Effects of rising atmospheric concentrations of carbon dioxide on plants

Full text

By: Daniel R. Taub (
Biology Department, Southwestern University
) © 2010 Nature Education
Effects of Rising Atmospheric Concentrations of Carbon
Dioxide on Plants
Photosynthetic assimilation of CO2 is central to the metabolism of plants. As
atmospheric concentrations of CO2 rise, how will this affect the plants we
depend on?
Atmospheric concentrations of carbon dioxide have been steadily rising, from
approximately 315 ppm (parts per million) in 1959 to a current atmospheric average of
approximately 385 ppm (Keeling
et al.
,2009). Current projections are for concentrations to
continue to rise to as much as 500–1000 ppm by the year 2100 (IPCC 2007).
While a great deal of media and public attention has focused on the effects that such higher
concentrations of CO2 are likely to have on global climate, rising CO2 concentrations are
also likely to have profound direct effects on the growth, physiology, and chemistry of
plants, independent of any effects on climate (Ziska 2008). These effects result from the
central importance of CO 2 to plant metabolism. As photosynthetic organisms, plants take
up atmospheric CO2, chemically reducing the carbon. This represents not only an
acquisition of stored chemical energy for the plant, but also provides the carbon skeletons
for the organic molecules that make up a plants’ structure. Overall, the carbon, hydrogen
and oxygen assimilated into organic molecules by photosynthesis make up ~96% of the
total dry mass of a typical plant (Marschner 1995). Photosynthesis is therefore at the heart
of the nutritional metabolism of plants, and increasing the availability of CO2 for
photosynthesis can have profound effects on plant growth and many aspects of plant
physiology.
Our knowledge of plant responses to future CO2 concentrations rests on the results of
experiments that have experimentally increased CO2 and then compared the performance
of the experimental plants with those grown under current ambient CO 2 conditions. Such
experiments have been performed in a wide variety of settings, including greenhouses and
chambers of a variety of sizes and designs. However plants grown in chambers may not
experience the effects of increasing CO2 the same way as plants growing in more natural
Citation: Taub, D. (2010) Effects of Rising Atmospheric Concentrations of
Carbon Dioxide on Plants.
Nature Education Knowledge
1(8):21

experience the effects of increasing CO2 the same way as plants growing in more natural
settings. For this reason, techniques of Free-Air Carbon dioxide Enrichment (FACE) have
been developed that allow natural or agricultural ecosystems to be fumigated with elevated
concentrations of CO2 in the field without use of chambers (Figure 1). As these experiments
are the most naturalistic, they should provide the best indication of the responses of plants
to increased CO2 under the real-world conditions of the future. This article therefore
focuses on data from FACE experiments wherever these are available. Whenever possible, to
ensure the generality of conclusions, reference is made to analyses that have incorporated
data from multiple experiments independently conducted at various research facilities.
Figure 1: Free - air carbon dioxide enrichment allows experiments with controlled atmospheric
concentrations of carbon dioxide to be conducted in the field and avoids potential
experimental artifacts from growing plants in enclosed chambers.
Courtesy of David F. Karnosky.
One of the most consistent effects of elevated atmospheric CO2 on plants is an increase in
the rate of photosynthetic carbon fixation by leaves. Across a range of FACE experiments,
with a variety of plant species, growth of plants at elevated CO2 concentrations of 475–600
ppm increases leaf photosynthetic rates by an average of 40% (Ainsworth & Rogers 2007).
Carbon dioxide concentrations are also important in regulating the openness of stomata,
pores through which plants exchange gasses, with the external environment. Open stomata
allow CO2 to diffuse into leaves for photosynthesis, but also provide a pathway for water to
diffuse out of leaves. Plants therefore regulate the degree of stomatal opening (related to a
measure known as stomatal conductance) as a compromise between the goals of
maintaining high rates of photosynthesis and low rates of water loss. As CO2
concentrations increase, plants can maintain high photosynthetic rates with relatively low

stomatal conductance. Across a variety of FACE experiments, growth under elevated CO2
decreases stomatal conductance of water by an average of 22% (Ainsworth & Rogers 2007).
This would be expected to decrease overall plant water use, although the magnitude of the
overall effect of CO2 will depend on how it affects other determinants of plant water use,
such as plant size, morphology, and leaf temperature. Overall, FACE experiments show
decreases in whole plant water use of 5–20% under elevated CO2. This in turn can have
consequences for the hydrological cycle of entire ecosystems, with soil moisture levels and
runoff both increasing under elevated CO2 (Leakey
et al.
2009).
Since photosynthesis and stomatal behavior are central to plant carbon and water
metabolism, growth of plants under elevated CO2 leads to a large variety of secondary
effects on plant physiology. The availability of additional photosynthate enables most plants
to grow faster under elevated CO2, with dry matter production in FACE experiments being
increased on average by 17% for the aboveground, and more than 30% for the belowground,
portions of plants (Ainsworth & Long 2005; de Graaff
et al.
2006). This increased growth is
also reflected in the harvestable yield of crops, with wheat, rice and soybean all showing
increases in yield of 12–14% under elevated CO2 in FACE experiments (Ainsworth 2008;
Long
et al.
2006).
Elevated CO 2 also leads to changes in the chemical composition of plant tissues. Due to
increased photosynthetic activity, leaf nonstructural carbohydrates (sugars and starches) per
unit leaf area increase on average by 30–40% under FACE elevated CO2 (Ainsworth 2008;
Ainsworth & Long 2005). Leaf nitrogen concentrations in plant tissues typically decrease in
FACE under elevated CO2, with nitrogen per unit leaf mass decreasing on average by 13%
(Ainsworth & Long 2005). This decrease in tissue nitrogen is likely due to several factors:
dilution of nitrogen from increased carbohydrate concentrations; decreased uptake of
minerals from the soil, as stomatal conductance decreases and plants take up less water
(Taub & Wang 2008); and decreases in the rate of assimilation of nitrate into organic
compounds (Bloom
et al.
2010).
Protein concentrations in plant tissues are closely tied to plant nitrogen status. Changes in
plant tissue nitrogen are therefore likely to have important effects on species at higher
trophic levels. Performance is typically diminished for insect herbivores feeding on plants
grown in elevated CO 2 (Zvereva & Kozlov 2006). This can lead to increased consumption of
plant tissues as herbivores compensate for decreased food quality (Stiling and Cornelissen
2007). Effects on human nutrition are likely as well. In FACE experiments, protein
concentrations in grains of wheat, rice and barley, and in potato tubers, are decreased by
5–14% under elevated CO2 (Taub
et al.
2008). Crop concentrations of nutritionally important
minerals including calcium, magnesium and phosphorus may also be decreased under
elevated CO2 (Loladze 2002; Taub & Wang 2008).
Effects of Other Environmental Factors on Plant Response to Elevated
CO2
The effects of elevated CO2 on plants can vary depending on other environmental factors.
While elevated CO2 makes carbon more available, plants also require other resources
including minerals obtained from the soil. Elevated CO2 does not directly make these
mineral elements more available and, as noted above, may even decrease the uptake of
some elements. The ability of plants to respond to elevated CO 2 with increased

some elements. The ability of plants to respond to elevated CO 2 with increased
photosynthesis and growth may therefore be limited under conditions of low mineral
availability. This effect has been best documented for nitrogen. In FACE experiments, there
is less enhancement of photosynthesis by elevated CO2 under low than high soil N
conditions (Ainsworth & Long 2005; Ainsworth & Rogers 2007). Crop yield in FACE also
appears to be enhanced by elevated CO2 to a lesser extent under low-N than under high-N
(Ainsworth & Long 2005; Ainsworth 2008; Long
et al.
2006). Across studies using all types
of CO2 fumigation technologies, there is a lower enhancement of biomass production by
elevated CO2 under low-nutrient conditions (Poorter & Navas 2003). Crops grown with low
amounts of N fertilization also show a greater decrease in protein concentrations under
elevated CO2 than crops grown with higher N fertilization (Taub
et al.
2008).
Another environmental factor that interacts with elevated CO2 is atmospheric ozone (O3), a
gaseous toxin. Ground-level O3 concentrations have been increasing worldwide (and are
expected to continue to increase) due to increased emissions of pollutants that react to
produce O3 (Vingarzan 2004). High atmospheric concentrations of ozone can cause damage
to leaves and decreased plant growth and photosynthesis (Feng
et al.
2008; Morgan
et al.
2003). The primary location of O3 injury to plants is the internal tissues of leaves.
Decreased openness of stomata under elevated CO2 can therefore decrease exposure of
sensitive tissues to ozone. Elevated CO2 substantially decreases the negative effects of high
ozone on photosynthesis, growth, and seed yield in both soybeans and rice (Feng
et al.
2008; Morgan
et al.
2003). Across experiments with all plant species, the enhancement of
growth by elevated CO2 is much greater under conditions of ozone stress than otherwise
(Poorter & Navas 2003).
Differences among Plant Functional Types in Response to Rlevated
CO2
The preceding discussion has presented the average effects of elevated CO2, but obscures
important patterns of difference in response among plant species. One of the most
important determinants of species differences in response to elevated CO2 is photosynthetic
type. Most plant species (~90%) utilize a photosynthetic process known as C3
photosynthesis. Other species use either of two physiologically distinct processes known as
C4 and CAM photosynthesis (Figure 2). C4 plants include most tropical and sub-tropical
grasses and several important crops, including maize (corn), sugar cane, sorghum, and the
millets. There has therefore been considerably more research on the responses to elevated
CO2 in C4 than in CAM plants.

Figure 2: Each plant species utilizes one of several distinct physiological variants of
photosynthesis mechanisms, including the variants known as C3 and C4
photosynthesis.
C4 plants use a biochemical pump to concentrate CO2 at the locations within the leaf where
the RUBISCO enzyme mediates incorporation of CO2 by the Calvin-Benson photosynthetic
cycle. Since CO2 concentrations are already high within the bundle sheath cells, increasing
atmospheric CO2 concentrations above current levels has little direct effect on
photosynthetic rates for C4 species. C4 species do respond to elevated CO2 by decreasing
stomatal conductance; this may lead to some indirect enhancement of photosynthesis by
helping avoid water stress under drought conditions (Leakey 2009). In FACE experiments,
stimulation of photosynthesis by elevated CO2 in C4 plants is only about one-third of that
experienced by C3 species. C4 plants also show little or no enhancement of growth (dry
matter production) in these studies (Ainsworth & Long 2005). The very limited data
available also shows no increase in C4 crop yield in FACE studies (Long
et al.
2006). While
there is little FACE data available on effects of elevated CO2 on plant nitrogen and protein
concentrations, data from chamber experiments shows C4 plants to be much less
responsive than C3 plants in this regard (Cotrufo
et al.
1998). The picture that emerges is
that C4 plants are in general relatively unresponsive to elevation of atmospheric CO2 above
current ambient levels.
In contrast to C4 species, another group of plants, legumes (members of the botanical
family Fabaceae) may be especially capable of responding to elevated CO2 with increased
photosynthesis and growth (Rogers
et al.
2009). For most plants, growth under elevated
CO2 can alter the internal balance between carbon (obtained in extra quantities through
enhanced photosynthesis) and nitrogen (either unaffected or taken up in decreased
amounts due to decreased uptake of water). In contrast, most legume species participate in

close mutualistic relationships with bacteria that live in nodules formed on the plant’s roots.
These bacteria are able to "fix" atmospheric nitrogen, chemically reducing it to a form that
can be taken up and used by plants. Under elevated CO2 conditions, legumes may be able
to shunt excess carbon to root nodules where it can serve as a carbon and energy source
for the bacterial symbionts. In effect, legumes may be able to exchange the excess carbon
for nitrogen and thereby maximize the benefits of elevated atmospheric CO2. Many studies
in controlled environments have shown that, compared to other plant species, legumes
show greater enhancement of photosynthesis and growth by elevated CO 2 (Rogers
et al.
2009). Decreases in tissue nitrogen concentrations under elevated CO2 are also smaller for
legumes than for other C3 species (Cotrufo
et al.
1988; Jablonski
et al.
2002; Taub
et al.
2008). In FACE experiments, soybeans (a legume) show a greater response to elevated CO2
than wheat and rice in photosynthesis and overall growth, although not in harvestable yield
(Long
et al.
2006).
Plant Community Interactions under Elevated CO2
A number of experiments have found that some plant species that respond positively to
elevated CO2 when grown alone experience decreased growth under elevated CO2 when
grown in mixed plant communities (Poorter & Navas 2003). This effect likely results
because the direct positive effects of elevated CO2 are outweighed by negative effects due
to stimulation of the growth of competitors. Rising atmospheric concentrations of CO 2 may
therefore lead to changes in the composition of plant communities, as some species reap
more of an advantage from the increased CO2 than do others. In mixed-species
experiments under high fertility conditions, C4 plants decrease as a proportion of the
biomass of plant communities under elevated CO2. Similarly, under low fertility conditions,
legumes increase as a proportion of the biomass of plant communities under elevated CO 2
(Poorter & Navas 2003).
Summary
Current evidence suggests that that the concentrations of atmospheric CO 2 predicted for
the year 2100 will have major implications for plant physiology and growth. Under elevated
CO2 most plant species show higher rates of photosynthesis, increased growth, decreased
water use and lowered tissue concentrations of nitrogen and protein. Rising CO2 over the
next century is likely to affect both agricultural production and food quality. The effects of
elevated CO2 are not uniform; some species, particularly those that utilize the C4 variant of
photosynthesis, show less of a response to elevated CO2 than do other types of plants.
Rising CO2 is therefore likely to have complex effects on the growth and composition of
natural plant communities.
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