Download Photosynthesis, productivity and environment

Journal of Experimental Botany, Vol. 46, Special Issue, pp. 1449-1461, September 1995
Journal of
Experimental
Botany
Photosynthesis, productivity and environment
David W. Lawlor1
lACR-Rothamsted, Harpenden, Herts AL5 2JQ, UK
Received 2 March 1995; Accepted 12 June 1995
Abstract
The relation between photosynthetic rate per unit leaf
area (Pn), total photosynthesis by canopies and dry
matter production {DMP) of crops is reviewed.
Although Pn is the driving force for all plant growth,
total DMP is determined by processes integrated over
the canopy, primarily light interception and thus by
leaf area index (LAI) and canopy architecture and leaf
area duration [LAD). The processes are not linearly
related so that effects on DMP of changes in the efficiency of conversion of energy of radiation to dry matter
are smaller than those associated with LAI.
Photosynthesis is much less sensitive to changing
environmental conditions than development of leaf
area. This explains the apparent anomaly that Pn does
not determine the variation in productivity of a crop
under normal agronomic practice, despite the role of
photosynthesis in providing all the assimilates for
DMP. Breeding and selection of crops for higher yield
has not resulted in improvements in dry matter production. Indeed, potential photosynthetic rate has
decreased under selection breeding, compensated by
increased leaf area: the causes are considered. Crops
growing at or near their potential rate use most of the
available solar energy and there is a strong correlation
between radiation absorbed and DMP and canopy
photosynthesis is not light saturated. To increase production it will be necessary to extend either the growing season or to improve light conversion efficiency;
the latter is best achieved by increasing Pn. The limiting factors in photosynthetic metabolism which determine Pn under different environmental conditions, are
reviewed. Increased Pn is not likely to come from
altering light harvesting, electron transport or ATP and
NADPH synthesis which are potentially very flexible
and have large capacity: there is large genetic variation. Synthesis of ribulose bisphosphate (RuBP)
depends on activity of Calvin cycle enzymes which
1
Fax: + 44 1582 760981.
Oxford University Press 1995
may be limiting due to environmental factors.
Increasing the atmospheric C 0 2 supply increases production of C 3 plants under current conditions: this is
due to a decrease in the oxygenase function of ribulose
bisphosphate
carboxylase-oxygenase
(Rubisco).
Improving the specificity factor of Rubisco is a longterm goal to decrease photorespiration. Even if Pn is
increased, evidence from theoretical and crop canopy
studies suggest that the increase in biomass production will only be a small proportion of the increase in
Pn, and DMP also depends on the crop's sink capacity.
Crop production is a function of many processes, at
the level of the chloroplast, the leaf and the canopy.
To increase Pn and production of crops will require
knowledge of processes at all levels in the plant-environment system.
Key words: Photosynthesis, dry matter production, leaf
area index, environment.
Introduction
The aims of this review are (1) to examine the relation
between photosynthesis, plant productivity and yield and
to clarify the roles of photosynthetic rate per unit leaf
area (Pn) and total leaf area, in determining dry matter
production (DMP): (2) to analyse the limitations to Pn,
which it will be necessary to overcome to increase productivity. Examination of these wider aspects is necessary
given the possibilities offered by genetic engineering
(Gasser and Fraley, 1989) to modify Pn and other crop
processes. This review specifically addresses the confusion
over the links between Pn and DMP, arising because
there is poor correlation between them in many situations
(Elmore, 1980; Evans, 1983, 1984, 1993). This conflicts
with the logical expectation that Pn, as the factor responsible for all dry matter production, should correlate very
strongly with dry matter production and harvestable yield
(Hesketh, 1963; Zelitch, 1982). Comparison of plants
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Lawlor
with C4 and C3 metabolism does indeed show a strong
correlation between Pn and DMP: in warm, high radiation environments C4 plants have greater Pn and accumulate more dry matter than do C3 plants, although in
cool, dim conditions the superiority of the C4 syndrome
may not be apparent (Gifford, 1974; Evans, 1993).
Similarly, there is a good, positive correlation for crops
grown with different amounts of fertilizer (Zelitch, 1975).
Yet, surprisingly, breeding and selection for greater harvested yield in cereals and other crops has not resulted
unequivocally in increased Pn or total dry matter production (Evans and Dunstone, 1970; Austin et al., 1980,
1982, 1986; Evans, 1993).
Poor correlation between Pn, DMP and yield arises
from the involvement of many processes in total production, not least the development of leaf area and yield
bearing organs (Bingham, 1969; Evans, 1983). Although
the driving force for dry matter production is photosynthesis, agronomic and physiological studies indicate that
the variation in production under different conditions
and in different seasons is more related to plant development and organ formation than to variation in Pn. The
importance of the apparent contradiction is that it highlights the need for careful appraisal of the productive
system—the crop in a particular environment—rather
than assuming that one process, for example, photosynthesis or a single step in a complex metabolic sequence,
will limit productivity over a wide range of conditions.
The factors limiting Pn in different conditions have
been analysed from many perspectives (Sharkey, 1985;
Woodrow and Berry, 1988; Woodrow, 1994).
Photosynthetic processes capture the physical energy of
sunlight and convert it to chemical forms which are
consumed in the biochemical reactions associated with
organ development and growth which are required for
resource capture (e.g. nutrient uptake and assimilation)
and reproduction (Lawlor, 1993). The limitations to Pn
may be environmental—deficiency or excess of light,
nutrients or water and sub- or supraoptimal temperatures
while current atmospheric CO2 concentration limits C3
plants. They may also be inherent in the photosynthetic
mechanism—inadequate capacity or inefficiency of
enzymes etc. These limiting environmental and plant
factors interact strongly so the optima depend on species,
the plant's previous history and conditions (Stitt, 1986;
Woodrow and Berry, 1988). To achieve maximum rates
of photosynthesis and maximum productivity, i.e. to
approach the genetic potential of the individual plant in
the context of the community (crop), requires that all the
conditions approach the optimum (Rabbinge et al., 1990).
If the environmental conditions are close to the optimum,
and the efficiency with which they are used approaches
the maximum possible for that level of production, then
the way forward is to increase the genetic potential by
altering the plant's genome (Evans, 1983; Gasser and
Fraley, 1989; Connett and Barfoot, 1992). Alterations
will be required both to the basic mechanisms of photosynthesis in order to increase Pn for given environmental
conditions, and to partitioning in order to increase
accumulation of assimilates and harvested yield.
Understanding of the limitations to Pn inherent in the
mechanism and the regulation imposed by peripheral, but
vital, processes such as sink development (Gifford, 1986;
Geiger, 1987), is essential if the major goals of agriculturally-related plant sciences are to be achieved. Such
goals are: understanding the mechanisms of biomass
production, prediction of production under a range of
conditions, increasing production by modifying the plant
environment with a minimum use of resources so as to
avoid pollution, and improvement of both the quality of
products and the efficiency of their production (related
to specific requirements of agro-industrial application).
Altering the plant's genome (Connett and Barfoot, 1992)
has a role to play in all of these. Here, only some aspects
of the problem of increasing DMP (and, by implication,
yield) of crops are considered, specifically related to CO2
assimilation, its efficiency and which of the underlying
mechanisms must be modified to increase Pn.
Crop photosynthesis and productivity
Capture of solar radiation and use of the energy to drive
the biophysical and biochemical processes which ultimately result in the synthesis of all components of plant
structure, are the key processes in production of dry
matter (Monteith, 1977; Lawlor, 1993). Net total (root
plus shoot) DMP from emergence to harvest (time t — 0
to H) of a crop is determined, (Monteith, 1977, 1981;
Kiniry et al., 1989) by the total photosynthetically active
radiation (PAR) intercepted (I{), and the efficiency with
which the energy is converted into dry matter (Pn/I{),
where Pn is the net CO2 assimilation per unit leaf area.
The fraction of photosynthate lost by respiration, root
exudates etc. is expressed by F.
DMP=
(IPn/I)dtF.
oj
The net rate of photosynthesis is the difference between
gross photosynthesis (Ps) and photorespiration (PT) plus
respiration (Rd) from the tricarboxylic cycle or related
process in the light ('day respiration') not directly linked
to photosynthesis:
Radiation interception
The value of /i5 (the difference between the incident
radiation, I, and the radiation penetrating below the base
Photosynthesis, productivity and environment
of the canopy) between emergence and harvest depends
on the leaf area of the crop (the leaf area index, LAI)
and its duration (LAD, i.e. LAI over time, dt) and on
crop structure, s, which is a function of factors such as
leaf angle (Legg et al., 1979; Monteith, 1981). The total
radiation intercepted over the season is given by:
4>tai=
Idt(LAIxs).
oj
Only a fraction of the radiation intercepted is used in
photosynthesis as some is reflected and some absorbed in
the tissues. Interception of radiation by crops well supplied with water and nutrients, and protected from pests
etc., increases from zero at sowing to almost 100% as
LAI exceeds c. 3 or 4, when the canopy covers the ground,
and decreases as the crop senesces and LAI falls (Irvine,
1975; Monteith, 1977). The LAI is a function of the
number and size of leaves and both, but particularly the
latter, are decreased by cool temperatures, water deficits,
nutrient deficiency etc. giving smaller LAI and LAD. The
rate of canopy development has marked effects on the
interception of radiation early in crop growth and thus
greatly affects yield in many crops. For example, in cool
springs in Britain sugar beet grows slowly so that the
rapidly increasing incident radiation is not used and
subsequent yield is poor compared to that resulting from
warmer springs (Milford et al., 1980).
Differences in I{ due to LAI, s and leaf spectral characteristics of crops may play a role in differences between
species and in variations in productivity with changing
conditions. Canopy architecture, particularly leaf angle
and morphology, has an effect on the amount of energy
intercepted in different layers of the canopy (Legg et al.,
1979).
Canopy photosynthesis
Simulation models suggest that erect and dissected leaves
allow greater penetration of radiation into the canopy
and also reduce the energy load on the uppermost leaves
whilst increasing it for the lower leaves, thus allowing
photosynthesis at low light where it is most efficient (in
terms of CO2 assimilated per unit of intercepted radiation). Young leaves have greater Pn in bright light than
old leaves, so optimizing the efficiency of light use. Old
leaves senesce, reducing the respiratory burden on the
crop, and nutrients etc., are remobilized to the growing
organs, thus improving the efficiency of nutrient use, but
decreasing leaf area (Lawlor et al., 1989). The marked
inefficiency of Pn at large photon flux in most C3 leaves
is not seen in canopy photosynthesis, which is generally
not saturated even in very bright light (Bugbee and
Salisbury, 1988; McCree and Troughton, 1966; Vietor
and Musgrave, 1979; Sinclair and Horie, 1989; Mahon,
1990a; Sinclair, 1994). With very large photon flux,
1451
particularly under stress conditions, the upper, but not
the lower, leaves in the canopy may become photoinhibited without major decrease in canopy photosynthesis
(see reviews in Baker and Bowyer, 1994). Some studies
with wheat and rice have shown greater production in
varieties with erect leaves (Gale and Youssefian, 1985; Le
Cain et al., 1989; Fischer and Quail, 1989; Morgan et al.,
1990). Also, under very large radiant energy fluxes, some
of the advantage of C4 crops over C3 crops, is from better
radiation penetration to lower leaves (Kanemasu and
Hiebsch, 1975). However, the expected advantages of
canopy architecture and other traits are not generally
large, in part, because too little attention has been paid
to diffuse radiation conditions (Goudriaan and van Laar,
1978; Feil, 1992; Evans, 1993). Simulation modelling of
photosynthesis in canopies, based on the light response
of photosynthesis by individual leaves and the attenuation
of PAR in the canopy, shows that the apparent quantum
yield is of greater importance to productivity than the
maximum rate of photosynthesis (Pmax) in environments
with relatively low, diffuse radiation. Integrated over time,
a 10% increase in apparent quantum yield was calculated
to have more effect than an equivalent change in Pmax.
However, in brightly lit canopies, increasing P max would
be an advantage (Day and Chalaby, 1988). Theoretical
analysis shows that crop radiation use efficiency increased
as a function of leaf Pn but reached a plateau well before
the maximum rate of Pn was reached, as observed experimentally (Sinclair, 1994). The photosynthetic mechanism
and Pn are apparently optimized in canopies, but the
importance to production and the mechanisms of optimization are poorly understood (R.A.C. Mitchell, personal
communication) and have not been targeted for
improvement.
Canopy architecture interacts with many other factors
so the complexity of the system decreases the supposed
advantage of a single factor. Probably the scope for
increasing productivity in crops with large LAI and LAD
by modifying these characteristics is small, but current
agriculture world-wide is substantially limited by inadequate LAI and light interception and, to a smaller extent,
by direct effects of stresses on Pn. Total net photosynthesis
depends on the integrated activities of all photosynthetically active organs and the response of Pn of individual leaves to radiation.
Respiration
Respiration is an important factor in crop production. In
C3 crops Pr may be 15-45% of Pn but it is almost zero
in C4 crops: respiration from 'day' respiration is poorly
quantified under field conditions, but may be 70-80% of
dark respiration, which itself is perhaps 10-15% of Pn
under normal photosynthetic conditions. Thus, Pn
depends not only on photosynthesis but on other pro-
1452
Lawlor
cesses, principally photorespiration (Amthor, 1989,
1994). Respiration during darkness is a factor of great
importance for biomass production. In C3 crops it is
about 50% of the carbon assimilated, a large demand and
one substantially reducing DMP compared to the total
photosynthetic potential of the canopy. If respiration is
changed to even a small extent, it may cause large
variation in DMP (Amthor, 1989). The rate of dark
respiration per unit DM varies according to conditions,
particularly temperature, generally increasing linearly
with a g io of 2 to 3. Total net productivity and efficiency
of radiation use depend on environmental conditions, for
photosynthesis and respiration and growth processes are
not affected in the same way over the range of conditions,
so the balance between them varies (Heichel, 1971). The
ratio of respiration to photosynthesis is probably a major
factor in production despite adjustment of dark respiration to changes in Pn so that the processes are, in part,
optimized (Amthor, 1994). Grain yields of wheat in the
UK are generally greater in the (cooler but long-day)
north than (warmer, short-day) south, possibly due to
reduced respiration relative to photosynthesis (Russel and
Wilson, 1994). Respiration has been separated, functionally, into growth and maintenance components. These
are related to the synthesis of new tissue and the turnover
of existing tissue, respectively. Growth respiration is large
(80% of total respiration) in the phase of vegetative
growth, decreasing during reproductive growth (e.g. grain
filling, 20%) with maintenance respiration changing reciprocally. Growth respiration is relatively independent of
the environment and, as it is a small component of
respiration in mature canopies, is not regarded as a major
target for modification. Reduction in maintenance respiration is the process which has probably been modified
in cases where selection for low respiration rates has
increased productivity (Amthor, 1989). Although respiration consumes assimilates it should not be considered
wasteful for it is essential to production, providing the
energy and substrates for growth and maintenance of the
existing plant structures. However, decreased rates of
respiration per unit of plant dry matter can be selected
for and do contribute to increased productivity (Wilson,
1975; Eagles and Wilson, 1982; Medrano et al, 1995).
Production and radiation use efficiency
There is very strong correlation between canopy dry
matter production, crop growth rate (CGR) and I{ over a
very wide range of / for C3 and C4 crops in many different
environments (Monteith, 1977; Christy and Porter, 1982;
Kiniry et al., 1989; Evans, 1993), including very large
photon fluxes (Bugbee and Salisbury, 1988). Efficiency
of energy conversion is generally greater in C4 than C3
plants, but similar within each group, although the superior performance depends on the environment (Evans,
1993). For C3 plants the maximum efficiency is about 3 g
of dry matter per megajoule (DM MJ" 1 ) of PAR intercepted or an efficiency of c. 5%. C4 plants achieve
efficiencies of 4-5 g M J 1 PAR. This implies that in many
environments with different temperatures and incident
radiation, but with water, nutrients etc., approaching
optimal, the physiological and metabolic processes determining dry matter production are very similar for a wide
range of C3 crops and that their metabolism is less
efficient than C4 crops. Efficiency depends on the products
being made, for example, it may decrease during formation of yield (particularly of oil or protein yielding crops),
when energy demand for biochemical syntheses increases.
Correlation between radiation interception and harvested
yield, for example, of grain in cereals, is generally poorer
than that with dry matter (Kiniry et ah, 1989; Evans,
1993). The explanation is in the many, variable processes
contributing to the formation of storage and particularly
reproductive organs (Bingham, 1969), their greater sensitivity to conditions during particular stages of growth (e.g.
pollen formation and flowering) compared to vegetative
organs and to the varying source of assimilates, for
example, current photosynthesis or stored (Bonnett and
Incoll, 1992). The more steps occurring between photosynthesis and the end products, the poorer the coupling
and the weaker the correlation.
The relative importance of LAI, light interception and
photosynthesis in DMP in crops is illustrated by the
response of winter wheat (Triticum aestivum L. cv. Avalon)
as a function of nitrogen and water supply in a field
experiment at IACR-Rothamsted. Briefly, wheat was
grown in replicated small plots with standard non-limiting
applications of phosphorus and potassium. Three different amounts of N were applied to achieve a very wide
range of crop production and yield; (1) no N, the crop
growing on soil containing about 40 kg Nha" 1 ; (2)
75 kg ha" 1 N as nitrate; (3) 300 kg ha" 1 N as nitrate.
Ten per cent of the fertilizer was applied in autumn, and
the remainder in two equal proportions in March and in
April. Each N treatment was combined with either full
irrigation to minimize soil water deficits or a continuously
developing drought after emergence to harvest. Plots were
protected from rain by a mobile rain shelter. Rates of
photosynthesis were measured on the flag leaves shortly
after attaining maximum size. Leaf area and dry matter
of the crops was measured regularly and straw and grain
dry matter at maturity, together with components of
yield. Throughout crop growth, PAR incident on and
below the canopy was measured by tube solarimeters;
intercepted energy and radiation conversion efficiency
(net total DMP per unit /j over the crop's life) were
calculated.
Nitrogen and water deficiency decreased the maximum
LAI and LAD (Fig. la), and radiation interception
(Fig. lb). The decrease in DMP is related to total inter-
Photosynthesis, productivity and environment
Irrigated
5
Draughted
kgN
x 4
B
80
60
40
300N,.
75N
/ | ' .
20
April
May
June
July
Aug
Fig. 1. Effects of different amounts of nitrogen fertilizer and of
irrigation on winter wheat grown in the field with three N fertilizer
applications, 0, 75 and 300 kg h a " 1 at Rothamsted. (A) Development
of leaf area index during the growing season and (B) the interception
of total PAR radiation (total, solid line): interception for the droughted
crops is omitted for clarity.
cepted PAR in Fig. 2 and Table 1: both N deficiency and
drought decreased radiation interception and conversion
efficiency. The effects on grain yield were similar to those
on total dry matter so harvest index was unaffected. The
changes in yield were largely caused by variation in grain
number not individual grain mass. Comparison of the
24H
irrigated
300 kg N
drought
C.16
I8
I
(0
S
irrigated
75 kg N
drought
irrigated
0 kg N
drought
200
400
600
800
Total photosynthetically active radiation
absorbed (MJ m~2)
Fig. 2. Total above-ground dry matter as a function of the total PAR
intercepted by the crops during their growing season. The irrigated
crop with 300 kg N provides a measure of total potential production
(solid line). Deficient N decreases DMP at a particular radiation
absorption and drought decreases it yet further.
1453
relative reductions in the components of productivity as
a function of N supply (Fig. 3) shows the progressively
greater decreases in P max of young, mature flag leaves,
conversion efficiency, light interception, dry matter production, and LAI as N supply decreased. The DMP was,
therefore, not only a function of radiation intercepted,
but of plant metabolism. The effect of the N deficiency
(and water deficit—data not given) was to decrease the
maximum Pn (Fig. 4). The smaller LAI is caused by
decreased tillering, fewer, smaller leaves and increased
senescence (Pearman et al, 1979); nitrogen and waterstressed crops mature earlier thus decreasing the duration
of photosynthesis.
The decrease in radiation use efficiency with deficient
nitrogen and water supply is a consequence of less efficient
metabolism, particularly decreased net photosynthesis:
respiration per unit of dry matter was not affected by the
treatments (Mitchell et al., 1991). The decrease in Pn in
response to nitrogen deficiency (Fig. 4) results from
decreased content of photosynthetic (and other) components per unit leaf area, as is well established. There is less
chlorophyll and Rubisco, reducing, respectively, energy
capture by thylakoids and carboxylation capacity (Evans,
1986; Makino et al, 1988; Lawlor et al, 1989). The
change in radiation use efficiency is relatively small,
suggesting that photosynthetic and respiratory metabolism are affected much less than organ number and size.
Thus, variation in dry matter production in wheat is due
primarily to variation in leaf area production (Feil, 1992)
and Pn and other metabolic processes are conserved:
whilst they are not invariant they change much less than
organ growth. Analysis of the complete production system
shows the limitations more clearly than an analysis of
separate processes.
For existing crops under good husbandry, radiation is
almost fully used. Decreased production due to nutrient
and water deficiencies is primarily due to poor development of leaf area decreasing light interception. Reduced
photosynthesis and light conversion efficiency have
smaller effects on production. World-wide, growth conditions are inadequate for exploitation of available radiation
to achieve existing genetic potential. However, when
environmental conditions are not limiting, further increase
in production will require greater rates of canopy photosynthesis or reduced respiration or longer duration of
crop and photosynthesis. Characteristics of the crop and
the biochemical and physiological mechanisms of the
plant must be altered to increase the genetic potential for
production and yield.
Photosynthetic rate and productivity
Correlation between the rate of photosynthesis and productivity has been analysed in several reviews (Evans,
1993, 1994; Sinclair, 1994), coming to the general conclu-
1454
Lawlor
Table 1. Production of dry matter and grain by winter wheat (cv. Avalon) with nitrogen and irrigation treatments
Nitrogen
(kg ha" 1 )
Grain
(gm"2)
Total
dry matter
LAI
Total
PAR
(MJirT
2
Conversion
efficiency
(gMJ"1)
season" 1 )
300
75
0
300
75
0
Irrigated
Dry
2240
1240
690
1670
1040
520
900
510
260
670
320
190
18
16
<0 V
0) CA
S.E
*
tt^
S
CM
8
E
13-
0.5
1 1.5
2 2.5
Leaf N (g m 2 )
3
Fig. 3. Maximum rates of photosynthesis of wheat leaves as a function
of leaf nitrogen content for the crops grown with 0 (open circles) and
300 (solid circles) kg h a " 1 applied N, as described in Fig. 1.
photosynthetic rate
conversion efficiency
PAR interception
dry matter production
LAI max
,,
0
100
200
Applied N (kg ha~1)
300
Fig. 4. Relative effects of the amount of N fertilizer applied on processes
in the wheat crop: photosynthetic rate measured at saturating light and
350 /urnol mol" 1 CO 2 on young, fully mature flag leaves was much less
affected by N deficiency than conversion efficiency, PAR interception,
dry matter production or leaf area index at its maximum (LAI max).
sion that the correlation is, at best, weak (Bunce, 1989)
and usually negative for crops in the field (Evans, 1993;
Sinclair, 1994). However, there is considerable conflict in
the results for different crops. Measurement of Pn was
expected to provide a direct measure of plant production
(Elmore, 1980; Zelitch, 1982; Evans, 1993), based on the
argument (Cannell et al, 1969; Zelitch, 1975) that photo-
5.5
2.5
1.2
3.9
2.4
1.0
642
491
298
533
419
236
3.49
2.53
2.31
3.13
2.48
2.21
synthesis underpins the whole complex mechanism ultimately leading to dry matter production, so knowledge
of Pn should allow prediction of productivity (Natr, 1966;
Nelson et al, 1975; Peterson and Zelitch, 1982). A
corollary was that DMP could be increased by selection
of genotypes for large Pn or by altering the photosynthetic
mechanisms (Austin, 1989). Also, there is substantial
inherent quantitative variability in photosynthesis (Natr,
1966; Cannell et al, 1969; Byrne et al, 1981; Johnson
et al, 1987; Austin, 1989). Some studies do show good
correlation between Pn and productivity, for example, in
grain sorghum (Peng et al, 1991); increased Pn was
found in maize following cycles of selection for the trait
(Crosbie and Pearce, 1982) and there is heritability for
canopy photosynthesis and seed yield in soybean
(Harrison et al, 1981). However, total biomass has not
increased with recent selection of wheat for high yield:
comparison of old and new wheat varieties on Broadbalk
field at Rothamsted shows the old to have slightly greater
DMP (Austin et al, 1993) as reported earlier (Austin
et al, 1980). In contrast, Waddington et al. (1987)
observed a 30% increase in biomass of durum wheats
over 25 years. The failure to select for larger Pn, despite
increased wheat yield, has been apparent. Indeed, there
is frequently a negative correlation between photosynthetic rate and size of the leaf in wheat (Evans and
Dunstone, 1970; Dunstone et al, 1973; Austin et al,
1982, 1986) and rice (Cook and Evans, 1983) when wild
progenitors, old cultivars and high yielding modern varieties are compared (Khan and Tsunoda, 1970). Zelitch
(1982) identified the apparent 'paradox' that increasing
the rate of photosynthesis (e.g. by fertilizer application)
does increase biomass and, generally, yield of most crops
but genetic selection does not. As Evans (1993) says '...
the very crux of the paradox, [is] that yield is favoured
by environmental improvement of [photosynthetic rate
per unit area] but not, so far, (Evans' italics) by genetic
improvement of the individual leaf rates'.
This suggests that selection during breeding, for yield
presumably, has decreased the components responsible
for photosynthesis ('dilution hypothesis', see Evans,
1993). However, there is evidence for selection increasing
Pn (but decreasing electron transport) with date of culti-
Photosynthesis, productivity and environment
var introduction of Australian wheats, probably related
to the introduction of dwarfing genes (Watanabe et al.,
1994). The tendency to increase leaf area and to decrease
the photosynthetic components (Dunstone and Evans,
1974) is related to increasing ploidy and increasing cell
size, which affect the leaf anatomy and gas exchange
(Dornhoff and Shibles, 1976; Le Cain et al., 1989; Byrne
et al., 1981). The result of selecting larger leaves has been
to increase the light interception (Gent and Kiyomoto,
1985; Mahon, 19906) and perhaps reduce weed competition. Large biomass production was desirable as straw is
valuable in many rural economies for animal feed etc.
(but not in industrialized agriculture). Similarly, increasing N supply, for example, increases leaf area by increasing cell size and number, but generally stimulates
production of components of the photosynthetic system
and photosynthetic rate (Lawlor et al., 1989). Not only
has selection not resulted in greater Pn, neither has more
specific selection aimed at apparently wasteful processes.
Attempts to select individuals with small rates of photorespiration within populations of C3 plants (Zelitch, 1975;
Zelitch and Day, 1973; Evans, 1983) have generally not
had the desired effect, with the ratio of photorespiration
to photosynthesis remaining stubbornly constant,
although the selection methods employed appear to have
selected for reduced rates of dark respiration (Medrano
et al., 1995). The assumption that altering photorespiration of C3 crops will confer long-term advantages, particularly in changing or stressful environments, such as under
water stress where photorespiration may have a protective
role (Lawlor, 1979) against photoinhibition (Baker and
Bowyer, 1994) has been questioned by Evans (1993).
Why is it that selection for high productivity (possibly)
and yield (certainly) has not increased photosynthetic
rate? Explanation of why breeding selection should have
resulted in the converse relation of Pn to other characteristics have not been given. Perhaps the genetic changes
required for greater numbers of cells or, more likely, for
larger cells (related to wall growth perhaps) are relatively
more easily achieved than those related to increasing the
number of genes for photosynthetic components or to
increasing the copies. Advances in plant genetic engineering open the prospect of modifying photosynthesis and
decreasing photorespiration (Bainbridge et al., 1995)
although there is still uncertainty about the potential to
modify complex multigenic traits expressed in 'systems*
such as photosynthesis. Evans (1993) suggests the need
for better evaluation of how changes at the cellular level
of organization are transferred directly through to the
crop. Often the effects are attenuated (Gifford, 1974). To
this end it is legitimate to ask is there a 'proper view' of
the events in plant production to direct genetic engineering
towards effective targets within photosynthesis and the
use of assimilates? With respect to photosynthesis the
questions are:
1455
1. What parts of the photosynthetic mechanism must be
altered to improve the rate of CO2 assimilation:
NO3" metabolism is ignored here although very important (Foyer et al., 1995)?
2. What must be done to increase the ability of the
mechanisms to function efficiently over a wide range
of environmental conditions and to avoid damage?
3. How do the various sub-processes link to achieve the
productivity obtained in particular environments?
4. Can alterations in biochemistry, which increase photosynthesis under laboratory conditions, increase production in the field?
Factors limiting photosynthetic rate
Photosynthetic rate is determined by the interaction of
several processes and systems (Lawlor, 1993): (1) light
harvesting, electron transport and NADPH and ATP
synthesis associated with the thylakoid membranes, (2)
the capacity of the enzymes of the photosynthetic carbon
reduction (Calvin) cycle in the chloroplast stroma for
ribulose bisphosphate (RuBP) regeneration and of ribulose bisphosphate carboxylase-oxygenase (Rubisco) for
CO2 assimilation, (3) consumption of the assimilates to
avoid feedback inhibition of photosynthesis by its products or shortage of inorganic phosphate in the stroma.
Light capture, electron transport and ATP and NADPH
synthesis
There are substantial differences in the ability of different
species to capture solar radiation and use the energy for
electron transport and NADPH and ATP synthesis.
Similarly, there are great differences between species in
their ability to adapt to the light environment during
growth. Many are very adaptable in their capacity to
capture photons, to transport electrons and to form the
pH gradient across the thylakoids for ATP synthesis.
Others, however, are obligate (genetically adapted) sun
or shade plants. Obligate shade plants are unable to
increase their performance effectively in bright light.
Obligate sun plants are similarly unable to adjust to dim
light (Evans et al., 1988). Some C3 plants achieve large
maximum rates of CO2 assimilation in bright light, comparable to C4 plants which are virtually never saturated
even at the highest terrestrial photon fluxes, yet their
photosystems, electron transport and photophosphorylation and NADP + reduction mechanisms appear not to
differ fundamentally in components, but do in system
organization, from those of plants less effective at large
rates of assimilation.
Generally, plants are able to intercept radiation and
convert energy into ATP and NADPH very efficiently
(Stitt, 1986), this is so in crops at high irradiance even if
the processes in individual leaves are saturated. Indeed,
1456
Lawlor
for many environments and crops, light availability limits
photosynthesis over much of the growing period. Energy
transduction in the photosystem reaction centres is efficient and similar in different plants. The quantum yields
of C3 plants approach the theoretical limit of efficiency
given by the mechanism requiring 8 quanta per oxygen
evolved and the apparent quantum yields (slope of the
response of Pn to incident PAR) of a range of species,
even for obligate sun and shade plants (see papers in
Evans et al., 1988) are similar and determined by the
characteristics of Rubisco. Therefore, the possibilities of
improving the basic processes—energy capture and transfer in the chlorophyllTprotein complexes and reaction
centres—are limited (Ehleringer and Pearcy, 1983). Only
by radical change to the mechanism could major advances
be made: how it could be done is unclear. Increasing the
efficiency of energy captured, for example, in the green
wavelengths or extending capture towards unexploited
parts of the spectrum are probably not options given the
current understanding of the mechanisms. As PAR incident on the crop may be insufficient to saturate photosynthesis for much of the growing season, energy must be
used more effectively for assimilation of CO2, NO3~ etc.
Calvin cycle limitations
Limitations in the cycle may be analysed in terms of the
synthesis of ATP (by chloroplast coupling factor, CF1-0),
NADPH and RuBP and their relation to Rubisco activity
and to whole leaf photosynthesis (von Caemmerer and
Farquhar, 1981; Farquhar and von Caemmerer, 1982).
Low light limits ATP, NADPH and RuBP synthesis and
therefore Pn: electron and proton transport are simply
insufficient. As illumination increases, so does synthesis
of ATP, etc. until, in the normal atmosphere, the (low)
concentration of CO2 then limits Pn. However, with
increasing CO2 Pn rises and eventually saturates. At this
point it is probable that Rubisco is the limiting factor. It
is, however, unclear if ATP also becomes limiting or
Rubisco and CF1-0 'co-limit' (Sharkey, 1985; Woodrow,
1994): it is unlikely that NADPH would limit as plants
adapted to large irradiance have a large capacity for
electron transport. However, complex feedback regulation
of enzymes serves to maintain relatively stable
metabolism.
Photosynthesis and DMP of C3 plants, grown as crops,
increases when atmospheric CO2 is raised. Winter wheat,
grown with ample nutrition and water in 700 jixmol mol ~x
CO2 compared to 355 ^mol mol" 1 under simulated field
conditions at Rothamsted, has 15-40% greater biomass
and 18-23% greater grain yield in different experiments
(Lawlor et al., 1993; Mitchell et al, 1993), similar to the
response in many studies (Cure and Acock, 1986). Note
that this is when interception of radiation by the crop
canopy is maximal, showing that yield potential at that
radiation is not achieved with the current atmospheric
CO2. As the response of C4 crops to elevated CO2 is very
much smaller or negligeable (Cure and Acock, 1986) this
shows the need for improvement of photosynthetic potential in C3 crops to exploit the current CO2 concentration
and radiation fully.
Plants exposed to elevated CO2 have, initially, very
substantially increased Pn, but there is good evidence
that the high rates are often not maintained over long
periods, even with ample nutrients, water etc.
Photosynthetic rates and capacity often decrease substantially with time (Cure and Acock, 1986; Yelle et al., 1989;
Lawlor and Keys, 1993), due to accumulation of carbohydrates related to limited sink capacity (RowlandBamford et al., 1990). However, the effects are variable:
Delgado et al. (1994) found no evidence of acclimation
in winter wheat grown with elevated CO2 in one experiment, but in another (Delgado et al., unpublished) there
was progressive 'down-regulation' and acclimation in the
same cultivar. Possibly such differences are related to
differences in assimilate storage and sink development.
The effect of elevated CO2 is to increase Pn and to
decrease photorespiration, so clearly there would be benefits to DMP and yield of wheat and other C3 crops if this
could be achieved by altering the photosynthetic characteristics rather than by attempting to alter the environment (although anthropogenic CO2 release to the
atmosphere may achieve the same ends!). The response
of Pn to CO2 supply at less than saturating radiation is
analogous to the light response: at limiting CO2, ATP,
NADPH and RuBP synthesis are in excess and Rubisco
capacity as well. As CO2 increases so eventually RuBP
becomes limiting, but Rubisco may not limit. However,
further increase in radiation increases RuBP synthesis so
that increasing the CO2 results in saturation of Pn, again
with Rubisco the likely limiting factor (Woodrow, 1994).
Although Rubisco has been identified as the enzyme
limiting Pn in C3 plants, other enzymes in the Calvin
cycle may also, under some conditions be expected to be
limiting, namely phosphoribulosekinase (PRK; Gray
et al., 1995) and sedoheptulose bisphosphatase and fructose bisphosphatase (Sharkey, 1989). In the current atmosphere, the CO2 concentration is too small to achieve
saturation of Rubisco and oxygen competes for the
reaction sites. Indeed, there is evidence that the CO2
concentration at the reaction sites of Rubisco in the
chloroplast is substantially below that in the intercellular
spaces (Evans et al., 1994). Increasing atmospheric CO2
increases the intercellular CO2 concentration and CO2/O2
ratio at the reaction sites of the Rubisco, thus decreasing
oxygenation and hence photorespiration (Andrews et al.,
1995; Bainbridge et al., 1995). Under warm conditions in
bright light Pn may be increased substantially (20-50%)
by increasing the atmospheric CO2 concentration from
350 to 700 ^mol mol" 1 (Cure and Acock, 1986). Also, in
Photosynthesis, productivity and environment
dim light the quantum efficiency is increased by elevated
CO2, so that there is a positive response to increasing
CO2 concentration under most conditions, particularly
very warm. Factors such as nutrient deficiency which
decrease growth and assimilate consumption reduce or
prevent the response. In the current atmosphere C3 photosynthesis is not saturated with CO2 so production
increases with elevated CO2 (Lawlor and Keys, 1993).
This is due to the oxygenase function of Rubisco: elimination of this has long been a goal of biochemists (Zelitch
and Day, 1973) and is feasible based on the evidence.
There has been improvement in the specificity factor
(Bainbridge et al, 1995) during evolution of Rubisco and
this parameter varies in higher plant Rubiscos suggesting
that there is potential for further improvement of the
enzyme. Selection for decreased photorespiration may
increase Pn by 20-50%, productivity by 15-30% and yield
by about the same depending on species, conditions etc.
However, this assessment is based on physiological
information (elevated CO2 studies). The failure to select
low photorespiration plants means that a direct test
of the consequences of eliminating the oxygenase
function of Rubisco has not been possible.
If Rubisco can be modified, why then was the route
taken by C4 plants not to improve the Rubisco specificity
factor, but to modify leaf anatomy and also metabolism
by using phosphoenolpyruvate carboxylase as a CO2
'pump'? Organic acids are transported from the mesophyll
to the bundle sheath and decarboxylated, providing CO2
to Rubisco. Also, O2 generation in the bundle sheath is
much decreased, so the CO2/O2 ratio under which
Rubisco operates in C4 plants is greater than in C3 plants,
decreasing photorespiration (Dever et al, 1995). Perhaps
surprisingly, Rubisco in C4 plants is less efficient than in
many C3 plants (lower specificity factor) yet net photosynthesis is greater due to the CO2 'pump'. This suggests
that, even if Rubisco can be modified, the time-scale is
long, so that it has proved easier in evolutionary terms
to adapt multi-gene processes ancillary to Rubisco, involving more complex and larger carbon fluxes between cells
of different types. If genetic alteration of Rubisco requires
many, co-ordinated steps then this may be very difficult
via mutation in vivo whilst maintaining a viable photosynthetic system, but genetic engineering may be able to
achieve the changes in vitro and then incorporate the
changes into the plant (Andrews et al, 1995).
The enzyme capacity of the Calvin cycle appears
adequate to match the energy available under the illumination experienced during growth, but may be inadequate in bright light, as shown by studies with reduced
Rubisco and PRK activity produced by antisense gene
techniques (Stitt, 1986; Paul et al, 1995). The apparent
excess activity of Rubisco (Krapp et al, 1994) and
phosphoribulokinase (Paul et al., 1995) in leaves grown
in relatively dim light is required for maximum photosyn-
1457
thesis when leaves are placed in bright light. Increasing
the amount of Rubisco above the current concentrations
in leaves of many plants would seem not to be the best
way to improve Pn and productivity. Large nitrogen
supply greatly increases concentrations of Rubisco, but
does not improve CO2 assimilation in normal environmental conditions, but does under bright light and elevated CO2 (Lawlor et al, 1989; Krapp et al, 1994). Little
attention has been directed to whether over-expression of
the limiting enzymes results in greater Pn. If, for example,
over-expression of Rubisco resulted in increased Pn then
clearly other photosynthetic processes would not be limiting (as indeed is shown by the increase in Pn with elevated
CO2). If no stimulation resulted from over-expression
then increasing other components (e.g. CF1 or PRK if
possible) would show if they limit Pn. With current
knowledge the real improvement in Pn of C3 plants is
expected to come from avoiding the intrinsic inefficiency
of Rubisco. The adverse effects of low atmospheric concentration of CO2 (despite its rapid rise over the last
century) and the limitations of CO2 (Evans et al, 1994)
and metabolite diffusion to Rubisco in the stroma (Lawlor
et al, 1989) would be avoided or substantially decreased
if the oxygenase activity of Rubisco could be eliminated.
Less Rubisco would be needed, decreasing the requirement for nitrogen used in its synthesis. However, if an
improved Rubisco were achieved it might become necessary to alter Calvin cycle regulation to improve the
synthesis of RuBP.
Nitrogen assimilation
Photosynthetic N assimilation by the reduction of nitrate
ions and synthesis of amino acids is well understood
(Lawlor, 1993), but the links to C assimilation are less
so, particularly the partitioning of energy in the chloroplast and regulation of the combined processes of C and
N metabolism. A consequence of increasing Pn by elevated CO2 is to decrease the N content of tissues, both
vegetative and reproductive (e.g. cereal grain). This arises
from accumulation of carbohydrates, mainly soluble
sugars, fructans and starch without increased accumulation of N-containing components, nitrate ions, amino
acids and, particularly, proteins. However, as total DMP
increases with increased Pn so total N uptake may be the
same or increases. To overcome the decrease in N content
will require accumulation (increased synthesis of)
N-containing components of the system and in the same
proportions to avoid alterations to the machinery. This
may also be necessary in future if Rubisco characteristics
are improved and other limitations (e.g. Calvin cycle
enzyme activity) become important. Mechanisms for and
consequences of making such alterations have yet to be
evaluated but it is likely that control resides in protein
synthesis rather than nitrate reduction.
1458
Lawlor
End product regulation of photosynthesis and sink limitation
If the capacity of the sinks for assimilates (Bonnett and
Incoll, 1992) is too small then accumulation of carbohydrates in source tissue frequently reduces Pn by feedback
processes (Blechschmidt-Schneider et al., 1989; see Evans,
1993, for a compilation of many experiments).
Translocation of assimilates does not limit assimilate
movement and accumulation in sink organs except in
extreme conditions (Gifford, 1986; Wardlaw, 1990). The
physical size of the phloem and the rates of assimilate
transport increase in proportion to the photosynthetic
potential and the sink: rather it is the capacity of the
sinks which is important (Wardlaw, 1990). The advantages accruing in crops as a consequence of selection
breeding relate more to the utilization of assimilates,
altering the sink distribution, including increasing harvest
index which has so influenced yield (Austin et al., 1980)
and changing the time over which the crop grows, rather
than increasing photosynthesis (see Evans, 1993, for discussion and literature).
Increasing the capacity to utilize assimilates should
ensure that inhibition of the photosynthetic system,
especially decreased rates of enzyme activity ('downregulation') and possibly inhibition of the synthesis of—
and thereby decreased content of—photosynthetic components ('acclimation'; Lawlor and Keys, 1993) do not
occur and, therefore, allow the maximum photosynthesis
possible for the light and CO2 available. The occurrence
of acclimation is demonstrated regularly in some species,
for example, tomato (Yelle et al., 1989) but in others, for
example, winter wheat, it may not occur in some experiments (Delgado et al., 1994), but do so in others which
are very similar (Delgado et al., unpublished). Suggested
mechanisms of feedback reduction of activity are inadequate rates of recycling of inorganic phosphate due to
end-product accumulation and slower Calvin cycle turnover and direct allosteric control of metabolites on
enzymes (Sharkey, 1985, 1989). Acclimation is related to
the inhibition by carbohydrates of gene transcription and
translation of RNA into protein (Sheen, 1994). By ensuring that sink demand for photosynthetic products is
maintained over a wide range of conditions, limitations
to photosynthesis should be minimized (Humphries and
Thorne, 1964; Geiger, 1987); for example, reduced temperatures of growing organs may decrease Pn, in the long
term, by preventing the consumption of carbohydrates
(Paul et ah, 1991). Plants grown under elevated CO2 may
show down-regulation and acclimation because, presumably, the storage pools can not accommodate the excessive
carbohydrate production, allowing metabolism to be
affected. By increasing the capacity of the sinks and by
extending the periods over which those sinks fill, total
photosynthesis might well be increased and total biomass
and yield production improved. As sink size (e.g. the
tillering capacity and stem length of cereals) seem to be
under the control of relatively few genes (Gale and
Youssefian, 1985) then increasing sink capacity under
adverse conditions might, in the long run, be more feasible
to maintain photosynthesis and increase productivity,
than genetically altering the photosynthetic system.
Alteration of sink capacity by genetic engineering
appears feasible. Recently, increasing the expression of
the enzyme sucrose phosphate synthase (SPS) from maize
in all tissues of tomato under the control of the 35S
promoter from cauliflower mosaic virus, was shown
(Foyer et al., 1995) to increase the flux of carbon to
sucrose rather than starch and increased biomass production substantially. This was achieved with only a 10%
increase in Pn above the untransformed plant. Clearly,
these changes increased the use of assimilates and suggests
that altered sink behaviour is of great importance for
maximizing Pn and productivity.
Conclusions
1. Photosynthesis is the ultimate determinant of dry
matter production, but Pn is only one aspect and the
LAI and LAD are important aspects of crop
production.
2. Losses of assimilate by dark respiration and the ratio
of respiration to photosynthesis are important determinants of production.
3. The main limitation to Pn in C3 plants is the oxygenase
function of Rubisco; overcoming that and reducing or
eliminating Pr or increasing the affinity of the enzyme
for CO2 are long-term goals to increasing productivity.
4. Increasing Pn and productivity in low light would
require increasing the apparent quantum yield rather
than the maximum Pn: decreasing photorespiration
would be advantageous in these conditions.
5. If Pn is increased by overcoming the Rubisco limitation, or by elevated CO2 then full expression of dry
matter production will require development of sinks
for assimilate to be optimized to particular environmental conditions.
Acknowledgement
IACR receives grant-aided support from the Biotechnology and
Biological Sciences Research Council of the UK.
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