plant metabolic processes.
Quantum yield variation across the three pathways of photosynthesis 1653
Consequently, it is surprising that, under light-limiting
conditions, as much as 22% of absorbed light energy in
C3 plants appears to be diverted away from carbon
fixation and its unavoidable partner, photorespiration. Of
course, essential constitutive energy-demanding processes
that are intimately linked to photosynthetic activity (e.g.
starch synthesis) would be expected to require assimilatory power in direct proportion to that being used in
carbon fixation, even in low light. At maximum efficiency, the assimilatory requirement for the fixation of six
CO2 molecules to produce a single hexose is 18 ATP and
12 NADPH. Polymerizing one hexose molecule to starch
in the chloroplast requires one additional ATP, raising the
overall assimilatory requirement to 19 ATP and 12
NADPH (Heldt, 2004). This represents, at most, a 6%
reduction in the /. Cytosolic sucrose synthesis should
have an even smaller effect on photosynthetic efficiency if
the necessary ATP equivalents are derived from mitochondrial respiration. Thus, starch and sucrose synthesis
only explain a small portion of the apparent 22%
reduction in /. The remaining fractional reduction in /
(;16%) must be due to other ancillary processes.
However, unlike starch and sucrose synthesis, these other
ancillary processes tend to be facultatively active, depending upon plant environmental and developmental status.
For example, chloroplast fatty acid production cannot be
a substantial drain on assimilatory power in mature
photosynthetic tissues where growth rates and glycerolipid
synthesis rates are low. In addition, these other ancillary
processes are not as tightly coupled to photosynthesis as
carbohydrate synthesis is. For example, the assimilation of
nitrate can take place in either roots or leaves. Root nitrate
assimilation relies upon energy derived from mitochondrial respiration and therefore cannot act as a drain on
foliar assimilatory power. In order to maximize the
efficient use of energy for carbon gain, light-dependent
regulatory mechanisms might be expected to be in place
that preferentially allocate assimilatory power to carbon
gain and away from these facultative ancillary processes
when light is limiting. Accordingly, only at brighter light
levels would there be assimilatory power directed to these
other reactions.
Among various ancillary processes other than starch/
sucrose synthesis, foliar nitrate assimilation has received
considerable attention as a potential competitive sink for
photogenerated ATP and reductant. Nitrate photoassimilation is a four-step process beginning with nitrate reduction
to nitrite in the cytosol, nitrite reduction to ammonia in the
chloroplast (Fig. 4), and the assimilation of ammonia first to
glutamine and then to glutamate in the chloroplast (Fig. 4).
Robinson (1988) was unable to detect an inhibitory effect
of CO2 assimilation on nitrite reduction even in very low
light in isolated spinach chloroplsts. Likewise, induction of
nitrite reduction activity did not inhibit light-limited CO2
fixation (Robinson, 1988). This was interpreted to mean
that carbon fixation and nitrite reduction do not actually
compete for assimilatory power even in low light and that
nitrite assimilation does not affect the maximum efficiency
of carbon fixation. This argues against the necessity of
light-dependent regulation of assimilatory power to these
two processes. On the other hand, light regulation is
implicated in both the expression of genes encoding nitrate
reductase and the activity of nitrate reductase (Heldt, 2004).
Rachmilevitch et al. (2004) also point out that the relative
affinities of chloroplast enzymes for reduced ferredoxin
(Fd) may provide a means for regulated flux of reductant to
carbon fixation over nitrite reduction and ammonia assimilation (Fig. 4). For example, the relative affinity of FdNADP reductase for Fd is about six times that of nitrite
reductase. Consequently, Fd-dependent nitrite reduction
should proceed only if the Fd concentration in the
chloroplast exceeds that needed for maintaining NADPH at
sufficient levels for carbon assimilation (Rachmilevich
et al., 2004). Thus, at the levels of gene expression, enzyme
activity, and enzyme kinetics, there appear to be regulatory
mechanisms in place that regulate the allocation of
assimilatory power preferentially to PCR (and PCO)
activity and away from foliar nitrate assimilation in low
light. Comparative studies of the assimilatory quotient
under bright light in tomato and wheat leaves from plants
fertilized with nitrate or ammonia support this expectation,
but wild-type Arabidopsis thaliana did not conform to this
expectation (Searles and Bloom, 2003; Rachmilevitch et al.,
2004). More research is needed to achieve a consensus on
whether or not N assimilation reactions compete directly
with photosynthesis for assimilatory power under lightlimiting conditions.
Another of the ancillary processes that has received
considerable interest is the water–water cycle (Fig. 4).
Direct photoreduction of O2 at photosystem I to the
superoxide radical (O
2 ), followed by the enzymatic
reduction of superoxide ultimately back to H2O, is widely
believed to be an important alternate sink for photosynthetic reducing power in high light but not at low light
(Asada, 1999; Ort and Baker, 2002). However, the
evidence in support of this proposal is modest and
equivocal (Badger et al., 2000). Moreover, the means of
regulation for differences in relative activity of the water–
water cycle at low compared to high light is not well
understood. The limited and conflicting evidence for the
possibility of light-dependent regulation of just two of the
many ancillary energy-demanding processes (i.e. N assimilation and the water–water cycle) indicate that, at this
point, the unexpected suggestion that approximately
20–25% of photosynthetic assimilatory power is allocated
to reactions other than PCR and PCO cycles under lightlimiting conditions cannot be rejected. Because of the farreaching implications of C3 photosynthetic efficiency for
our understanding of plant biology, agricultural and
ecological production, and the global carbon cycle, this
1654 Skillman
area of research deserves greater attention. Importantly,
modern integrative approaches incorporating microarray
analyses and metabolite profiling of the expression of key
genes and key metabolites in these various interacting
ancillary pathways, coupled with biochemical models and
innovative gas exchange studies should allow us to
quantify better the effect of these assorted ancillary
processes on carbon gain efficiency.
Observed photosynthetic quantum yield values
for terrestrial C4 and CAM plants
The carbon-concentrating mechanisms of CAM and C4
photosynthesis are widely believed to have evolved as
means for minimizing the energetically wasteful process
of photorespiration. Interestingly, data summarized by
Tcherkez et al. (2006) indicate that the Sc/o of Rubisco in
C4 plants is more variable than that in C3 plants and that
the mean value is significantly lower in C4 plants than in
C3 plants. Comparable data for Rubisco from multiple
CAM species are not available. However, the C3/C4
contrast in Rubisco kinetic properties is consistent with
the idea that photorespiration-avoidance is the raison
d’être for C4. But, as discussed in this section, avoidance
of photorespiration by means of the C4 cycle also comes
with a penalty for photosynthetic efficiency. As will be
seen, the comparative role of photorespiration avoidance
in the evolution and energetics of CAM is less clear.
C4 photosynthesis
The distribution of values from a set of authoritative /
studies in terrestrial C4 plants is presented in Fig. 5A. All
data were collected on healthy, non-stressed plants over
a narrow range of temperatures (25–30 C). This plot
encompasses measurements made under both artificial
non-photorespiratory atmospheres and ambient atmospheric conditions. Among data collected under nonphotorespiratory conditions are included measurements of
both the / of CO2 uptake and the / of O2 evolution.
Little variation in observed / values in C4 plants exists
regardless of the methodological approach employed (Fig.
5A). The average / of C4 photosynthesis, pooled for all
measurement methods and conditions, is 0.058 mol mol1
(N¼74, CV¼12%). This difference in total / variation
compared with that for the C3 plants reflects the fact that
C4 plants normally exhibit greatly reduced rates of
photorespiration. Indeed, a t test indicated that the average
C4 / of CO2 uptake measured under non-photorespiratory
conditions (0.054 mol mol1, N¼18, CV¼15%) is not
significantly different from the C4 / of CO2 uptake under
ambient conditions (0.057 mol mol1, N¼56, CV¼10%;
Table 1). This narrow distribution is even more remarkable given that the dataset includes different taxonomic
and biochemical groups of C4 plants.
Fig. 5. Distribution of photosynthetic / values (absorbed-light basis) of
(A) C4 species and (B) CAM species from selected publications. Data
are summarized for measurements made under both photorespiratory
and non-photorespiratory atmospheric condition. C4 measurements were
made at temperatures between 25 C and 30 C. Temperatures used for
CAM measurements varied among the different studies but were made
under ecologically relevant temperatures. Sources: Ehleringer and
Björkman, 1977; Nobel, 1977; Ku and Edwards, 1978; Nobel and
Hartsock, 1978; Robichaux and Pearcy, 1980; Spalding et al., 1980;
Monson et al., 1982; Nobel, 1982; Ehleringer and Pearcy, 1983; Nobel
and Hartsock, 1983; Adams et al., 1986; Monson et al., 1986;
Björkman and Demmig, 1987; Monson et al., 1987.
Systematic differences in C4 photosynthetic efficiencies
are known to exist between monocots and dicots, among
members of the different C4 subtypes, and among plants
with different propensities for bundle sheath leakage
(Pearcy and Ehleringer, 1984; Ogle, 2003; Kubásek et al.,
2007). Bundle sheath leakage of CO2 in particular may be
Quantum yield variation across the three pathways of photosynthesis 1655
the biggest source of variation in photosynthetic efficiency
among C4 plants. Leakage of previously fixed CO2 out of
the bundle sheath cells reduces photosynthetic efficiency
by raising the ATP requirement for the C4 cycle. Bundle
sheath leakage of CO2 as a portion of carbon fixed by PEP
Carboxylase (PEPCase) in C4 plants is greater in low-light
than in high-light (Henderson et al., 1992; Meinzer and
Zhu, 1998; Kubásek et al., 2007; Tazoe et al., 2008).
Tazoe et al. (2008) examined the effect of bundle sheath
leakage on / estimates in Amaranthus edulis, a dicotyledonous NAD-malic enzyme C4 plant. Simultaneous
measurements of carbon assimilation and carbon isotope
discrimination over a range of low-light levels demonstrated that CO2 leakage increases proportionally with
decreasing irradiance in the linear portion of the light
response curve. This implies that conventional / measurements (i.e. from the slope of the linear portion of the light
response curve of net CO2 uptake) in this C4 plant may
actually overestimate the maximum efficiency of C4
carboxylation by as much as 10% (Tazoe et al., 2008).
This is particularly interesting because / values of net
CO2 uptake for NAD-malic enzyme dicots, like A. edulis,
are about 10% lower than other C4 subtype dicots and all
C4 monocots when assessed through conventional lightresponse curve methods (Ehleringer and Pearcy, 1983). It
will be interesting to see if the strict light dependence of
bundle sheath leakage observed in A. edulis generalizes to
other C4 taxonomic groups and biochemical subtypes. The
possibility of differential rates of bundle sheath leakage
notwithstanding, it is difficult to imagine a better argument in support of the CQY hypothesis than the narrow
distribution of C4 / values observed across biochemically,
anatomically, and taxonomically distinct groups even
when assessed under distinct measurement conditions
(Fig. 5A).
Few measurements have been made on C4 plants under
non-photorespiratory conditions because there is little to
be learned in studying the effect of these artificial
atmospheres on plants that exhibit little photorespiration.
Nevertheless, two intriguing patterns are suggested. First,
comparing C3 and C4 data, the C4 / of O2 production
(0.069 mol mol1, N¼5, CV¼14%) is significantly lower
than that of C3 plants (0.106 mol mol1). This difference
is due to the additional energy required to drive the C4
cycle. C4 photosynthesis minimally requires 2ATP per
CO2 fixed over and above that of photorespiration-free C3
photosynthesis (Edwards and Walker, 1983). Taking this
additional ATP requirement into account (and assuming
no CO2 leakage), Ehleringer and Pearcy (1983) calculated
that the maximum potential / for C4 plants is 0.067 mol
mol1 (compared with the 0.111 mol mol1 maximum
value in C3 plants). Assuming the additional ATP is made
up in cyclic photophosphorylation, this would lower the /
of O2 production in C4 plants. The congruence between
the predicted and the observed values for the / of O2
production in C4 plants is exceptional. This implies that
our overall understanding of photosynthetic efficiency in
C4 plants is robust and that other factors (e.g. CO2leakage, C4 subtype) have only minor effects on steadystate photosynthetic efficiency in low light. Secondly,
considering the two sets of measurements in C4 plants
made under atmospheres designed to eliminate photorespiration, the C4 / of O2 production in elevated CO2 at
0.069 mol mol1 is significantly higher than the C4 / of
CO2 uptake in reduced O2 at 0.054 mol mol1. The ratio
of these two mean values gives an AQ for C4 photosynthesis of 0.78. Remarkably, this is identical to the AQ
estimate in C3 species under the same paired conditions.
As before, if it is assumed that these differences are real
rather than a methodological artefact, this would again
implicate processes other than carbon fixation and
photorespiration as a sink for 22% of the absorbed energy
in C4 plants operating at maximum photosynthetic
efficiency.
Although temperature effects have been intentionally
avoided in the / data included in this review, the
differential effect of temperature on the / of CO2 uptake
in C3 and C4 plants needs to be mentioned. As discussed
above, in C3 plants the ratio of Rubisco oxygenase to
carboxylase activity increases with temperature. This
lowers the C3 / of CO2 uptake from approximately 0.07
mol mol1 at 10 C down to approximately 0.04 mol
mol1 at 40 C (Ehleringer and Björkman, 1977; Ku and
Edwards, 1978). The / of CO2 uptake in C4 plants is
constant at about 0.06 mol mol1 across this same
temperature range. Thus, the photosynthetic efficiency of
C4 plants under ambient atmospheres is less than that of
C3 plants at cool temperatures and surpasses them at
warmer temperatures. Only at intermediate temperatures
of 20–30 C will C3 and C4 plants have a similar / of
CO2 uptake. As it turns out, this / ‘crossover’ temperature has been useful in describing ecological patterns for
C3 and C4 plants. For example, the latitude where C4
dominance gives way to C3 dominance can be accurately
predicted from the / crossover temperature (Ehleringer
et al., 1997; Sage et al., 1999). Similarly, temporal
variation in CO2 and temperature have been used to
predict how the trade-offs in photosynthetic efficiency
between C3 and C4 plants should affect the photosynthetic
composition of vegetation over different time periods.
There is good agreement between these predictions and
available paleoecological data (Ehleringer et al., 1997;
Collatz et al., 1998). Sage and Kubien (2003) have argued
that it is unlikely that these ecological patterns are actually
driven by differences in photosynthetic performance in
low light. The strength of the association between
ecological distributions and the / crossover temperature
must reflect the fact that the / differences between C3 and
C4 plants are determined by the relative rates of RuBP
oxygenation and carboxylation in these two photosynthetic
1656 Skillman
types. Differences between C3 and C4 plants in the temperature effect on RuBP carboxylation and oxygenation
rates will ultimately have a larger effect on the efficiency of
carbon fixation under high- rather than low-light conditions. Even so, these ecological observations provide potent
circumstantial evidence that there has been and continues to
be strong selection for maximizing the realized efficiency
of photosynthesis, regardless of pathway. This is precisely
what the CQY hypothesis predicts.
Crassulacean acid metabolism
The distribution of values from a set of authoritative /
studies in terrestrial CAM plants is presented in Fig. 5B.
As before, this plot encompasses measurements made
under either artificial non-photorespiratory conditions or
ambient atmospheric conditions. It also encompasses
several methodological approaches, including, but not
limited to, / estimates from IRGA-based CO2 flux
measurements and from CTOE-based O2 flux measurements. It is immediately obvious that the photosynthetic /
in CAM has received relatively little attention. In order to
include as many / estimates for this photosynthetic type
as possible, the narrow temperature range requirement that
was used for C3 and C4 plants has been relaxed. However,
all data included in Fig. 5B were made under ecologically
realistic temperature regimes for each of the study species.
As before, all measurements were conducted on healthy,
non-stressed plants.
The average / of photosynthesis in CAM, pooled for all
measurement methods and conditions, is 0.073 mol mol1
(N¼17, CV¼48%). The high variation among published
CAM / values would seem to refute the CQY hypothesis
(Fig. 5B; Table 1). In general, we cannot account for that
variation by focusing on differences among methods as
was done for C3 plants because so few CAM / studies
have been done and they have relied on a broader number
of methods, including diel (i.e. 24 h) CO2 flux measurements (Nobel, 1977; Nobel and Hartsock, 1983), nocturnal tissue acidification rates (Nobel and Hartsock, 1978;
Nobel, 1982), diurnal malate consumption rates (Spalding
et al., 1980), and instantaneous O2 flux rates (Adams
et al., 1986; Björkman and Demmig, 1987). Each of these
different methods actually measure different, albeit related, metabolic processes and each method has its own
set of assumptions and uncertainties. Adding to the
uncertainty, most of the methods are not used for C3 or
C4 plants and so most CAM data cannot be referenced
against these other photosynthetic types. Among these
different methods, only the O2 electrode measurements are
directly comparable with data available for C3 and C4
plants. The average / of O2 production in CAM plants is
0.10 mol mol1 (N¼10, CV¼10%). A t test verified that
the efficiency of photosynthetic oxygen production in
CAM plants is not different from that of C3 plants. The
CAM O2 electrode data account for the entire right side of
the histogram in Fig. 5B. This leaves very few data
compiled from a disparate set of methods and measurement conditions from which to estimate the / of CO2
fixation in CAM. The average photosynthetic / for the
remaining CAM data is 0.033 mol mol1 (N¼6,
CV¼53%; Table 1). The AQ from these data, if taken at
face value, would indicate that at maximum efficiency (i.e.
in low light) only 33% of absorbed photoenergy is used
for carbon fixation compared to ;50% in C3 plants and
;75% in C4 plants. But with the limited number of
samples and the variety of methods employed, this
estimated / of CO2 fixation in CAM has to be considered
of only limited reliability. It is not possible from these
data to discern how much of this variation is due to real
biological differences in photosynthetic efficiency. A
consideration of the photosynthetic efficiency of CAM
from a physiological perspective and/or an evolutionary
perspective may provide insight into this problem.
Carbon gain physiology of CAM plants is conventionally characterized by the diel pattern of gas exchange
which can be divided into four distinct phases (Leegood
et al., 1997). Nocturnal PEPCase-mediated uptake and
fixation of atmospheric CO2 and vacuolar storage of the
resulting malic acid distinguish CAM Phase I. Diurnal
deacidification and Rubisco-mediated fixation of endogenous CO2 in the light behind closed stomates distinguish
CAM Phase III. Early morning transitional Phase II is
characterized by uptake of atmospheric CO2 via open
stomates and fixation by some combination of PEPCase/
C4-cycle activity and Rubisco/C3-cycle activity. Finally,
the late afternoon transitional Phase IV is also characterized by uptake of atmospheric CO2 via open stomates and
fixation by some combination of PEPCase/C4-cycle
activity and Rubisco/C3-cycle activity.
There are three central aspects to this diel cycle that
challenge our ability to predict (and measure) the / of
CO2 fixation in CAM, starting with the temporal separation between nocturnal CO2 uptake in Phase I and diurnal
photosynthetic CO2 fixation in Phase III. Because Phase
III photosynthetic fixation of endogenous CO2 takes place
under closed stomata, midday photosynthesis per se
cannot be monitored in CAM plants by ‘instantaneous’
IRGA measurements as is routinely done with C3 and C4
plants. This also means that a full accounting of the
energetic requirements for CO2 fixed during Phase III
must include the ‘hidden’ energy costs of malate production and accumulation from the previous night (Winter
and Smith, 1996).
A second set of challenges arises upon more careful
consideration of the entire diel CAM cycle with particular
emphasis on Phase II and Phase IV. Despite having open
stomata during Phases II and IV, strong intercellular
resistances to external CO2 diffusion in succulent CAM
tissues still result in very low chloroplast CO2 concentrations
Quantum yield variation across the three pathways of photosynthesis 1657
(Maxwell et al., 1997; Nelson et al., 2005). Limiting CO2
availability at the Rubisco active site will necessarily
lower carbon gain efficiency during these daytime
transitional phases of CAM. Furthermore, the overall
energetics of these transitional phases are not obvious
since they can involve varying levels of PEPCase/C4-like
activity and Rubisco/C3-like activity. For example, prolonged C4-like activity during Phase II will be expected to
come at a greater quantum cost than Phase II activity
dominated by Rubisco-mediated fixation (Roberts et al.,
1997; Maxwell et al., 1999). In addition, there is potential
for sequential co-occurring carboxylation by PEPCase and
Rubisco during these transitional phases when both
enzymes are active which would permit an energetically
wasteful futile cycle (Leegood et al., 1997). Although
complementary regulation of the two carboxylases is
thought to minimize this possibility (Griffiths et al., 2002;
Winter and Holtum, 2002), even modest or transient
episodes of futile cycling would markedly lower the
overall / of C gain in CAM. In addition, the relative
expression of the different phases of CAM is highly
variable, responding to both developmental and environmental cues. In the extreme, facultative CAM plants like
certain Clusia species or Mesembryanthemum crystallinum can fully switch from predominantly C3 photosynthesis to CAM in response to environmental factors such
as water availability (Holtum and Winter, 1982; Cushman
and Dodds, 2002; Lüttge, 2006). Constitutive CAM plants
also exhibit remarkable plasticity for adjusting the
absolute and relative amounts of carbon taken up during
the day and night in response to various environmental
factors including light availability (Nobel, 1982; Skillman
et al., 2005). Strong internal diffusion resistances, the
uncertain quantum costs of Phase II and IV, the possibility
of futile cycling between the two carboxylases, and the
highly variable contribution of different CAM phases to
the overall daily carbon gain represents a second set of
complications in trying to predict the maximum / of CO2
fixation in CAM from physiological considerations.
The third challenge for predicting the / in this
photosynthetic type arises when considering the question
of photorespiration during Phase III in CAM tissues.
Drawing on the analogy of C4 photosynthesis, it is widely
believed that carbon-concentrating via CAM minimizes
PCO cycle activity in CAM plants during Phase III (e.g.
Nobel, 1991; Black et al., 1996; Winter and Smith, 1996).
This would improve the / of CO2-gain in CAM compared
with plants that were otherwise expending energy on
photorespiration during Phase III. The conclusion of
reduced Phase III photorespiration is supported by the
early work of Spalding et al. (1979) who found that the
intercellular O2:CO2 concentrations for a variety of CAM
species during Phase III were approximately one-third that
of ambient air. Assuming those intercellular concentrations are indicative of concentrations at the active site of
Rubisco, Spalding et al. (1979) concluded that photorespiration should be largely suppressed during CAM Phase
III. But more recent work by Maxwell and colleagues
indicate that chloroplastic O2:CO2 concentrations are
considerably more favourable for Phase III photorespiration than previously believed (Maxwell et al., 1997,
1998). Reviewing these studies and others, Lüttge (2002)
concluded that the suppression of photorespiration during
CAM phase III is incomplete and that there are likely
situations such as severe drought where high rates of
Phase III photorespiration may occur in CAM tissues. For
now, Phase III photorespiration remains an unknown that
further complicates our ability to predict the efficiency of
photosynthesis in CAM. As a result of these complications, the realized / of CAM can only be determined
empirically by carrying out 24 h gas exchange studies
under different limiting light levels. For purposes of
assessing the generality of the CQY hypothesis, these 24
h / values in CAM plants would only take on meaning if
they were related directly to comparably measured values
in C3 and C4 plants. Unfortunately, such comparative 24 h
gas exchange data are not available.
From a physiological perspective, it can only be
concluded that it is plausible that the maximum realized
efficiency for light-driven carbon gain in CAM is, in fact,
highly variable, possibly refuting the CQY hypothesis.
From an evolutionary perspective, there are three possible
causes for increased variation in a trait worth our
consideration; there has been selection for high variability
(phenotypic plasticity) for the trait of interest, there is
reduced selection on the trait of interest, or the trait of
interest is highly correlated with another trait that is under
strong selection.
Has there been selection for high phenotypic plasticity
in the / of CAM plants? Physiological plasticity seems to
be a central feature of CAM. Depending upon environmental and developmental conditions, the metabolic
complexities described above may play out differently
over each and every 24 h cycle (Dodd et al., 2002;
Griffiths et al., 2002; Lüttge, 2006). But, this general
pattern of high plasticity in CAM notwithstanding, it is
difficult to imagine a situation wherein there would be any
advantage to having a low or flexible / per se that is
unique to CAM plants. It is unlikely that the putative high
variation in / in CAM is a result of selection for greater
plasticity in this trait.
Has there been reduced selection for maintaining
a maximum realized / in CAM plants? Among desert
succulents that thrive in one of the few biomes where light
is seldom a limiting factor, one might speculate that
relaxed selection for efficient light use has allowed for
more variation in this trait. However, there is no evidence
among desert C3 plants for / differences. Also, the similar
/ of O2 production values in CAM and C3 plants argues
against there being reduced selection for maintaining
1658 Skillman
overall photosynthetic efficiency in CAM. Moreover,
CAM diversity is greatest in the tropics (Gentry and
Dodson, 1987; Zotz, 2004) where the efficient use of light
in carbon gain should be at a premium (Yoda, 1974;
Chazdon and Fetcher, 1984; Graham et al., 2003). It is
unlikely that the putative high variation in / in CAM is
a result of relaxed selection on this trait.
If the / in CAM is indeed highly variable, it probably
represents a correlated response to selection for other
traits. The fundamental compromise in carbon gain for all
terrestrial vascular plants, regardless of photosynthetic
pathway, is with water loss through open stomata. In C3
and C4 plants the balance between carbon gain and water
loss can be regulated ‘in real time’ with changes in
stomatal conductance. This allows for relatively rapid
changes in gas exchange behavior for the optimization of
both water use and light use. In CAM, the compromise
between water loss and carbon gain is largely regulated
through the differential expression of the different phases
of CAM. The temporally variable pattern of carbon
acquisition means that the effective efficiency of light use
in carbon gain among CAM plants only emerges over the
course of a 24 h cycle. Perhaps there is a trade-off
between the expressed / of 24 h carbon gain and the
water use efficiency of 24 h carbon gain in CAM plants
which is fundamentally different from that of C3 and C4
plants. Unfortunately, there are no available data from
which to evaluate this suggestion.
Summarizing this section, available CAM / data are
insufficient for discerning whether or not plants in this
photosynthetic pathway conform to predictions of the CQY
hypothesis. A consideration of CAM from both a physiological and an evolutionary perspective suggests that this
photosynthetic type may indeed prove to have a greater
range in photosynthetic efficiencies as a result of the
inherent flexibility of CAM which is regulated largely in
the service of water conservation. Comparative 24 h gas
exchange studies of CAM plants with C3 and C4 plants
over a range of low light levels are needed to verify this
interesting possibility.
Conclusions
Emerson and Warburg’s great debate of 50 years ago was
over a 2-fold difference in their respective estimates of the
true maximum / of photosynthetic oxygen production.
Warburg (1958) interpreted his data to indicate a maximum / of ;0.25. Emerson estimated a maximum / of
;0.125 (Emerson and Lewis, 1941). Emerson’s estimate
has better stood the test of time and most questions
regarding the maximum efficiency of photosynthesis
seemed to have been settled as of 25 years ago. In
particular, seminal studies by Ehleringer and Björkman
(1977) and Björkman and Demmig (1987) showed that
the maximum potential / of light-driven CO2 fixation and
O2 production in intact C3 and C4 leaves agreed well with
expectations from the current understanding of the
energetic mechanisms of these two different photosynthetic pathways. However, the present analysis of these
and several other leaf-level / studies reveals two remaining uncertainties in our understanding of in vivo photosynthetic efficiency. First, estimates presented here
suggest that for both C3 and C4 plants, 20–25% of the
absorbed energy cannot be accounted for in photosynthesis or photorespiration. Numerous metabolic processes
besides the PCR and PCO cycles are known to rely upon
photogenerated assimilatory power and, in principle,
could explain this surprisingly high level of diverted
energy. Unfortunately, the regulation and magnitude of
the individual and integrated fluxes through these numerous other pathways are not well quantified, especially in
low light where competition for assimilatory power would
be the greatest. It would be interesting to know if this
same level of energy diversion away from carbon gain
also occurs in CAM species but, because of the second
identified deficiency in our understanding of / biology,
we are a long way from being able to address this
question with any confidence. Indeed, the best available
estimates for the / in CAM differ by a factor of ten (Fig.
5B), easily dwarfing the kinds of differences over which
Emerson and Warburg debated those many years ago.
There are clearly unavoidable and perhaps even essential
inefficiencies in light-limited carbon gain in all plants,
regardless of photosynthetic type. However, evolutionary
theory predicts that any avoidable and non-essential
reductions in photosynthetic efficiency will be continually
winnowed from populations. Without further research, the
inefficiencies in photosynthesis characterized in this review will continue to cast long shadows on our greater
understanding of the evolutionary energetics of terrestrial
photoautotrophy.
Acknowledgements
This paper is dedicated to Professors Gerry Edwards and Barry
Osmond as they approach retirement. Each, in his own way, has
long served as a distinguished leader in the study of photosynthesis.
I am indebted to Ichiro Terashima for access to the pre-published
research from his laboratory. This review has benefited from the
thoughtful comments made by Rowan Sage and an anonymous
reviewer.
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