Plant Cell Physiol. 39(1): 1-7 (1998)
JSPP © 1998
The Effects of Increased Atmospheric Carbon Dioxide on Growth,
Carbohydrates, and Photosynthesis in Radish, Raphanus sativus
Hideaki Usuda and Kousuke Shimogawara
Laboratory of Chemistry, Teikyo University, School of Medicine, 359 Ohtsuka, Hachioji, Tokyo, 192-03 Japan
The effects of sink capacity on the regulation of the acclimation of photosynthetic capacity to elevated levels of
carbon dioxide are important from a global perspective.
We investigated the effeocts of elevated (750/onol mol"1)
and ambient (350 //mol mol -1 ) atmospheric CO2 on growth,
carbohydrate levels, and photosynthesis in radish seedlings from 15 to 46 d after planting. In radish, a major sink
is the storage root, and its thickening is initiated early.
Elevated CO2 increased the accumulation of dry matter by
111% but had no effect on the acclimation of the rate of
photosynthesis or on the levels of carbohydrates in leaves
at dawn. Elevated CO2 increased the dry weight in storage
roots by 105% by 46 d after planting, apparently enhancing the sink capacity. This enhanced capacity seemed to be
responsible for absorption of elevated levels of photosynthate and to result in the absence of any over-accumulation
of carbohydrates in source leaves and the absence of negative acclimation of photosynthetic capacity at the elevated
level of CO2.
Key words: Elevated CO 2 — Photosynthesis — Radish —
Source-sink.
The atmospheric concentration of CO2 will likely rise
from its present level of about 350 //mol mol"' to about
700/imol mol" 1 by the end of the next century (Watson et
al. 1990). Several decades of research have demonstrated
that atmospheric enrichment with CO2 tends to cause significant increases in the growth rates and harvestable yields
of most agricultural species. Comprehensive analysis of
this phenomenon by Kimball (1983) suggested that an increase of 300 //mol mol~' in the CO2 content of the air generally increases plant productivity by an average of 30%.
The contribution of photosynthesis to this increase, however, is unclear, because, for example, the photosynthetic
fixation of CO2 exhibits complicated responses to elevated
CO2, as discussed below.
The present concentration of CO 2 in the atmosphere,
350//molmol~', imposes a limit to photosynthesis of C3
Abbreviations: A, net rate of assimilation of CO2; Ci, partial
pressure of CO2 in the intercellular spaces of leaves; DAP, days
after planting; LAR, leaf area ratio; RGR, relative growth rate;
Rubisco, ribulose 1,5-bisphosphate carboxylase-oxygenase.
plants (Bowes 1991). In the short term, enhancement of
levels of CO2 generally stimulates the net photosynthetic
fixation of CO2 in C3 plants, because (1) the present atmospheric concentration of CO2 is insufficient to saturate the
primary carboxylation by Rubisco in photosynthesis, and
(2) CO 2 suppresses the competing process of photorespiration. Elevation of the concentration of CO 2 , therefore, increases the net rate of the photosynthetic uptake of CO2 in
C3 plants, regardless of whether or not Rubisco activity or
the regeneration of ribulose-l,5-bisphosphate is limiting
and regardless of whether the incident light is saturating
or limiting (Long 1991, Stitt 1991). Many studies have
shown that short-term gain may be offset, in the longer
term, by a negative acclimation in photosynthetic capacity,
even though examples of no negative acclimation and even
of positive acclimation of photosynthetic capacity have
been reported (see Sage 1994, Bowes 1996). The underlying
causes of the acclimation of photosynthetic capacity after
long-term treatment with elevated levels of CO2 have been
the focus of experimentation and speculation, but they
have been only partially identified (Bowes 1996). The negative acclimation might be related to an imbalance between
source capacity and sink capacity. The rate of photosynthesis at the source might exceed the capacity of the sinks to
utilize the photosynthate, for example, for growth and storage, at an elevated concentration of CO 2 . Negative acclimation is associated with decreased activity and content
of Rubisco in some species (Stitt 1991). Sheen (1990) showed clearly that carbohydrates play a crucial role in the
regulation of the expression of the photosynthetic gene.
Decreased levels of Rubisco and other photosynthetic enzymes might result from an accumulation of carbohydrates
that is due to limited sink capacity (Stitt 1991). Recently,
Nie et al. (1995a, b) demonstrated the very complex response of the photosynthetic capacity to elevated levels
of CO 2 in wheat at different developmental stages, which
might have been related to changes in the source-sink relationship during development. They emphasized that the
nature of the effect of elevated levels of CO 2 on the photosynthetic fixation of CO2 and the expression of photosynthetic genes was strongly dependent on the stage of development at which samples were harvested or studies
were conducted.
In this study, we addressed the question of the effect of
sink capacity on the acclimation of photosynthesis in leaves
grown in an atmosphere with an elevated CO2, investigat-
Effects of high CO2 on growth and photosynthesis
ing the rate of photosynthesis and the growth rate during
the developmental stages in 15- to 46-d radish seedlings. In
radish, a major sink is the storage root, and its thickening
growth is initiated early. Therefore, radish seemed to be a
very suitable plant to address this question.
fructose, sucrose and starch with freeze-dried leaf discs were determined enzymatically as described previously (Usuda and Shimogawara 1991).
Materials and Methods
Growth—An elevated CO2 had a positive effect on the
accumulation of dry weight (Fig. 1). "Total dry weight" of
plants grown under elevated and ambient CO2 increased
from 0.77±0.13 to 46.0±1.5g and from 0.36±0.06 to
25.2± 1.4 g (means±SE, n = 4) from 15 DAP to 46 DAP,
respectively (Fig. 1). These growth rates were within the
ranges of values obtained in previous studies (Idso and Kimball 1989, Overdieck et al. 1988, Sionit et al. 1982, Wong
1993, Morison and Gifford 1984). They indicate that the
growth environments employed in this study were reasonable for the growth of radish plants, although the light intensity for growth was lower than that required to saturate
photosynthetic CO2 fixation. The rate of photosynthesis under 350//mol mol" 1 CO2 was saturated at a light intensity
of 900//mol m~ 2 s~ 2 (400-700 nm) (data not shown). The
fresh weights of storage roots grown under elevated and
Plant material and growth conditions—Seeds of radish,
Raphanus sativus L. (cv. White Cherish), were obtained from
Sakata Seed Co. (Yokohama, Japan). Plants were grown in a controlled growth chamber (Conviron S10H; Conviron, Winnipeg,
Canada) with a 14-h Iight/10-h dark cycle. Light was provided
by fluorescent and incandescent lamps. The photon irradiance at
plant height from 7:00 to 7:15, from 7:15 to 7:30, from 7:30 to
20:30, from 20:30 to 20:45, from 20:45 to 21:00, and from 21:00
to 7:00 were 80±20, 190±40, 4O0±50, 190±40, 80±20, and 0
(imo\ m~ 2 s" 1 (400-700 nm), respectively. The temperatures from
6:30 to 7:00, from 7:00 to 7:15, from 7:15 to 7:30, from 7:30 to
20:30, from 20:30 to 20:45, from 20:45 to 21:00, from 21:00 to
22:00, and from 22:00 to 6:30 were set at 22, 23, 24, 25, 24, 23, 22,
and 20°C, respectively. The concentration of CO 2 in the chamber
was monitored with a CO 2 controller (ZFP 9; Fuji Electric Co.,
Tokyo, Japan) and maintained at 350 (ambient CO2) or 750//mol
mol"' (elevated COJ with a CO 2 injection and absorption system.
Plants were grown in 1-liter pots (one plant/per pot) containing
commercially premixed nutrient-rich soil (Planter Soil; AirisuOhyama, Sendai, Japan). The pots were watered with a modified
version of Nakayama's solution 5 to 7 times a week (Shinozaki et
al. 1988). The positions of all pots were rotated 5 to 7 times a week
to reduce the effects of heterogeneity of the conditions within the
growth chamber and of shading on plant growth. Relative humidity was maintained at approximately 70%. Ten days after planting,
uniformly grown plants were selected and used for further analysis.
Growth analysis—Four plants were harvested at each sampling time and separated into leaves (including mid rib), petioles
and storage roots. Fibrous roots were not harvested. Leaf area
was determined with a leaf area meter (AM 100; Analytical Development Corp., Hoddesdon, U.K.). Harvested materials were
dried at 80 c C for 7 to 20 d and then weighed. Relative growth rate
(increase in dry weight per unit of dry weight present and per unit
of time) and leaf area ratio (the leaf area per unit of dry weight of
plant material present) were calculated without inclusion of the
weights of fibrous roots, because, in radish, the contribution of
fibrous roots to total weight is small (e.g., Wong 1993). Thus,
"total weight" in this study refers to the sum of the weight of the
shoot plus storage root without fibrous roots.
Determination of the rate of photosynthesis—The rates of
the photosynthetic assimilation of CO 2 and transpiration by leaves
of plants of different ages were determined under various conditions with an open system using an infrared gas analyzer (ADC
LCA 4; Analytical Development Corp.). The temperature of the
leaf chamber was controlled at 25±0.5°C. The light source was
four 400-W metal halide lamps (DR 400, Toshiba, Tokyo, Japan).
Partial pressure of CO 2 in the intercellular spaces of leaves were
calculated according to the equations in von Caemmerer and Farquhar (1981).
Determination of levels of carbohydrates—For each assay of
carbohydrate, eight leaf discs (2 cm2 each) were collected from
eight different fifth leaves and frozen in liquid nitrogen. The
samples were stored at — 80°C prior to lyophilization. Glucose,
Results and Discussion
15
Leaf
Elevated CO
10
Shoot
15
£ 10
C? 5
0
40
TotaTO. •)
Storage root ID. •)
30
20
10
10 15 20 25 30 35 40 45 50
Days after planting
Fig. 1 Effects of ambient and elevated CO2 on the accumulation
of dry weight in radish. Open and closed symbols represent plants
grown under elevated (750//mol mol~') and ambient CO 2 (350
//mol mol" 1 ), respectively. This convention applies also to Fig. 2
through 9. Values are means±SE (n=4).
Effects of high CO2 on growth and photosynthesis
ambient CO2 at 15 DAP were 1.85±0.6 and 0.6±0.17g
(means±SE, n=4), respectively. The thickening growth of
storage roots had already started at 15 DAP. The "total dry
weight" was increased over 2-fold by enrichment for CO2
(Fig. 1). A similar increase in dry weight by elevated CO2
has been reported for radish in a range of 1.5- to 2-fold (Idso and Kimball 1989, Morison and Gifford 1984, Overdieck
et al. 1988, Sionit et al. 1982, Wong 1993). Elevated CO2
shortened the time to harvest of marketable storage roots
(ca. 2 g in dry weight) from 26 to 19 d. Thus, CO 2 enhancement shortened the growth period for commercial harvest
by 21%; the annual yield of radish per land area might increase up to 37% with elevated CO2. This observation is
consistent with the previous estimate that a doubling of ambient CO 2 levels under horticultural or agro-industrial conditions would result in CO2-stimulated enhancement of
seasonal yields by about one-third compared with controls
(Cure 1985).
10
15 20 25
30 35 40 45
50
Days after planting
Fig. 3 Effects of ambient and elevated CO 2 on the ratio of storage root to shoot in radish. Values are means ±SE (n=4).
elevated CO2 (data not shown, see also Fig. 6). The initiation of leaf death was also accelerated by elevated CO 2
The rate of leaf expansion was increased by elevated (Fig. 2a), indicating that elevating CO 2 accelerates ontogenCO2 (Fig. 2a). The leaf area ratio (LAR) provides an indica- esis. The ratio of storage root to shoot in dry weight was intion of the proportion of a plant that is active in photosyn- creased by CO2 enrichment (Fig. 3). Again elevating CO2 acthesis. LAR decreased as the plants grew older (Fig. 2b), celerated development. The thickening growth of storage
mainly as a result of a rapid increase in the weight of the roots was initiated earlier under elevated CO2 (Fig. 1,3).
storage roots (Fig. 1). Plants grown in elevated CO 2 had Therefore, the effect of an elevated CO2 on the contribusmaller LARs, mainly due to larger storage roots (Fig. 1) tion of the storage root to "total dry weight" was compared
and also to decreased specific leaf area (leaf area per dry in terms of "total dry weight" to correct for the accelerated
weight of leaf; data not shown except for the following ex- ontogenesis (Fig. 4). The patterns of changes in the conample). The larger storage roots under elevated CO 2 seem- tribution for plants grown under elevated and ambient CO 2
ed to be produced by an increased rate of photosynthesis were similar (Fig. 4). Comprehensive analysis of the effect
under an elevated CO2 (see the next section). The specific of a doubling of CO 2 level on the ratio of root to shoot in
leaf areas of the fifth leaves grown under elevated and am- 25 studies suggested that it increases about 10% (Long and
bient CO 2 at 23 DAP were 23.2±0.9 and 27.2±0.6m 2 Drake 1992). In radish, the stimulatory effect of elevated
kg" 1 (means±SE, n=4), respectively. These results are CO2 on the ratio of root to shoot was also reported previconsistent with the earlier ones (Sionit et al. 1982, Wong ously without any mention of an acceleration of ontogene1993). The emergence of new leaves was accelerated by sis (Knecht 1975, Overdieck et al. 1988, Wong 1993). The
results obtained in this study are consistent with previous
20
Elevated COjio.O)
Ambient COji* •)
o
• » - ?
o •
•
•
4°
10 15 20 25 30 35 40 45 10 15 20 25 30 35 40 45 50
Days after planting
Fig. 2 Effects of ambient and elevated CO2 on leaf area (a) and
leaf area ratio (b) in radish. Circles represent sums of green leaf
areas. Sums of fully expanded leaf areas of yellowed and
defoliated leaves (O, • ) were estimated from the mean values for
similar leaves when they were fully expanded, namely, from the
results of earlier sampling. The leaf area ratio was obtained from
the green leaf area and the "total dry weight". Values are means ±
SE (n=4).
0
Elevated C 0 2 0
Ambient CO 2 (•)
10
20
30
40
Total weight" (g dry wt)
50
Fig. 4 Effects of ambient and elevated CO 2 on the contribution
of storage root to the "total dry weight" in radish. The results are
plotted in terms of "total dry weight" to correct for the acceleration of ontogenesis. For details, see text. Each symbol represents a
single plant.
Effects of high CO2 on growth and photosynthesis
Elevated COjO b
Ambient COjWi
0
S
S-
02
\
b> 0.15
6>
V
A
\\
\\
025
02
T
015
\
0.1
|
0.05
10 15 20 25 30 35 40 45
Days after planting
5
0
10 15 20 25 30 35 40
Total weight" (g dry wt)
Fig. 5 Effects of ambient and elevated CO 2 on relative growth
rates in radish. The results are shown with respect to day after
planting (a) and with respect to "total dry weight" (b) to correct
for the acceleration of ontogenesis. For details, see text.
ones, but they clearly indicate that one of the main reasons
for the increased ratio of storage root to shoot induced by
elevated CO 2 was due to the acceleration of ontogenesis.
Alterations in the timing of developmental events by elevated CO 2 have been reported by others (see Bowes 1993).
Mitchell et al. (1993), however, found that development of
wheat was not affected by elevated CO 2 treatment.
The relative growth rate was increased from 0.229 to
0.264 g g" 1 d~' with an elevated CO 2 at 19 DAP. However,
the relative growth rate of plants grown under an elevated
CO 2 decreased rapidly as compared to that of plants grown
under an ambient CO 2 and actually fell below that of
plants grown under an ambient CO 2 (Fig. 5). As mentioned
above, the elevated CO 2 accelerated ontogenesis. Therefore, we replotted the relative growth rate against "total
dry weight" to correct for this phenomenon. The "total dry
weight" of plants grown under elevated CO 2 was estimated
to be 2.86 g at 19 DAP, 9.91 g at 27 DAP, 20.8 g at 34.5
DAP and 35.8 g at 42 DAP, and that of plants grown under ambient CO 2 was estimated to be 0.91 g at 19 DAP,
4.66 g at 27.5 DAP, 10.9 g at 35 DAP, and 19.3 g at 42
DAP, respectively, from the results in Figure 1 (Fig. 5b).
These results indicate that elevated CO 2 has a positive effect
on RGR when comparisons are made at the same "developmental stage" but the extent of stimulation decreases as
plants grow larger.
Photosynthesis—The effects of elevated CO2 on the
rate of the photosynthetic fixation of CO 2 under ambient
concentrations of CO 2 of 350 and 750 //mol mol" 1 at a light
intensity of 900//molm~ 2 s~ 1 (400-700 nm) were investigated with fifth leaves grown under elevated and ambient
CO 2 . Leaf development was accelerated by elevated CO2
(Fig. 6). CO 2 enrichment had little effect on the maximum
rate of photosynthesis during the experimental period, but
the rate in leaves grown under elevated CO2 decreased
rapidly, perhaps because of the earlier initiation of leaf senescence brought about by accelerated ontogenesis. The
rate of photosynthesis was also measured using first, third,
seventh, and ninth leaves of plants of different ages. The
10 15 20 25
30 35 40 45
50
Days after planting
Fig. 6 Effects of ambient and elevated CO2 on the rate of photosynthesis (a) and the area of the green leaf (b) for fifth leaves of
radish. The rates of photosynthesis were measured under ambient
concentrations of CO2 of 350 (A, A) or 750//mol mol" 1 (o, •) and
a light intensity of 900/^mol m ~ 2 s " ' (400-700 nm). Values are
means ±SE (n=4).
results were essentially the same as that with fifth leaves
(data not shown). These results indicate that elevated CO2
has no effect on the maximum rate of photosynthetic
CO2 fixation. The enhancement of photosynthesis by CO2
enrichment during growth was assessed by comparing the
rate of photosynthesis with first, third, fifth, seventh, and
ninth leaves from 15 to 46 DAP under ambient concentrations of CO2 of 350 and 750 //mol mol" 1 at a light intensity
of 400//m~ 2 s~', which is close to the light intentsity at
plant height in the growth chamber. With plants grown under elevated CO2, enhancement of 39.2±2.4% (mean±
SE, n=12) was observed. With plants grown under
ambient CO2, enhancement of 37.0±2.0% (mean±SE,
n = 12) was found. Comparing the rates of photosynthesis
in plants grown and measured under 750//mol m o P ' CO2
and plants grown and measured under 350//mol mol" 1
CO2, we observed enhancement of 28.4±6.6% (mean±
SE, n=12), although accelerated leaf senescence occurred
in the former plants (cf. Fig. 6). With elevated CO 2 , the net
assimilation of carbon by a plant should be increased by an
increased rate of photosynthesis and also by an increase in
leaf area (Fig. 2a). This enhancement of the photosynthetic
capacity of the source might be one of the reasons for the
stimulated growth, especially for the growth of storage
roots, under elevated CO2. However, there is some debate
as to the degree to which enhanced photosynthesis translates into improving growth and yield (Bowes 1993, Evans
Effects of high CO2 on growth and photosynthesis
40
30
20
A
10
Elevated CO; grown (Q A . V )
Ambient CO; grown ( • . A . • )
0
200
400
600
Cifrunol/mol)
800
Fig. 7 Effects of ambient and elevated CO2 on the response of
photosynthesis (A) to the partial pressure of CO2 in the intercellular spaces of leaves (Ci). The rate of A was measured at a light intensity of 900/imol m~2 s"1 (400-700 nm). The fifth leaves of 24to 26-d-old plants were used. Each symbol refers to a single leaf.
1994). Further studies are needed to clarify the contribution of enhanced photosynthesis to the stimulation of
growth.
All the results described above also indicate that, in
radish during development up to 46 d, no negative acclimation of photosynthesis results from exposure to elevated
CO2. For further analysis of the effect of elevated CO2 on
photosynthetic nature, we compared A-Ci curves for fifth
leaves with maximum rates of photosynthesis during development. Such analysis of A-Ci curves is very informative
for analysis of the photosynthetic character (von Caemmerer and Farquhar 1981, Farquhar and Sharkey 1982).
The initial slope of the CO 2 response was the same for
leaves grown under elevated and ambient CO2 (Fig. 7),
indicating that the amount of catalytically competent
Rubisco was the same in both types of plant. The CO2-saturated rate of photosynthesis was also the same in both
types (Fig. 7), suggesting that the capacity for the regeneration of ribulose 1,5-bisphosphate was also unaffected by
elevated CO2 in the atmosphere.
Changes in levels of carbohydrates—The levels of
carbohydrates in fifth leaves of 27- to 28-d-old plants were
compared (Fig. 8). The daily accumulation of starch, sucrose, and glucose was increased with CO2 enrichment.
However, during the night, these carbohydrates were metabolized and/or transported, and their levels decreased to
the same levels as those found in leaves grown under ambient CO2. These results suggest that radish plants grown
under elevated CO2 do not over-accumulate photosynthates to the level which might cause a negative acclimation
of photosynthesis.
Sink capacity—It is clear that evaluation of the effect
of elevated CO2 on sink capacity is essential for clarification of the effect of elevated CO2 on the rate of photosynthesis. An effort to characterize sink capacity at the molecular level has been initiated, but still we know little. The
10
15
20
Time of day (h)
5
10
15
20
1
Time of day (h)
Fig. 8 Effects of ambient and elevated CO2 on changes in levels
of starch, sucrose, glucose, and fructose during the course of a
day. The fifth leaves of 27- to 28-d-old plants were used. Values
are means±SE (n = 8). Dark bars indicate darkness. For details,
see text.
concept of sink strength and sink activity was introduced
by Warren-Wilson (1967). The validity of this concept has
been evaluated controversially (see, e.g., Farrar 1993, Stitt
1993). However, the concept does give us some insights
about sink capacity under elevated and ambient CO2. In
radish, a major sink is the storage root. Young leaves,
petioles, and fibrous roots are also sinks, but the contribution of these organs to the total sink seemed to be relatively
small (cf. Fig. 3). Therefore, we evaluated the sink capacity
of the storage root according to the concept that sink
strength (gd~') = sink activity (gg~* d~')xsink size (g).
The sink activity of the storage root was estimated from
equation (1):
Sink activity = (lnW 2 -InW,)/T
(1)
where W2 and W, are the dry weights of the storage root at
the end and the beginning of a certain time period and T is
the time period. Sink size, namely dry weights of storage
root grown under elevated CO2, was estimated to be 1.29 g
at 19 DAP, 5.93 g at 27 DAP, 13.5 g at 34.5 DAP, and
24.5 g at 42 DAP, and dry weight of storage root grown under ambient CO 2 was estimated to be 0.28 g at 19 DAP,
2.65 g at 27.5 DAP, 6.56 g at 35 DAP and 11.7 g at 42
DAP, respectively, from the results shown in Figure 1. The
sink strengths and sink activities obtained in this way were
compared in terms of days after planting (Fig. 9a, c) and
also in terms of the ontogenic growth stage, which was compared on the basis of "total dry weight", estimated as described above (Fig. 9b, d). Sink strength increased as plants
grew older. Elevated C0 2 had a positive effect on sink
Effects of high CO 2 on growth and photosynthesis
lated by elevated levels of sugars (Koch 1996). Therefore,
we have to consider at least two possibilities: accelerated
sink growth might be simply due to an elevated supply of
sugars, and/or it might be due to the up-regulation of the
expression of genes for proteins responsible for sink capacity by an enhanced supply of sugars.
This work was supported in part by a grant-in-aid for
"Research for the Future" Program (JSPS-RFTF97R16001) from
the Japan Society for the Promotion of Science.
0
0.4
J
03
3
0.25
10 15 20 25 30 35 40 45
Days after planting
References
5
10
15
20
Total weight* (g dry wt)
Fig. 9 Effects of ambient and elevated CO2 on sink strength and
sink activity. Sink strength (gd~')=sink activity (gg"'d"')x
sink size (g). Sink strength and sink activity were plotted in terms
of days after planting (a, c) and in terms of "total dry weight" (b,
d). For details, see text.
strength in terms of growth period (Fig. 9a). However,
when we evaluated sink strength in terms of "developmental stage", the positive effect of elevated CO2 on sink
strength decreased (Fig. 9b). The lower value for younger
plants grown under ambient CO 2 might be due to a slow initiation of thickening growth of storage roots (Fig. 9a, b).
Sink activity was enhanced by elevated CO 2 at 19 DAP, but
it decreased as plants grew older. A negative effect of
elevated CO 2 on sink activity was found after 27 DAP. To
correct for the acceleration of ontogensis, as mentioned
above, sink activity was plotted against "developmental
stage" ("total dry weight"; Fig. 9d). The sink activity under
elevated CO 2 was higher than that under ambient CO2 during the early phase of growth, but the stimulatory effect of
elevated CO 2 became less as plants grew older (Fig. 9d).
These results indicate that elevated CO 2 has a positive effect
on sink capacity, but the extent of the enhancement is influenced by plant size.
Concluding remarks—In radish, with a major sink in
the early developing storage root, elevated CO2 has a positive effect on growth rate and harvestable yield but no effect
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(Received July 4, 1997; Accepted October 16, 1997)