Journal of Experimental Botany, Vol. 65, No. 13, pp. 3471–3478, 2014
doi:10.1093/jxb/eru163 Advance Access publication 17 April, 2014
Review paper
Light to liquid fuel: theoretical and realized energy
conversion efficiency of plants using Crassulacean Acid
Metabolism (CAM) in arid conditions
Sarah C. Davis1,*, David S. LeBauer2 and Stephen P. Long2,3
1 Voinovich School of Leadership and Public Affairs and Department of Environmental and Plant Biology, Ohio University, Athens, OH,
USA
2 Energy Biosciences Institute, Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA
3 Department of Plant Biology and Department of Crop Sciences, University of Illinois at Urbana-Champaign, Urbana, IL, USA
* To whom correspondence should be addressed. E-mail: [email protected]
Received 3 December 2013; Revised 5 March 2014; Accepted 14 March 2014
Abstract
There has been little attention paid to Crassulacean Acid Metabolism (CAM) as a mechanism for bioenergy crop
tolerance to water limitation, in part, because potential yields of CAM plants have been assumed to be lower than
those of most commonly studied bioenergy crops. The photochemical efficiency, water-use efficiency (WUE), biomass production, and fuel yield potentials of CAM, C3, and C4 plants that are considered or already in use for bioenergy are reviewed here. The theoretical photosynthetic efficiency of CAM plants can be similar to or greater than
other photosynthetic pathways. In arid conditions, the greater WUE of CAM species results in theoretical biomass
yield potentials that are 147% greater than C4 species. The realized yields of CAM plants are similar to the theoretical
yields that account for water-limiting conditions. CAM plants can potentially be viable commercial bioenergy crops,
but additional direct yield measurements from field trials of CAM species are still needed.
Key words: Agave, bioenergy, biofuel, drought, photochemical efficiency, radiation use efficiency, semi-arid, sisal, water use
efficiency.
Introduction
Drought-tolerant crop varieties are being developed in
anticipation of more frequent extreme climatic events that
will occur with climate change. Much of this research is
focused on C4 and C3 species that are common food crops
despite the fact that CAM is the most efficient photosynthetic pathway in water-limited conditions (Nobel, 1991).
There has been relatively little attention focused on developing CAM plants for agricultural products in regions that
are prone to drought. Recently, though, there has been
increased attention to CAM plants that may serve as bioenergy feedstocks in semi-arid parts of the world, especially
since these will rarely compete with food crop production
(Borland et al., 2009; Davis et al., 2011; Yan et al., 2011;
Holtum et al., 2011).
The lack of attention to CAM for agricultural resources
may, in part, be because CAM plants are associated with
arid regions that generally have lower overall net primary
productivity (NPP) than more mesic regions (Cramer et al.,
1999). While it is true that arid ecosystems generally have
lower NPP, and agro-ecosystems in these conditions would
support lower yielding crops on average (without substantial
irrigation), it is also true that CAM species are neither limited
to arid condition nor always low-yielding. There are aquatic
plants, for example, that demonstrate CAM (Keeley, 1981,
1998), and reported yields of some CAM species, for example, Agave spp. and Opuntia spp., meet or exceed the yields
of the many dominant C3 and C4 crop species (Nobel, 1991;
Somerville et al., 2010).
© The Author 2014. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved.
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3472 | Davis et al.
The classic eco-physiological struggle to balance water loss
with CO2 uptake leads one to question if the conservation
of water in CAM plants necessitates a lower theoretical CO2
uptake than C3 and C4 plants. Just in contrasting C3 and C4
photosynthetic efficiencies, where the latter uses carbon-concentrating mechanisms, it is evident that there are trade-offs
associated with water conservation. Generally, greater photosynthetic rates are observed in C4 species at high temperatures
than can be achieved in C3 species, although the opposite is
true at lower temperatures. There is a greater energetic cost to
concentrate carbon dioxide at the site of RUBISCO (ribulose
bisphosphate [RubP] carboxylase/oxygenase), but the energy
conserved through the minimization of photorespiration
results in a greater net theoretical energy conversion efficiency
of C4 photosynthesis compared with C3 photosynthesis (Zhu
et al., 2008). If, like C4 photosynthesis, the carbon-concentrating mechanisms of CAM photosynthesis afford plants
greater energetic gain by avoiding photorespiration, CAM
should have a similar advantage in converting solar energy
to chemical energy. CAM photosynthesis uses the same carbon assimilation pathway as C4 photosynthesis, but instead
of separating the PEP (phosphoenolpyruvate) carboxylation
and RubP carboxylation in space, CAM separates them in
time, i.e. night and day, respectively.
However, CAM is distinguished by four phases that require
twice as many conversions of C molecules as the C4 pathway
(Winter and Smith, 1996). The four phases allow conservation
of water through nocturnal CO2 uptake with PEPC (phosphoenolpyruvate carboxylase) fixing carbon that is stored as
malic acid (phase I), a shift from PEPC to RUBISCO activity
after dawn (phase II), stomatal closure during the heat of the
day while malic acid is decarboxylated and CO2 is refixed by
RUBISCO (phase III), and stomatal opening in the cooler
evening hours with RUBISCO activity briefly coupled to
light reactions (phase IV). Even with the extra biochemical
conversions relative to C4 photosynthesis, photorespiration is
not essential to CAM and oxygenase activity at RUBISCO is
suppressed by the high internal concentration of CO2 during
phase III. Thus, the maximum theoretical energy conversion
efficiency could be similar to C4 photosynthesis, although
direct comparisons have rarely been made. The relative photochemical efficiency of the C3, C4, and CAM photosynthetic
pathways has been reviewed with a particular focus on potential biomass productivity under arid conditions. Here, the
term photochemical efficiency is the ratio of energy captured
in biomass per unit land area to the incident solar energy
received on that area of land.
Biomass production is controlled both by the amount of
light intercepted by leaves and by the efficiency with which
available light is converted to biomass. For a given amount of
available light, the photochemical conversion efficiency of a
crop influences its productivity. Cloud cover associated with
precipitation will reduce the amount of photosynthetically
active radiation (PAR) that is available to plants for photochemical conversion. Mesic regions experience greater cloud
cover than xeric regions. Thus, the theoretical maximum conversion of solar radiation to biochemical energy is affected
by cloud cover, and CAM species cultivated in semi-arid to
arid regions would probably experience greater solar radiation, on average, than C4 and C3 plants cultivated on mesic
agricultural land, as is true for the majority of Zea mays L.,
the most widely used biofuel crop in the world and the crop
that accounts for greater total global grain production than
any other (Long and Spence, 2013).
In hot, semi-arid and arid environments such as the desert
south-west of the USA, productivity is more limited by precipitation and WUE than radiation use efficiency. Biochemical
differences among the three photosynthetic pathways, which
affect the affinity for CO2 and timing of CO2 assimilation,
impart intrinsically different water use efficiencies. To a first
approximation, C3 plants which include trees, small grains
(e.g. wheat, Triticum aestivum L.), and oil crops (e.g. soybean,
Glycine max L.) are the least water use efficient. The intrinsic
WUE of C4 plants proposed as bioenergy crops (e.g. sugarcane, Saccharum officinarum L.; maize, Z. mays; miscanthus,
Miscanthus×giganteus Greef & Deuter ex Hodkinson &
Renvoize; and sorghum, Sorghum bicolor (L.) Moench) is
approximately 85% greater than C3 plants (Table 1).
Obligate CAM plants have high WUE, but have received
less attention as bioenergy crops than C3 and C4 plants. As
such, WUE of CAM plants is not typically quantified on a
crop yield basis and is more often reported as an instantaneous WUE. Based on these instantaneous measurements,
CAM plants are estimated to exchange CO2 and water at a
Table 1. Water use efficiency of bioenergy crops (dry mass per unit mass water per unit daytime atmosphere–crop water vapour
pressure deficit; calculated from the sources listed)
Crop (country)
Scientific name
Mg ha–1/mm kPa–1
Source
Soybean (Australia)
Canola (Australia)
Wheat (Argentina)
Willow (Sweden)
C3 crop average
Miscanthus (England)
Sugarcane (Australia)
Cord-grass (England)
Bulrush millet (India)
Maize (US average)
C4 crop average
Glycine max L.
Brassica napus L.
Triticum aestivum
Salix viminalis L.
0.044
0.057
0.045
0.048
0.049 (±0.006)
0.095
0.083
0.082
0.095
0.101
0.091 (±0.008)
Bhattarai et al., 2008
Zeleke et al., 2011
Lindroth and Cienciala, 1996
Lindroth and Cienciala, 1996
Miscanthus x giganteus
Saccharum officinarum
Spartina cynosuroides L.
Pennisetum typhoides L.
Zea mays
Beale et al., 1999
Inman-Bamber and McGlinchey, 2003
Beale et al., 1999
Squire, 1990
Tanner and Sinclair, 1983
Energy conversion efficiency of CAM | 3473
rate of 4–10 mmol CO2 mol–1 H2O (Szarek and Ting, 1975;
Nobel, 1991; Borland et al., 2009). CAM plants open their
stomata predominantly at night and assimilate CO2 into
organic acids. Since they assimilate CO2 via PEPC like C4
plants, a similar WUE might be expected. However, because
they open their stomata predominantly at night, they realize
a greater WUE than C4 plants because the leaf-atmosphere
water vapour pressure deficit (VPD) is lower under the cooler
conditions at night. Day–night temperature differences and,
in turn, VPD, are often particularly pronounced in desert
environments.
The full energy balance for the CAM-mediated conversion of solar energy to liquid fuel energy has been reviewed
and synthesized using Agave spp. as a model. The theoretical
maximum photochemical efficiency of CAM was calculated
based on the more thorough description of the biochemical
efficiency of CAM provided by Winter and Smith (1996) and
contrasted with the more frequently reviewed C3 and C4 pathways (based on Zhu et al., 2008). The net reduction of solar
radiation in response to cloud cover in mesic conditions was
calculated and then the theoretical solar energy conversion
efficiency of the three photosynthetic pathways in xeric conditions were contrasted by characterizing the environmental
limitations and water use efficiencies of the three pathways.
Lastly, the theoretical and realized energy yields in the form
of sugar and ethanol for biofuel were calculated.
Methods
The theoretical efficiency of energy conversion from sunlight to
biofuel was calculated in three basics steps that will be described in
detail below: (i) by estimating the biochemical efficiency of photosynthesis in CAM, (ii) by estimating the effect of precipitation on
incoming solar radiation, and (iii) by estimating the conversion efficiency of biofuel production. All conversion coefficients are based
on previously published data that have not been synthesized in this
way in the past. Following the methods of Zhu et al. (2008) for calculating maximum photochemical efficiency, the light conversion
efficiency of CAM relative to C3 and C4 photosynthetic pathways
was estimated. The maximum energy conversion for CAM in xeric
conditions was calculated based on the biochemical stoichiometry
of the CAM pathway (Winter and Smith, 1996).
Theoretical limitations on growth that would be imposed by the
differing water use efficiencies of each photosynthetic pathway
were also estimated. Water limitation of growth in an arid climate
was calculated based on the previously published measurements of
WUE by crops with the different photosynthetic pathways. Realized
energy yields in biomass (raw and after conversion to fuel) of existing and potential bioenergy crops were then compared with the theoretical yields. Theoretical potential yields in arid conditions were
calculated as a function of the radiation use efficiency and WUE
(described in more detail below).
Photochemical efficiency
After accounting for the reduced solar radiation expected in a mesic
climate, the theoretical photochemical efficiency of C4, C3, or CAM
crops in their respective climates (mesic or xeric) and in arid conditions was calculated. In this way, the efficiencies of these systems as
they would be managed for bioenergy in different growing regions
can be compared. These photochemical efficiencies are based on the
methods described by Zhu et al. (2008), and the CAM biochemical
efficiencies are based on Winter and Smith (1996). Because CAM
operates on a 24 h cycle instead of only during the day, as with C3
and C4 photosynthesis, measurements of CO2 uptake in CAM over
a 24 h period reflect a net CO2 exchange. To understand the net
energy conversion, the energy requirements of the biochemical reactions associated with CO2 assimilation must be separated from those
associated with respiration.
The photon energy demand required for CAM was calculated
using the standard stoichiometric balance of 3ATP:2NADPH.
Following Zhu et al. (2008), 4 moles of photons are required for
the reduction of one NADPH (to yield 1.5 ATP). Thus, 2.4 moles
of photons (or 416 kJ of photon energy) are required for each ATP
generated. With a demand of 4.8 ATP for every CO2 assimilated
through the 24 h CAM pathway (Winter and Smith, 1996), the light
energy required to assimilate each CO2 molecule can be calculated
according to equation (1).
4.8
ATP
kJ
kJ
×416
= 1997
CO2
ATP
CO2 (1)
Glucose, the final product that would be converted to fuel has an
energy content of 2870 kJ mol–1, or 478 kJ mol–1 CO2. Thus, the
theoretical efficiency of chemical energy stored per unit light energy
in a CAM plant is 24% (478/1997).
Solar radiation moderated by precipitation/cloud cover
The reduction in solar radiation that occurs as a result of cloud
cover in a mesic environment was determined relative to a xeric
environment. Using data available from the SURFRAD network
(NOAA, 2013), the net difference in PAR observed at a xeric site
in the south-western USA (Desert Rock Airport, NV) compared
with a mesic Midwestern site representative of rainfed agriculture
(Bondville, IL) was calculated. Both of these locations have continuous records of radiation that are maintained according to the
same SURFRAD standards. Over a three-year period, all days were
ranked according to the amount of precipitation in Bondville, IL.
The daily solar radiation and PAR profile for every tenth day in
the ranking was analysed for all the days with precipitation greater
than 0.5 cm. Annually, there are, on average, 118 d with precipitation
at the Bondville site with an average annual total precipitation of
100 cm. Using SURFRAD data from a site in the arid south-western
USA (located at Desert Rock Airport, NV), where average annual
rainfall is 15 cm, the net PAR was calculated on the same days analysed for the mesic mid-west. Precipitation on any given day in this
arid climate is rarely greater than 0.5 cm. PAR was corrected for the
number of hours of daylight at each site.
To determine the net reduction of PAR annually due to cloud
cover, the mean reduction in PAR was calculated on days when
precipitation was >0.5 cm, and the net daily reduction was multiplied by the proportion of days in a year that meet this condition
(50/365=0.14). The mean difference in net PAR that results at a xeric
site relative to a mesic site that supports rainfed agriculture (94% of
total agriculture in the USA) provided an estimate for the degree to
which incoming radiation is moderated by cloud cover.
The contrast of PAR in mesic and xeric conditions is defined here
according to the difference between two sites for which long-term
radiation data are available and collected according to the same
protocol. Using only one site to represent each climate type may
seem like a limitation, but the nature of the effects of humidity,
vapour pressure deficit, and clouds should be similar at other locations within these regional climate zones (south-west and mid-west
regions of the USA). In fact, global relationships have been demonstrated between temperature and radiation that can be corrected for
cloud cover with universal constants (e.g. Thornton and Running,
1999). Because detailed climate and radiation data are available for
these two sites, the use of the actual measurements of radiation in
the regions of interest are preferred instead of generalized global
predictions.
3474 | Davis et al.
WUE
For all plants, it was assumed that the air within a leaf is saturated
with water. The saturation vapour pressure (es, in kg H2O kg–1 air)
increases with temperature, and the water content of the leaf air is
therefore determined by leaf temperature. VPD is defined as the difference between es and the water vapour pressure of the ambient air
(ea). While ea will vary little between night and day, es will be much
lower at night because leaf temperature is lower and, therefore, the
VPD is lower at night. This is because ambient temperature typically
declines at night as there is no solar radiation load on the leaf. This
diurnal variation in temperature and thus VPD is most pronounced
in hot deserts where daytime maxima can be many degrees higher
than night-time minima, resulting in a much lower VPD at night.
Obligate CAM plants, that open stomata at night, are therefore
exposed to less potential evapotranspiration than C4 plants.
Using average monthly data for October 2012–October 2013 in the
Sonoran Desert region (Maricopa, AZ), VPD during the day and
night was calculated (see Supplementary Table S1 at JXB online).
Averaged over 12 months, daytime temperature was 27 °C and VPD
was 3.0 kPa, compared with night-time values of 17 °C and 1.3 kPa,
with a total precipitation of 201 mm. It was assumed that one-third
of the precipitation is lost in run-off, deep drainage, and soil surface evaporation. It was also assumed that production was only possible when the minimum temperature exceeded 2 °C. Using VPD
and WUE derived from literature, the potential biomass production
of each photosynthetic pathway in arid conditions was calculated.
It was assumed that CAM and C4 plants have the same fundamental WUE, but night-time VPD was applied to calculate the biomass
potential of CAM because stomata open nocturnally in CAM plants.
Fuel conversion efficiency
To estimate the theoretical net chemical energy that could be converted from biomass of CAM, C4, and C3 plants, to liquid fuel,
the mass equivalent for each theoretical estimate of carbohydrate
energy was first calculated. The proportion of carbohydrate mass
that could be converted to ethanol using current technologies was
then calculated according to literature estimates. Fuel conversion
efficiencies reflect current technology (Humbird et al., 2011) and are
described in greater detail in the next section.
Realized biomass and fuel yield
Realized net chemical energy available in plant biomass was calculated based on literature estimates of yield, tissue composition, and
fuel conversion efficiencies. Fuel conversion efficiencies reflect current technology for converting molecules of sugar that are either
freely available in plant tissue or can be produced through pretreatment and hydrolysis (Humbird et al. 2011). The net sugar yield for
Agave spp. was calculated according to the following equation:
Ysugar =Ybiomass  fleaf × ( fcellulose × cg + fhemicellulose × cx )
(2)
+ fstem × ( fsoluble carbohydrates ) 
where variables denoted with Y indicate yields and those denoted
with f indicate fractions, cx is the conversion efficiency of xylan to
xylose, and cg is the conversion efficiency of glucan to glucose. These
conversion efficiencies were based on estimates provided by Humbird
et al. (2011) for pretreatment and enzymatic hydrolysis (cg=90% from
cellulose and cx=80% from hemicellulose). 100% of soluble carbohydrates are assumed to be available as sugar for fermentation.
Fermentation efficiency after hydrolysis is assumed to be a 95% sugarto-ethanol conversion to be consistent with Humbird et al. (2011).
In practice, the conversion of soluble carbohydrates to fuel would be
separate from the conversion of lignocellulosic biomass (from leaves)
to fuel. For this reason, neither the cellulose and hemicellulose content
of the stems nor the soluble carbohydrates of the leaves are included.
Realized energy conversion efficiencies of C4 and C3 photosynthesis were calculated based on productivity measurements reported in
previous literature that describe current and potential biomass crops
(Somerville et al., 2010). The estimated proportion of carbohydrates
that become harvested soluble carbohydrates, starch, cellulose or
hemicellulose were based on measurements reported previously in the
literature (Sheehan et al., 2003; Sannigrahi et al., 2010; Davis et al.,
2011). In this case, Z. mays (C4) fuel yield reflects the current practice of converting the grain to ethanol, while Miscanthus×giganteus
(C4) and Poplar spp. (C3) both reflect cellulosic ethanol production.
Realized energy conversion efficiencies of CAM were based on
the commercial crops Agave fourcroydes Lemaire (Nobel and Meyer,
1985), Agave tequilana F.A.C. Weber (Nobel and Valenzuela-Zapapta,
1987), and Agave sisalana Perrine (Common Fund for Commodities,
2005). Although yields of Agave species have been reviewed in the
past (Nobel, 1991; Somerville et al., 2010; Garcia-Moya et al., 2011),
some assumptions used to estimate biomass potential in the past that
may lead to errors in yield projections were identified. Because yield
estimates of A. fourcroydes and A. tequilana were extrapolated from
individual plant measurements in the original studies using different
assumptions, each estimate was recalculated using more standardized assumptions about cultivation practices. Instead of extrapolating annual biomass increments per unit area based on ground area
of individual plants (as in Nobel and Meyer, 1985; and Nobel and
Valenzuela-Zapata, 1987), yields were calculated based on the standing above-ground biomass of individual plants divided by the age of
the plantation and scaled up to the farm based on observed planting
densities in the region. In each case, any root biomass included in
the original estimate was also subtracted from the harvest total to be
consistent with current harvest practices.
Results
The theoretical maximum energy conversion efficiency of
CAM photosynthesis is greater than C3 photosynthesis, and
meets or exceeds C4 photosynthetic efficiency (Fig. 1). This
theoretical maximum assumes that 37% of total solar radiation is photosynthetically active radiation (PAR) available to
plants (after reflectance, transmittance, and light harvesting
limitations) as described by Zhu et al. (2008). The biochemical efficiency of CAM depends on the recycling rate of CO2
relative to the CO2 fixed (Winter and Smith, 1996), but can
be up to 16% more efficient than C4 photosynthesis and 52%
more efficient than C3 photosynthesis. After accounting for
respiration and fuel conversion efficiency (based on typical
plant tissue composition), CAM-derived fuel can theoretically be a 15% more efficient use of solar energy than C4 and
54% more efficient than C3 photosynthesis (Fig. 1).
Cloud cover substantially reduces net incoming solar radiation on a daily basis when heavy rainfall occurs (Fig. 2), but
the net reduction of incoming radiation over the course of a
year is a modest 7% based on observations at Bondville, IL
(Fig. 3). Water limitation is far more important for realized
production in xeric climates than cloud cover in mesic climates.
This is evident in the large difference in WUE between CAM,
C4, and C3 photosynthetic pathways relative to the estimated
differences in radiation use efficiency (Fig. 3). From the average daytime VPD for each month and the average WUE in
Table 1, a potential production of 2.0 Mg ha–1 was estimated
for C3 crops and 3.6 Mg ha–1 for C4 crops in the arid conditions of the Sonoran Desert. If the same WUE for CAM
is assumed as C4 photosynthesis, but the night-time VPD is
Energy conversion efficiency of CAM | 3475
Fig. 1. Theoretical and incremental energy conversion efficiency of CAM (estimates taken from Winter and Smith, 1996), C4 and C3 photosynthesis
(estimates taken from Zhu et al., 2008). The inverted pyramid shows the incremental efficiency of the conversion of sunlight to liquid fuel (ethanol) based
on theoretical maximums. The box below the pyramid reflects actual fuel energy potentials that have been measured and reported in previous literature
as a percentage of annually available solar energy. (This figure is available in colour at JXB online.)
with Z. mays serving as an example of grain-based fuel from
a C4 crop and Miscanthus×giganteus serving as an example
of cellulosic fuel from a C4 crop. After revisiting assumptions made in past literature estimates of field-scale production, and applying consistent calculations of above-ground
biomass accumulation rate for Agave spp., realized yields of
these CAM plants ranged from 8.5 to 22 Mg ha–1 depending
on the species (Table 2). The low end of this range is similar
to the theoretical yields expected after accounting for water
limitation in arid conditions (8.9 Mg ha–1).
Discussion
Fig. 2. Mean radiation on days with precipitation exceeds 0.5 cm in the
mesic mid-west at Bondville, IL, and mean radiation in the arid south-west
at Desert Rock, Nevada on the same days. Error bars represent standard
error. Data source: SURFRAD database (NOAA Earth System Research
Laboratory). (This figure is available in colour at JXB online.)
applied, given nocturnal stomatal opening as described in the
Methods, then the same low level of precipitation would support 8.9 Mg ha–1, or almost 2.5 times the productivity of C4
photosynthesis under these conditions.
Realized production of current and potential bioenergy
crops is far lower than the theoretical maxima. The energy
conversion efficiencies of the final fuel product were calculated based on crop yields previously reported in the literature (Fig. 1; Table 2). Agave spp. (CAM), Z. mays (C4),
Miscanthus×giganteus (C4), and Poplar spp. (C3) served as
model crop species for the three photosynthetic pathways
CAM plants in some cases have a greater theoretical maximum energy conversion efficiency than C4 and C3 plants,
although the realized conversion efficiency is often much
lower (Fig. 1). In arid conditions, yields of CAM plants can
clearly exceed those of C3 and C4 crops due to the greater
intrinsic WUE (Fig. 3). Agave, a model for obligate CAM
crops, range in realized yields across species (Table 2), but our
analysis supports the recent hypothesis that CAM plants, and
Agave more specifically, can theoretically meet the expectations for a commercially viable bioenergy feedstock. While
findings of other recent studies also support this hypothesis
(Somerville et al., 2010; Davis et al., 2011; Holtum et al., 2011;
Yan et al., 2011), our analysis provides a direct comparison of
both photochemical and fuel conversion efficiencies of CAM
plants relative to well-known bioenergy crops.
The WUE estimated for CAM plants in this study is conservative because it is based entirely on the physiological
3476 | Davis et al.
Fig. 3. Theoretical radiation use efficiencies of CAM, C4, and C3 photosynthesis in their respective native environments (top) and water use efficiencies
of CAM, C4, and C3 photosynthesis in an arid climate (bottom). Reduced PAR in mesic conditions is calculated according to an estimated 0.14 y with
daily precipitation >0.5 cm, when PAR is 49% lower on average than arid conditions. Water use efficiency (WUE) is calculated based on precipitation,
temperature, and vapour pressure deficit recorded in Maricopa, AZ (see Supplementary Table S1 at JXB online for details). (This figure is available in
colour at JXB online.)
processes that drive photosynthesis. Previous studies have
estimated WUE to be anywhere from 2 to 20 times greater in
CAM plants relative to C4 plants and up to 40 times greater
relative to C3 plants (Nobel, 1991; Borland et al., 2009).
However, most of these estimates are based on instantaneous
WUE measurements, i.e. units of CO2 uptake per unit H2O
transpired by a leaf during a brief gas exchange measurement (Neales, 1973; Nobel, 1977; Desanto and Bartoli, 1996),
because CAM plants are not as commonly studied in crop
agricultural systems as are the species reported in Table 1.
This might be expected to exaggerate the differences in WUE
when direct comparisons are made between plant types based
on literature values. However, there are adaptations beyond
photosynthesis that are likely to further enhance WUE in
CAM plants. These include thick waxy cuticles, succulent
leaves, low stomatal conductance (Szarek et al., 1973), low
boundary layer conductance (Nobel, 1975; Ting and Szarek,
1975) and the ability of roots to become hydraulically isolated from drying soil (Nobel and Cui, 1992). Together, these
traits allow CAM plants to avoid water stress by maintaining
high leaf water potential despite environmental conditions.
While the purpose of this study was to contrast the theoretical efficiency of CAM photosynthesis against that of C3
and C4 photosynthesis, more detailed models of CAM plant
production have been developed that project potential yields
of CAM plants in a wide range of environmental conditions
(Nobel, 1984; Owen and Griffiths, 2013). The environmental productivity index (EPI) is the longest standing model for
predicting the productivity of CAM plants (Nobel, 1984).
Early versions of EPI included indices for photosynthetic
responses to light, water, and temperature; of these variables,
water status was the strongest driver of growth (Nobel and
Quero, 1986). Strong correlations between water availability
and production have been repeatedly demonstrated in subsequent models that improved upon the original EPI (Nobel,
1988, 1991; Owen and Griffiths, 2013). Here, the focus has
been on the production of CAM plants in arid conditions
where land use for bioenergy may be less controversial, but
Energy conversion efficiency of CAM | 3477
Table 2. Conversion efficiencies and fuel yields for Agave spp
Yields
Harvestable biomass (Mg ha–1)
Leaves (fraction of biomass)
Stem (fraction of biomass)
Cellulose (fraction of leaves)a
Hemicellulose (fraction of leaves)a
Soluble carbohydrates (fraction of stem)a
Conversion efficiencies
Agave fourcroydes
Agave tequilana
Agave sisalana
(Mexico)
(Mexico)
(Tanzania)
8.5
0.38
0.62
0.78
0.06
0.55
22
0.38
0.62
0.65
0.05
0.78
13
0.38
0.62
0.43
0.32
0.55
Xylan→Xylose efficiency (cg)
0.9
0.9
0.9
Glucan→Glucose efficiency (cx)
0.8
0.8
0.8
Sucrose→ Ethanol efficiency
Net sugar (Mg ha–1)b
Ethanol product (l ha–1)
Energy output (MJ ha–1)
0.95
0.95
0.95
5
3 300
76 000
16
9 700
228 000
8
4 700
110 000
a
It is assumed that the conversion of soluble carbohydrates in stems would be separate from the conversion of cellulosic biomass from leaves
to fuel. Thus, neither the cellulose/hemicellulose content of the stems nor the soluble carbohydrates of the leaves is included in the energy
yields.
b
According to Equation 2.
even greater yields can be expected from CAM plants in wetter climates.
In this analysis, respiration is assumed to account for
a 30% reduction in net energy stored in biomass, regardless of the photosynthetic pathway. The realized respiration will vary with climatic conditions, the life stage of the
plant, and the photosynthetic pathway. Because CAM photosynthesis occurs over a 24 h period, respiratory losses are
often accounted for in direct measurement of gas exchange,
although the respiratory flux is rarely parsed from the net
CO2 flux. In C4 and C3 photosynthetic systems, on which the
30% assumption is based (Zhu et al., 2008), gas exchange is
not typically measured over a 24 h period, but the diurnal
cycle of photosynthesis allows estimates of dark respiration
to be parsed easily from photochemically driven exchanges
of CO2. In other words, evidence that the proportion of gross
photosynthesis lost to respiration is different in CAM plants
relative to other plants is weak.
The theoretical maxima estimated here assume that all of
the available solar radiation reaches the crop canopy year
round, even though some may be reflected or transmitted
to the ground. In reality, the growing seasons of each crop
are limited and thus the realized annual efficiencies are
much lower. Still, the gap between realized and theoretical
energy conversion efficiencies indicates that there is room for
improvement. Crops can, for example, be bred to have longer
growing seasons, as has been demonstrated in some varieties
of sorghum (Rooney et al., 2007), a strategy that would result
in greater energy yields. Bioenergy crops can also be bred or
engineered to optimize foliar display in the canopy for light
capture, to optimize enzymatic efficiencies under regional
environmental conditions, or to optimize WUE (Karp and
Shield, 2008; Drewry et al., 2014).
The efficiency of biomass conversion to fuel products was
based on known conversion efficiencies but it was assumed
that all carbohydrate products were potentially precursors to
liquid fuel. Just as environmental conditions, pests, and other
risks will vary from year to year with an effect on crop yields,
variation in biomass composition and operating efficiencies
will affect fuel conversion efficiencies over time. Fermentation
efficiencies range in other studies, for example between 82%
when the yeast Saccharomyces cerevisiae is used for hydrolysis and fermentation of cellulosic biomass (Jin et al., 2010)
and 97% (with a longer reaction time) when the bacterium
Zymomonas mobilis is used for hydrolysis and fermentation
of sugar products (Doelle and Greenfield, 1985).
Water use efficiency is the primary advantage for CAM crops,
as they can be grown in arid regions where other crops would
not be viable. This WUE is also a favourable trait for crops
grown in regions where more frequent drought is expected to
occur as climate change progresses. The photosynthetic efficiency of CAM can equal or exceed that of common bioenergy crops, and fuel yields from CAM cropping systems can be
viable for bioenergy production. Still, there have been few systematic replicated field trials with plots of CAM crops grown
for bioenergy and such trials will be necessary to establish the
real potential of these plants on semi-arid lands without irrigation before commercial production can be considered.
Supplementary data
Supplementary data can be found at JXB online.
Supplementary Table S1. Calculated productivity that may
be supported by precipitation at Maricopa AZ, for different
photosynthetic types.
Acknowledgement
This work was supported in part by the Energy Biosciences Institute.
3478 | Davis et al.
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