Journal of Experimental Botany, Vol. 62, No. 4, pp. 1523–1530, 2011
doi:10.1093/jxb/erq401 Advance Access publication 20 December, 2010
REVIEW PAPER
Effects of elevated CO2 concentration on seed production in
C3 annual plants
Kouki Hikosaka1,*, Toshihiko Kinugasa2, Shimpei Oikawa3, Yusuke Onoda4 and Tadaki Hirose3
1
2
3
4
Graduate School of Life Sciences, Tohoku University, Aoba, Sendai 980-8578, Japan
Faculty of Agriculture, Tottori University, Tottori, Japan
Department of International Agricultural Development, Tokyo University of Agriculture, Tokyo 156-8502, Japan
Department of Biological Sciences, Faculty of Science, Kyushu University, Fukuoka 812-8581, Japan
* To whom correspondence should be addressed: E-mail: [email protected]
Received 6 July 2010; Revised 15 November 2010; Accepted 17 November 2010
Abstract
The response of seed production to CO2 concentration ([CO2]) is known to vary considerably among C3 annual
species. Here we analyse the interspecific variation in CO2 responses of seed production per plant with particular
attention to nitrogen use. Provided that seed production is limited by nitrogen availability, an increase in seed mass
per plant results from increase in seed nitrogen per plant and/or from decrease in seed nitrogen concentration ([N]).
Meta-analysis reveals that the increase in seed mass per plant under elevated [CO2] is mainly due to increase in
seed nitrogen per plant rather than seed [N] dilution. Nitrogen-fixing legumes enhanced nitrogen acquisition more
than non-nitrogen-fixers, resulting in a large increase in seed mass per plant. In Poaceae, an increase in seed mass
per plant was also caused by a decrease in seed [N]. Greater carbon allocation to albumen (endosperm and/or
perisperm) than the embryo may account for [N] reduction in grass seeds. These differences in CO2 response of
seed production among functional groups may affect their fitness, leading to changes in species composition in the
future high-[CO2] ecosystem.
Key words: Carbon dioxide, functional groups, meta-analysis, nitrogen use, reproduction, seed nitrogen concentration, seed
quality.
Introduction
Atmospheric CO2 concentration ([CO2]) has increased from
280 lmol mol1 before the industrial revolution to the
present 390 lmol mol1. The rate of increase is currently
1.9 lmol mol1 per year and [CO2] at the end of this century
may reach 500–1000 lmol mol1 (IPCC, 2007). Because
plant functions such as photosynthesis, transpiration, and
biomass production are sensitive to [CO2], elevated [CO2]
influences future ecosystem functions and agricultural yield.
Seed production is a vitally important event in plant life.
For wild (undomesticated) plants, seed quantity and quality
directly influence their fitness. Seeds are also important for
humans as they provide foods, oil, and other useful
materials. Several authors have reviewed CO2 response of
seed production (Kimball, 1983, 1986; Cure, 1985; Cure and
Acock, 1986; Amthor, 2001; Jablonski et al., 2002; Ziska
and Bunce, 2007). These reviews showed that elevated [CO2]
significantly enhanced seed mass per plant by 28–35%.
However, considerable variations are observed in the extent
of seed production enhancement. Miyagi et al. (2007)
reported that the ratio of seed mass per plant in elevated
[CO2] to that in ambient [CO2] ranged from 0.54 to 4.45 in
the literature (Fig. 1).
Here, we analyse the interspecific variation in CO2
response of seed production with respect to nitrogen use.
Nitrogen is one of the most important resources that limit
plant growth and seed production in natural and agricultural ecosystems (Aerts and Chapin, 2000). An increase in
carbon availability due to elevated [CO2] may enhance
nitrogen limitation, leading to a reduction in plant nitrogen
concentration ([N]). We hypothesize that nitrogen use in
ª The Author [2010]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved.
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1524 | Hikosaka et al.
reproductive organs accounts for the variation in CO2
response of seed production.
Variation in CO2 response of seed
production in annual plants
Large variation in CO2 response of seed production is
found not only between species but also within a species. In
our literature survey, the enhancement ratio of seed mass
per plant by [CO2] elevation ranged from 0.75 to 4.45 in rice
(42 observations), from 0.93 to 1.87 in soybean (28 experiments), and from 0.88 to 2.07 in wheat (51 experiments).
These variations were due to the different growth conditions
in the studies. In addition, large variations were observed
among species grown under the same conditions (Garbutt
and Bazzaz, 1984; Garbutt et al., 1990). For example,
11 annual species showed that seed production enhancement due to elevated [CO2] ranged from 0.84 to 2.12
(Miyagi et al., 2007; see Fig. 3a).
Why does the CO2 response of seed production vary
between species? The variation in seed production may
reflect the variation in total plant mass. However, previous
studies have demonstrated that seed production enhancement was not closely associated with vegetative growth
enhancement. In the meta-analysis by Jablonski et al.
(2002), the mean relative yield increase due to elevated
[CO2] was 12% and 25% in fruits and seeds respectively,
which was lower than the response of total plant mass
(31%). In some cases, elevated [CO2] did not affect, or even
reduced, reproductive yield, although vegetative mass was
increased (Larigauderie et al., 1988; Fajer et al., 1991;
Farnsworth and Bazzaz, 1995; Kinugasa et al., 2003; Lewis
et al., 2003). Comparing six old-field annuals, Ackerly and
Bazzaz (1995) demonstrated that the CO2 effect on total
mass was correlated with that on seed production; however,
the correlation was rather weak. Therefore, CO2 responses
of reproductive yield should be considered differently from
the CO2 responses of vegetative growth.
CO2 response differed between reproductive tissues in
a species. Kimball et al. (2002) reported that free-air CO2
enrichment enhanced the boll (seed+lint) yield of cotton by
40%, while it increased the lint fibre portion of the yield
even more, by ;54%. In soybean, elevated [CO2] increased
the pod-wall mass more than seed yield (Allen et al., 1988).
Kinugasa et al. (2003) found that seed production in
Xanthium canadense did not respond to [CO2 ], but capsule
mass increased by 86% with elevated [CO2] (Fig. 2a).
Elevated [CO2] may increase the mass of a reproductive
structure with a low [N] more than a structure with a high
[N] (Hikosaka et al., 2005; Hirose et al., 2005). Indeed
capsules had very low [N] in X. canadense (Fig. 2b).
Nitrogen use in reproductive growth and CO2
response
Two hypotheses were postulated on the variation in CO2
response of seed production in annuals (Miyagi et al., 2007):
6.0
30
Dry mass (g plant-1)
Mean 1.33
25
15
**
4.0
NS
2.0
0
12.0
10
5
0
0.6 0.8 1.0 1.2 1.4 1.6 1.8 2.0 2.2
> 2.5
Enhancement of seed production
(elevated [CO2] / ambient [CO2])
Fig. 1. Literature survey of the effect of elevated [CO2] on seed
production per plant in annual plants (n¼156; 22 species). Data were
collected for C3 annuals grown at ambient (350650 lmol mol1)
and elevated (700650 lmol mol1) [CO2]. Observations under
stressful conditions (e.g. water deficit, ozone exposure, and UV
enrichment) are excluded. The arrow denotes the mean
enhancement ratio (1.33). Redrawn from Miyagi et al. (2007).
N concentration (%)
Observation
20
a
b
NS
8.0
4.0
NS
0
Seed
Capsule
Fig. 2. (a) Dry mass and (b) nitrogen (N) concentration of the
reproductive part (seed and capsule) of X. canadense at ambient
(white bars, 360 lmol mol1) and elevated (black bars, 700 lmol
mol1) [CO2]. Error bars represent 61 SE (n¼10). *P<0.05; **P<0.01;
NS, not significant (t-test). Data from Kinugasa et al. (2003).
Seed production at elevated CO2 | 1525
(i) CO2 response of seed production varies between species
because the limiting factor of seed production differs from
species to species. Elevated [CO2] would enhance seed
production only in the species whose seed production was
limited by carbon as in capsules of X. canadense. If seed
production is limited to a greater extent by nitrogen in
species with high seed [N], as in seeds of X. canadense,
a negative correlation is expected between seed [N] and CO2
enhancement of seed production; (ii) alternatively, if seed
production is always limited by nitrogen availability (Hirose
et al., 2005), it would be enhanced by elevated [CO2] only
when nitrogen became more available for seed production.
If there were no additional nitrogen available at elevated
[CO2], there would be no enhancement in seed mass per
plant. The enhancement ratio of seed mass per plant would
be correlated with the enhancement ratio of seed nitrogen
per plant. These hypotheses were tested with 11 C3 annuals
grown at different [CO2] (Miyagi et al., 2007). The
enhancement of seed mass per plant by elevated CO2 was
not correlated with mean seed [N]; therefore, the first
hypothesis was rejected. In contrast, a strong 1:1 relationship was observed between the enhancement ratio of seed
mass per plant and that of seed nitrogen per plant (Fig. 3).
This result supported the second hypothesis that seed
production was enhanced only when nitrogen became more
available at elevated [CO2]. Seed production was limited by
nitrogen rather than by carbon, and elevated [CO2] increased seed production only in plants that exhibited
increased nitrogen in seeds.
Why was seed nitrogen per plant enhanced to a greater
extent in some species at elevated [CO2] than in others? Seed
nitrogen per plant may be enhanced if: (i) plants absorb
more nitrogen during vegetative growth; or (ii) plants
allocate acquired nitrogen more to reproductive growth,
which involves nitrogen retranslocation from vegetative
organs (Miyagi et al. 2007). Miyagi et al. (2007) found that
the fraction of acquired nitrogen allocated to reproduction
tended to decrease at elevated [CO2], and that the increase
in seed nitrogen per plant at elevated [CO2] was due mainly
to increased nitrogen acquisition. In addition, among the 11
species, legumes exhibited a more pronounced increase in
nitrogen acquisition and enhanced seed production with
elevated [CO2] than non-leguminous species. Symbiotic
bacteria perform nitrogen fixation, which entails carbon
cost for nitrogen assimilation with nodule construction. As
a greater amount of carbon is available at elevated [CO2],
legumes may allocate more carbon for nitrogen fixation,
and hence increase nitrogen assimilation (Poorter, 1993;
Soussana and Hartwig, 1996; Stewart and Potvin, 1996;
Hebeisen et al., 1997; Lüscher et al., 2000; Jablonski et al.,
2002; Lee et al., 2003). In fact, elevated [CO2] enhanced
nodulation and seed production increased to a greater
extent in species that produced more nodules at elevated
[CO2] (Miyagi et al., 2007). Using an isogenic line of
soybean that lacks the ability to form nodules, Oikawa
et al. (2010) showed that elevated [CO2] enhanced seed
production in nodulated soybean but not in its nonnodulated mutant (Fig. 4).
Some non-nitrogen-fixing species exhibited increased
nitrogen uptake at elevated [CO2] but others did not. The
different nitrogen uptake rate may be ascribed to differences
in root size or in kinetics of nitrogen uptake. The former
may be responsible if elevated [CO2] enhanced root size, as
has been shown in some studies (e.g. Rogers et al., 1992;
Dippery et al., 1995). Some authors hypothesized that
elevated [CO2] increases nitrogen uptake per unit root mass
(BassiriRad et al., 2001), because the nitrogen absorption
rate in roots often increases when plant [N] is lowered (Lee
and Drew, 1986; Lee and Rudge, 1986) and enhanced
carbon availability is expected to provide additional energy
for nitrogen absorption and assimilation. However, there
are many reports that are not consistent with these
Enhancement of seed production
(elevated [CO2] / ambient [CO2])
2.5
a
b
P. vulgaris
P. vulgaris
2.0
C. album
C. album
G. max
G. max
V. angularis
V. angularis
1.5
P. sativum
H. annuus
P. sativum
A. trifida
F. esculentum
P. lapathifolium
X. canadense
X. canadense
1.0
1.0
1.5
H. annuus
P. lapathifolium
A. artemisiaefolia
A. artemisiaefolia
0.5
0.5
A. trifida
F. esculentum
2.0
Enhancement of seed N per plant
(elevated [CO2] / ambient [CO2])
2.5
0.5
1.0
1.5
2.0
2.5
Enhancement of N acquisition rate
(elevated [CO2] / ambient [CO2])
Fig. 3. (a) Relationship between the enhancement ratio of seed production by elevated [CO2] and that of seed nitrogen (N) per plant.
Regression line: y¼1.08x–0.058, r2¼0.94. (b) Relationship between the enhancement ratio of seed production and the rate of nitrogen
acquisition during the reproductive period. Regression line: y¼0.562x+0.055, r2¼0.42. Squares and circles denote legumes and other
dicot species, respectively. Abbreviated genus: Ambrosia, Chenopodium, Fagopyrum, Glycine, Helianthus, Phaseolus vulgaris, Pisum
sativum, Polygonum lapathifolium, Vigna, and Xanthium. Redrawn from Miyagi et al. (2007) with modifications.
1526 | Hikosaka et al.
20
***
15
NS
10
5
greater in the non-nodulated mutant than in the wild type in
the vegetative growth phase, while the inverse was true in
the reproductive growth phase. Because large quantities of
carbohydrates are consumed by nodules, nitrogen fixation
may be less advantageous when soil nitrogen is available.
This may partly explain the variation across studies with
regard to CO2 responses in legumes.
CO2 response of seed [N] and its effect on
seed production
0
10
b
8
NS
6
***
4
2
0
1.5
c
***
-1
Seed nitrogen (g N plant )
Seed nitrogen concentration (%)
-1
Seed mass (g DM plant )
a
1
0.5
NS
0
Nodulated
Non-nodulated
Fig. 4. (a) Dry mass, (b) nitrogen concentration, and (c) nitrogen of
seeds of nodulated soybean (Glycine max cv. Enrei) and the nonnodulated isogenic line (G. max cv. En1282) grown at ambient
(white bars, 385 lmol mol1) and elevated (black bars, 593 lmol
mol1) [CO2]. Error bars represent+SE (n¼5). *** P<0.001, NS not
significant (t-test). Data from Oikawa et al. (2010).
hypotheses (BassiriRad et al., 1996, 1997; Zerihun and
BassiriRad, 2001). Different responses of nitrogen uptake to
elevated [CO2] among species (Roumet et al., 1996) would
lead to different reproductive outputs and, subsequently,
the number of offspring that potentially influence species
composition in a future high-[CO2] world.
It should also be noted that legumes are not always more
responsive to elevated [CO2] compared with non-legumes;
CO2 responses in whole-plant mass, leaf area index, and
photosynthetic rates were not greater in legumes than in
other functional types (Long et al., 2004; Ainsworth and
Long, 2005; Ziska and Bunce, 2007). Some legumes even
responded negatively to elevated [CO2] (West et al., 2005).
Oikawa et al. (2010) found that biomass production was
There was a strong 1:1 relationship between the enhancement of seed mass and seed nitrogen per plant (Fig. 3a).
This was caused by seed [N], which did not change much
with elevated [CO2]. In contrast to that in seeds, [N] in
vegetative tissues of many species decreased with elevated
[CO2] (Lutze and Gifford, 1998; Ishizaki et al., 2003; Miyagi
et al. 2007). These results suggest that [N] in seeds is more
conservative than [N] in vegetative tissues.
Other analyses, however, revealed that CO2 response of
seed [N] differed significantly between species. Jablonski
et al. (2002) demonstrated a significant decrease in seed [N]
in wheat and barley but not in soybean. Taub et al. (2008)
also demonstrated a significant decrease in seed [N] in
wheat, barley, and rice but not in soybean. They argued
that seed [N] decreased at elevated CO2 in non-legumes but
not in legume species because of nitrogen fixation. However, these studies compared only a few species of legumes
and grass species but no species from other groups, and
thus the hypothesis has not been thoroughly tested.
If seed [N] decreased with elevated [CO2], how does it
impact seed production? A decrease in seed [N] may
imply increment in seed production under limited nitrogen
availability.
Here we present a simple model to evaluate CO2 response
in seed production. Seed mass per plant (M) is expressed as
seed nitrogen per plant (N) divided by seed [N] ([N]):
M ¼ N3M=N ¼ N31=½N
ð1Þ
Then seed-mass response to elevated CO2 is given as
follows:
RM ¼ RN 31=R½N
ð2Þ
where RM, RN, and R[N] are enhancement ratios, respectively, of M, N, and [N] due to elevated [CO2]. This
equation implies that, if seed production is limited by
nitrogen availability, plants may enhance seed mass per
plant at elevated [CO2] by increasing seed nitrogen per plant
or by reducing seed [N].
Figure 5 illustrates the relationship between the enhancement ratio of seed nitrogen per plant (RN) and that of seed
[N] (R[N]). Isoclines represent the enhancement ratio of seed
production (RM). This figure indicates whether enhancement of seed production is due to enhancement of seed
nitrogen per plant or reduction of seed [N] (Equation 2).
Data are compiled from the literature (see Supplementary
Seed production at elevated CO2 | 1527
data), including 61 observations of 23 species from 22
studies, where plants were grown at ambient (350650 lmol
mol1) and elevated (700650 lmol mol1) [CO2]. We did
not include data obtained under stressful conditions such as
water deficit, ozone exposure, and UV enrichment. Because
large variations were observed within species among different studies, data were presented for each observation rather
than using a species average. We separated the species into
three functional groups: grass (Poaceae), legume (Fabaceae), and non-legume dicot species. Most observations
were distributed on isoclines RM>1 (Fig. 5), indicating that
seed mass per plant was enhanced by elevated [CO2]. Total
Fig. 5. Responses of seed nitrogen (N) per plant and seed [N] to
elevated [CO2]. Values are in ratios of elevated-to-ambient [CO2].
Data have been compiled from literature (see Supplementary data
for literature used). Symbols denote grass (filled circle), legume
(open square), and non-legume dicot species (open circle).
Isoclines (dashed lines) represent the enhancement ratio of seed
mass with elevated [CO2].
seed nitrogen per plant increased in 43 out of 61 observations (70%) and seed [N] decreased in 52 observations
(85%); however, variation in seed [N] was 3.5 times lower
than that of seed nitrogen per plant (standard deviation was
0.083 and 0.293, respectively; Fig. 5): seed [N] was less
variable compared with seed nitrogen per plant. There were
significant differences in CO2 responses in seed nitrogen per
plant and seed [N] between functional groups (Figs 5, 6).
Although all groups (grass, legume, and non-legume dicot
species) exhibited increased seed mass per plant with elevated
[CO2], legumes exhibited a greater extent of increased seed
nitrogen per plant than other groups (Kruskal–Wallis test,
P<0.05). In contrast, seed [N] decreased in grass species by
12% and in non-legume dicots by 4% with elevated [CO2] but
not in legumes. A non-parametric multiple comparison test
(Kruskal–Wallis test) indicated that grass species had a larger
reduction in seed [N] with elevated [CO2] than did legume
species (P<0.001) and also marginally larger than did nonlegume species (P¼0.057), while there was no significant
difference between legume and non-legume dicot species in
this respect (P¼0.37).
These results suggest that contributions to the enhancement of total seed mass of the two underlying factors (seed
nitrogen per plant and seed [N]) were different for different
functional groups. Contributions may be calculated from
Equation 2 after log10 transformation.
Log10 RM ¼ Log10 RN þ Log10 1=R½N
ð3Þ
Log transformation was performed because the ratios
showed skewed distribution (0<R<N). This, in turn, makes
the equation additive; therefore, the contributions of the
two underlying factors can be calculated as (log10RN/
log10RM) and [log10(1/R[N])/log10RM], respectively (sum to
1) (Poorter and van der Werf, 1998).
This calculation was applied for all observations that
had >10% seed-mass enhancement (46 observations). Across
all species, three-quarters of the variation in seed-mass
enhancement with elevated [CO2] was explained by an increase
Fig. 6. (a) Changes in seed nitrogen (N) per plant and (b) in seed [N] with elevated [CO2] for the three functional groups, presented as
enhancement ratios. The central box in each box plot indicates the interquartile range and median; whiskers indicate the 10th and 90th
percentiles.
1528 | Hikosaka et al.
Fig. 7. Relative contributions of the two underlying factors, enhancement of seed nitrogen per plant (Seed N) and dilution of seed [N], to
seed-mass enhancement with elevated [CO2]. The central box in each box plot shows the interquartile range and median; whiskers
indicate the 10th and 90th percentiles.
in seed nitrogen per plant and a quarter by reduction of seed
[N] (median 75% compared with 25%). Within grass species,
reduction of seed [N] was a relatively important contributor
(median 37%) for seed-mass enhancement with elevated [CO2]
while the rest (63%) was due to the enhancement of seed
nitrogen per plant (Fig. 7). In contrast, in legumes, reduction
in seed [N] was approximately zero and seed-mass enhancement was nearly entirely due to increased seed nitrogen per
plant. Non-legume dicot species showed an intermediate
response; 85% (median) of seed-mass enhancement was due
to increased seed nitrogen and the rest due to reduction of
seed [N]. These results suggest that the reduction of seed [N]
under elevated [CO2] was an important mechanism in increasing seed production in grass species but not as much in
other groups.
The presence of albumen (endosperm and perisperm) in seed
may account for different CO2 responses of seed production in
different functional groups. Albumen stores large quantities of
carbohydrates and its [N] is relatively low (e.g. Cakmak et al.,
2010). Grass species produce albuminous seeds, while legumes
produce exalbuminous seeds. In the present study, other nonlegume dicot species consisted mainly of Asteraceae species,
which also produce exalbuminous seeds. The embryo has
higher [N] (Cakmak et al., 2010) and may not change its
composition with elevated [CO2]. If elevated [CO2] increased
the amount of albumen relative to the embryo, seed [N] would
decrease. This is analogous to the amount of accessory tissues,
such as lint in cotton and capsules in X. canadense that are
more responsive to elevated [CO2], as discussed above.
Then why did seed [N] not change in exalbuminous
species with [CO2] elevation? Seed [N] may be important for
germination and subsequent growth. It has been shown that
high seed [N] is advantageous for quick germination
(Andalo et al., 1996, 1998; Hara and Toriyama, 1998) and
in competition with other plants after germination (Parrish
and Bazzaz, 1985; Huxman et al., 1998), especially under
low nitrogen availability (Naegle et al., 2005). Seed [N] may
be regulated to a certain level to maintain ‘quality’ of
growth after germination. If so, we may hypothesize that
reduction of seed [N] in grass species is due to an increased
albumen content, not at the expense of seed quality.
However, some species have exhibited decrease in both seed
[N] and seed nitrogen per plant (Fig. 5). In such species,
growth and survivorship of seedlings may be negatively
affected by elevated [CO2].
Conclusion
Nitrogen limitation is a key factor in understanding CO2
responses of seed production in annual plants. Plants can
increase seed production with elevated [CO2] when they
increase nitrogen acquisition or decrease seed [N]. Legumes
are advantageous in this respect because they may increase
nitrogen fixation with an increased supply of assimilates.
Grass species increase seed production with elevated [CO2]
by decreasing seed [N] as well as increasing nitrogen
acquisition. Decrease in seed [N] in grass may not imply
reduction in seed quality if it occurs due to increased
albumen content without reduced [N] in embryos. However,
if reduction in seed [N] is associated with reduced seed
quality, it will affect survivorship and growth of their
progeny. Increasing atmospheric [CO2] may affect species
composition in future ecosystems through differential
effects on seed quality and quantity in different plant
functional groups.
Supplementary data
Supplementary data are available at JXB online.
Suplementary data are the references used in the metaanalysis shown in Fig. 5.
Seed production at elevated CO2 | 1529
Acknowledgements
We thank Y. Suzuyama, S. Iwamoto, Y. Kawachi,
E. Miwa, H. Tanaka, Y. Furudate, S. Oda for kind help in
the literature survey. This study was supported by
KAKENHI, the Global Environment Research Fund
(F-092) by the Ministry of the Environment, Japan, and
the Global COE Program j03 (Ecosystem management
adapting to global change) by the MEXT.
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13–20.
Fajer ED, Bowers MD, Bazzaz FA. 1991. The effects of enriched
CO2 atmospheres on the buckeye butterfly, Junonia coenia. Ecology
72, 751–754.
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