Plant Responses to

Elevated CO2

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Article Contents
. Introduction

Jinyoung Y Barnaby, Crop Systems and Global Change Laboratory, Beltsville, Maryland, USA
Lewis H Ziska, Crop Systems and Global Change Laboratory, Beltsville, Maryland, USA

. Effect of Elevated CO2 at the Genetic and Biochemical

Level
. Effect of Elevated CO2 at the Single Leaf Level
. Effects of Elevated CO2 at the Whole Plant Level
. Effects of Elevated CO2 at the Plant Community and
Ecosystem Level
. Effects of Elevated CO2 at Evolutionary Levels
. Elevated CO2 and other Tropic Levels
. Elevated CO2 and Plant Responses: Challenges
. Elevated CO2 and Plant Responses: Addressing the
Challenges
. Plant Responses to Elevated CO2: Conclusions

Online posting date: 16th July 2012

Carbon dioxide (CO2) has two unique properties: physically it absorbs in the infra-red (heat) portion of the spectrum, and plays a role in maintaining global surface
temperatures; secondly, it is the source of carbon for plant
photosynthesis and growth. Recent, rapid anthropogenic
increases in CO2 have been well-characterised with
respect to climatic change; less recognised is that increase
in CO2 will also impact how plants supply food, energy and
carbon to all living things. At present, numerous experiments have documented the response of single leaves or
whole plants to elevated CO2; however, it is difficult to
scale up or integrate these observations to plant biology
in toto. To that end, a greater emphasis on multiple factor
experiments for managed and unmanaged systems, in
combination with simulative vegetative modelling, could
increase our predictive capabilities regarding the impact
of elevated CO2 on plant communities (e.g. agriculture,
forestry) of human interest.

Introduction
At biologically relevant temperatures, it is recognised that
there are four physical resources necessary for plant growth
to occur: (a) light; (b) nutrients; (c) water; and (d) CO2.
Since 1959, concentrations of atmospheric CO2 have
increased from 318 to 392 mmol mol21; and, depending on
anthropogenic emission rates, may exceed 1000 mmol
mol21 by the end of the century (cdiac.ornl.gov/pns/
eLS subject area: Plant Science
How to cite:
Barnaby, Jinyoung Y; and Ziska, Lewis H (July 2012) Plant Responses to
Elevated CO2. In: eLS. John Wiley & Sons, Ltd: Chichester.
DOI: 10.1002/9780470015902.a0023718

current_ghg.html). Aside from any association with

increased surface temperatures, such a rapid increase in
CO2 represents a sudden availability of a resource necessary for plant function.
In this review we describe the present understanding of
plant responses to carbon dioxide across a range of temporal and spatial scales. This understanding is derived from
a synthesis of dierent research methodologies including
growth chambers, greenhouses, SPAR (Soil, Plant,
Atmosphere, Research) units, open-top chambers and Free
Air CO2 Enrichment (FACE) systems. Additional information regarding the strengths and weaknesses of these
methodologies can be found elsewhere (e.g. Ziska and
Bunce, 2007; Tubiello et al., 2007).
Although plant responses to elevated CO2 have been
studied since the 1960s, much of what is known reects
short-term (usually 51 year) exposure studies where
individual plants are grown at ambient and twice ambient
CO2 concentrations (Kimball, 1993). This reects, in part,
the high cost and complexity of methodologies (e.g. FACE)
for exposing plants to elevated CO2. As a result, while
single leaves and whole plants represent the most experimentally accessible data, less is known for either very large
(e.g. ecosystem) or very small (e.g. transcriptomics, proteomics) bio-processes (Figure 1).
With these methodological caveats in mind, the goal of
the current article is to review the impacts of elevated CO2
with respect to molecular, genetic and physiological
responses, and to address the issues of integration and
scaling at the ecosystem level. Overall, we recognise that
rising CO2, unlike climate change, is likely to be uniform
across the globe, but plant species are expected to vary
inter- and intra-specically in their response. Understanding the basis for this variation to elevated CO2 may
provide valuable insight into alterations in the biology and
function of managed and unmanaged plant systems, and
subsequent availability of ecosystem services provided for
the global population.

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Plant Responses to Elevated CO2

Macro

Physiology
genetics

Plant

Environmental biology
population biology
ecology

Controlled

n (a)

Environmental growth chamber

(EGC), soil plant atmosphere
research (SPAR)

Approach

EGC, SPAR, Open top channel

(OTC), free air CO2 enrichment
(FACE)

Top-d
ow

Cell/Organ

Establish
Ecosystem

Molecular biology
biochemistry
cell biology

Growth condition

)
-up (b
Bottom

Level

Determine
Plant performance

Micro

Scale

Face

Population

Natural, uncontrolled

(1) Controlled system study

Pro: can control all the factors to investigate the direct effect of the factor interested.
Con: can only study the limited number of interactions
(2) Natural, uncontrolled system study
Pro: unexpected results that cannot be obtain from controlled study can be found
Con: can determine outcome (e.g. yield), but not the exact reason of the outcome;
possible chances to misinterpret data due to unknown variable factors
Figure 1 Overview of different temporal and spatial scales of studies to understand plant biological processes in response to rising CO2 levels. The
combination of molecular, biochemical, genetic, and physiological studies determines whole plant performance, and genotypic and phenotypic variations of
plant performance with environmental interactions at the population level establishes ecosystem. Studies can be viewed as using two different approaches; a
top-down approach (a) is having a global view of plant responses to elevated CO2 at the ecological level, to provide insight into mechanisms occurring at
the micro-scale; and a bottom-up approach (b) characterisation of CO2 effects at smaller scales (e.g. single leaf) followed by simulating this effect for the
whole plant and/or plant system at different abiotic environments (see also Ziska and Bunce, 2007). With permission from US Government.

Effect of Elevated CO2 at the Genetic

and Biochemical Level
Using micro-array analysis, elevated CO2 levels have been
shown to alter the transcriptome responses of soybean
(Ainsworth et al., 2006), corn (Kim et al., 2006), sugarcane
(De Souza et al., 2008), Arabidopsis (Bae and Sicher, 2004),
inter alia. Such alterations are thought, in turn, to be
associated with gene expression and key physiological/
biochemical events including, oral-initiation (Springer
et al., 2008), respiratory breakdown of starch (Ainsworth
et al., 2006), stomatal development (Kim et al., 2006),
decreases in herbivore defense compounds (Sun et al.,
2011) and changes in ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco), the enzyme that catalyses CO2
assimilation, the initial step in the CalvinBenson cycle
(Makino et al., 2000). However, both the number of genes
that respond to increasing CO2, and the magnitude of their
response are, in general, less than those observed when
plants are exposed to biotic and abiotic stress.
Despite the relative lack of response, recent genetic
screening and functional characterisation studies have led
to the identication of key regulators in the CO2 signalling
pathway (Kim et al., 2010). One such regulator may be
carbonic anhydrase, the enzyme that catalyses the conversion of carbon dioxide and water to bicarbonate
and may also control stomatal response to atmospheric
CO2 (Hu et al., 2010). Another mutant demonstrates
2

insensitivity to both CO2 and Abscisic acid (ABA), suggesing that there may be overlapping step(s) between the
ABA and CO2 transduction pathways (Young et al., 2006).
Other hypersensitive CO2 mutants (Hashimoto et al., 2006)
have been examined to determine whether malate uptake
into guard cells may also regulate CO2 induction of stomatal closure (Lee et al., 2008). Overall, the use of mutants
may allow researchers to identify potential regulators
associated with molecular mechanisms that translate CO2
concentration into stomatal closure.

Effect of Elevated CO2 at the Single

Leaf Level
One of the best characterised eects of rising atmospheric
CO2 relates to carbon dynamics and leaf photosynthesis.
For plants only possessing the C3 photosynthetic pathway
(i.e. where the rst product of photosynthesis is a three
carbon compound), increasing CO2 concentration initially
stimulates photosynthesis by increasing the concentration
gradient from air to leaf, and by reducing the loss of CO2
through photorespiration. See also: Photosynthesis;
Photosynthesis: The Calvin Cycle
Photorespiration occurs because Rubisco acts as both a
carboxylase and oxygenase. When oxygen is assimilated,
utilisation of oxygenated products occurs with a release of
CO2, that is, the photorespiratory cycle. This release of

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Plant Responses to Elevated CO2

carbon dioxide, in turn, lowers the eciency of photosynthesis (i.e. CO2 xation by Rubisco); by reducing rates
of net CO2 assimilation. Because this reaction is temperature dependant (i.e. oxygen concentration increases with
temperature within the leaf), increasing CO2 ensures that
Rubisco is more fully saturated with CO2, thus suppressing
the oxygenase reaction and increasing CO2 assimilation.
See also: Photorespiration; Photosynthetic Carbon Metabolism; Rubisco
At present it is thought that the C3 pathway is representative of approximately 94% of all known plant species,
and should respond photosynthetically to increasing CO2
(Figure 2a). Alternatively, plants with the C4 pathway
(12% of all plant species) have an internal mechanism for
concentrating CO2 around Rubisco, eliminating photorespiratory losses. Hence, it is expected that rising CO2
should have minimal eects on leaf photosynthesis for C4
plants (Figure 2a). Relative to C3 and C4 plants, fewer
studies have addressed the photosynthetic responses of
crassulacean acid metabolism (CAM) plants, approximately 46% of all plant species. Among the dierent
CAM morphologies (succulents, epiphytes, etc.), the
average stimulation of photosynthesis with a doubling of
ambient CO2 is ca 3540%; however, there is a large
variation between species, and the basis for this variation is

40
C3

Leaf photosynthesis (mol CO2 m2 s1)

30

C4

20

10
(a)

0
40

C3
Rubisco
limited

30

Pi
regeneration
limited

20
RuBP
regeneration
limited

10
(b)
0

200

400

600

800

1000

CO2 concentration (mol mol1)

Figure 2 Theoretical responses of C3 and C4 photosynthesis to rising
atmospheric carbon dioxide (a); and identification of biochemical
limitations associated with feedback inhibition in the photosynthetic
response of C3 species to rising CO2 (b). Adapted from Sage and Coleman,
2001. With permission from US Government.

unclear (Ceusters and Borland, 2010). See also: Crassulacean Acid Metabolism; Kranz Anatomy and the C4
Pathway
Although exposure of leaves to elevated CO2 results in
photosynthetic stimulation, it has been observed in a
number of studies with C3 species that photosynthetic rates
will diminish over time following exposure. This observation, deemed photosynthetic acclimation, or downregulation, is thought to limit the temporal stimulation of
photosynthesis in association with elevated CO2 conditions
and may occur in a few days to a few months. The basis for
such a response has been attributed to a number of
potential physiological mechanisms, including (1) sugar/
carbohydrate accumulation and reduced expression of
Rubisco small subunit genes (Sheen, 1994); (2) shifts in
nitrogen supply associated with carbohydrate accumulation (Stitt and Krapp, 1999); (3) a tie-up of inorganic
phosphate (pi) with carbohydrate accumulation and a
subsequent limitation in Ribulose bisphospate (RuBP)
regeneration capacity (Sharkey, 1985) and/or (4) a potential eect on photosynthesis through accelerated ontogeny
and early senescence (Stitt and Krapp, 1999; Lewis et al.,
2002) (Figure 2b). Yet, acclimation is not always observed in
the long-term, for example, exposure to elevated CO2 of a
C3 marsh species, Scirpus olneyi, has not resulted in
photosynthetic acclimation over a seventeen year period
(Rasse et al., 2005). In addition, acclimation may also vary
temporally with sourcesink phenological changes negating its occurrence in swiss chard and sugarbeet (Ziska
et al., 1995).
Another well-characterised eect of elevated CO2 at the
leaf level is that of stomatal closure and reduced transpiration. Stomata, leaf apertures delineated by a pair of
guard cells at the leaf epidermis, play a major role in gas
exchange between leaf and atmosphere. Stomata regulate
CO2 uptake for photosynthesis and water loss during
transpiration. The eect of CO2 concentration on stomatal
movement and density (i.e. the number of stomata per unit
leaf area) has been studied since the 1970s (Morrison, 1987;
Woodward and Kelly, 1995) as well as stomatal index, the
ratio of stomata relative to total epidermal cell numbers
(Royer, 2001). Kim et al. (2006) showed that the signalling
process leading to guard cell formation (SDD1, Berger and
Altmann, 2000; YD, Bergmann et al., 2004) and stomatal
initiation (TMM1, Nadeau and Sack, 2002) were altered in
response to elevated CO2 in maize, conrming the
involvement of CO2 concentration on regulation of
stomatal development. See also: Stomata; Stomatal
Patterning
Interestingly, a mutant screening study (Gray et al.,
2000) found CO2-induced changes in stomatal density
through a role of High Carbon Dioxide (HIC), which is
associated with synthesis of specialised waxes found in the
plants extracellular matrix. Furthermore, Franks and
Beerling (2009) also showed that elevated CO2 can alter
stomatal density with a high density of small stomata
occurring at low atmospheric CO2, and low density with
large stomata as CO2 increases. They inferred that smaller,

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Plant Responses to Elevated CO2

rapidly responding stomata could be a protective mechanism to minimise exposure to excessive water loss at lower
CO2 concentrations. These studies suggest that stomatal
development may reect, in part, adaptation to climate,
including CO2 concentration.
The response of stomata to elevated CO2 appears to be
ubiquitous among the dierent photosynthetic sub-types
(e.g. C3, C4, CAM). Overall, rising CO2 should reduce
stomatal aperture and transpiration water loss with a
subsequent increase in leaf water-use-eciency (WUE)
usually dened as the ratio of leaf carbon uptake to
water loss. Allen et al. (2011) inter alia have reported that
elevated CO2 can improve leaf WUE by maintaining
photosynthesis in water-stressed maize and sorghum (i.e.
C4 species).

Effects of Elevated CO2 at the Whole

Plant Level
In conjunction with the response of leaf photosynthesis,
there are a number of well-documented increases of plant
growth in response to elevated CO2 (Kimball, 1993).
However, this observation may be indicative of a number
of complex biological changes at the whole plant in addition to photosynthetic stimulation at the leaf level.
For example, a number of studies for herbaceous plants
demonstrated that an approximate doubling of ambient
CO2 could enhance seed germination (Esashi et al., 1987),
as could CO2 concentrations above low Pleistocene levels
(i.e. 180, 270, 360 and 600 ppm CO2) (Mohan et al., 2004)
for some species such as red maple. Following germination
and emergence, elevated CO2 may also stimulate tiller
formation in C3 and C4 grasses (e.g. sorghum, Ottman
et al., 2001; wheat, Ziska et al., 2004) as well as a stimulation in leaf formation, growth and leaf size reported for
herbaceous and woody C3 species (Bazzaz, 1996) and some
C4 species (Seneweera et al., 2001). Root growth may also
be stimulated by increasing CO2, especially in early development with observed increases in length, diameter and
cortex (Rogers et al., 1992). Changes in root production, in
turn, may also be associated with increases in ne root
colonisation of arbuscular mycorrhizal fungi (Olesniewicz
and Thomas, 1999), and increased nodule formation in
leguminous plants such as soybean (Temperton et al., 2003;
Prevost et al., 2010). Sexual reproduction can also be
inuenced by elevated CO2 with observed increases in oral
number and pollen production (e.g. ragweed, Ziska et al.,
2003), as well as seed and fruit size (e.g. Bromus, Steinger
et al., 2000), and decreases in nutritional quality, particularly protein content in agronomic crops (Taub et al.,
2008). Changes in asexual reproduction, particularly
increases in root or rhizome development have also been
observed in weedy species in response to elevated CO2 (e.g.
Canada thistle, Ziska, 2003).
The range of whole plant responses to elevated CO2 may
reect carbon partitioning from carbon sources (e.g.
4

leaves) to carbon sinks (e.g. non-photosynthetic plant

organs) that could represent a limiting resource. For
example, if elevated CO2 stimulates leaf growth and
development with a subsequent need for nutrients, then
additional carbon could go to stimulate root growth
(Rogers et al., 1992). If additional carbon is lacking to
maximise reproduction, then oral number or branching
could be stimulated (Ward and Strain, 1999). Shifts in
carbon partitioning are also likely to alter temporal changes in plant development, or phenology. For example, in
common ragweed, time to reproduction was shortened at
elevated, relative to ambient CO2, in part by faster growth
rates (Ziska et al., 2003) whereas for other species, elevated
CO2 altered the size at which plants initiated reproduction
(e.g. Reekie and Bazzaz, 1991). Elevated CO2 may also
accelerate plant senescence (e.g. wheat, Zhu et al., 2009) or
delay it (Taylor et al., 2008).
The observations reported at the whole plant level suggest that the response to elevated CO2 is probably not a
function of leaf level processes (e.g. photosynthesis) per se.
Is there an underlying mechanism that determines carbon
allocation during plant development? It has been shown in
cotton that elevated CO2 can alter plant hormonal concentration (e.g. cytokinin, Yong et al., 2000); is there a
hormonal function that can control ecient use of additional carbon to increase fecundity? Unfortunately, with
few exceptions (e.g. Masle, 2000), little eort has gone into
providing a mechanistic basis for understanding how
plants scale-up or integrate the response to elevated CO2
from the cytological to single leaf, from single leaf to the
whole plant (see Figure 3).

Effects of Elevated CO2 at the Plant

Community and Ecosystem Level
As with any change in a resource, particularly a global one,
how dierent plant species respond to rising CO2 levels will
alter plant competition, biodiversity and ecosystem function. For simplicity, we can divide plant communities into
one of two subtypes, a managed community, such as an
agricultural eld or rangeland (sometimes referred to as an
agroecosystem); or a less managed system, such as a secondary forest. See also: Biocomplexity; Evolutionary
Responses to Climate Change
As a managed plant community, agriculture can be
viewed as consisting of a desired plant species (the crop)
and a set of undesired plant species (weeds). Unfortunately,
a number of studies indicate that among plant species in an
agricultural system, weeds, rather than crops, are likely to
show the strongest relative response to rising carbon dioxide (Ziska, 2003). That is, even though individual crop
plants can respond to carbon dioxide, the greater response
of weedy species to CO2 may result in increased competition and exacerbated losses in crop production at the
systems level. The basis for the greater response among
weedy species to elevated CO2 is not entirely clear. In some

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Plant Responses to Elevated CO2

CO2

CO2

CO2

CO2

CO2

CO2
Leaf
carbon
dynamics

Disparity in
germination
and leaf
emergence

Whole
plant
response

Spatial
and temporal
changes in
CO2 response

Differential
species
growth

Changes in
seed bank
demographics

Variation
in seed yield
Figure 3

Simplified construct of plant and plant community responses to elevated CO2.

instances, whether a crop or a weed is a C3 or C4 plant will

determine its relative response to carbon dioxide and its
competitive abilities (Ziska, 2010). However, many of the
worst weeds for a given crop are wild (uncultivated) plants
of the same genus or species (e.g. rice and wild rice, oat and
wild oat, sorghum and shattercane) and are likely to have
the same photosynthetic pathway. Alternatively, it has
been suggested (Treharne, 1989) that the greater range of
responses observed for weeds with increasing atmospheric
CO2 is related to their greater genetic diversity relative to
crops; in other words, the greater the gene pool, the more
likely it is for a species to respond to a resource addition.
See also: CropWeed Competition
Less has been reported regarding how elevated CO2
alters plant competition in unmanaged systems. This is due,
in part, to the larger array of plant species present in such
systems (e.g. forests, wetlands, prairie, desert, etc.).
Nevertheless, we can begin to assess the role of elevated
CO2 in altering competition and ecosystem function by

providing a simple example: elevated CO2 and invasive

plant species.
Invasive plants (i.e. exotic or alien species) are species,
nonnative to a given region, whose geographic introduction can result in environmental damage and biodiversity loss. One example of environmental damage
related to invasive plants is associated with re ecology.
For the Western United States, cheatgrass (Bromus
tectorum), an invasive grass species from central Asia,
grows quickly in dry environments, colonising open spaces
between perennial, native shrubs with a ne ammable
material that increases the re frequency. As the number of
res increases, native species decline; conversely cheatgrass, a re adapted species, becomes dominant within the
community. The end result is an overall loss of biodiversity
and ecosystem function. A study of three cheatgrass
populations collected from dierent elevations within the
Sierra Nevada range revealed that even small increases in
atmospheric carbon dioxide (ca 50 ppm) could increase

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Plant Responses to Elevated CO2

Table 1 A review of plant community studies that examined whether elevated CO2 preferentially increased the growth or
fecundity of invasive plant species within the community
Species

Community

Favoured?

Reference

Yellow star thistle

Honey mesquite
Japanese Honeysuckle
Cherry Laurel
Red Brome

California grassland
Texas prairie
Forest understory
Forest understory
Desert

Yes
Yes
Yes
Yes
Yes

Dukes et al. (2011)

Polley et al. (1994)
Belote et al. (2004)
Hatenschwiler and Korner (2003)
Smith et al. (2000)

With permission from US Government.

growth rate and combustibility of cheatgrass, while reducing digestibility (Ziska et al., 2005), all factors linked to
enhanced ammability and increased re occurrence.
Although these data were laboratory based, there have
been a handful of in situ studies demonstrating that elevated CO2 could potentially enhance the growth of invasive
species within plant communities (Table 1). Overall, of the
ve seminal studies conducted to date, all show preferential
selection for the invasive species (Table 1). While additional
studies are obviously desired, these data suggest that elevated CO2 per se, could reduce biodiversity and ecological
function in unmanaged plant systems.

Effects of Elevated CO2 at

Evolutionary Levels
It seems likely, given the rapid increase in global atmospheric CO2 concentration (i.e. approximately 25% since
1960), that few plant species have evolutionary adapted to
this change (e.g. Bunce, 2001). From the previous section,
we have illustrated that elevated CO2 can act as a selective
agent on both managed and less managed plant populations. However, some evolutionary responses have been
observed experimentally in response to elevated CO2 (e.g.
Arabidopsis, Ward and Kelly, 2004) or climate (e.g. drought
in wild mustard (Franks et al., 2007)) in only a few generations. However, we recognise that evolutionary changes in
plant communities in response to elevated CO2 will be difcult to elucidate because of the temporal discrepancies
between experimental and evolutionary time scales.
Nevertheless there have been a handful of studies that
could provide some additional insight into ecosystem and
evolutionary changes that could occur with continued
exposure to elevated CO2. For example, plants originating
near natural CO2 vents show long-term evolutionary
responses related to stomatal conductance and reduced
starch accumulation (i.e. reduced incidence of photosynthetic acclimation) (Onoda et al., 2009). Another study
demonstrated that the rate of secondary succession (an
important function of ecosystem regeneration) could be
shortened with elevated CO2 and increased temperature
associated with an urban versus rural environment (George
et al., 2009). Recent research suggests that new ragweed
genotypes could emerge in response to elevated CO2, with
associated ecological and evolutionary changes for this
6

plant species (Stinson et al., 2011). In general, however,

changes in biodiversity and demographics, long-term
evaluations of species evolution and dierentiation of
evolution versus plasticity within ecosystems at spatial
scales larger than the plant population level are lacking.

Elevated CO2 and other Tropic Levels

We recognise empirically that dierential plant responses
to rising CO2 levels will alter plant competition and species
abundance, with likely consequences with respect to evolutionary processes; yet we lack sucient information,
particularly in regard to elevated CO2 and other tropic
interactions, to describe future ecosystem distribution and
function at a global scale.
For example, it is probable that insect biology will be
impacted by the physiological eects of elevated CO2 on
host plant metabolism, particularly with respect to the
concentration of defensive compounds (Lincoln and
Couvet, 1989). Recent work with Ascelpia syriaca indicated
dierential responses among genotypes with respect to
production of chemical defenses, with potential consequences for relative tness and selection of this plant
species (Vannette and Hunter, 2011). Similarly, indirect
eects of the host plant in responding to rising CO2 could
aect the biology of plant pathogens. For example, isolates
of Colletotriehum gloeosporioides showed increased
fecundity with elevated CO2; and the increased population
size, in addition to any stimulation in plant canopy
with elevated CO2, could accelerate pathogen evolution
(Chakraborty and Datta, 2003). By altering the root biology of host plants, elevated CO2 may change the species
composition of soil microbial communities (Janus et al.,
2005), mycorrhizal fungi (Antoninka et al., 2011) as well as
nematode biology (Neher et al., 2004) with subsequent
associated eects on soil properties, from carbon cycling
to nutrient availability. See also: Biological Impacts of
Climate Change

Elevated CO2 and Plant Responses:

Challenges
From an experimental point of view, it may be straightforward to conduct a test to quantify the response of

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Plant Responses to Elevated CO2

elevated CO2 for a given level of biological organisation

(e.g. single leaf) (Figure 3). Complexity arises however,
because: (a) the amount of atmospheric CO2 is rising
quickly for all biogeographical regions and plant communities; (b) CO2 is the principal source of carbon for
plants, and is limiting in at least 90% of all plant species;
and (c) carbon dioxide is likely to impact all spatial and
temporal aspects of plant (and hence, global) biology.
Ideally, all studies from micro- to macro-scales (Figure 1)
could be combined to obtain an estimate of the spatial and
temporal aspects of species responses to elevated CO2
within an ecosystem. Integration of plant species
responses, in turn, could potentially be used to derive
forecasts for ecosystem responses and function in toto.
However, researchers and scientists who wish to consider plant responses to rising CO2 at these levels are faced
with two primary challenges. These challenges can be
expressed as either scaling, that is, taking a result obtained
for an elevated CO2 response at a given level of organisation (e.g. leaf photosynthesis) and trying to understand
how that response might aect up (e.g. whole plant carbon uptake) or down (e.g. photosynthetic biochemistry)
processes; or, integration, that is, understanding the
implications of a given response to elevated CO2 at dierent spatial and temporal scales (e.g. if CO2 stimulates leaf
photosynthesis at the whole plant level, will the same
degree of photosynthetic stimulation occur for that species
in a plant community?). Because of these dual challenges,
caution should be exercised for publications that claim to
provide a comprehensive, integrative review of plant biological responses to elevated CO2 based on experiments
that report the response of a few plant species to one or two
organisational levels (e.g. leaf, cell).
(There is, of course, a third challenge. While the global
increase in atmospheric CO2 remains one of the most predictable anthropogenic changes, CO2 is also a recognised
greenhouse or infra-red absorbing gas. As such, CO2 is
also likely to alter a number of other abiotic parameters,
particularly surface temperatures. Consequently, while
understanding how elevated CO2 will aect plant biology is
of obvious importance, quantifying the extent of these
eects, particularly in regard to other abiotic variables such
as temperature and water availability, is also essential, if
beyond the scope of the current review.)

Elevated CO2 and Plant Responses:

Addressing the Challenges
There is a critical need to understand how a rapid increase
in atmospheric CO2 is likely to impact ecosystem functions
of signicance to human society, from agriculture to forestry. It is also clear that such an understanding will be
dicult to obtain based on short-term experimental
approaches which typically examine one or two plant
variables in a controlled setting.

Unfortunately, much of what is known regarding the

impact of elevated CO2 on plant function remains
descriptive and nonmechanistic; focused at the level of
single plants, nonintegrative and dicult to scale (Ziska
and Bunce, 2007). Although progress is being made in the
use of mutant lines to determine the mechanistic response
of CO2 at the cellular level (e.g. stomatal formation), we
still know relatively little about CO2 induced changes at the
molecular level, or how those changes could be integrated
in an evolutionary sense to determine species demography;
similarly, we know relatively little about how elevated CO2
will impact the distribution and function of both managed
(e.g. agriculture) and unmanaged (e.g. forests) ecosystems
in the long-term (decades).
Which organisational levels should be the focus of additional experimental inquiry? First, we would suggest that
ecosystems are integrators of genetic, structural, competitive, trophic level interactions that incorporate abiotic
selection over time and space. Assessments of elevated CO2
responses, from an economic or environmental viewpoint,
are most likely evidenced in the response of either managed
or unmanaged ecosystems. Such evidence can be manifested with respect to biodiversity and invasive species
success in unmanaged systems with elevated CO2; conversely, dierential responses between weeds and crops to
elevated CO2 will have implications for food security in
managed systems.
We recognise that there are engineering and methodological challenges associated with studying ecosystems (e.g.
abiotic vicissitude, and year to year variation in biomass
productivity, herbivory, soil dynamics, etc.), in part
because their spatial and temporal dimensions do not lend
themselves to a quintessential short-term reductionist
approach. However, we would argue that it is exactly for
these reasons that experimental approaches that consider
multi-factor parameters at the ecosystem level over multiyear periods are necessary if we are to understand organismal responses to elevated CO2 between dierent levels
of scale (e.g. leaf versus whole plant versus community).
We also recognise that the ecosystem complexity is such
that reductionist approaches may not be fully capable of
integrating across dierent organismal levels.
To meet this challenge we would suggest that modelling
be utilised in combination with experimental data
obtained at the system level. Simulation modelling can be
used to increase understanding between organismal scales,
or between species, or for biomes that are experiencing
changing environmental conditions; such models may
focus on climatevegetation interactions, or climate
driven snapshots of ecosystem dynamics, as well as estimating ows of carbon, nutrients and water through
ecosystems. There are a number of vegetation-based
models, including statistical, bioclimatic, habitat or nichebased assessments that allow a stochastic explanation of
climate variables (Heikkinen et al., 2006). However,
all models do have a range of physiological and physical
assumptions that must be considered prior to
interpretation.

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Plant Responses to Elevated CO2

To that end, we would suggest that, whenever possible,

experimental data obtained at the system level be used to
verify the models, to point out additional areas of inquiry
and to substantiate spatial and temporal dimensions of key
outcomes, from carbon and nitrogen cycling to changes in
the biological success of invasive species. It is especially
important in this context to make certain that ecosystem
processes among dierent organisational levels be fairly
represented with respect to model outcomes (Ollinger et al.,
2008). This will be necessary if we are to have condence in
any model-generated predictions with respect to impact on
human systems.
Another focus of additional experimental inquiry would
be at the molecular, genetic levels of study. Researchers
have found that plants can become accustomed to new
environments (e.g. sub- or elevated CO2 conditions) by
regulating several major genes in CO2 signalling (e.g. CO2
insensitive and/or CO2 hypersensitive mutants) in conjunction with stomatal development pathways (i.e. opening
or closing of stomata or changing stomatal number). We
can use the mutants of those major genes as a genetic tool to
understand how plants respond to elevated CO2 when
those main regulators are perturbed. Using this approach
we could potentially predict the direction in which plants
have evolved to new environments (e.g. elevated CO2
condition).

Plant Responses to Elevated CO2:

Conclusions
The physical characteristics of carbon dioxide in its role as
a greenhouse gas and the resulting consequences in
increasing surface temperatures have been well established.
Less recognised however, is the role of CO2 as the primary
source of carbon for plant biology, and hence, for all living
systems. It is very likely, given the recognised biological
function of CO2 in the various organisational levels of plant
biology, that the anthropogenic increase in atmospheric
CO2, of and by itself, will signicantly alter biology at a
global scale. It is hoped therefore, that the current review,
while incomplete, can provide a timely synthesis of what is
known, and serve as a tentative guide for additional inquiry
regarding plant biology and elevated CO2 by interested
readers.

References
Ainsworth EA, Rogers A, Vokin LO, Walter A and Schurr U
(2006) The eects of elevated CO2 concentration on soybean
gene expression. An analysis of growing and mature leaves.
Plant Physiology 142: 135147.
Allen LH, Kakanib VG, Vu JCV and Boote KJ (2011) Elevated
CO2 increases water use eciency by sustaining photosynthesis
of water-limited maize and sorghum. Journal of Plant Physiology 168: 19091918.

Antoninka A, Reich PB and Johnson NC (2011) Seven years of

carbon dioxide enrichment, nitrogen fertilization and plant
diversity inuence arbuscular mycorrhizal fungi in a grassland
ecosystem. New Phytologist 192: 200214.
Bae H and Sicher R (2004) Changes of soluble protein expression
and leaf metabolite levels in Arabidopsis thaliana grown in
elevated atmospheric carbon dioxide. Field Crops Research 90:
6173.
Bazzaz FA (1996) Plants in Changing Environments: Linking
Physiological, Population and Community Ecology. Cambridge,
UK: Cambridge University Press, 320 pages.
Belote RT, Weltzin JF and Norby RJ (2004) Response of an
understory plant community to elevated CO2 depends on differential responses of dominant invasive species and is mediated
by soil water availability. New Phytologist 161: 827835.
Berger D and Altmann T (2000) A subtilisin-like serine protease
involved in the regulation of stomatal density and distribution of
Arabidopsis thaliana. Genes and Development 14: 11191131.
Bergmann DC, Lukowitz W and Somerville CR (2004) Stomatal
development and pattern controlled by a MAPKK kinase.
Science 304: 14941497.
Bunce JA (2001) Are annual plants adapted to the current
atmospheric concentration of carbon dioxide? International
Journal of Plant Science 162: 12611266.
Ceusters J and Borland AM (2010) Impacts of elevated CO2 on the
growth and physiology of plants with Crassulacean Acid
Metabolism. In: Luttge U, Beyschlag W, Budel B and Francis D
(eds) Progress in Botany, vol. 72 pp. 163182. Berlin: Springer.
Chakraborty S and Datta S (2003) How will plant pathogens
adapt to host plant resistance at elevated CO2 under a changing
climate? New Phytologist 159: 733742.
De Souza AP, Gaspar M, Da Silva EA et al. (2008) Elevated CO2
increases photosynthesis, biomass and productivity, and
modies gene expression in sugarcane. Plant Cell and Environment 31: 11161127.
Dukes JS, Chiariello NR, Loarie SR and Field CB (2011) Strong
response of an invasive plant species (Centaurea solstitialis L.)
to global environmental changes. Ecological Applications 21:
18871894.
Esashi Y, Hase S and Kojima K (1987) Light actions in the germination of cocklebur seeds: V. Eects of ethylene, carbon dioxide, oxygen on germination in relation to light. Journal of
Experimental Botany 38: 702710.
Franks PJ and Beerling DJ (2009) Maximum leaf conductance
driven by CO2 eects on stomatal size and density over geologic
time. Proceedings of the National Acadamy of Sciences of the
USA 106: 1034310347.
Franks SJ, Sim S and Weis AE (2007) Rapid evolution of
owering time by an annual plant in response to a climate
uctuation. Proceedings National Academy of Sciences 104:
12781282.
George K, Ziska LH, Bunce JA et al. (2009) Macroclimate associated with urbanization increases the rate of secondary succession from fallow soil. Oecologia 159: 637647.
Gray JE, Holroyd GH, van der Lee FM et al. (2000) The HIC
signalling pathway links CO2 perception to stomatal development. Nature 408: 713716.
Hashimoto M, Negi J, Young J et al. (2006) Arabidopsis HT1
kinase controls stomatal movements in response to CO2. Nature
Cell Biology 8: 391397.

This is a US Government work and is in the public domain in the United States of America.
eLS. www.els.net. John Wiley & Sons, Ltd

Plant Responses to Elevated CO2

Hattenschwiler S and Korner C (2003) Does elevated CO2 facilitate naturalization of the non-indigenous Prunus laurocerasus
in Swiss temperate forests? Functional Ecology 17: 778785.
Heikkinen RK, Luoto M, Araujo MB et al. (2006) Methods and
uncertainties in bioclimatic envelope modeling under climate
change. Progress in Physical Geography 30: 751777.
Hu H, Boisson A, Israelsson M et al. (2010) Carbonic anhydrases
are upstream regulators of CO2-controlled stomatal movements in guard cells. Nature Cell Biology 12: 8793.
Janus LR, Angeloni NL, McCormack J et al. (2005) Elevated
atmospheric CO2 alters soil microbial communities associated
with trembling aspen (Populus tremuloides) roots. Microbial
Ecology 50: 102109.
Kim S-H, Sicher RC, Bae H et al. (2006) Canopy photosynthesis,
evapotranspiration, leaf nitrogen, and transcription proles of
maize in response to CO2 enrichment. Global Change Biology
12: 588600.
Kim TH, Bohmer M, Hu H, Nishimura N and Schroeder JI (2010)
Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annual Review
of Plant Biology 61: 561591.
Kimball BA (1993) Eects of increasing atmospheric CO2 on
vegetation. Vegetatio 104/105: 6583.
Lee M, Choi Y, Kim B et al. (2008) The ABC transporter
AtABCB14 is a malate importer and modulates stomatal
response to CO2. Nature Cell Biology 10: 12171223.
Lewis JD, Wang XZ, Grin KL and Tissue DT (2002) Eects of
age and ontogeny on photosynthetic responses of a determinate
annual plant to elevated CO2 concentrations. Plant, Cell and
Environment 25: 359368.
Lincoln DE and Couvet D (1989) The eect of carbon supply on
allocation to allelochemicals and caterpillar consumption of
peppermint. Oecologia 78: 112120.
Makino A, Nakano H, Mae T, Shimada T and Yamamoto N
(2000) Photosynthesis, plant growth and N allocation in
transgenic rice plants with decreased Rubisco under CO2
enrichment. Journal of Experimental Botany 50: 383389.
Masle J (2000) The eects of elevated CO2 concentrations on
cell division rates, growth patterns, and blade anatomy in
young wheat plants are modulated by factors related to leaf
position, vernalization and genotype. Plant Physiology 122:
13991416.
Mohan JE, Clark JS and Schlesinger WH (2004) Genetic variation
in germination, growth and survivorship of red maple in
response to subambient through elevated atmospheric CO2.
Global Change Biology 10: 233247.
Morrison JIL (1987) Intercellular CO2 concentration and stomatal response to CO2. In: Zeiger E, Cowan IR and Farquhar
GD (eds) Stomatal Function, pp. 229251. Stanford, CA:
Stanford University Press.
Nadeau JA and Sack JD (2002) Control of stomatal distribution
on the Arabidopsis leaf surface. Science 296: 16971700.
Neher DA, Weicht TR, Moorhead DL and Sinsabaugh R (2004)
Elevated CO2 alters functional attributes of nematode communities in forest soils. Functional Ecology 18: 584591.
Olesniewicz KS and Thomas RB (1999) Eects of mycorrhizal
colonization on biomass production and nitrogen xation of
black locust (Robinia pseudoacacia) seedlings grown under
elevated atmospheric carbon dioxide. New Phytologist 142:
133140.

Ollinger SV, Goodale CL, Hayhoe K and Jenkins JP (2008)

Potential eects of climate change and rising CO2 on ecosystem
processes in northeastern U.S. forests. Mitigation and Adaptation Strategies for Global Change 13: 467485.
Onoda Y, Hirose T and Hikosaka K (2009) Does leaf photosynthesis adapt to CO2 enriched environments? An experiment
on plants originating from three natural CO2 springs. New
Phytologist 182: 698709.
Ottman MJ, Kimball BA, Pinter PJ et al. (2001) Elevated CO2
increases sorghum biomass under drought conditions. New
Phytologist 150: 261273.
Polley HW, Johnson HB and Mayeux HS (1994) Increasing CO2:
comparative responses of the C4 grass Schizachyrium and
grassland invader Prosopis. Ecology 75: 976988.
Prevost D, Bertrand A, Juge C and Chalifour F-P (2010) Elevated
CO2 induces dierences in nodulation of soybean depending on
bradyshizobial strain and method of inoculation. Plant Soil
331: 115127.
Rasse DP, Peresta G and Drake BG (2005) Seventeen years of
elevated CO2 exposure in a Chesapeake bay wetland: sustained
but contrasting responses of plant growth and CO2 uptake.
Global Change Biology 11: 369377.
Reekie EG and Bazzaz FA (1991) Phenology and growth in four
annual species grown in ambient and elevated CO2. Canadian
Journal of Botany 69: 24752481.
Rogers HH, Peterson CM, McCrimmon JN and Cure JD (1992)
Response of plant roots to elevated atmospheric carbon dioxide. Plant, Cell and Environment 15: 749752.
Royer DL (2001) Stomatal density and stomatal index as indicators of paleoatmospheric CO2 concentration. Review of
Palaeobotany and Palynology 114: 128.
Sage RF and Coleman JR (2001) Eects of low atmospheric CO2
on plants: more than a thing of the past. Trends in Plant Science
6: 1824.
Seneweera S, Ghannoum O and Conroy JP (2001) Root and shoot
factors contribute to the eect of drought on photosynthesis
and growth of the C4 grass Panicum coloratum at elevated CO2
partial pressures. Australian Journal of Plant Physiology 28:
451460.
Sharkey TD (1985) O2-insensitive photosynthesis in C3 plants.
Its occurrence and a possible explanation. Plant Physiology 78:
7175.
Sheen J (1994) Feedback control of gene expression. Photosynthesis Research 39: 427438.
Smith SD, Huxman TE, Zitzer SF et al. (2000) Elevated CO2
increases productivity and invasive species success in an arid
ecosystem. Nature 408: 7982.
Springer CJ, Orozco RA, Kelly JK and Ward JK (2008) Elevated
CO2 inuences the expression of oral-initiation genes in Arabidopsis thaliana. New Phytologist 178: 6367.
Steinger T, Gall R and Schmid B (2000) Maternal and direct
eects of elevated CO2 on seed provisioning, germination and
seedling growth in Bromus erectus. Oecologia 123: 475480.
Stinson KA, Brophy C and Connolly J (2011) Catching up on
global change: new ragweed genotypes emerge in elevated CO2
conditions. Ecosphere 2: 111.
Stitt M and Krapp A (1999) The interaction between elevated
carbon dioxide and nitrogen nutrition the physiological
and molecular background. Plant, Cell and Environment 22:
583621.

This is a US Government work and is in the public domain in the United States of America.
eLS. www.els.net. John Wiley & Sons, Ltd

Plant Responses to Elevated CO2

Sun Y, Yin J, Cao H et al. (2011) Elevated CO2 inuences

nematode-induced defense responses of tomato genotypes differing in the JA pathway. PLoS One 6: e19751.
Taub DR, Miller B and Allen H (2008) Eects of elevated CO2 on
the protein concentration of food crops: A meta-analysis. Global Change Biology 14: 565575.
Taylor G, Tallis MJ and Giardina CP (2008) Future atmospheric
CO2 leads to delayed autumnal senescence. Global Change
Biology 14: 264275.
Temperton VM, Grayston SJ, Jackson G et al. (2003) Eects of
elevated carbon dioxide concentration on growth and nitrogen
xation in Alnus glutinosa in a long-term eld experiment. Tree
Physiology 23: 10511059.
Treharne K (1989) The implications of the greenhouse eect for
fertilizers and agrochemicals. In: Bennet RC (ed.) The Greenhouse Eect and UK Agriculture, pp. 6778. UK: Ministry of
Agriculture, Fisheries and Food.
Tubiello FN, Amthor JS, Boote KJ et al. (2007) Crop response to
elevated CO2 and world food supply: A comment on Food for
Thought_ by Long et al., Science 312: 19181921, 2006.
European Journal of Agronomy 26: 215223.
Vannette RL and Hunter MD (2011) Genetic variation in
expression of defense phenotype may mediate evolutionary
adaptation of Asclepias syriaca to elevated CO2. Global Change
Biology 17: 12771288.
Ward JK and Kelly JK (2004) Scaling up evolutionary responses
to elevated CO2: lessons from Arabidopsis. Ecology Letters 7:
427440.
Ward JK and Strain BR (1999) Elevated CO2 studies: past, present and future. Tree Physiology 19: 211220.
Woodward FI and Kelly JK (1995) The inuence of CO2 concentration on stomatal density. New Phytologist 131: 311327.
Yong JWH, Wong SC, Letham DS, Hocart CH and Farquhar
GD (2000) Eects of elevated [CO2] and nitrogen nutrition on
cytokinins in the xylem sap and leaves of cotton. Plant Physiology 124: 767779.
Young JJ, Mehta S, Israelsson M et al. (2006) CO2 signalling in
guard cells calcium sensitivity response modulation a Ca2+independent phase, and CO2 insensitivity of the aca2 mutant.
Proceedings of the National Academy of Sciences of the USA
103: 75067511.
Zhu C, Zhu J, Zeng Q et al. (2009) Elevated CO2 accelerates ag
leaf senescence in wheat due to ear photosynthesis which causes
greater ear nitrogen sink capacity and ear carbon sink limitation. Functional Plant Biology 36: 291299.
Ziska LH (2003) Evaluation of the growth response of six invasive
species to past, present and future carbon dioxide concentrations. Journal of Experimental Botany 54: 395404.

10

Ziska LH (2010) Global climate change and carbon dioxide:

assessing weed biology and management. In: Rosenzweig C and
Hillel D (eds) Handbook of Climate Change and Agro-Ecosystems: Impacts, adaptation and mitigation, pp. 191208.
Hackensack, NJ: World Scientic Publishing.
Ziska LH and Bunce JA (2007) Predicting the impact of changing
CO2 on crop yields: some thoughts on food. New Phytologist
175: 607618.
Ziska LH, Gebhard DE, Frenz DA, Faulkner S and Singer BD
(2003) Cities as harbingers of climate change: common ragweed, urbanization, and public health. Journal of Allergy and
Clinical Immunology 111: 290295.
Ziska LH, Morris CF and Goins EW (2004) Quantitative and
qualitative evaluation of selected wheat varieties released since
1903 to increasing atmospheric carbon dioxide: can yield sensitivity to carbon dioxide be a factor in wheat performance?
Global Change Biology 10: 18101819.
Ziska LH, Reeves JB III and Blank R (2005) The impact of recent
increases in atmospheric CO2 on biomass production
and vegetative retention of Cheatgrass (Bromus tectorum):
implications for re disturbance. Global Change Biology 11:
13251332.
Ziska LH, Sicher RC and Kremer DF (1995) Reversibility of
photosynthetic acclimation of swiss chard and sugarbeet grown
at elevated concentrations of carbon dioxide. Physiologia
Plantarum 95: 355364.

Further Reading
Ehleringer JR, Cerling TE and Dearing MD (eds) (2005) A History of Atmospheric CO2 and its Eects on Plant, Animals and
Ecosystems. New York, NY: Springer, 530 pages.
Karnosky DF, Ceulemans R, Scarascia-Mugnozza GE and Innes
JL (eds) (2001) The Impact of Carbon Dioxide and Other
Greenhouse Gases on Forest Ecosystems. Wallingford, UK:
CABI Publishing, 361 pages.
Koch GW and Mooney HA (eds) (1996) Carbon Dioxide and
Terrestrial Ecosystems. San Diego, CA: Academic Press, 357
pages.
Luo Y and Mooney HA (eds) (1999) Carbon Dioxide and
Enviornmental Stress. Sand Diego, CA: Academic Press, 418
pages.
Taub D (2010) Eects of rising atmospheric concentrations of
carbon dioxide on plants. Nature Education Knowledge 1(8): 21.
Ziska LH and Dukes JS (2010) Weed Biology and Climate Change.
Ames, Iowa: Wiley-Blackwell, 248 pages.

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