Plant Physiol.
(1983) 73, 681-686
0032-0889/83/73/0681/06/$00.50/0
Inhibition of Photosynthesis by Carbohydrates in Wheat Leaves
Received for publication March 9, 1983 and in revised form May 25, 1983
JOAQUIN AZCON-BIETO'
Department of Environmental Biology, Research School of Biological Sciences, The Australian National
University, P.O. Box 475, Canberra City, A.C. T. 2601 Australia
ABSTRACT
The rate of net CO2 assimilation of mature wheat (Triticum aestivum
L.) leaves in ambient air (21% 02. 340 microbars C02) declined with
time of illumination at temperatures lower than 25°C, but not at higher
temperatures, and the rate of decline increased when maintained in air
with higher CO2 concentration (700425 microbars). In this latter case,
the decline in the rate of net CO2 assimilation also occurred at high
temperatures. Stomatal conductance also declined with time in some
cases and stomata became more sensitive to C02, but this was not the
primary cause of the decrease in CO2 assimilation because internal partial
pressure of CO2 remained constant. Treatments which reduced the rate
of translocation (e.g. lower temperatures, chilling the base of the leaf)
produced a marked decline in CO2 assimilation of leaves in atmospheric
and high CO2 concentrations. The decreased net CO2 assimilation was
correlated with carbohydrate accumulation in each case, suggesting end
product inhibition of photosynthesis. Analysis of CO2 assimilation in
high carbohydrate leaves as a function of intercellular CO2 partial
pressure showed reduction in the upper part of the curve. The initial
slope of this curve, however, was not affected. Photosynthetic rates in
the upper part of this curve generally recovered after a short period in
darkness in which carbohydrates were removed from the leaf. The
stimulation of net CO2 assimilation by 2% 02 (Warburg effect), and the
apparent quantum yield, decreased after several hours of light.
Accumulation of carbohydrates in leaves during photosyn-
thesis is a common phenomenon which can be enhanced by
several means including high photosynthesis rates, low translo-
cation rates, or low sink demand (16). It has long been hypoth-
esized that "the accumulation of assimilates in an illuminated
leaf may be responsible for a reduction in the net photosynthesis
rate of that leaf' (Boussingault, 1868; see 16). This hypothesis
has been variously tested by manipulating (a) photosynthate
source, (b) translocation of photosynthate, and (c) photosynthate
sinks (see reviews by Guinn and Mauney [9], Herold [11], and
Neales and Incoll [16]). The evidence of the occurrence of end
product inhibition of photosynthesis from such experiments
remains equivocal. The conclusions are often complicated by
the fact that hormonal, nutritional, or other interactions may
occur following defoliation and sink manipulation, especially in
long-term experiments. In wheat leaves, Birecka and Daki&c
Wlodkowska (3) and King et al. (12) were able to inhibit flag leaf
photosynthesis by removing the sink (removal of the ear) and
stimulate flag leaf photosynthesis by spraying the ear with
DCMU (which inhibited photosynthesis in the ear, thereby in-
creasing the sink). However, Austin and Edrich (1) were unable
' Present address: Department of Plant Physiology, Faculty of Biology,
University of Barcelona, Diagonal 637-647, Barcelona-28, Spain.
681
to confirm the ear removal response. Nevertheless, King et al.
(12) showed that ear removal caused an accumulation of carbo-
hydrates in the flag leaf. They were able to simulate this response
by keeping plants in continuous light for a week. Leaf carbohy-
drates built up and photosynthesis was inhibited.
Although these results suggest the occurrence of end product
inhibition of photosynthesis in wheat, the treatments and the
measurement methods used do not exclude other factors. Hor-
monal and stomatal responses could be involved. Thus, in this
paper we describe experiments which are designed to avoid these
difficulties and to determine if the photosynthetic rate is related
to the carbohydrate status in wheat leaves. Carbohydrate status
was increased by increasing the rate of photosynthesis under
otherwise comparable conditions, by increasing CO2 concentra-
tion or reducing 02 concentration. In other experiments, a
portion of the leaf below the region in which photosynthesis was
monitored was chilled to reduce transport of photosynthate (8,
21).
MATERIALS AND METHODS
Plant Material. Triticum aestivum L. (cv Gabo) plants were
grown from seed in a controlled environment cabinet in pots of
soil. They were watered twice a day, and were fertilized every
other day with nitrate-type Hewitt's solution containing: KNO3,
4 mM; Ca(NO3)2, 4 mM; MgSO4, 1.5 mM; NaH2PO4, 1.33 mM;
EDTA FeNa, 60 gM; MnSO4, 10 uM; ZnSO4, 1 ,uM; CuSO4, 1
ALM; H3BO3, 50 uM; Na2MoO4, 0.5 jiM; NaCl, 0.1 mM; Co(NO3)2,
0.2 uM. The pH of the solution was 6.5. PPFD2 was about 600
to 700 gE _m 2 -s-'. The day/night temperature regime was 25/
20°C with a daylength of 13 h. RH was between 60 and 80%.
Gas Exchange Techniques. Wheat plants were selected from
the growth cabinet near the end of the night period (10 AM). One
or two attached recently mature leaves were enclosed in a pho-
tosynthetic chamber, which received an incident PPFD of 1000
iE -m2 - s-'. The rest of the plant, which was kept intact, was
also illuminated. CO2 and water exchanges were measured in
leaves using an open system gas analysis apparatus (2). Calcula-
tions of gas exchange parameters were made as before (20). Leaf
to air water vapor pressure differences were maintained at about
8 to 12 mbar at 20 to 23°C and at 20 to 23 mbar at 30°C in most
experiments.
Light Responses of Photosynthesis. Net rate of CO2 assimila-
tion (A) was measured in wheat leaves for 1 h at a PPFD of 1000
jiE *m-2.s-' to open stomata. Incident PPFD was measured with
a quantum sensor (Lambda Instruments, model LI- 190 SR).
PPFD was then decreased by interposing copper screens, and A
was measured at every step. Finally, dark CO2 efflux was meas-
ured. Leaf temperature was kept constant during these proce-
dures. These measurements were repeated after a period of 4 h
2
Abbreviations: PPFD, photosynthetic photon flux density; A, rate of
net CO2 assimilation; pi, intercellular partial pressure of C02; RuBP,
ribulose bisphosphate.
682 AZCON-BIETO Plant Physiol. Vol. 73, 1983
A from a bath through a sandwich-type brass jacket in close contact
_ -* -
22C with both sides of the leaf. The surface of both sides of the jacket
3C ---- --

formed a square of 4 cm2. Temperature of the leaf region in

E contact with the jacket was 0 to 2C. These procedures did not
0
E 25
la30C E
produce alterations in the temperature of the enclosed portion
0.9 of the leaf, which was kept at 21 °C. No changes in the leaf
E
0
c 2C _ 9 30C A a A a turgidity were apparent. Two experimental procedures were
0.7 C
0

22C adopted.
c
0
E 15 - ~ ____ _____
(a) A leaf was allowed to photosynthesize for 4 h at external
V0 -0 CO2 pressures of either 350 or 700 ,ubar. Then the chilling
0.5

10 treatment was applied as described above and the gas exchanges

0

0 of the enclosed part of the leaf were monitored for a subsequent

0.3
0

S period of 4 h. At the end of this period, the cooling jacket was

0

z removed, and the leaf gas exchanges were measured for about an
n
vI additional 1 h.
2 3 4 5 6
(b) In other experiments, leaves were subjected to the chilling
Time in the light (Hours) treatment from the start ofthe light period, and the gas exchanges
were monitored for 5 h. CO2 pressures inside the chamber were
FIG. 1. Time course of net CO2 assimilation (0, A) and total leaf either 310 or 800 ,abar.
conductance to diffusion of water vapor (0, A) in wheat leaves at two All experiments were duplicated.
temperatures. External CO2 pressure was 340 ,bar and 02 concentration Carbohydrate Determination. Free glucose plus fructose, in-
was 21%.
vertase sugars (mostly sucrose), and starch fractions were deter-
mined as described by Azcon-Bieto and Osmond (2).
at a PPFD of 1000 gE * m2 s'. The leaf temperature and CO2
-

pressure were varied as indicated in the text. Each experiment

was replicated three times.
RESULTS
CO2 Responses of Photosynthesis. Net CO2 assimilation (A) Effect of Prior Photosynthesis on Subsequent Rate of Net CO2
and transpiration rates were first measured in flag wheat leaves Assimilation. Under certain conditions, in ambient air (340 jbar
at ambient CO2 and 02 pressures for about 1 h until steady state C02, 21 %02) A reached a maximum within the first few hours
rates were reached. Measurements were then repeated at several of illumination and subsequently declined. This pattern was most
CO2 concentrations below ambient, and finally at CO2 pressures frequently observed in leaves illuminated in air at temperatures
higher than ambient. After the determination of the first curve below 25°C (especially in leaves with high rates of photosyn-
of A versus Pi which took 2.5 to 3 h from the start of the light thesis), and was normally absent at higher temperatures (Fig. 1).
period, leaves were allowed to photosynthesize for 5 h at external If wheat leaves were allowed to photosynthesize at 22°C in
partial pressures of CO2 of either 800 ubar (Exp. A) or 50 to 60 atmospheres with elevated, ambient or depleted CO2 partial
gbar (Exp. B). The curve of A versus pi was then determined pressure, the decline in A was more dramatic at 740 ,ubar than
again over the next 1.5 to 2 h. At the end of this time, a piece of at 350 ubar and was absent at 125 pbar (Fig. 2A). This response
the enclosed leaf was taken for carbohydrate analysis (see below) was further exaggerated by increasing CO2 partial pressure to 740
by carefully sectioning the leaf with a sharp razor blade. In the ,ubar and reducing the 02 concentration to 2%, resulting in a
experiments where the rate of photosynthesis declined with time 35% decrease in A after 9 h photosynthesis (29-19 Umol CO2.
(Exp. A), the remaining leaf fragment was kept in darkness for 3 m 2 s'). The decline in A also occurred at 30°C when the CO2
h. At the end of this period, the curve of A versus pi was concentration in the air was high (Table I).
determined again to study recovery. The rest of the leaf was then The decline in A was not due to stomatal closure. In ambient
used for carbohydrate analysis. Experiment A was performed air, the declining CO2 assimilation was accompanied by no
three times and experiment B two times. Leaf temperatures change, or even a slight increase, in stomatal conductance (Fig.
during the light and dark periods were 20 and 1 8C, respectively. 1) and corresponding small increases (from 260 to 280 ,bar) in
Leaf Base Chilling Methods. A small portion (about 2 cm2) pi. Although larger decreases in stomatal conductance were ob-
of the base of a wheat leaf, whose upper part was enclosed in the served following prolonged exposure to elevated atmospheric
photosynthetic chamber, was chilled by circulating icy water CO2 partial pressure, this only resulted in small changes in pi

Table Time Course of Net CO2 Assimilation (A), Stomatal Conductance to Water Vapor (gj), Intercellular Partial Pressure ofCO2 (p,) and
I.
Carbohydrate Levels in Wheat Leaves at High External CO2 Pressures (825 ,ubar)
Carbohydrate concentration was measured in leaf fragments sampled from the leaf enclosed in the photosynthetic chamber after 7 h in the light,
and after an additional period of 2 h in darkness. The values shown are means ± SE of three experiments (except for the values shown in section C,
which correspond to a single experiment.
Period of
Temperature A g5 Pi Carbohydrate
Concn.
Experiment
°c OMOC2MmolC2O2.m2-sI' mol.mM2 S-r I bar CO2 mmol C.m2
A. I h in the light 20 43.0 ± 1.1 0.67 ± 0.1 713 ± 24 Notmeasured
30 51.0 ± 0.5 0.45 ± 0.01 588 ± 2 Not measured
B. 7 h in the light 20 34.6 ± 0.2 0.45 ± 0.06 690 ± 21 526 ± 39.5
30 43.3± 1.1 0.28±0.02 524± 15 463±23

C. 7 h in the light plus 30 49.4 0.30 495 325

2 h in the dark
 END PRODUCT INHIBITION OF PHOTOSYNTHESIS IN WHEAT 683

35 - A 0

c
0
E 0"~
0 30F 0----~ 740 pbor CO2
E E

%.
a
25f E
350 pbar CO2
.-_

201 E
0
.2_
=L
.

0
15
0
U
10
125 pbar CO2
z
100 0 100 200 300 0
5
Carbohydrate concentration
L (mmol C mrn
VI II

FIG. 4. Relationship between the depression of net CO2 assimilation

B and several carbohydrate fractions in wheat leaves.
600_ -
-
-
0---- - O ~ ~ O
O-.......... -1
C

-o
-a 40)o B
-* *--- * In

X *,"
'E
2C
_o40S
*'1 *2 3 * 6* Z E
4

1 2 3 4 5 6 Z.

Time in the light (Hours) 0 300

-2
FIG. 2. Time course of net CO2 assimilation (A) and intercellular
partial pressure of CO2 (B) in wheat leaves at several external CO2 6-
I-o-o
II**0i4
200
pressures. Leaf temperature was 22°C, and 02 concentration was 21 %. l,
2 4 6 8 10 0 2 4

10 00 Time in the light (hours)

S
c
0 0 * FIG. 5. Effect of chilling the base of a wheat leaf on the rate of net
-

-8
- 0
~~~~~~~0
00 CO2 assimilation and pi in the rest of that leaf. The chilling treatment
was applied (as indicated by the arrows) either after 4 h of photosynthesis
0E (A), or at the beginning of the photosynthetic period (B). In A, an
E unchilled control is also shown (0). External partial pressures of CO2
0
* 0
were 350 ubar (A) and 310 ubar (B). Temperature was 2 1C.
-54
05.0
0
0
0
Carbohydrates accumulate in wheat leaves under some con-
0
QA ditions used in the above experiments and respiratory rates in
4A
2 the light increase (2). However, the increase in respiration is 1.5
70 A Amol CO2 m 2 .s' at most, and cannot account for the large
decrease in photosynthesis observed in Figures 1 and 2 and in
I
1 1 Table I. The correlation between the decline in A and the total
0 100 200 300 400 500 600 carbohydrate content (except fructosans) of wheat leaves after a
period of photosynthesis under a variety of conditions (e.g.
Carbohydrate concentration different CO2 concentrations and temperatures) is shown in
(mmol Cm-2) Figure 3. There seems to be no effect on A below 100 mmol
FIG. 3. Relationship between the depression of net CO2 assimilation carbohydrate carbon m2 (about 3.1 g glucose eq m-2). Carbo-
and total carbohydrate concentration in wheat leaves. This relationship hydrates accumulated significantly less in leaves photosynthe-
includes data obtained in experiments performed at different tempera- sizing at 30°C than at 20°C, in spite of the much higher assimi-
tures from 20°C to 30°C. lation rates observed at 30C (Table I). This suggests that trans-
location of recently accumulated assimilates is more effective at
which did not affect A (Table I; Fig. 2B). For example, in the higher temperatures. Similar effects of temperature on translo-
30°C treatment at 825 Abar (Table I), stomatal conductance cation have been reported (8). This increased translocation effi-
declined by about 38%, A by about 15%, and pi by about 11% ciency may have been the reason for the low carbohydrate levcls
after 7 h photosynthesis. After 2 h recovery in the dark, stomatal measured in leaves photosynthesizing at high temperatures and
conductance had not changed, A had returned to within 3% of ambient CO2 concentrations, which were less than 100 mmol
the starting value, and pi declined further. Clearly, A was not carbon m2, which is the critical level for photosynthesis (see
responsive to stomatally controlled pi over the range 495 to 588 above). All carbohydrate fractions increased in about the same
,gbar CO2 in this experiment. proportions. Although the concentrations of free glucose plus
684 AZCON-BIETO
.2 I decline (Fig. 6), but again, the major effect of chilling on A
5 30.
v ,;N
E 25 -
°=;*_.C
6 shown). When the chilling was halted, the inhibition of A and
~~~20~~~~~
700
-) 2 0
0O I'-o -
700-
400 0~~~~~~~~
0 00 2 4 6 8 0
Time in the light ( hours)
FIG. 6. Effect of chilling the base of a wheat leaf on the rate of net
CO2 assimilation and p, in the rest of that leaf. External CO2 pressures
were 700 to 770 \bar (A) and 800 Mbar (B). Other conditions and symbols
are as in Figure 5.
fructose and of starch were lower than those of invertase sugars
(mostly sucrose) at maximum inhibition of A (Fig. 4), there is
no evidence that any one component of the carbohydrate frac-
tions was specifically more inhibitory than another.
Effect of Chilling the Leaf Base on Net CO2 Assimilation.
Chilling of the basal portion of wheat leaves is known to inhibit
translocation, and in the present experiments it accelerated the
rate of decline in photosynthesis. In wheat leaves allowed to
photosynthesize in ambient air, cooling the leaf base to near 0°C
accelerated the decline in A more than 2-fold, but had no effect
on pi (Fig. 5). That is, the inhibition of photosynthesis was not
due to stomatal closure. In leaves kept in the light at elevated
CO2 partial pressures, the response to chilling the leaf base was
even more dramatic (Fig. 6). It was immaterial whether the
chilling was applied after 4 h photosynthesis or almost immedi-
ately after illumination; in both cases the rate of decline in A,
compared to an unchilled control, accelerated from about less
Plant Physiol. Vol. 73, 1983
than 1 to about 1.5 to 3 umol CO2. m2. s-' each hour. About 2
h after the commencement of the chilling treatment, pi began to
occurred before the Pi response. Very high carbohydrate levels
were measured in the leaves after the chilling treatments (not
the closure of stomata persisted for at least 1 h. There was no
evidence of recovery.
Effect of Prior Photosynthesis on the Properties of Photosyn-
thesis. It was routinely found that the apparent quantum yield
(the initial slope of the curve of A versus PPFD, excluding the
point in darkness) was lower in leaves after a period of photosyn-
thesis at 20C (Fig. 7, A and C). If leaves were allowed to
photosynthesize at 30°C at ambient C02, the apparent quantum
yield was similar before and after the photosynthetic period (Fig.
7B). Apparent quantum yield was lower at higher temperature
and higher at high C02, as expected in C3 plants (5). These
comparisons indicate that light itself was not responsible for the
decline in apparent quantum yield, i.e. photoinhibition was
probably not a contributory factor. No changes in the light
transmission properties of the leaves (6-7% transmission) were
detected following these periods of photosynthesis; leaf absorb-
ance could not be measured, but it is unlikely that changes in
absorbance were large enough to account for the large variations
observed in the apparent quantum yield. Carbohydrates were
not measured in this experiment, but it is probable that they are
also involved in these responses.
The relationship between A and pi in flag wheat leaves before
and after a period of photosynthesis which caused accumulation
of carbohydrates is shown in Figure 8A. The initial slope was
unaffected, but the saturated region of the curve was depressed.
This depression was relieved by 3 h in darkness which also
resulted in a decline in leaf carbohydrate status. If leaves were
treated under the same illumination conditions, but at low CO2
(60-70 gbar), carbohydrates did not accumulate to the same
extent and there were no changes in the shape of the curve of A
versus pi (Fig. 8B).
The 02 sensitivity of CO2 assimilation in wheat leaves also
declined following an extended period of photosynthesis (Fig. 9),
and the reduction in the 02 sensitivity of photosynthesis was less
in leaves with lower photosynthetic rates (Table II).
Stomatal conductance to water vapor was rather insensitive to
pi changes at the beginning of the light period, but it decreased
and showed sensitivity to pi after a high CO2 light period (not

'E 4 - A 320 ObarCO2 X B

E 200C

Before *
2 0.064
2
.2

C4
0.051
1.
PPFD (pEEm2s1)
FIG. 7. Light response curves of net CO2 assimilation in wheat leaves determined before (@) and after (0) a period of photosynthesis of 4 h.
Three typical experiments are shown. External partial pressures of CO2 and temperatures during the experiments are shown. 02 concentration was
21%. The apparent quantum yield values (mol C02E-'; which were calculated excluding the point in darkness) are also shown,in the figures.
External CO2 pressure during quantum yield measurement was the same as during the photosynthetic period.
 END PRODUCT INHIBITION OF PHOTOSYNTHESIS IN WHEAT 685
Table II. Effect of Decreasing 02 Concentration from 21 to 2% on the Rate ofNet CO2 Assimilation (A) at
Different Times during the Light Period
Temperature was 21C. For other details, see legend to Figure 9.
Time in the Light (h)
Experiment 1.5-2 4-5
A21 A2 Increase A2, A2 Increase
molCO2 m-2.sr' % Osmol CO2 m-2.s' %
1 19.3 25.2 31 18.8 21 12
2 21.9 29.0 32 19.9 21 6
3 12.5 19.2 54 13.5 18 33

A B 30
30
21%02 21%02 21%02
E
0
/, E
E
------- --O v~~~~~~
0 /, o/ j~~~~~~

07l1
E 0 25
C 20[ OS / E
0
0
VI

1.)
0

zn 10
f0 u

z
20
2%02 2%02
/0

2%02
I--
.

n
1 I 1)
1~~
A art

0
1 I 200
I1
400 600 200 400 600
Time in the light (Hours)
FIG. 9. Changes in the 02 sensitivity of photosynthesis in wheat leaves
Intercellular CO2 partial pressure (pbar) with time. Net CO2 assimilation was initially measured in air (330 Mbar
FIG. 8. Effect of a period of photosynthesis on the curve of A versus CO2; 21% 02); but, at intervals, the 02 concentration was temporarily
pi in flag wheat leaves. A, The curve was determined at the beginning of reduced to 2%. The arrows indicate transfer to 2% 02 or 21% 02, and
the light period (0), after 5 h in the light at 800 sbar CO2 (0), and after the dotted lines represent the periods at 2% 02 during which measure-
a further 3 h in the dark (A). The carbohydrate concentration of these
ments were not taken. Temperature was 21 C
leaves increased from 12 to 260 (±40) mmol C m-2 after 5 h in the light,
_

observed. However, assimilation was very low in this study

and declined to 197 (± 11) after 3 h in the dark. B, The curve of A versus was
(about 2 Amol C02 m 2 s-') and a large carbohydrate build-up
pi was determined at the beginning of the light period (0) and after 5 h
is not expected under these conditions. The inhibition of pho-
in the light at 50 to 60 ,bar CO2 (0). The carbohydrate concentration
tosynthesis in wheat is correlated with accumulation of soluble
increased to only 99 (± 10) mmol C. m2 after 5 h in the light. The arrows
sugars. Starch also accumulated in wheat leaves, but to a much
indicate the direction in which the pi level was changed (i.e. increased or
decreased). less extent than soluble sugars. Accumulation of starch in leaves
of other species has also been negatively correlated with the rate
shown). In contrast, the stomatal responses topi were not affected of photosynthesis (9, 18).
by a period of photosynthesis at low CO2 pressures. The changes in photosynthetic properties following carbohy-
drate accumulation in wheat leaves can be interpreted in terms
DISCUSSION of major biochemical processes in leaves of C3 plants, as outlined
by Farquhar and von Caemmerer (6). Reduced quantum yield
These results and those obtained by Birecka and Dakic-WIod- suggests that carbohydrate accumulation impairs the production
kowska (3) and King et al. (12) are consistent with the occurrence or consumption of ATP/NADPH in photosynthesis itself. Re-
of end product inhibition of photosynthesis in wheat leaves. The duction of the CO2-saturated rate of photosynthesis (Fig. 8A)
decline in the rate of net CO2 assimilation with time of illumi- implies that carbohydrate accumulation leads to impaired regen-
nation was greatest under conditions of reduced export (leaf base eration of the carboxylation substrate RuBP. It has been sug-
chilling, low temperatures) or higher rates of photosynthesis (high gested that soluble sugar accumulation may reduce the rate of
CO2 and low 02 pressures in the air). The decline in CO2 RuBP regeneration by decreasing available stromal Pi (I 1). Very
assimilation was related to carbohydrate concentration above a low phosphate levels inside the chloroplasts can restrict the rates
certain critical level. The increase in respiration was not large of photophosphorylation and electron transport, probably via a
enough to account for this decline (2). On the other hand, CO2 decreased ATP/ADP ratio and depression of 3-phosphoglycerate
assimilation recovered substantially after a short period of dark- reduction (17). The use of mannose and glucosamine, which
ness in which leaf carbohydrate levels declined. Factors such as sequester cytosolic phosphate, produces a decline in assimilation
stomatal closure, photoinhibition and endogenous rhythms do and ATP levels which is consistent with this hypothesis of
not seem to be involved in these responses. Similar observations phosphate limitation (1l, 14, 17).
have been reported in other species (4, 13, 15, 18). In contrast, This interpretation receives some support from the observation
Geiger (7) chilled the primary leaf petiole and node of a bean that the 02 response of C3 photosynthesis is also impaired when
plant but no effect on the rate of net photosynthesis of that leaf carbohydrate accumulate (Fig. 9). A similar desensitivity of CO2
686 AZCON-BIETO Plant Physiol. Vol. 73, 1983
fixation to 02 has been observed in spinach leaves infiltrated to environmental conditions. In OL Lange, PS Nobel, CB Osmond, H
with mannose (10), and Usuda and Edwards (19) have discussed Ziegler, eds, Physiological Plant Ecology, Vol B, Water Relations and Pho-
tosynthetic Productivity. Springer-Verlag, Heidelberg, pp 549-587
the sparing effect of RuBP oxgenation on phosphate deficiency 7. GEIGER DR 1976 Effects of translocation and assimilate demand on photosyn-
in experiments with isolated chloroplasts. It is possible that the thesis. Can J Bot 54: 2337-2345
rate of photosynthesis becomes insensitive to the ratio of carbox- 8. GEIGER DR, SA SOVONIK 1975 Effects of temperature, anoxia and other
yation to oxygenation when phosphate is sequestered in the metabolic inhibitors on translocation. In M Zimmermann, JA Milburn, eds,
Encyclopedia of Plant Physiology, New Series Vol 1, Phloem Transport.
cytoplasm by mannose (10) or by the accumulation of carbohy- Springer-Verlag, Berlin, pp 256-286
drates in the leaf cells, because under these conditions the rate 9. GUINN G, JR MAUNEY 1980 Analysis of CO2 exchange assumptions: feedback
of CO2 assimilation may be controlled by the rate of release of control. In JD Hesketh, JW Jones, eds, Predicting Photosynthesis for Eco-
phosphate in the cytosol (6, 10, 11). These data establish a 10. HARRIS system Models, Vol 2. CRC Press, Boca Raton, FL, pp 1-16
GC, JK CHEESBROUGH, DA WALKER 1983 Effect of mannose on
correlation between inhibition of photosynthesis and carbohy- photosynthetic gas exchange in spinach leafdiscs. Plant Physiol 71: 108-1 1 1
drate build-up, and suggest control of the regeneration of RuBP. 11. HEROLD A 1980 Regulation of photosynthesis by sink activity-the missing
The phosphate limitation hypothesis provides one framework 12. KING link. New Phytol 86: 131-144
RW, IF WARDLAW, LT EVANS 1967 Effect of assimilate utilization on
for further investigation of the mechanisms involved. photosynthetic rate in wheat. Planta 77: 261-276
13. Ku SB, GE EDWARDS, D SMITH 1978 Photosynthesis and nonstructural
Acknowledgments-I am very grateful to Professor C. B. Osmond for his help carbohydrate concentration in leaf blades of Panicum virgatum as affected
and encouragement. I also thank Dr. S. C. Wong for his assistance in technical and by night temperature. Can J Bot 56: 63-68
experimental matters, and Drs. D. A. Walker, G. D. Farquhar, and D. A. Day for 14. MIGINIAc-MASLOW M, A HOARAU 1982 Variations in the adenylate levels
useful comments. during phosphate depletion in isolated soybean cells and wheat leaf frag-
ments. Z Pflanzenphysiol 107: 427-436
15. MILNER HW, WM HIESEY 1964 Photosynthesis in climatic races of Mimulults.
LITERATURE CITED II. Effect of time and CO2 concentration on rate. Plant Physiol 39: 746-750
16. NEALES TF, LD INCOLL 1968 The control of leaf photosynthesis rate by the
1. AUSTIN RB, J EDRICH 1975 Effects of ear removal on photosynthesis, carbo- level of assimilate concentration in the leaf: a review of the hypothesis. Bot
hydrate accumulation and on the distribution of assimilated "4C in wheat. Rev 34: 107-125
Ann Bot 39: 141-152 17. ROBINSON SP, DA WALKER 1981 Photosynthetic carbon reduction cycle. In
2. Azc6N-BIETo J, CB OSMOND 1983 Relationship between photosynthesis and MD Hatch, NK Boardman, eds, The Biochemistry of Plants. A Comprehen-
respiration. The effect of carbohydrate status on the rate of CO2 production sive Treatise, Vol 8, Photosynthesis. Academic Press, New York, pp 193-
by respiration in darkened and illuminated wheat leaves. Plant Physiol 71: 236
574-581 18. UPMEYER DJ, HR KOLLER 1973 Diurnal trends in net photosynthetic rate and
3. BIRECKA H, L DAKIC-WLODKOWSKA 1963 Photosynthesis, translocation, and carbohydrate levels of soybean leaves. Plant Physiol 51: 871-874
accumulation of assimilates in cereals during grain development. III. Spring 19. USUDA H, GE EDWARDS 1982 Influence of varying CO2 and orthophosphate
wheat-photosynthesis and the daily accumulation of photosynthates in the concentrations on rates of photosynthesis, and synthesis of glycolate and
grain. Acta Soc Bot Pol 32: 631-650 dihydroxyacetone phosphate by wheat chloroplasts. Plant Physiol 69: 469-
4. CHATTERTON NJ 1973 Product inhibition of photosynthesis in alfalfa leaves as 473
related to specific leaf weight. Crop Sci 13: 284-285 20. VON CAEMMERER S, GD FARQUHAR 1981 Some relationships between the
5. EHLERINGER J, 0 BjORKMAN 1977 Quantum yields for CO2 uptake in C3 and biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:
C4 plants. Dependence on temperature, CO2 and 02 concentrations. Plant 376-387
Physiol 59: 86-90 21. WARDLAW IF 1968 The control and pattern of movement of carbohydrates in
6. FARQUHAR GD, S VON CAEMMERER 1982 Modelling of photosynthetic response plants. Bot Rev 34: 79-105