Download Yield Potential, Plant Assimilatory Capacity, and Metabolic Efficiencies

Yield Potential, Plant Assimilatory Capacity, and Metabolic Efficiencies
R. S. Loomis* and J. S. Amthor
ABSTRACT
supplies of water and nutrients, and in occurrence of
pests and disease, flexibility in morphogenesis and acclimation of the physiological systems is a key requirement
for achieving high and stable performance.
With limited space, we focus on photosynthesis and
on respiration related to synthesis and maintenance.
Whether the biological efficiency of these processes has,
or might be, improved through breeding are important questions.
The structure, control, and efficiency of photosynthetic and respiratory systems are examined. Genetic control is complex and highly
conserved. While many features are still unresolved, basic efficiency
seems little altered by domestication and breeding of crops. Rubisco,
the carboxylase–oxygenase enzyme central to photosynthesis and photorespiration, remains a weak point but may be amenable to improvement. However, the actual radiation-use efficiency of crops is generally
less than the potential with present rubisco kinetics, leaving considerable room for improvement without change in rubisco. Good opportunities for progress lie in definition of optimal canopies of leaves having
suitable acclimation and photoprotection. The efficiency of the respiratory system also seems unaffected by plant breeding. Precise evaluation of the roles and efficiencies of the glycolytic pathway and the
tricarboxylic acid cycle in production is difficult because, in addition
to being sources of energy carriers and reductant, those systems also
supply carbon skeletons for biosyntheses. How those systems are
controlled and balanced for such diversions is largely unknown. The
alternative oxidase found in mitochondria may be involved in that
balance but its true role(s) is also unknown. Distinguishing two components of respiration, one related to maintenance and the other to
growth, remains a powerful tool in theoretical studies. In such work,
the respiratory system appears efficient, but proving that in experiments remains elusive.
Photosynthetic Production
Whether a canopy (amount of leaf area, LAI, and its
manner of display) is optimal for photosynthesis in a
particular environment is reciprocally linked with development and properties of individual leaves, including
their longevity. According to a leaf’s position in the
canopy, variations occur in the components of its photosynthetic system, its acclimation to changing conditions,
and its protection from excess photon flux density
(PFD).
Leaf Components
The solar-energy-capturing apparatus of higher plants
is located in thylakoid membranes of chloroplasts. As
summarized in Fig. 1, it consists of light-harvesting antennae complexes composed of carotenoids and chlorophylls a and b connected to Photosystem (PS) I and II
reaction centers, a cytochrome b6f complex, and ATP
synthase. The b6f complex transfers electrons from PSII,
the water-oxidizing center, to PSI leading to NADP1
reduction. The proton gradient that develops across the
thylakoid between an interior lumen and the exterior
stroma is employed by ATP synthase (coupling factor
complex, CFo-CF1) to produce ATP from ADP.
The photosynthetic reductive pentose phosphate cycle (“dark reactions” involving CO2 assimilation) is
found in the stromal solution. The key enzyme, rubisco,
catalyzes both the oxygenation and carboxylation of
ribulose-1,5-bisphosphate (RuP2). Rubisco’s activity as
an oxygenase, the initial step in the process of photorespiration, increases as the ratio [O2]/[CO2] at the enzyme
and/or temperature increase. Also in the stroma are
enzyme systems that manufacture and repair chloroplast
P
lant production is driven by photosynthesis. Key
elements in the system are (i) the interception of
photosynthetically active radiation (PAR, 400–700 nm
spectral band), (ii) use of that energy in the reduction
of CO2 and other substrates (photosynthesis), (iii) incorporation of the assimilates into new plant structures
(biosynthesis and growth), and (iv) maintenance of the
plant as a living unit. Achieving high yield is conceptually simple—maximize the extent and duration of radiation interception; use the captured energy in efficient
photosynthesis; partition the new assimilates in ways
that provide optimal proportions of leaf, stem, root, and
reproductive structures; and maintain those at minimum cost.
In detail, the processes are complex. The dynamic
pattern of partitioning is particularly important. Crop
yield comprises only a portion of biomass that accumulates over a crop cycle. Effective root and canopy systems (including stem structure for foliage display), for
example, generally must be established before the onset
of reproductive effort. In addition, the cost of maintenance increases as vegetative biomass accumulates during the season. Because crops are at the mercy of spatial
and temporal variations in weather, plant spacing, and
Abbreviations: AMP, ADP, and ATP, adenosine mono-, di-, and
triphosphate, respectively; C3 plants, plants that employ only the reductive pentose phosphate cycle in photosynthesis; C4 plants, plants
that employ PEP carboxylase to concentrate CO2 as the first step in
photosynthesis; CH2O represents a unit of carbohydrate with MW 5
30 g mol21; LAI, leaf area index; NADP1 and NADP(H), oxidized and
reduced nicotinamide adenine dinucleotide phosphate, respectively;
PAR, photosynthetically active radiation; PEP, phosphoenolpyruvate;
PFD, photon flux density; PSI and PSII, photosystems I and II, respectively; RuP2, ribulose-1,5-bisphosphate; RUE, radiation-use efficiency; SB, SM, and SR, substrate carbon (or carbohydrate) retained in
new biomass, or expended in maintenance or biosynthesis, respectively; TCA, tricarboxylic acid.
R.S. Loomis, Agronomy & Range Science, Univ. of California, Davis,
CA 95616, USA; J.S. Amthor, Environmental Sciences Division, Oak
Ridge National Lab., Oak Ridge, TN 37831-6422. Received 12 Dec.
1998. *Corresponding author ([email protected]).
Published in Crop Sci. 39:1584–1596 (1999).
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LOOMIS & AMTHOR: METABOLIC EFFICIENCY
1585
Fig. 1. Light reactions of photosynthesis and photophosphorylation associated with thylakoid membranes inside chloroplasts leading to production
of NADPH and ATP used in CO2 assimilation. Photons are absorbed by chlorophyll antennae in both photosystem II (PSII) and photosystem
I (PSI). Water is oxidized by PSII, yielding O2 and protons in the lumen. Coordinated activity of PSII and the cytochrome (cyt) b6 f complex
pumps protons from stroma to lumen. This involves cycling of plastoquinone between oxidized (Q) and reduced (QH2) states. As drawn, a
“Q-cycle” is associated with cyt b6 f. Electrons are transferred from cyt b6 f to PSI via plastocyanin (PC). In noncyclic electron transport, e2
are then transferred from PSI via ferredoxin (Fd) to FNR (ferredoxin-NADP reductase), which leads to reduction of NADP. The dashed
line (– – –) indicates cyclic transport in which e2 flow from PSI back to the cyt complex via Fd. Protons move from lumen to stroma through
CFo-CF1 ATP synthase, which catalyzes ADP phosphorylation (about 3 protons/ATP).
constituents, reduce nitrite and sulfite, and synthesize
starch. The scene is further complicated by the presence
of the glycolytic system in the stroma (as well as in
cytosol) and by exchange of various compounds between cytosol and chloroplast. For example, triose phosphate moves to cytosol, where sucrose synthesis occurs,
in exchange for inorganic phosphate, Pi. Any slowing
of this Pi recycling, or accumulation of end products,
can slow photosynthesis. The Q10 of the reductive cycle
is near 2 and low temperature limits CO2 reduction
unless the capacity is increased through increases in
enzyme concentrations.
All chloroplasts of C3 plants contain the full set of
enzymes for CO2 assimilation. In C4 crop plants, rubisco
and most of the carbon reduction cycle occur only in
chloroplasts of bundle sheath cells. C4 mesophyll cells,
by contrast, lack rubisco but rely on an important cytosolic enzyme, phosphoenolpyruvate (PEP) carboxylase,
to assimilate CO2. In C4 plants of the NADP-malic enzyme type (maize, Zea mays L., and sugarcane, Saccha-
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rinum spp.), PEP carboxylase fixes CO2 into oxaloacetate, a four-carbon organic acid, which is then reduced
to malate. Malate is transferred to bundle sheath cells
where it is decarboxylated to pyruvate, thus concentrating the dilute supply of CO2 around rubisco and greatly
reducing photorespiration. The pyruvate returns to
mesophyll chloroplasts where it is converted to PEP
through conversion of ATP to AMP. The cycle is completed when the PEP returns to mesophyll cytosol. An
additional complexity in C4 plants is that 3-phosphoglycerate (PGA) is also exported from bundle sheath cells
and is reduced in mesophyll chloroplasts, thus utilizing
reducing power that is available there.
Genetic Control of Photosynthesis
Considerable progress has been made towards understanding the molecular biology of photosynthetic systems (Ort and Yocum, 1996). Thylakoid and carbon
reduction systems comprise well over 100 proteins, and
the stroma and outer membranes of chloroplasts are
sites for an array of proteins related to transport, coordination, and regulation of chloroplast activity. Hankamer
et al. (1997) list 27 genes and protein subunits solely
for PSII. Genes for most chloroplast proteins are known
and sequencing is well advanced. That work offers evidence that the PSI and PSII reaction centers were derived some 2 3 109 years ago from several endosymbioses with photosynthetic bacteria. The principal
source was cyanobacteria and as many as five endosymbioses may have occurred (Reith, 1996). Genetic control
over synthesis of these proteins is divided between nuclear and chloroplastic DNA. Chloroplast DNA, which
is circular with a high level of ploidy (20–900 copies
per chloroplast), may code for 100 proteins (Erickson,
1996). Additional problems for genetic manipulation
arise from the maternal cytoplasmic (nonnuclear) inheritance of chloroplasts (and mitochondria) and the large
numbers of these organelles in higher plant cells.
C4 species evolved at various times (10–15 3 106 years
ago) from many different C3 species resulting in numerous variations in the system. The CO2-concentrating
action and anatomical modifications greatly improve
adaptation to high temperatures and to low atmospheric
[CO2], conditions that accelerate photorespiration in C3
plants. Other benefits include better water-use efficiency than C3 species and, perhaps more important,
need for much less rubisco (and thus less N) per unit
leaf area for rapid photosynthesis. Genetic control is
similar to that for C3 systems, and key enzymes are
homologous with ancient C3 genes, but the genes are
expressed differently (Monson, 1999).
There is no evidence that important beneficial
changes in the structure of thylakoid and CO2-reduction-cycle components occurred during domestication
of crop plants or more recently through breeding. Properties of most components are highly “conserved” in
the sense that very little genetic variation is found
among higher plants and, indeed, between higher plants
and their ancestral green algae (Chlorophyta).
An obvious target for genetic engineering is to im-
prove rubisco’s affinity for CO2 thus reducing photorespiration (Long, 1998) and, perhaps, need for a high
concentration of this enzyme. With an improved enzyme, the amount of N per square meter of leaf area
needed to achieve a given photosynthesis rate might be
less because rubisco accounts for a large fraction of the
N in C3 leaves. Considerable genetic variation is found
in rubisco—not surprising considering its very large molecular weight (.500 000)—and the enzyme’s properties
vary within and among crop species (e.g., Makino et
al., 1988). Rubiscos from C4 species have higher Km
(Michaelis-Menton constant) for CO2 (i.e., less affinity
for CO2) than those from C3 species (Yeoh et al., 1980,
1981). The high Km values are correlated with greater
catalytic capacity of the C4 carboxylases and less inhibition by high [CO2] (Yeoh et al., 1980). Yeoh et al. (1980)
speculated that a tradeoff exists between capacity and
affinity. It may be that reduction in C3 photorespiration
through greater rubisco affinity for CO2 would be linked
with a lower catalytic capacity, and thus a need for
greater amounts of the enzyme and N in leaves.
Much remains to be done in identifying roles for many
of the proteins found in thylakoids. Given the complexity of the thylakoid system and its genetic control, advances through genetic engineering may come slowly,
if at all. Progress seems more likely through changes in
rubisco, in leaf acclimation within the canopy, and in
protection from excessive excitation of chlorophyll.
Many of the advances in yield achieved during the past
50 yr have come through improvements in canopies.
In maize, for example, large increases in plant density
coupled with much greater N supply and “stay green”
character resulted in more rapid achievement and
greater duration of full cover. Further progress will require better understanding of what constitutes an optimal canopy. Acclimation and protection are central issues in that question and deserve special attention.
Acclimation
Crop plants are exposed to widely fluctuating conditions of light and temperature, and supplies of water
and nutrients, and have evolved with a leaf-level photosynthetic apparatus that is highly flexible in structure
and activity. Depending upon environment, leaves develop with different numbers and sizes of cells, different
numbers of chloroplasts per cell, and with variations
in amounts and proportions of thylakoid and carbonreduction-cycle components. Changes in these factors
seem more related to photosynthetic activity per unit
C and N invested in leaf structure than per unit leaf
area. Acclimative changes depend on light environment
and position in the canopy and continue on a time scale
of days to weeks throughout the life of a leaf.
Acclimation to light is proportional to mean daily
irradiance of the leaf rather than to peak irradiance
(Chabot et al., 1979). This ability is important because
new leaves generally emerge at the top of a crop in full
sun and later are submerged into the shade of the canopy
as other leaves develop above them. C3 leaves in full sun
typically have more of their leaf N involved in electron
LOOMIS & AMTHOR: METABOLIC EFFICIENCY
transport and carbon reduction and less in light harvesting (and fewer grana stacks) than is the case for shade
leaves (Terashima and Evans, 1988; Evans, 1993; Pons
and Pearcy, 1994). These properties also vary with depth
within the leaf from its sunlit surface (Evans, 1995; Terashima and Hikosaka, 1995). In Evans’ (1993) study of
alfalfa (Medicago sativa L.) canopies, soluble proteins
(e.g., rubisco) declined more with depth in the canopy
than did thylakoid proteins. In addition, chlorophyll
a/b decreased with increasing depth in the canopy, reflecting a decline in reaction centers relative to lightharvesting antennae. These changes resulted in a decline
in chloroplast N/chlorophyll in a way that maintained
photosynthetic capacity per unit N, a key trait for optimal distribution of N within the canopy.
Leaf adjustments to limiting supplies of N are especially important, involving changes in number and size
of new leaves as well as in proportions of thylakoid and
carbon-reduction-cycle components with depth in the
canopy. Optimal distribution of N among leaves within
a canopy is important and has received attention in
recent years (Dreccer et al., 1998). The problem also
involves canopy architecture, solar track, sky condition,
and time remaining in the season (Loomis, 1993). For
young crops with small leaf area, increasing leaf area
for greater radiation interception provides more benefit
than increasing photosynthetic capacity of existing
leaves (through greater N content per unit leaf area).
Protection
Leaves exposed to full sun encounter challenges in
balancing electron transport with their capacity for carbon reduction and/or the supply of CO2. For crop plants
well supplied with water and nutrients, present low atmospheric CO2 concentration (near 360 mmol mol21
air) is a greater problem than reduction capacity. Daily
photosynthesis of such crops can be equivalent to all of
the CO2 in 100 m of air. Although atmospheric turbulence extends the mixing to much greater heights and
ensures that concentrations within the canopy generally
remain above 250 mmol CO2 mol21 air, CO2 concentration within leaves (Ci) limits maximum photosynthesis
rates in C3 crops. At the heart of the situation is rubisco’s
low affinity for CO2.
As light flux increases and Ci becomes limiting to the
carbon reduction cycle (Fig. 2), the light-response curve
of CO2 uptake departs from a linear increase (minimum
number of quanta required per CO2 reduced) and plateaus at a maximum, light-saturated rate (Amax). Absorption of light energy continues but the excitation energy
cannot be dissipated in the usual way because ADP and
NADP1 substrates are not available to accept electrons;
i.e., the reaction centers are “closed”. Limitations to
CO2 supply because of stomatal closure (e.g., drought
stress) or low capacity for CO2 reduction (e.g., N deficiency or low temperature) increase the likelihood that
PFD will be in excess of rate of use.
Closure places reaction centers at risk of short- or
long-term photodamage. The D1 protein in the core of
PSII is particularly vulnerable given the large redox
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Fig. 2. CO2 uptake (PS rate) by a leaf with increasing photon flux
density (PFD). Departure from the initial slope (which defines the
minimum quantum requirement) occurs as CO2 becomes limiting
and photosynthesis approaches a maximum, light-saturated rate
(Amax). The shaded area represents what Björkman and DemmigAdams (1994) term “excess PFD”.
potential (about 1.17 eV) developed there and the presence of singlet oxygen (1O2) (Barber, 1998). As a result,
this protein turns over very rapidly (once or twice per
hour) in illuminated leaves. Repair is expensive: the
protein must be ejected from the PSII center, rebuilt,
and reinserted. Such photodamage increases the minimum quantum requirement and reduces Amax.
With small leaf area, canopy photosynthesis is maximum with spreading leaves despite high levels of light
saturation and the potential for photodamage. With
more leaf area, canopy architectures that result in less
irradiance per unit leaf area (e.g., erect leaves) are effective in limiting these problems. Some crops, notably
legumes, alter leaf display during the day in ways that
reduce light absorption in high light (reviewed by
Koller, 1990) and, in all crops, small portions of the
excess energy may be expended in nitrite or sulfite reduction or in leaf maintenance.
In C3 leaves, the reaction centers may be kept open
and excess energy dissipated by utilization of NADPH
and ATP in photorespiration. In this, rubisco catalyzes
the condensation of O2 with RuP2, rather than CO2, and
glycolate (a potentially toxic compound) and PGA are
generated. In terrestrial plants, glycolate is metabolized
in peroxisomes and mitochondria (where CO2 is released), producing glycerate. Glycerate is taken up by
chloroplasts where it and PGA participate in regeneration of the RuP2 substrate used by rubisco. In this way,
three of every four C atoms are recycled allowing another cycle of O2 or CO2 reduction unless serine (which
is involved in a mitochondrion-to-peroxisome transfer)
is “drained” off to protein synthesis.
Unfortunately, photorespiration increases with tem-
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perature because of decreased solubility of CO2 in the
stroma and decreased affinity of rubisco for CO2 relative
to O2 (i.e., decreased specificity for CO2). Even in dim
light, when there is no need for protection, photorespiration increases the quantum requirement for CO2 reduction (qr) of C3 plants from a minimum value near 11
mol photons mol21 CO2 at low temperature (,158C) to
about 25 at temperatures near 358C (Ehleringer and
Björkman, 1977). The slow rate of photorespiration at
low temperature means that it cannot offer much protection against over-excitation under those conditions.
Björkman and Demmig-Adams (1994) offered data on
performance of cotton (Gossypium hirsutum L.) (Table
1) as evidence that photorespiration also provides only
modest protection under drought.
To what extent rubisco acts as carboxylase or oxygenase depends upon the relative concentrations of CO2
and O2 presented to the enzyme. Under elevated atmospheric CO2, the CO2 concentration within C3 leaves
increases and oxygenase activity is suppressed. C4 plants
suppress photorespiration in ambient air by the same
principle—the CO2-concentrating action of their mesophyll cells keeps rubisco (in bundle sheath cells) well
supplied with CO2. Oxygenase activity is then only a
small percentage (2–6%) of the net CO2 flux (de Veau
and Burris, 1989).
Osmond and Grace (1995) considered another form
of protection based in Mehler and ascorbate-peroxidase
reactions, which operate well in water-stressed plants,
as perhaps more important than photorespiration for
protection of C3 leaves. This involves formation at PSII
of peroxide (H2O2), which is then reduced by ascorbate
peroxidase. The oxidized ascorbate is regenerated by a
reductase with expenditure of NADPH. These reactions
keep both reaction centers open without a net exchange
of O2. Because study of this pathway depends on examining oxygen isotope discrimination, which is difficult,
little is yet known about its protective role.
Another system of protection exists in interconversion of carotenoid pigments found in association with
chlorophyll in light-harvesting complexes (DemmigAdams and Adams, 1996; Gilmore, 1997). With high
PFD, pH changes in the thylakoid lumen induce conversion of violaxanthin to zeaxanthin (Fig. 3), which can
accept resonance energy from chlorophyll. When reaction centers close, excitation energy passes from chlorophyll to zeaxanthin and is converted to thermal energy
(increasing leaf temperature) before it reaches the PSII
reaction center. The leaf thermal energy is dissipated
to the environment through convection, transpiration,
and long-wave (infrared) radiation emission. Such “nonphotochemical quenching” of excited chlorophyll is assayed easily through measurements of variable chlorophyll fluorescence. In dim light, zeaxanthin recycles to
violaxanthin, which cannot intercept energy from chlorophyll. Björkman and Demmig-Adams (1994) and Gilmore (1997) view nonphotochemical quenching as a
major mechanism for protection of PSII from excess
PFD.
Little is yet known about the need for photoprotec-
Table 1. Carbon dioxide assimilation (PS-CO2) and photorespiration (PR-O2) per unit leaf area and their contributions to dissipation of chlorophyll excitation energy in cotton leaves under
full sun with variations in water supply. Leaves of well-watered
plants (Cleaf 5 21.0 MPa) were compared with leaves from
plants under extended drought. Adapted from Björkman and
Demmig-Adams (1994).
Well-watered → Moisture stressed
Cleaf (MPa)
PS-CO2 (mmol m22 s21)
PR-O2 (mmol m22 s21)
Energy dissipation (%):
PS
PR
Total
21.0
44
33
21.9
27
24
22.8
13
13
26
20
46
16
14
30
9
9
18
Fig. 3. Daily course of the xanthophyll photoprotective system in
cotton under field conditions (adapted from Björkman and Demmig-Adams, 1994). (Top) Incident PFD, efficiency of PSII, and
fraction of PSII centers that were closed. This amount of closure is
much less than would occur without intervention of the xanthophyll
cycle. (Bottom) Concomitant changes in concentrations of xanthophyll pigments during the day as violaxanthin was converted to
zeaxanthin, which is capable of accepting excitation energy from
chlorophyll.
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LOOMIS & AMTHOR: METABOLIC EFFICIENCY
tion by crops. Young crops with spreading leaves are at
the most risk. Within canopies, leaves are displayed at
angles to the sun’s rays that greatly limit the amounts
of excess PFD they absorb. In addition, most crop plants
are “sun” plants with a large capacity for photosynthesis
and less need for photoprotection than plants having
less capacity. Sun plants generally have high stomatal
conductance that helps maintain Ci and allows sunlit
leaves to dissipate heat by transpiring freely. Yield advance in CIMMYT wheat (Triticum aestivum L. var.
aestivum) lines, for example, has been associated with
increased stomatal conductance (Fischer et al., 1998).
That trait obviously is most useful for well-watered conditions.
Debate continues on the relative roles and merits of
various protective systems. Osmond and Grace (1995)
viewed photorespiration and the ascorbate-peroxidase
reactions as the main protection. Andrews and Baker
(1997) suggested that photorespiration buffers against
imbalances in PFD absorption by PSI and PSII. Björkman and Demmig-Adams (1994) and Long (1998), by
contrast, saw little merit in photorespiration and view
leaf acclimation, canopy architecture and the xanthophyll cycle as the principal means of protection. Long
(1998) suggested that photorespiration persists only because evolution has reached a “barrier” for improvements in rubisco’s affinity for CO2. He noted that rubisco
in some Rhodophyta has greater affinity for CO2 and
might serve as a source of genetic material.
Radiation-Use Efficiency
Crop growth rate and yield are functions of canopy
photosynthesis and they generally correlate poorly if at
all with maximum photosynthesis rates of individual
leaves. Given the oblique display and mutual shading
of leaves within canopies, few leaves are exposed to
PFD sufficient to achieve Amax. Other reasons for the
discrepancy can be found in acclimation to radiation
level, temperature and stress, and the amount of standing crop (and thus the amount of maintenance respiration). As a result, crop physiologists have sought other
measures that would relate yield and canopy photosynthesis. Light-conversion efficiency (commonly termed
radiation-use efficiency, RUE) has received the most
attention. RUE is measured and reported in various
units, e.g., g new biomass produced MJ21 radiation intercepted or absorbed by leaves. A useful feature of RUE
is that experimental values can be compared with estimates of potential rates of dry matter production that
might be possible by a canopy of well-acclimated leaves.
Potential RUE would be attained with all leaves exposed to only moderate PFD (little or no light saturation
and, thus, minimum qr). If that crop at the same time
intercepted most of the incoming radiation, its rate of
biomass production per unit land area would also be
maximized.
We recently reexamined potential RUE for C3 plants
in light of modern understanding of quantum requirements and C losses in respiration (Loomis and Amthor,
1996). Calculations were done for a C3 crop with 1000
g m22 standing biomass (the midseason amount for a
crop producing 10 Mg grain ha21), moderate maintenance respiration, and a growth yield in biosynthesis
(YG) of 0.72 g new biomass g21 assimilate consumed.
(YG is discussed below in the section on a Functional
Model of Respiration.) Calculated RUE varied from
4.1 g MJ21 solar radiation absorbed for qr 5 10 to only
1.1 at qr 5 30. This wide range of qr embraced the large
increase in photorespiration that occurs in C3 leaves
with increasing temperature (Ehleringer and Björkman,
1977). By these calculations, the average performance
observed for high-yielding wheat crops (near 1.5 g MJ21
solar radiation absorbed, with roots included; Fischer,
1983) corresponded to a qr of 24 (Loomis and Amthor,
1996). Some wheat crops reached 2 g MJ21, however,
corresponding to qr 5 14.
Similar calculations for maize-type C4 species are presented in Table 2. Given the small amount of photorespiration in C4 leaves, only a small range of qr values
around 16 is considered. The minimum possible qr for
C4 plants is larger than for C3 species because ATP is
expended in malate production, a cost that is increased
by leakage of concentrated CO2 from the bundle sheath
leading to “over-cycling” of malate (Jenkins, 1997).
Ehleringer and Pearcy (1983) reported minimum values
for several C4 species in a narrow range around qr 5
15.4 mol photons mol21 CO2. That high efficiency seems
to require participation of the thylakoid Q-cycle (enhanced ATP production) to offset the cost of malate
over-cycling (Jenkins, 1997). With qr 5 16, 1400 g bioTable 2. Estimates of potential radiation-use efficiency (RUE)
of C4 crops at different quantum requirements. Assumptions
are for a maize crop with a closed canopy completely intercepting incident solar radiation and with all leaves functioning
at a uniformly small quantum requirement. For convenience,
calculations are based on 1 MJ of incoming solar radiation
(with PAR 5 0.5 total solar) and all values scale linearly with
the level of incoming radiation. CH2O is a unit of carbohydrate
with MW 5 30.
PAR absorption:
Solar radiation intercepted
PAR quanta intercepted by crop
Canopy reflection
PAR quanta absorbed by crop
RUE calculation:
CH2O produced (mmol)
CH2O used in maintenance‡ (mmol)
CH2O available for growth (mmol) (g)
RUE, solar radiation basis§
(g/MJ intercepted)
RUE, PAR basis
(g/MJ PAR intercepted)
(g/MJ PAR absorbed)
1.00 MJ
2.20 mol
20.13 mol
2.07 mol
Quantum requirement†
14
148
25
123
3.69
16
18
129
115
25
25
104
90
3.12
2.70
2.7
2.3
2.0
5.5
5.8
4.6
4.9
4.0
4.2
† Units are mol photosynthetically active quanta/mol CO2 reduced; 15 mol
quanta/mol CO2 is near the minimum possible by maize-type C4 plants
(NADP-dependent malic-decarboxylating enzyme).
‡ Assumptions are a maintenance respiration rate of 0.5 mmol CH2O g21
biomass d21 (20–308C; 0.015 g g21 d21) with 1400 g m22 biomass intercepting 28 MJ solar radiation m22 d21. That biomass is 0.5 of the amount
accumulated by a crop that produces 14 t grain ha21.
§ At YG 5 0.74 for growth of aboveground biomass including grain from
glucose and NO3–N. That value was derived from studies on grain sorghum [Sorghum bicolor (L.) Moench.] (Lafitte and Loomis, 1988). This
YG corresponds to biomass containing 43% C and <1.1% N (<7%
N compounds.)
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mass m22, and YG 5 0.74, the calculation presented in
Table 2 predicts an RUE of 2.3 g MJ21 solar radiation
intercepted (4.6 g MJ21 PAR intercepted).
Calculated RUE values are sensitive not only to variation in qr (which varies with radiation level; see Fig. 2)
but also to variation in maintenance respiration, which
depends on temperature, maintenance coefficient, and
size of standing crop. For the system presented in Table
2 with qr 5 16, variations in maintenance lead to the following:
Maintenance (mmol CH2O):
RUE(g MJ
21
solar):
0
2.7
20
2.4
40
2.0
60
1.5
where CH2O represents carbohydrate with MW 5 30
and maintenance is per megajoule solar radiation intercepted. RUE is also sensitive to variation in YG, which
declines as concentrations of protein and/or lipid increase; i.e., the amount of assimilate used per gram new
biomass increases. Thus, the largest RUE occurs for
crops with a large content of carbohydrates (cellulosic
material, starch, sugars). Where comparisons are to be
made between crops differing in composition, RUE
should be expressed either in glucose equivalents required in synthesis (see below; and Flenet and Kiniry,
1995) or in energy content of the biomass. At qr 5 16,
RUE of 2.3 g biomass MJ21 solar radiation intercepted
can be expressed as equivalent to 104/6 5 17.3 mmol
glucose MJ21 (Table 2). Biomass of this composition
would have a heat of combustion near 17.6 kJ g21 corresponding to over 4% of absorbed solar radiation (and
near 9% of absorbed PAR).
Gallo et al. (1993) and Sinclair and Muchow (1999)
discussed difficulties inherent in experimental determination of RUE (large SEs for both growth rate and
radiation interception) and offered protocols for good
results. There have been reports of seemingly valid measurements of 4 to 5 g MJ21 PAR intercepted by healthy
maize crops during vegetative growth but Sinclair and
Muchow rejected those larger than 3.2 to 3.4 g MJ21
PAR as failing to meet their standards. Their maximum
values can be increased by about 10% to 3.5 to 3.7 g
MJ21 PAR to account for roots but they still fall well
short of the 4.6 g MJ21 PAR estimated in Table 2. As
was found with calculated RUE values, measured values
for C4 crops generally exceed those of C3 crops, and, for
maize, smaller values were found during cool weather
(Andrade et al., 1993) and under stress, such as high
evaporative demand (Kiniry, 1999). In one of the few
successful comparisons of cultivars, Tollenaar and
Aguilera (1992) found that postanthesis RUE of a maize
hybrid released in 1988 exceeded that of a 1959 hybrid.
The difference was related to the “stay-green” trait possessed by the 1988 hybrid.
Contrary to the hopes of crop physiologists, the variable nature of RUE and difficulties in its measurement
prevent it from serving, as a sensitive measure for exploring the fine structure of photosynthetic systems. Uncertainty about what constitutes a “reliable” value of
RUE also raises serious questions about its wide use as
a driving variable for crop simulation models. Perhaps
the RUE era should be closed. It persists, however,
because the alternatives for study of canopy photosynthesis are difficult or expensive and because crop modelers resist replacing it by submodels that simulate canopy photosynthesis.
Respiration and Biosynthesis
The Respiratory System
Respiration in higher plants is commonly viewed as
a sequence of enzymic steps. With hexose as a generic
substrate, flow of carbon can be traced through the
glycolytic pathway (found in cytosol and plastids) to the
tricarboxylic acid (TCA) cycle in the matrix solution
of mitochondria. Mitochondria, like chloroplasts, are
enclosed by an outer membrane that encompasses a
convoluted inner membrane, inside which is the matrix
(Fig. 4). The basic scheme of respiration is that hexose
(e.g., glucose) is partially oxidized to pyruvate, which
is then taken up by mitochondria where it is completely
oxidized to CO2. A portion of the energy released is
captured in reduced nucleotides (NADH and FADH2),
which may in turn transfer their protons (H1) and associated e2 to a series of protein complexes located in and
on the inner mitochondrial membrane. These complexes
serve in electron and proton transport. Protons are
moved to the intermembrane space, creating a gradient
across the inner membrane that serves to drive Fo-F1
ATP synthases (Boyer, 1997) that convert ADP and
Pi to ATP. The H1 and e2 are eventually reunited in
reduction of O2 to H2O.
Several variations may occur in this pathway. The
oxidative pentose pathway, for example, routes some
of the glucose-6-P from the beginning of the glycolytic
pathway through pentose sugars to fructose-6-P and
glyceraldehyde-3-P (glycolytic intermediates). CO2 is
liberated and NADP1 is reduced. Possible functions of
this oxidative pentose phosphate pathway, in addition
to production of NADPH, are production of ribose-5P and erythrose-4-P, which are important precursors in
biosyntheses. Another alternative route occurs at the
end of glycolysis where a “malate shunt” (Amthor,
1994a) may bypass pyruvate kinase through production
of malate from PEP by PEP carboxylase. The shunt is
favored when ADP is in short supply. Malate serves as
substrate in amino synthesis and can be stored in vacuoles (balanced by K1, it serves there as an important
osmoticum) or metabolized in the TCA cycle. An interesting point is that pyrophosphate (PPi), rather than
ATP, can be used in phosphorylating hexose at the start
of the glycolytic scheme and this may be an essential
process in some plants (Plaxton, 1996).
The products of glycolysis (pyruvate and malate) can
be completely oxidized in the TCA cycle with production of ATP and reduced nucleotides. As detailed in
Fig. 4, the great bulk of ATP production then occurs
through oxidation of the nucleotides by protein complexes located in the mitochondrial inner membranes.
If all reducing agents produced by glycolysis and the
TCA cycle are employed in ATP production, a total
of about 30 mol ATP mol21 glucose can be produced
LOOMIS & AMTHOR: METABOLIC EFFICIENCY
1591
Fig. 4. Respiratory-chain reactions associated with the inner mitochondrial membrane. Mitochondria are enclosed by two membranes; the outer
membrane (not shown) is permeable to metabolites but the inner one is not. NAD(P)H in the mitochondrial matrix and in the cytosol can
be oxidized by several mitochondrial dehydrogenases. Complex I oxidizes matrix NADH and in so doing pumps protons from the matrix to
the cytosolic side of the inner membrane. Other inner-membrane-bound dehydrogenases (indicated by DH) do not pump protons. Innermembrane dehydrogenases (including complex II, which functions as part of the TCA cycle) transfer electrons (and protons) to ubiquinone
(Q), which is reduced to ubiquinol (QH2) in the process. A mobile Q/QH2 pool exists in the inner membrane. Complex III oxidizes QH2 and
passes electrons to cytochrome (cyt) c, which in turn passes electrons to complex IV. Electron transport through complexes III and IV is
coupled to proton translocation across the inner membrane; a “Q-cycle” associated with Complex III is included in the diagram. Free O2 is
reduced to water by complex IV. The alternative oxidase (alt ox) can also oxidize QH2, and form water, but this bypasses two sites (complexes
III and IV) of proton translocation in the mitochondrial electron transport chain. Protons may enter the matrix through membrane leaks,
but Fo-F1 ATP synthase (similar to the CFo-CF1 ATP synthase in Fig. 1) is the main route of proton entry. Apparently, one ADP is
phosphorylated when three protons pass through the F0-F1 ATP synthase. The ADP required for ATP formation enters the mitochondrial
matrix only as ATP exits the matrix through an antiporter. A symporter couples the transport of Pi and H1 into the matrix.
(Amthor, 1994a; Stryer, 1995). (This amount is less than
36 mol ATP commonly quoted in older biochemistry
texts.) About half of the free energy of hexose is cap-
tured in ATP when a hexose molecule is completely
oxidized in respiration; the rest is lost as heat. Most of
the “retained” energy is also lost as heat when ATP is
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CROP SCIENCE, VOL. 39, NOVEMBER–DECEMBER 1999
subsequently used (hydrolyzed). Thus, when hexose is
completely used for the formation of ATP, nearly all
its free energy is eventually lost as heat.
Alternative Oxidase
The alternative oxidase found in mitochondria (alt
ox in Fig. 4) deserves special comment. Electrons that
pass to this oxidase bypass two sites (complexes III and
IV) of proton translocation with the result that less ATP
is formed. Lambers et al. (1998, p. 106–111) summarize
possible roles for the oxidase. Most relevant to competitively grown crops is the theory that it serves to waste
protons and e2 when ATP is already in abundance,
allowing the TCA cycle and glycolysis to proceed in
production of carbon intermediates needed in biosyntheses. The oxidase is under a high degree of coarse and
fine control (including induction by organic acids and
rapid activation), however, indicating that its role may
be more fundamental (Vanlerberghe and McIntosh,
1997).
The magnitude of e2 flux through the alternative oxidase remains uncertain but we found no evidence that
it has a significant impact on crop performance. Early
studies were done with cyanide (inhibits e2 transport
to complex IV) and SHAM (salicylhydroxamic acid;
inhibits the alternative oxidase) but these have side effects that affect respiratory rates. Better information is
obtained with noninvasive isotope methods (alternative
oxidase discriminates against heavy O2 more than complex IV; Guy et al., 1989). Little alternative oxidase
activity was observed in rapidly growing roots with the
isotope method, whereas more than half the total e2
flux in older roots terminated at the alternative oxidase
(Millar et al., 1998).
System Nature and Control of Respiration
It is important to emphasize the system nature of
respiration. Many of the steps are reversible and may
be employed, for example, in synthesis of sugars from
lower-level compounds. In addition, rather free exchange of various intermediates (e.g., hexose phosphates, dihydoxyacetone-P, and PEP) occurs between
the cytosolic and plastid glycolytic schemes. Particularly
significant is the diversion of glycolytic intermediates
to synthetic pathways: PEP to shikimic acid pathways
to various alkaloids and lignin; dihydroxyacetone and
acetyl CoA to lipid synthesis; and acetyl CoA to isoprenoids (carotenoids, abscisic acid).
The TCA cycle is also a factory for intermediates
with oxoglutarate serving as precursor to porphyrins
(chlorophyll, cytochrome) and amino acids (and thus
protein). As a result, respiration rarely (perhaps only in
some nongrowing tissues) operates in the simple linear
series outlined earlier. This remarkable flexibility is important in balancing widely varying demands for ATP,
reductant, and intermediates found in various tissues
and at various times. The ability to employ reducing
agents directly in syntheses or in production of ATP is
particularly important. The oxidative pentose phos-
phate pathway and the malate shunt also contribute
flexibility (and complexity).
The flexibility of the system depends upon coarse
control at several levels with the PEP-to-pyruvate conversion (pyruvate kinase) being one key. Except in rapidly growing tissues, however, respiration is seldom limited by substrate or enzyme capacity. Experiments with
agents that uncouple respiratory metabolism from proton transfer, for example, reveal that normal rates are
only a small fraction of capacity. In most tissues, the
system is ultimately dependent upon the supply of ADP
for ATP production. If ATP is not used rapidly in metabolism, respiration slows or stops. This “close coupling” is an important and useful concept. Shortage of
ADP could slow production of intermediates, for example, in green tissues when chloroplasts take up ADP
and Pi and release ATP to cytosol. More generally, it
occurs when there is little use of ATP within the cells
as may occur when growth is slow.
Genetic Control of Respiration–Biosynthesis
Like chloroplasts, mitochondria are thought to have
resulted from ancient endosymbioses with bacteria and
this is reflected in their circular, polyploid, DNA. The
protein complexes of mitochondrial electron transport,
like their counterparts in chloroplasts (Fig. 2) are composed of numerous subunits. Genetic control is much
simpler than for photosynthesis, however. Glycolytic
and TCA cycle enzymes are encoded by nuclear genes
while mitochondrial DNA encodes most of the e2 transfer complexes (Siedow and Umbach, 1995; Taiz and
Zeiger, 1998). The alternative oxidase is under nuclear
control. Isozymes are found for some glycolytic enzymes, the proportions of which may vary with tissue,
developmental stage, and environment (Plaxton, 1996).
This may be important for regulation and/or tissue-specific metabolism.
Because respiration is driven by demands for its products (ATP, reductant, C-skeletons), much of the genetic
control resides with nuclear genes that determine form,
structure, and composition (i.e., growth and development) of the whole plant.
A Functional Model of Respiration
Before 1940, when respiratory pathways and the role
of ATP were not fully understood, research on respiration depended on measurement of substrate use or gas
exchange. Microbiologists concerned with production
efficiency of fermentation gave particular attention to
the fate of substrate carbon. Duclaux (1898, cited by
Pirt, 1965) was perhaps the first to distinguish between
substrate used in microbial growth and that used in
maintenance of cells. Animal scientists also recognized
a maintenance component, in feed requirements and
gas exchange, that included basal metabolism and was
distinct from requirements for growth and work. Plant
scientists, by contrast, focused in their early work on
special cases where respiration rates were increased, for
example, by ion uptake, ripening of fruit, or germination.
LOOMIS & AMTHOR: METABOLIC EFFICIENCY
K.J. McCree (1970) demonstrated through regression
analysis of gas exchange by white clover (Trifolium repens L.) plants of different sizes that whole-plant respiration could be partitioned into two components, one
related to gross photosynthesis and the other to dry
mass of living tissue. This opened a new era in plant
research. Thornley (1970) showed that McCree’s equation could be derived from Pirt’s (1965) version of the
Duclaux equation. Pirt’s definition of maintenance as
“energy consumed for functions other than production
of new cell material” was carried forward by default.
Penning de Vries (1975) identified protein turnover and
active intracellular transport (e.g., maintenance of ion
gradients) as the most important maintenance processes. Some workers distinguish intercellular transport
as a third component, but this is normally distributed
between growth and maintenance components.
Two useful definitions derive from Pirt’s equations:
Observed growth yield, Y 5 Dw/(DSG 1 DSM), [1]
where Dw is the amount of biomass formed, DSG is
the amount of substrate used in growth and DSM is the
amount of substrate used in maintenance during the
same period of time, Dt. DSM can be further defined as
mW, where m is the “maintenance coefficient” and W
is total living mass. Observed growth yield was recognized in the “growth efficiency” of Tanaka and Yamaguchi (1968). When mW is zero, or removed,
True growth yield, YG 5 Dw/DSG.
[2]
DSG is composed of two parts: DSR, which is completely
respired to provide energy for synthesis (i.e., “growth
respiration”), and DSB, which is retained in the new
biomass as carbon skeletons. Total respiration for the
period Dt then is
R 5 DSM 1 DSR.
[3]
The concept of close coupling of respiration with constructive use of ATP and reductant is implicit in these
equations. Where it can be identified, however, a term
for “wasteful respiration” can be included (Thornley, 1971).
Maintenance Respiration
Methods for estimating maintenance coefficients (m)
in higher plants were reviewed earlier (Amthor, 1989).
All are subject to some criticism. In particular, none
has the ability to account for the high rates of protein
turnover that occur in leaves in light and for interactions
between respiration, photosynthesis, and photorespiration (see above and discussion by Amthor, 1994b). Values of m of 15 to 50 mg hexose g21 biomass d21 have
been reported at temperatures near 258C. The rate increases with temperature with Q10 of about 2 and with
N content of the material. The increase in m with N
content is expected on the basis that protein turnover
is probably a major factor in maintenance. Zerihun et
al. (1998) calculated turnover costs of 0.41 g glucose/g
protein with 30% amino acid cycling. On this basis,
protein turnover would account for only 3 to 20% of
observed maintenance respiration. Maintenance also in-
1593
creases during senescence and McCree (1982) and others found that m tended to increase with growth rate.
It is well to keep in mind, however, that rapid growth
requires rapid respiration for biosynthesis. And, growth
per unit respiration is greatest with efficient respiration.
Given the difficulties in measurement, few attempts
have been made to determine the value of m under
field conditions (all have employed McCree’s regression
method). Early work reviewed by Amthor (1989) and
a more recent study by Mitchell et al. (1991) support
the general conclusion that seasonal maintenance respiration about equals seasonal growth respiration. This
question has also been approached theoretically with
simulation models. For example, Ng and Loomis (1984)
employed m values appropriate to each type of tissue
in simulating total-season mW for a potato (Solanum
tuberosum L.) crop; total maintenance equaled 21% of
seasonal gross photosynthesis compared with 20% for
growth respiration. The sensitivity of such models to
values of m indicates that a small reduction in m might
correspond to an appreciable advance in yield. Wilson
(1982) made the promising discovery that ryegrass (Lolium perenne L.) selections having low rates of respiration in mature leaves had higher yields of simulated
swards in growth chambers. The work was based on the
common assumption that respiration of mature leaves
is mainly maintenance although phloem loading and
biosynthesis of amino acids and other compounds may
occur there. Wilson’s selections have been subjected to
considerable study without resolving the basis for the
smaller value of m and Kraus’ (1992) report that the
yield advantage disappeared when the simulated swards
were grown at low density is a bit sobering. More recently, Earl and Tollenaar (1998) found a strong negative association across a series of maize hybrids between
seasonal dry matter production and respiration rates of
mature leaves.
It remains unclear whether crops already operate efficiently or whether reduction in m might be possible.
This will require more knowledge about membrane
leakage and turnover of individual proteins and about
whether present rates of those processes are necessary
for healthy plants. Much of our existing knowledge was
obtained with plants grown in nutrient cultures under
low PFD; good data for crops growing under field conditions (e.g., Mitchell et al., 1991) are rare and are needed.
Growth Respiration
Equation [2] offered a method for analysis of true
growth yield that was elegantly pursued by Penning de
Vries et al. (1974). By tracing “least-cost” biochemical
pathways, they constructed balance sheets for use of
substrate, ATP, and reductant and release of CO2 during
synthesis of individual compounds. From these, they
calculated general YG values (which they termed production values, PV) for carbohydrates, proteins, lipids,
lignin, and other constituents of plant mass. Given a
proximal analysis of biomass, this allows calculation of
the amount of substrate and respiration involved in its
synthesis if all goes well in the plant and least-cost pathways are actually used.
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CROP SCIENCE, VOL. 39, NOVEMBER–DECEMBER 1999
Penning de Vries et al. (1974) assumed a yield of 38
ATP per glucose oxidized (P:O 5 3) (rather than about
30 as given above) causing a 3% overestimate of YG for
maize in their Table 6. They showed in a sensitivity
analysis (their Fig. 6) that variation of P:O between 2
and 3 had only a slight effect on YG because the bulk
of carbon used in synthesis was retained in the C-skeleton of the product and use of reductant was as important
as was use of ATP. YG values (Penning de Vries et al.,
1983), in grams of product per gram of glucose consumed, for typical lipid (0.33), protein (0.40 from NO3N and 0.62 with amide-N), and lignin (0.47) are much
smaller than for carbohydrates (0.83) and organic acids
(.1). Calculating protein yields starting with amide-N
mimics metabolism during seed formation that utilizes
N mobilized from vegetative tissues.
Comparison of YGs for various grains and types of
biomass helps rationalize differences in yields among
crops (Sinclair and de Wit, 1975; Penning de Vries et
al., 1983). With other constituents of a seed held constant, YG declines almost 0.50% for each percentage
increase in lipid concentration (replacing carbohydrate)
and about 0.25% for each percentage increase in protein
concentration (again, replacing carbohydrate). This illustrates why, for some purposes, RUE comparisons
should be made in glucose or energy content equivalents. Comparing maize and soybean [Glycine max (L.)
Merr.] grains starting with nitrate:
Maize: YG 5 0.74 g grain g21 glucose
Soybean: YG 5 0.50 g grain g21 glucose.
Thus, for the same amount of assimilate, soybean can
yield only 2/3 as much as maize (soybean yield is even
less when it depends on N2 fixation). Similar exercises
explain why high-lysine grains, which have a smaller YG
than normal grains, generally yield less (Mitra et al.,
1979), and why suggestions for increasing proline and
betaine contents as osmotica in moisture-stressed plants
would be counter-productive.
YG can also be estimated from complete (McDermitt
and Loomis, 1981) or partial (Vertregt and Penning de
Vries, 1987; Williams et al., 1987) elemental analyses
of biomass. Complete elemental analysis provides the
reduction level of the biomass relative to standard states
and closely correlates with heat of combustion of the
biomass (McDermitt and Loomis, 1981; Jenkins and
Ebeling, 1985). In line with the P:O sensitivity analysis of
Penning de Vries et al. (1974), McDermitt and Loomis
(1981) concluded that only about 20% of the energy
content of glucose is lost in least-cost biosynthesis.
Growth respiration may be calculated directly with
the pathway method of Penning de Vries et al. (1974).
In their Table 6, they found that growth respiration (SR)
for young maize plants with a large (23%) content of
N compounds equaled 12 mmol CH2O g21 biomass, or
about 24% of substrate used for growth. Our Table 2,
with about 7% N compounds, qr of 16, and RUE of 2.3
g MJ21 intercepted begins with 129 mmol C in gross
photosynthesis. Of this, 25 mmol C (19%) was expended
in maintenance, 82 mmol C (64%) was retained in bio-
mass, and 22 mmol went to growth respiration. Total
respiration consumed 47 mmol C (36%). Thus pathway
and elemental analyses provide useful hypotheses about
how the productivity of crops varies with composition.
The calculated values are in line with limited and somewhat imprecise experimental observations for good
crops (Amthor, 1989) but we don’t yet know the extent
that crops attain those levels of efficiency.
Assessments
We have emphasized selected physiological aspects
of photosynthesis and respiration to demonstrate how
much remains to be accomplished in sorting out the
regulation and function of various components. If there
are inefficiencies in these systems and if the causes can
be identified, they would represent legitimate targets for
genetic manipulation. Properties of rubisco, alternative
oxidase, and the photorespiration process already loom
as opportunities for genetic manipulation. Those factors
evolved and have survived during millions of years, however, indicating utilities of which we are as yet uncertain.
With help of antisense RNAs and other methods, progress in deciphering genetic control is good, but much
remains to be learned.
Serious reinvestigation of foliage canopies offers
promise for important gains in photosynthetic productivity of crops. The first cycle of such research, begun
over 50 yr ago, demonstrated the importance of such
things as rapid and complete canopy cover, and the
strong advantages of erect leaves in dense canopies and
minimum interception by emergent reproductive structures. Those properties are now credited with contributing to yield progress in maize (Fischer and Evans, 1999).
Our discussion of acclimation and protection processes
was aimed at emphasizing fine details of canopy affairs
about which we have information for only a few crops.
Many more crops need to be studied in the way that
Evans (1995) looked at alfalfa. Given the multifaceted,
time-dependent nature of those issues, experimental
work will need support from sophisticated simulation
models to explore weaknesses in performance of present
crops. To do that, the models will need to be constructed
with fine details of morphology and physiology (Amthor
and Loomis, 1996)—details that embrace such matters
as variations in leaf and chloroplast structure and rubisco kinetics.
Understanding of photosynthetic and respiratory metabolism is now advanced enough to calculate potential
efficiencies of using sunlight to produce plant biomass.
These can be compared with best available observed
efficiencies in order to obtain a hint of whether crops
can be improved, and by how much, with respect to
basic metabolic pathways and biophysical reactions. Our
earlier analysis of wheat RUE (Loomis and Amthor,
1996), and our present one for maize, indicate that scope
exists for improvement in yield (potential) for many
crops. This scope exists within the context of existing
intercepted (or absorbed) PAR. If radiation absorption
can be further improved by more rapid canopy development or longer growing seasons, then potential yield
will be improved further.
LOOMIS & AMTHOR: METABOLIC EFFICIENCY
ACKNOWLEDGMENTS
Our thanks to R.W. Pearcy for useful discussions of photosynthesis.
REFERENCES
Amthor, J.S. 1989. Respiration and crop productivity. Springer-Verlag, New York.
Amthor, J.S. 1994a. Respiration and carbon assimilate use. p. 221–258.
In K.J. Boote et al. (ed.) Physiology and determination of crop
yield. ASA, CSSA, SSSA, Madison, WI.
Amthor, J.S. 1994b. Higher plant respiration and its relationships to
photosynthesis. p. 71–101. In E.-D. Schulze and M.M. Caldwell
(ed.) Ecophysiology of photosynthesis. Ecol. Studies 100. SpringerVerlag, Berlin.
Amthor, J.S., and R.S. Loomis. 1996. Integrating knowledge of crop
responses to elevated CO2 and temperature with mechanistic simulation models: model components and research needs. p. 317–345.
In G.W. Koch and H.A. Mooney (ed.) Carbon dioxide and terrestrial ecosystems. Academic Press, San Diego.
Andrade, F.H., S.A. Uhart, and A. Cirilo. 1993. Temperature affects
radiation use efficiency in maize. Field Crops Res. 32:17–25.
Andrews, J.R., and N.R. Baker. 1997. Oxygen-sensitive differences
in the relationship between electron transport and CO2 assimilation
in C3 and C4 plants during state transitions. Aust. J. Plant Physiol. 24:495–503.
Barber, J. 1998. What limits the efficiency of photosynthesis, and can
there be beneficial improvements? p. 107–123. In J.C. Waterlow
et al. (ed.) Feeding a world population of more than eight billion
people. Oxford University Press, New York.
Björkman, O., and B. Demmig-Adams. 1994. Regulation of photosynthetic light energy capture, conversion, and dissipation in leaves
of higher plants. p. 17–70. In E.-D. Schulze and M.M. Caldwell
(ed.) Ecophysiology of photosynthesis. Ecol. Studies 100. SpringerVerlag, Berlin.
Boyer, P.D. 1997. The ATP synthase: A splendid molecular machine.
Annu. Rev. Biochem. 66:717–749.
Chabot, B.F., T.W. Jurik, and J.F. Chabot. 1979. Influence of instantaneous and integrated light-flux density on leaf anatomy and photosynthesis. Am. J. Bot. 66:940–945.
Demmig-Adams, B., and W.W. Adams III. 1996. The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends
Plant Sci. 1:21–26.
de Veau, E.J., and J.E. Burris. 1989. Photorespiratory rates in wheat
and maize as determined by 18O-labeling. Plant Physiol. 90:500–511.
Dreccer, M.F, G.A. Slafer, and R. Rabbinge. 1998. Optimization of
vertical distribution of canopy nitrogen: An alternative trait to
increase yield potential in winter cereals. J. Crop Prod. 1:47–77.
Earl, H.J., and M. Tollenaar. 1998. Differences among commercial
maize (Zea mays L.) hybrids in respiration rates of mature leaves.
Field Crops Res. 59:9–19.
Ehleringer, J., and O. Björkman. 1977. Quantum yields for CO2 uptake
in C3 and C4 plants. Plant Physiol. 59:86–90.
Ehleringer, J., and R.W. Pearcy. 1983. Variation in quantum yield for
CO2 uptake among C3 and C4 plants. Plant Physiol. 73:555–559.
Erickson, J.M. 1996. Chloroplast transformation: Current results and
future prospects. p. 589–619. In D.R. Ort and C.F. Yocum (ed.)
Oxygenic photosynthesis: The light reactions. Adv. Photosynthesis
Vol. 4. Kluwer Academic Publishers, Dordrecht, The Netherlands.
Evans, J.R. 1993. Photosynthetic acclimation and nitrogen partitioning
within a lucerne canopy. I. Canopy characteristics. Aust. J. Plant
Physiol. 20:55–67.
Evans, J.R. 1995. Carbon fixation profiles do reflect light absorption
profiles in leaves. Aust. J. Plant Physiol. 22:865–873.
Fischer, R.A. 1983. Wheat. p. 129–154. In W.H. Smith and J.J. Banta
(ed.) Potential productivity of field crops under different environments. IRRI, Los Baños, Philippines.
Fischer, R.A., and L.T. Evans. 1999. Yield potential: its definition,
measurement and significance. Crop Sci. 39:1544–1551 (this issue).
Fischer, R.A., D. Rees, K.D. Sayre, Z.-M. Lu, A.G. Condon, and A.
Larque Saavedra. 1998. Wheat yield progress associated with higher
stomatal conductance and photosynthetic rate, and cooler canopies.
Crop Sci. 38:1467–1475.
1595
Flenet, F., and J.R. Kiniry. 1995. Efficiency of biomass accumulation
by sunflower as affected by glucose requirement of biosynthesis
and leaf nitrogen content. Field Crops Res. 44:119–127.
Gallo, K., C.S.T. Daughtry, and C.L. Wiegand. 1993. Errors in measuring absorbed radiation and computing crop radiation use efficiency.
Agron. J. 85:1222–1228.
Gilmore, A.M. 1997. Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves. Physiol. Plant. 99:197–209.
Guy, R.D., J.A. Berry, M.L. Fogel, and T.C. Hoering. 1989. Differential fractionation of oxygen isotopes by cyanide-resistant and cyanide-sensitive respiration in plants. Planta 177:483–491.
Hankamer, B., J. Barber, and E.J. Boekma. 1997. Structure and membrane organization of photosystem II in green plants. Annu. Rev.
Plant Physiol. Plant Mol. Biol. 48:641–671.
Jenkins, B., and J.M. Ebeling. 1985. Correlation of physical and chemical properties of terrestrial biomass and conversion. p. 371–403.
In D.L. Klass (ed.) Energy and biomass from wastes IX. Institute
of Gas Technology, Chicago.
Jenkins, C.L.D. 1997. The CO2 concentrating mechanism of C4 photosynthesis: bundle sheath cell CO2 concentration and leakage. Aust.
J. Plant Physiol. 24:543–547.
Kiniry, J.R. 1999. Response to questions raised by Sinclair and Muchow. Field Crops Res. 62:245–247.
Koller, D. 1990. Light-driven leaf movements. Plant Cell Environ.
13:615–632.
Kraus, E. 1992. The absence of a consistent relation between yield
and the rate of dark respiration in selected populations of perennial
ryegrass. p. 567–571. In H. Lambers and L.H.W. van der Plas
(ed.) Molecular, biochemical and physiological aspects of plant
respiration. SPB Academic, The Hague.
Lafitte, H.R., and R.S. Loomis. 1988. Calculation of growth yield,
growth respiration and heat content of grain sorghum from elemental and proximal analyses. Ann. Bot. 62:353–361.
Lambers, H., F.S. Chapin III, and T.L. Pons. 1998. Plant physiological
ecology. Springer-Verlag, New York.
Long, S.P. 1998. Rubisco, the key to improved crop production for
a world population of more than eight billion people. p. 124–136.
In J.C. Waterlow et al. (ed.) Feeding a world population of more
than eight billion people. Oxford University Press, New York.
Loomis, R.S. 1993. Optimization theory and crop improvement. p.
583–588. In D.R. Buxton et al. (ed.) International crop science I.
CSSA, Madison, WI.
Loomis, R.S., and J.S. Amthor. 1996. Limits to yield revisited. p.
76–89. In M.P. Reynolds et al. (ed.) Increasing yield potential in
wheat: breaking the barriers. CIMMYT, Mexico, D.F.
Makino, A., T. Mae, and K. Ohira. 1988. Differences in wheat and rice
in the enzymic properties of ribulose-1,5-bisphosphate carboxylase/
oxygenase and the relationship to photosynthetic gas exchange.
Planta 174:30–38.
McCree, K.J. 1970. An equation for the rate of respiration of white
clover plants grown under controlled conditions. p. 221–229. In I.
Setlik (ed.) Prediction and measurement of photosynthetic productivity. Proc. IBP/PP Tech. Mtg., Trebon, Czechoslovakia. Pudoc,
Wageningen, the Netherlands.
McCree, K.J. 1982. Maintenance requirements of white clover at high
and low growth rates. Crop Sci. 22:345–351.
McDermitt, D.K., and R.S. Loomis. 1981. Elemental composition of
biomass and its relation to energy content, growth efficiency, and
growth yield. Ann. Bot. 48:275–290.
Millar, A.H., O.K. Atkin, R.I. Menz, B. Henry, G. Farquhar, and
D.A. Day. 1998. Analysis of respiratory chain regulation in roots
of soybean seedlings. Plant Physiol. 117:1083–1093.
Mitchell, A.C., D.W. Lawlor, and A.T. Young. 1991. Dark respiration
of winter wheat crops in relation to temperature and simulated
photosynthesis. Ann. Bot 67:7–16.
Mitra, R.K., C.R. Bhatia, and R. Rabson. 1979. Bioenergetic cost
of altering the amino acid composition of cereal grains. Cereal
Chem. 56:249–252.
Monson, R.K. 1999. The origins of C4 genes and evolutionary pattern
in the C4 metabolic phenotype. p. 377–410. In R.F. Sage and R.K.
Monson (eds.) C4 plant biology. Academic Press, San Diego.
Ng, E., and R.S. Loomis. 1984. Simulation of growth and yield of the
1596
CROP SCIENCE, VOL. 39, NOVEMBER–DECEMBER 1999
potato crop. Simulation monographs. Pudoc, Wageningen, the
Netherlands.
Ort, D.R., and C.F. Yocum (ed.). 1996. Oxygenic photosynthesis:
The light reactions. Adv. Photosynthesis Vol. 4. Kluwer Academic
Publishers, Dordrecht, the Netherlands.
Osmond, C.B., and S.C. Grace. 1995. Perspectives on photoinhibition
and photorespiration in the field: quintessential inefficiencies of
the light and dark reactions of photosynthesis. J. Exp. Bot. 46:
1351–1362.
Penning de Vries, F.W.T. 1975. The cost of maintenance processes
in plant cells. Ann. Bot. 39:77–92.
Penning de Vries, F.W.T., A.H.M. Brunsting, and H.H. Van Laar.
1974. Products, requirements and efficiency of biosynthesis: a quantitative approach. J. Theor. Biol. 45:339–377.
Penning de Vries, F.W.T., H.H. van Laar, and M.C.M. Chardon. 1983.
Bioenergetics and growth of fruits, seeds, and storage organs. p.
37–59. In W.H. Smith and S.J. Banta (ed.) Potential productivity
of field crops under different environments. International Rice
Research Institute, Los Baños, Philippines.
Pirt, S.J. 1965. The maintenance energy of bacteria in growing cultures.
Proc. Royal Soc. Lond. B 163:224–231.
Plaxton, W.C. 1996. The organization and regulation of plant glycolysis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47:185–214.
Pons, T.L., and R.W. Pearcy. 1994. Nitrogen reallocation and photosynthetic acclimation in response to partial shading in soybean
plants. Physiol. Plant. 92:636–644
Reith, M. 1996. The evolution of plastids and the photosynthetic
apparatus. p. 643–657. In D.R. Ort and C.F. Yocum (ed.) Oxygenic
photosynthesis: The light reactions. Adv. Photosynthesis Vol. 4.
Kluwer Academic Publishers, Dordrecht, the Netherlands.
Siedow, J.N., and A.L. Umbach. 1995. Plant mitochondria electron
transfer and molecular biology. Plant Cell 7:821–831.
Sinclair, T.R., and C.T. de Wit. 1975. Photosynthate and nitrogen
requirements for seed production by various crops. Science 189:
565–567.
Sinclair, T.R., and R.C. Muchow. 1999. Radiation use efficiency. Adv.
Agron. 65:215–265.
Stryer, L. 1995. Biochemistry, 4th edn. W.H. Freeman, New York.
Taiz, L., and E. Zeiger. 1998. Plant physiology, second edition. Sinauer
Assoc., Sunderland, MA.
Tanaka, A., and J. Yamaguchi. 1968. The growth efficiency in relation
to the growth of the rice plant. Soil Sci. Plant Nutr. 14:110–116.
Terashima, I., and J.R. Evans. 1988. Effects of light and nitrogen
nutrition on the organization of the photosynthetic apparatus in
spinach. Plant Cell Physiol. 29:143–155.
Terashima, I., and K. Hikosaka. 1995. Comparative ecophysiology of
leaf and canopy photosynthesis. Plant Cell Environ. 18:1111–1128.
Thornley, J.H.M. 1970. Respiration, growth and maintenance in
plants. Nature 227:304–305.
Thornley, J.H.M. 1971. Energy, respiration, and growth in plants.
Ann. Bot. 35:721–728.
Tollenaar, M., and A. Aguilera. 1992. Radiation use efficiency of an
old and a new maize hybrid. Agron. J. 84:536–541.
Vanlerberghe, G.C., and L. McIntosh. 1997. Alternative oxidase: from
gene to function. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:
703–734.
Vertregt, N., and F.W.T. Penning de Vries. 1987. A rapid method
for determining the efficiency of biosynthesis of plant biomass. J.
Theor. Biol. 128:109–119.
Williams, K., F. Percival, J. Merino, and H.A. Mooney. 1987. Estimation of tissue construction cost from heat of combustion and organic
nitrogen content. Plant Cell Environ. 10:725–734.
Wilson, D. 1982. Response to selection for dark respiration rate of
mature leaves in Lolium perenne and its affect on growth of young
plants and simulated swards. Ann. Bot. 49:303–312.
Yeoh, H.-H., M.R. Badger, and L. Watson. 1980. Variations in
Km(CO2) of ribulose-1,5-bisphosphate carboxylase among grasses.
Plant Physiol. 66:1110–1112.
Yeoh, H.-H., M.R. Badger, and L. Watson. 1981. Variations in kinetic
properties of ribulose-1,5-bisphosphate carboxylase among plants.
Plant Physiol. 67:1151–1155.
Zerihun, A., B.A. McKenzie, and J.D. Morton. 1998. Photosynthate
costs associated with the utilization of different nitrogen-forms:
influence on the carbon balance of plants and shoot-root biomass
partitioning. New Phytol. 138:1–11.