-
on June 3, 2018http://rstb.royalsocietypublishing.org/Downloaded
from
Phil. Trans. R. Soc. B (2012) 367, 613629
doi:10.1098/rstb.2011.0248
Review
* Autho
One conevolution
Evolutionary context for understandingand manipulating plant
responses to past,
present and future atmospheric [CO2]Andrew D. B. Leakey1,* and
Jennifer A. Lau2
1Department of Plant Biology and Institute for Genomic Biology,
University of Illinois,Urbana-Champaign, 1201 W. Gregory Drive,
Urbana, IL 61801, USA
2W. K. Kellogg Biological Station and Department of Plant
Biology, Michigan State University,3700 E Gull Lake Drive, Hickory
Corners, MI 49060, USA
Variation in atmospheric [CO2] is a prominent feature of the
environmental history over which vas-cular plants have evolved.
Periods of falling and low [CO2] in the palaeo-record appear to
havecreated selective pressure for important adaptations in modern
plants. Today, rising [CO2] is akey component of anthropogenic
global environmental change that will impact plants and the
eco-system goods and services they deliver. Currently, there is
limited evidence that natural plantpopulations have evolved in
response to contemporary increases in [CO2] in ways that
increaseplant productivity or fitness, and no evidence for
incidental breeding of crop varieties to achievegreater yield
enhancement from rising [CO2]. Evolutionary responses to elevated
[CO2] havebeen studied by applying selection in controlled
environments, quantitative genetics and trait-based approaches.
Findings to date suggest that adaptive changes in plant traits in
response tofuture [CO2] will not be consistently observed across
species or environments and will not belarge in magnitude compared
with physiological and ecological responses to future [CO2].
Thislack of evidence for strong evolutionary effects of elevated
[CO2] is surprising, given the large effectsof elevated [CO2] on
plant phenotypes. New studies under more stressful, complex
environmentalconditions associated with climate change may revise
this view. Efforts are underway to engineerplants to: (i) overcome
the limitations to photosynthesis from todays [CO2] and (ii)
benefit maxi-mally from future, greater [CO2]. Targets range in
scale from manipulating the function of a singleenzyme (e.g.
Rubisco) to adding metabolic pathways from bacteria as well as
engineering the struc-tural and functional components necessary for
C4 photosynthesis into C3 leaves. Successfullyimproving plant
performance will depend on combining the knowledge of the
evolutionary context,cellular basis and physiological integration
of plant responses to varying [CO2].
Keywords: adaptation; climate change; evolution; yield;
fitness
1. INTRODUCTION: WHY TAKE ANEVOLUTIONARY
PERSPECTIVE?Assimilation of CO2 from the atmosphere into biomassby
higher plants is fundamental to: (i) providing food,fuel and fibre
for human consumption; (ii) supplyingenergy to terrestrial
ecosystems; and (iii) regulatingthe concentration of atmospheric
CO2 ([CO2]) andclimate. In almost all higher plants,
photosyntheticCO2 fixation (A) and stomatal conductance (gs)
areinstantaneously sensitive to variation in [CO2] overthe range of
past to present and/or predicted future[CO2]. The rise in [CO2]
starting during the IndustrialRevolution and continuing today is
notable for howquickly it is altering plant function. Changes in A
andgs caused by increasing [CO2] initiate a set of cellularand
physiological responses, which typically increase
r for correspondence ([email protected]).
tribution of 12 to a Theme Issue Atmospheric CO2 and theof
photosynthetic eukaryotes: from enzymes to ecosystems.
613
growth and can increase reproductive output. Genoty-pic
variation in almost all elements of these responsescreates the
potential for ecological and evolutionaryconsequences over a wide
range of timescales.
Plant and ecosystem responses to varying [CO2] arecurrently best
understood at the physiological andecological levels and on
timescales of one generationor less. Investigating plant responses
to varying atmos-pheric [CO2] in an evolutionary context is
importantbecause variations in [CO2] over geological timescalesare
believed to have played important roles in the evol-ution of
ecologically and economically important traitsin extant species. In
addition, if plants evolve in responseto twenty-first century
[CO2], changes in future ecosys-tem structure, function and
services will extend beyondwhat can be predicted from knowledge of
physiologicaland ecological responses to elevated [CO2]. From
apractical perspective, there is the possibility that despitemajor
breeding successes, present elite crop varietiesmay not be adapted
for optimal performance under pre-sent and future [CO2].
Accordingly, improving plant
This journal is q 2012 The Royal Society
mailto:[email protected]://rstb.royalsocietypublishing.org/
-
614 A. D. B. Leakey & J. A. Lau Review. Plant adaptation to
atmospheric [CO2]
on June 3, 2018http://rstb.royalsocietypublishing.org/Downloaded
from
productivity in high [CO2] environments may be anopen
opportunity for biotechnology or breeding toimprove crop
performance now and in the future. Thispaper builds on previous
reviews [14] to synthesizethe present knowledge on each of these
topics. It dis-cusses how an evolutionary perspective could
advanceefforts to understand and manage plant and
ecosystemresponses to rising [CO2] by addressing the followingfive
questions:
(1) Have plants evolved in response to varying [CO2]on a
geological timescale?
(2) Have plants evolved by natural or artificial selec-tion in
response to contemporary increases in[CO2]?
(3) Will rising [CO2] drive natural selection in thefuture, and
if so how?
(4) What traits are favoured under high [CO2]?(5) How does
evolutionary history impact and
inform efforts to engineer crops for improvedperformance in
present and future [CO2]?
Detailed evaluation of the approaches available forintegrating
evolutionary biology with physiology andecology are reviewed
authoritatively elsewhere [57].
2. QUESTION 1: HAVE PLANTS EVOLVEDIN RESPONSE TO VARYING [CO2]
ON AGEOLOGICAL TIMESCALE?Variation in [CO2] is proposed to have
played a key rolein driving the evolution of plants since they
colonizedthe land 400 Ma [812]. Estimates of the palaeo-[CO2]
record have been generated by modelling theweathering and burial of
CaMg silicates and organiccarbon [13], as well as a range of
proxies includingstomatal characteristics of fossil leaves [14] and
thestable isotope composition of pedogenic carbonates,marine
organic matter and fossil bryophytes [1518].There is significant
uncertainty associated with eachindividual methodology and
variation across methods[13,16, 19,20]. Nevertheless, the following
generaltrend emerges. The earliest land plants became estab-lished
at high [CO2] (15003000 ppm) before aperiod of low [CO2] (less than
or equal to 1000 ppm),which started 350 Ma and lasted 50100
Myr(figure 1a). Between 250100 Ma [CO2] appears tohave been
maintained at approximately 1000 ppm.With the exception of a period
in the Eocene 4050 Ma, all proxies and models indicate [CO2] of
lessthan 1000 ppm for the last 100 Myr (figure 1a).
Periods of falling or low [CO2] have been linked tothe evolution
of a number of important plant traits aswell as diversification of
the vascular flora (figure 1b)[8,27]. The development of megaphyll
leaves in mul-tiple independent lineages was coincident with
thetransition from high to low [CO2] during the Devo-nian and
Carboniferous 400350 Ma [25,28]. As[CO2] dropped, rates of A would
have becomeincreasingly limited by the resistance to diffusion
ofCO2 from the atmosphere to the site of fixation byRubisco.
Changes in stomatal density and stomatalsize (a combination of pore
depth and pore cross-sectional area determined from measurements of
theentire guard cell complex, which better predicts gs
Phil. Trans. R. Soc. B (2012)
than pore cross-sectional area alone) observed infossil leaves
have been used to drive modelspredicting increases in maximum gs at
this time[14,23,29], which would have relieved resistance toCO2
diffusion through the epidermis and maintainedrates of A [30]. The
rise in gs is proposed to haveincreased the capacity for
evaporative cooling ofleaves, allowing greater leaf areas to
develop forintercepting radiation without causing
overheating[25,28]. These changes in the structure and functionof
leaves coincided with the first major increase in thenumber of
vascular plant species [24]. Although mostdata indicate that
periods of low [CO2] are associatedwith novel adaptations and
diversification, Willis &McElwain [12] found that over
geological timescales,periods of high [CO2] corresponded with
greater orig-ination rates of fossil species. These two
observationsappear contradictory on first examination.
However,origination rates are defined as the rate at which
newspecies appear in the fossil record, and this coulddiffer from
the rate of change of overall species richness.If this is the case,
a combination of decreasing rates ofspecies gain in low [CO2] with
even greater decreasesin the rate of species loss could be the
basis of theobserved patterns.
The second major period of falling and low [CO2](from 100 Ma
until the present day) also overlappedwith increases in stomatal
density and decreases in indi-vidual stomatal size that suggest
plants were developinggreater maximum gs to counteract the
CO2-limitationof photosynthesis (figure 1b) [14,23,29]. This
waspreceded by a rapid and significant increase of vein den-sity in
angiosperm leaves that started 150 Ma [26].Greater leaf hydraulic
conductance resulting fromgreater vein density would have allowed
plants topotentially achieve greater A by delivering more waterto
the leaf in order to sustain greater stomatal con-ductance.
Therefore, increasing vein density has beenproposed to have been a
major fitness advantage forangiosperms and contributed to their
subsequent radi-ation (figure 1a,b) [26,3133]. The magnitude of
thebenefit to A from greater hydraulic conductance sup-porting
greater gs is negatively correlated with [CO2].Modelling these
relationships suggests that increases inhydraulic conductance on
the scale observed would sup-port several fold greater A at [CO2]
of 280 ppm, but beof more modest benefit (13%) at [CO2] of 1000
ppm[26]. The interdependence of the reported variations in[CO2],
vein density and stomatal characteristics is hardto determine. The
change in vein density appears tohave significantly predated the
decrease in [CO2]during the Cretaceous, as well as changes in
stomatalcharacteristics (figure 1a,b) [34]. Uncertainties in
thepalaeo-[CO2] record and dating of samples in fossilstudies could
contribute to this disparity. This leavesopen the possibility that
additional datawill demonstratethat the three events were
coordinated, as understandingof physiology in extant species would
lead us to expect.On the other hand, the majority of papers in this
fieldopenly acknowledge that other environmental factorsalso varied
during these key periods of plant evolutionand could have been the
selective agent for adaptivetraits. A further possibility related
to this scenario isthat greater hydraulic capacity was an
exaptation [35]
http://rstb.royalsocietypublishing.org/
-
PalaeozoicO5000(a)
(b)
4000
3000
2000
1000
[CO
2] (
ppm
)re
lativ
e tr
ait v
alue
, cla
denu
mbe
r or
spe
cies
num
ber
1.0
0.8
0.6
0.4
0.2
0450 400 350 300 250
time (Myr)
200 100
GEOCARBSULFliverwortspalaeosolsmarine boronphytoplanktonstomatal
indices
stomatal conductancevascular speciesstomatal densityleaf sizeC4
grass cladesvein density
B/Ca
150 50 0
0
S D C P Pa NTr J KMesozoic Cen.
Figure 1. Comparative time courses over most of the Phanerozoic
of: (a) estimated atmospheric [CO2] predicted from a geo-chemical
model of the carbon cycle (GEOCARBSULF, adapted from Berner [13])
and multiple proxies of [CO2] (stomatal
indices and isotope analysis of liverworts, palaeosols, marine
boron, phytoplankton and B/Ca, updated from the compilation ofRoyer
[21]), with a dashed line at 1000 ppm indicating the atmospheric
[CO2] above which photosynthesis is saturated in mostmodern plants
[22]; (b) estimated maximum stomatal conductance (adapted from
Franks & Beerling [23]), estimated vascularspecies richness
(adapted from Knoll & Niklas [24]), stomatal density (redrawn
from Royer et al. [20]), Devonian andCarboniferous leaf size
(adapted from Osborne et al. [25]), C4 grass clade richness
(adapted from Edwards et al. [9]) andangiosperm vein density
(adapted from Brodribb & Feild [26]), all of which are
expressed relative to the maximum value inthe individual records of
each parameter from the cited studies.
Review. Plant adaptation to atmospheric [CO2] A. D. B. Leakey
& J. A. Lau 615
on June 3, 2018http://rstb.royalsocietypublishing.org/Downloaded
from
that developed under some other selective forcebut then resulted
in further fitness gains when [CO2]subsequently decreased.
An important constraint on the role of varying [CO2]in driving
plant evolution that has been rarely discussed isthe nonlinearity
of [CO2] effects on plant performanceand the concentration at which
[CO2] is saturating.A survey of a wide variety of modern plant
species,including angiosperms and gymnosperms, woodyand herbaceous
species, indicates that A is almostuniversally saturated at
intercellular [CO2] of less than700 ppm, which corresponds to
atmospheric [CO2] of1000 ppm [22]. Changes in leaf water use and
energybalance associated with altered gs are also minimalabove 1000
ppm [36]. If this saturating [CO2] was main-tained across the
course of plant evolutionary history, itwould set a threshold above
which variations in [CO2]would have no consequence for plant
physiology or fit-ness (figure 1). For example, in this scenario,
the initialdecline in [CO2] during the Devonian from peakvalues of
15003000 ppm would have no direct effecton plants until dropping
below 1000 ppm 350 Ma(figure 1a). However, the saturating [CO2] for
earlyplants may have been much higher than for modern
Phil. Trans. R. Soc. B (2012)
species. This is partly because the resistance for CO2 topass
through the epidermis was much greater, owing totheir large
stomatal sizes and lower stomatal densities[23,29]. In addition, it
is possible that cell wall and chlor-oplast envelope structures of
ancient species reducedmesophyll conductance relative to modern
species [37].Both of these factors would increase the saturating
atmos-pheric [CO2] for photosynthesis [38,39] and, therefore,the
threshold for atmospheric [CO2] effects on plant fit-ness. This
alternative scenario is consistent with the factthat stomatal
conductance and leaf size both started toincrease 390 Ma, when
[CO2] estimates from a varietyof proxies ranged from 1500 to 3000
ppm. Establish-ing that the saturating [CO2] for early plants is
thathigh will require further experimental and modellinganalysis.
Further investigation of changes in mesophyllconductance and
saturating [CO2] in plants from thelate Mesozoic and Cenozoic might
also clarify the rolethat changes in [CO2] played in triggering the
evolu-tion of high water use and photosynthetic capacityin
angiosperms.
Plants with C4 photosynthesis appear to have emergedduring the
most recent period of low [CO2] (less than1000 ppm), before
becoming ecologically important in
http://rstb.royalsocietypublishing.org/
-
616 A. D. B. Leakey & J. A. Lau Review. Plant adaptation to
atmospheric [CO2]
on June 3, 2018http://rstb.royalsocietypublishing.org/Downloaded
from
many ecosystems 38 Ma [9]. Molecular clock datacalibrated using
fossils suggest that the origins of all theknown C4 grass clades
occurred between 3 and32 Ma, and it has been proposed that this was
driven bya mid-Oligocene drop in [CO2] that favoured C4 speciesover
C3 species because of their greater photosyntheticefficiency at low
[CO2], particularly when combinedwith high temperatures and drought
stress (figure 1a,b)[4042].Carbon isotope analysis of pollen grains
suggeststhat a significant fraction (more than 25%) of grass
specieswere C4 1533 Ma [43]. Isotopic evidence fromorganic matter
in abyssal sediments of the AtlanticOcean were initially proposed
to suggest that C4 speciesmight have originated earlier, as much as
90 Ma, butcould alternatively be explained by expansion of
marinearchaea at that time [44,45]. Crassulacean acid metab-olism
(CAM) photosynthesis is another adaptation thatinvolves a CO2
concentrating mechanism to maximizewater-use efficiency, and it is
estimated to have alsoevolved in the orchids during the period of
relatively low[CO2] (65 Ma) [46], while the cacti diverged
fromtheir closest relatives 35 Ma [47].
In summary, there are several lines of evidence that fall-ing
and low [CO2] creates selective pressure for two majorclasses of
adaptation. First, adaptations to acquire and usewater in exchange
for [CO2] (smaller stomata, greater sto-matal density, megaphyll
leaves and greater vein density),which were presumably restricted
to plants existing inmesic environments. Second, adaptations for
CO2 con-centrating mechanisms that increase
photosyntheticefficiency and maximize water-use efficiency (C4
andCAM photosynthesis), which were presumably favouredin hot and
dry environments. The potential strength oflow [CO2] as an agent of
selection on plant traits hasbeen highlighted by work on plants
growing 855 Ka,which included a glacial period with very low
[CO2](180220 ppm). Isotopic evidence indicates that theratio of
intercellular [CO2] to atmospheric [CO2] wassimilar to that
observed in modern plants, and thereforeglacial trees were
operating close to the photosyntheticCO2 compensation point where
carbon starvation isexperienced [48]. In contrast, periods of
rising or high[CO2] have not widely been proposed to drive
majorevents in plant evolution. The relative rarity of major
evol-utionary events during periods of high [CO2] is unlikely
toresult from the absence of genetic variation in plant
sensi-tivity to high [CO2], or heritability of key traits
controllingplant response to [CO2] (see Question 3) [49].
Alterna-tively, it might reflect that fitness and selection
weremore strongly driven by genetic variation in plantresponses to
other environmental influences when[CO2] was high and imposing
little or no limitation onphotosynthesis and productivity.
3. QUESTION 2: HAVE PLANTS EVOLVEDBY NATURAL OR ARTIFICIAL
SELECTIONIN RESPONSE TO CONTEMPORARYINCREASES IN
[CO2]?Anthropogenically driven global environmental changesince the
mid-twentieth century has been detectableagainst the background
variability in climate andatmospheric composition [50]. In
addition, biologicalresponses to global environmental change are
detectable
Phil. Trans. R. Soc. B (2012)
in both natural and agricultural ecosystems [5154].Included in
these biological responses are evolutionarychanges across a range
of taxa in response to air pollu-tants, drought and temperature
[5558]. However,there is still no unequivocal evidence that plants
haveevolved in response to contemporary increases in[CO2]. Stomatal
density and stomatal size of ninediverse Floridian plant species
have changed over thelast 150 years, causing a decrease in maximal
gs as[CO2] has risen from 290 to 390 ppm [51]. However,these
changes were interpreted as being driven by anacclimation response,
not genetic changes. This is con-sistent with numerous other
studies on diverse taxa,finding that physiological adjustments play
moresignificant roles than evolutionary responses to
recentenvironmental change [59].
It is possible that crop breeding programmes will
haveincidentally selected for genotypes with improvedresponsiveness
to elevated [CO2]. This possibility hasnot been intensively
studied, but the available evidencesuggests that it is not the
case. In fact, the opposite scen-ario where [CO2] responsiveness
has been selectedagainst may have occurred. Two experimental
compari-sons of wheat genotypes released at different dates overthe
nineteenth and twentieth centuries both showed thatstimulation of
yield by elevated [CO2] predicted formid- to late twenty-first
century compared with ambientor pre-industrial [CO2] was greater in
genotypes withearlier release dates (figure 2) [60,61]). There is
alsono evidence for a greater CO2-fertilization effecton yield of
more recently released soybean genotypesin the US Department of
Agriculture germplasm collec-tion (R. Nelson & E. A. Ainsworth
2011, unpublisheddata). These findings have suggested that
optimizingthe performance of crops under [CO2] today and inthe
decades to come will not happen incidentally.Accordingly, high
yield under the elevated [CO2] pre-dicted in the future needs to be
included as a target incrop breeding and biotechnology programmes
[1,62].
4. QUESTION 3: WILL RISING [CO2] DRIVENATURAL SELECTION IN THE
FUTURE,AND IF SO HOW?While palaeoeological studies have implied
evolutionaryresponses to past changes in atmospheric [CO2],
recentquantitative genetic and selection experiments havetested
whether predicted future elevated [CO2] con-centrations will cause
further evolutionary change[6371]. The evolutionary effects of
rising atmospheric[CO2] are likely to be fundamentally different
fromevolutionary effects of other types of
anthropogenicenvironmental change because the rise in [CO2]occurs
almost uniformly across the globe. Whereas evol-ution in response
to other types of global change, suchas global warming, may be
facilitated by spatial variation(e.g. populations from warmer
regions may possessgenes that facilitate adaptation to warming
climates),[CO2] does not vary substantially across speciesranges,
and, therefore, little genetic differentiation in[CO2]
responsiveness among populations across aspecies range is expected.
Still, because the traitsthat mediate [CO2] responsiveness are
influenced by awide variety of abiotic environmental conditions
that
http://rstb.royalsocietypublishing.org/
-
35(a) (b) (c) (d)
400 600 800 400 600 800 400 600 800 400 600 800
25
15
yiel
d (g
pla
nt1
)
growth [CO2] (ppm)
10
5
0
20
30
Figure 2. Seed yield as a function of growth at [CO2] ranging
from subambient (293 ppm) to ambient (385 ppm) and elevated[CO2]
(715 ppm) for four different Spring wheat lines released in (a)
1903 (Marquis), (b) 1921 (Thatcher), (c) 1965 (Chris)and (d) 1996
(Oxen). Treatment means are adapted from Ziska et al. [60].
Review. Plant adaptation to atmospheric [CO2] A. D. B. Leakey
& J. A. Lau 617
on June 3, 2018http://rstb.royalsocietypublishing.org/Downloaded
from
vary both spatially and temporally (e.g. drought
andtemperature), genetic variation for the physiologi-cal traits
underlying [CO2] response may exist in bothnatural [72] and crop
species [73,74]. In this section,we review quantitative genetic
studies that test howelevated [CO2] will affect predicted future
evolutio-nary trajectories, what traits are likely to change
inresponse to further increases in [CO2], and constraintson
adaptation to future, elevated [CO2]. In addition,we highlight some
of the challenges to predictingevolutionary responses to future
increases in [CO2].
Evolutionary responses depend on: (i) selection, orwhether
elevated [CO2] alters the relationship betweenplant traits and
plant fitness; and (ii) heritability andgenetic covariance, or
whether trait and fitnessresponses to [CO2] are passed to
subsequent gener-ations. Two approaches have been employed
tounderstand how varying [CO2] will influence plant evol-ution. The
first approach uses selection in controlledenvironments experiments
(sensu [75] e.g. [68,71]).Replicated plant populations are grown
for multiplegenerations under ambient [CO2] or elevated
[CO2]predicted for mid- to late twenty-first century. Offspringfrom
populations that had evolved under ambient[CO2] conditions versus
elevated [CO2] conditions arethen compared, ideally in both ambient
[CO2] and elev-ated [CO2] environments. Any divergence
betweenpopulations can be attributed to genetic changes inplant
traits in response to the [CO2] environment, pro-vided that
maternal environmental effects are controlledfor. Increased fitness
of populations that had evolvedunder elevated [CO2] conditions
compared with popu-lations evolved under ambient [CO2] conditions
whengrown in elevated [CO2] environments is evidencefor adaptation
to elevated [CO2]. The second approachemploys quantitative genetics
to compare predictedevolution in ambient [CO2] versus elevated
[CO2]environments [6365,69]. This approach involves esti-mating
components of the evolutionary process(selection, heritability
and/or genetic covariances) onplant populations grown in ambient
[CO2] or elevated
Phil. Trans. R. Soc. B (2012)
[CO2]. The advantage of the selection in a controlledenvironment
approach is that it specifically tests forwhether an evolutionary
response occurs; however,the mechanisms underlying the response
cannot beidentified. The advantage of the quantitative
geneticapproach is that it identifies how the mechanismsof
evolutionary change (altered patterns of natural selec-tion,
heritabilities or genetic covariances between traits)are affected
by [CO2] and also can identify specifictraits underlying adaptation
to elevated [CO2] (seeQuestion 4). Predicting the effects of [CO2]
on long-term evolutionary change with this method, however,is
complicated by assumptions that heritabilities andcovariances
remain constant over time [76].
Most studies that employ the selection in controlledenvironments
approach find limited evidence thatplants adapt to elevated [CO2],
even though geneticchanges in plant traits are often observed.
Potvin &Tousignant [68] simultaneously manipulated
[CO2]concentration and temperature to simulate futureenvironmental
conditions by increasing [CO2] concen-trations from 370 to 650 ppm
and temperature from208C to 23.68C over seven generations. They
detectedlittle evidence that populations of Brassica junceaadapted
to simulated future environments. Althoughhalf of the 14 traits
measured had diverged betweenpopulations that had evolved under
present versusfuture environmental conditions, only one
measuredtrait showed an adaptive response, and no fitnessmeasures
showed a pattern of local adaptation. Simi-larly, Ward et al. [71]
isolated the effects of [CO2] byartificially selecting on fecundity
in replicate Arabidopsisthaliana populations grown under subambient
[CO2](200 ppm) and elevated [CO2] (700 ppm) for five gen-erations.
They found that subambient populations hadadapted to low [CO2] and
produced more seed thanlines selected under elevated [CO2] when
grown at200 ppm [CO2]; however, elevated [CO2] populationshad not
adapted to elevated [CO2]populations thathad evolved under 200 ppm
and 700 ppm did notdiffer significantly in seed production in
elevated
http://rstb.royalsocietypublishing.org/
-
618 A. D. B. Leakey & J. A. Lau Review. Plant adaptation to
atmospheric [CO2]
on June 3, 2018http://rstb.royalsocietypublishing.org/Downloaded
from
[CO2] environments. Moreover, elevated [CO2] selec-tion lines
actually increased biomass less in responseto elevated [CO2]
compared with control lines thatwere not artificially selected,
suggesting that the biomassincreases commonly observed in response
to elevated[CO2] in single generation studies will not be
increasedby evolutionary change. Finally, Collins & Bell
[77]used the model organism Chlamydomonas to
investigateevolutionary responses over 1000 generations in
eitherconstant [CO2] environments (430 ppm) or steadilyincreasing
[CO2] (4301050 ppm). As with the earliermentioned studies, no
Chlamydomonas populationsshowed evidence for adaptation to elevated
[CO2]even though changes in photosynthesis and respirationrates
occurred. These changes reduced the fitness ofpopulations evolved
under elevated [CO2] when theywere grown in lower [CO2]
environments but did notaffect fitness when they were grown in
elevated [CO2].Similar results were observed in natural
Chlamydomonaspopulations found in CO2 springs [78]. Collins &
Bellattribute their findings to the fixation of conditio-nally
neutral mutations in the carbon concentrationmechanismthese changes
had no effect when [CO2]was saturating, but reduced growth and
fitness when[CO2] was limiting. Together, these studies suggestthat
genetic changes may occur in response to eleva-ted [CO2], but that
these changes do not necessarilyresult in increased fitness or
productivity in elevated[CO2] environments.
Similar to the results observed from selection incontrolled
environment studies, quantitative geneticexperiments also find
little evidence that elevated[CO2] has large effects on predicted
evolutionary tra-jectories. For example, Lau et al. [64] failed to
detectevidence that elevated [CO2] alters patterns of natu-ral
selection on plant traits, heritabilities or geneticcovariances,
despite employing a statistically powerful,well-replicated
experiment on a highly variable popu-lation. Both Steinger et al.
[69] and Bazzaz et al. [63]found evidence that elevated [CO2]
alters patterns ofnatural selection and/or heritabilities; however,
effectsof [CO2] on evolutionary processes typically weresmall in
magnitude. All of these studies focus pri-marily on down-stream
traits, such as phenologyand growth. Selection acting on
physiological traits israrely measured, in part because of the
difficulty ofmeasuring physiological traits on the hundreds
orthousands of individuals necessary for rigorous quanti-tative
genetics analyses. This is unfortunate given that:(i) physiological
traits might be expected to respondmost strongly to elevated [CO2];
(ii) several studieshave shown that [CO2] alters phenotypic
integrationand the trade-offs between plant traits [70,79];
and(iii) results from selection in controlled environmentstudies
suggest genetic changes in physiological traitsin response to
variation in [CO2] [77,80,81].
Together, the selection in controlled environmentstudies and
quantitative genetic studies conducted todate indicate that
adaptive evolutionary responsesto elevated [CO2] will be weak
relative to ecologicaland physiological responses. The lack of
evidence forstrong evolutionary responses is surprising, given
thelarge effects of elevated [CO2] on plant phenotypes.However, it
is consistent with mixed results from
Phil. Trans. R. Soc. B (2012)
studies of populations growing along gradients of[CO2] at
natural CO2 springs. Many studies fail tofind evidence for
adaptation to elevated [CO2] or evi-dence for genetic changes
towards increasedproductivity, even though reduced allocation to
photo-synthetic apparatus is sometimes observed inpopulations with
an evolutionary history of high[CO2] [78,82,83] (but see [84]). One
recent examplein which adaptation to elevated [CO2] was
observeddocumented genetic divergence between Plantagoasiatica
populations growing near or far from naturalCO2 springs [83]. When
reared in common environ-ments, genotypes collected from locations
near thesprings (greater [CO2]) had lower photosyntheticcapacity
and gs compared with genotypes far awayfrom the springs (lesser
[CO2]), but also had greatershoot-to-root ratios and achieved
greater productivity.Interestingly, the study populations included
in theseexperiments had experienced [CO2] concentrationsranging
from 380 to 5338 mmol mol21. Genetic differ-ences in phenotypic
traits were observed betweenpopulations that experienced [CO2]
between 380and 1044 ppm. In contrast, there was no
additionaldifferentiation between the populations experiencing[CO2]
of 1044 and 5338 ppm. This is consistentwith the idea presented in
Question 1 that [CO2] willcease to be an agent of selection above
the [CO2](approx. 1000 ppm) at which physiological responsesare
saturated. Moreover, the physiological and growthstimulation
effects of elevated [CO2] begin to attenuateat [CO2] even lower
than 1000 ppm, potentiallyexplaining the minimal evolutionary
effects of elevated[CO2] but larger evolutionary responses to
subambient[CO2] [3,83].
Although most quantitative genetic studies have beenconducted in
relatively simplistic growth chamber andgreenhouse environments
where both abiotic andbiotic stressors are absent, some studies
suggest thatthe evolutionary effects of [CO2] may be heightened
inthe presence of competitors or herbivores [63,65].The effects of
[CO2] in more complex communitiesmay result through two processes.
First, if elevated[CO2] alters the intensity or likelihood of
biotic inter-actions and biotic interactions are strong agents
ofnatural selection, then elevated [CO2] may alter evol-ution when
those interactors are present, even ifelevated [CO2] has minimal
direct effects on evolution-ary processes. For example, if a plant
is grown in thepresence of competitors and elevated [CO2] altersthe
outcome of competition because species varyin the magnitude of
their growth response to [CO2],then the strength of competition as
a selective agentmay be altered. Lau et al. [65] provide empirical
evi-dence in support of this mechanism; elevated [CO2]reduces the
fitness effects of competition on A. thaliana.Because competition
is a strong agent of selection onA. thaliana size traits, elevated
[CO2] minimizes theselective effects of competition, and
differences in pat-terns of natural selection are observed
betweenpopulations grown in ambient [CO2] versus elevated[CO2]
environments when competitors are present,even though [CO2] has no
direct effects on predictedevolutionary trajectories in the absence
of competitors.Second, elevated [CO2] may alter evolutionary
process
http://rstb.royalsocietypublishing.org/
-
Review. Plant adaptation to atmospheric [CO2] A. D. B. Leakey
& J. A. Lau 619
on June 3, 2018http://rstb.royalsocietypublishing.org/Downloaded
from
if elevated [CO2] affects the expression of traits thatmediate
interactions with other species. For example,Vannette & Hunter
[85] find that five genotypes ofAsclepias syrica respond
differently to elevated [CO2]in terms of the expression of
defensive chemicalsbut not growth or reproductive traits. If
herbivoresnegatively impact plant fitness, then the effects
ofelevated [CO2] on defence trait expression could trans-late into
differential effects on plant fitness whenherbivores are abundant,
even though elevated [CO2]is unlikely to affect evolutionary
processes whenherbivores are absent.
In sum, the available evidence to date suggests thatevolutionary
responses to elevated [CO2] will not beconsistently observed or
large in magnitude relativeto ecological and physiological
responses. This isdespite substantial evidence indicating that
subambi-ent [CO2] concentrations are an important selectiveagent
[11,71], potentially responsible for large evol-utionary changes in
a wide variety of plant traitsand even the diversification of
vascular plants (seeQuestion 1). Most studies to date, however,
havebeen conducted in relatively simplistic
environmentalconditions, where biotic and abiotic stress is
minimal.Given that some evolutionary effects have beenobserved or
are predicted when plants experiencecompetition [63,65,69] or
herbivory [85,86], evol-utionary effects may be more likely in more
stressfulbiotic environments. Similarly, evolutionary effects
ofelevated [CO2] also may be more likely when plantsexperience
abiotic stress, such as drought or nutrientlimitation. Under
stressful environments, it is possiblethat the genetic changes in
physiological traitsobserved in numerous studies may change
frombeing conditionally neutral to beneficial, therebyresulting in
differential effects on growth and fitness.Few studies, however,
have investigated evolutionaryconsequences of rising atmospheric
[CO2] in subopti-mal environmental conditions. Given that
temperatureand potentially drought stress will increase
simul-taneously with [CO2], such studies are needed toidentify
evolutionary effects and traits under selectionin future
environments.
5. QUESTION 4: WHAT TRAITS ARE FAVOUREDUNDER HIGH
[CO2]?Physiological, palaeoecological and quantitative gen-etics
experiments suggest that leaf and photosynthetictraits are
responsive to [CO2] and, therefore, may playa key role in mediating
adaptive evolutionary responsesto elevated [CO2]. Moreover, both
inter- and intraspeci-fic comparisons reveal variations in [CO2]
response(reviewed by Poorter & Navas [87], see table 1 in Lauet
al. [64]). Still, we have a rather limited understandingof which
plant traits are most likely to produce higheryields or increased
fitness in the elevated [CO2] environ-ments predicted for the
future, as well as which specificcombinations of traits are
necessary for strong growthenhancement responses to elevated [CO2]
[88]. Therecent advent of trait-based approaches and
associatedmulti-species trait datasets, combined with
intraspecificcomparisons and genetic or phenotypic manipulationsof
traits, may provide improved methods to more
Phil. Trans. R. Soc. B (2012)
thoroughly understand the traits underlying [CO2]responsiveness
and to predict which genotypes andspecies will be favoured in an
elevated [CO2] world.
To date, most studies attempting to identify traitsunderlying
variation in [CO2] response have usedinterspecific comparisons and
have focused on differ-ences among broad functional groups (e.g. C3
forbs,C3 grasses, C4 grasses and legumes). Such studiestypically
find that C3 species have greater responsesto elevated [CO2] than
C4 species and that legumeshave relatively higher CO2 responses
than non-legumes, provided that other nutrients are not
limiting[89,90]. Fewer studies have focused on more specificgrowth,
phenological or physiological traits. Traitsunderlying adaptation
to elevated [CO2] may be ident-ified by growing species under
ambient or elevated[CO2] conditions and correlating phenotypic
traitswith the growth stimulation effects of elevated [CO2]or
fitness/yield in elevated [CO2] environments.In one such study,
Atkin et al. [91] compared thegrowth stimulation effects of
elevated [CO2] on tenAcacia species that varied in relative growth
rate(RGR), and found that fast-growing species (greaterRGR)
responded more to elevated [CO2] than slow-growing species.
However, later studies on the sameset of Acacia species found no
relationship betweenRGR or leaf traits (specific foliage area) and
CO2response [92]. Furthermore, studies on other systemshave found
the opposite pattern [93]. Such empiricalstudies have the advantage
of manipulating [CO2] onmultiple species grown in common
environmentalconditions, but are limited by the small number oftaxa
that can be considered in any one experiment.In addition,
manipulating [CO2] in a single environ-ment may be problematic
given that environmentalconditions affect [CO2] responses and these
environ-mental effects may vary across genotypes. In thestudy by
Atkin et al., for example, the [CO2] manipu-lation took place under
optimal nutrient and waterconditions, an environment that favours
the fast-growing species. Slow-growing species typically
inhabitmore stressful environments, and a very differentfinding may
have resulted if the experimental environ-ment more closely matched
environments to whichslow-growing species were adapted.
More recently, meta-analyses have been conductedon data from
hundreds of existing empirical studiesto look for broad patterns in
[CO2] response acrosstaxonomic scales. Poorter & Navas [87]
conducted ameta-analysis on 350 different experiments that
exam-ined the growth stimulation effects of elevated [CO2]on 350
different plant species. Surprisingly, only18 per cent of the
variation in growth response wasexplained by species, possibly
because CO2 stimulationeffects also depend on ontogeny, environment
andintraspecific variation. Still, the meta-analysis
confirmedexpectations: C3 plants exhibited the strongest
growthresponse to elevated [CO2]; C4 plants showed the smal-lest
growth response; and CAM plants demonstratedintermediate responses.
These functional group classifi-cations based on photosynthetic
mechanisms explainedonly 10 per cent of the variation among species
in CO2response. This may reflect the importance of
ontogeny,environment and genotypes as mentioned earlier, but
http://rstb.royalsocietypublishing.org/
-
620 A. D. B. Leakey & J. A. Lau Review. Plant adaptation to
atmospheric [CO2]
on June 3, 2018http://rstb.royalsocietypublishing.org/Downloaded
from
could also indicate that other traits play strong rolesin
mediating productivity responses to [CO2]. Forexample, among C3
forbs, fast growers respondedmore strongly to elevated [CO2] than
slow growers anddifferences were also observed between dicots
andmonocots as well as legumes versus non-legumes [87].Other
meta-analyses and reviews have focused onother traits. Kerstiens
[94] found that biomass responsesto elevated [CO2] were greater for
shade-tolerant speciesthan shade-intolerant species. Similarly,
Niinements[39] observed that plants with more robust leaves
(i.e.evergreen schlerophylls) responded more positively toelevated
[CO2] than species with less robust leaves,emphasizing the
importance of mesophyll conductanceand its role in influencing
[CO2] supply to chloroplasts.
Similar to the interspecific comparisons describedearlier,
intraspecific variation in plant traits also canbe correlated with
growth responses to elevated[CO2] or high fitness/yield in elevated
[CO2] environ-ments. A study measuring RGR on 29 Picea
glaucagenotypes found no association between RGR andstimulation of
productivity at elevated [CO2] [95].Moreover, P. glauca growth at
elevated [CO2] wastightly correlated with growth at ambient [CO2].
Inother words, the most productive genotypes in ambi-ent [CO2] were
also the most productive genotypes/highest yielders in elevated
[CO2]. This result wasused to argue that the association between
RGR andstimulation of productivity by elevated [CO2] observedin
prior interspecific comparisons was due to traitscorrelated with
both RGR and enhancement of pro-ductivity by elevated [CO2], rather
than a directrelationship between RGR and enhancement of
pro-ductivity by elevated [CO2]. Similarly, Liu et al. [96]observed
that four provenances of Populus tremuloidesexhibited different
responses to elevated [CO2] interms of gs and transpiration rate,
but these dif-ferences did not translate into differences among
theprovenances in biomass response to elevated [CO2].
Conclusions reached from both intra- and inter-specific
approaches illustrate an important challengeto identifying traits
associated with adaptation to elev-ated [CO2] environments. To
pinpoint exactly whattraits are responsible for high growth
responses to elev-ated [CO2] or high fitness/yield in elevated
[CO2]environments, all relevant traits must be measured. Ifall
relevant traits are included in the regressionmodel, then the
particular traits responsible for adap-tation to elevated [CO2] can
be identified. In anintraspecific context, this is essentially what
is donein the phenotypic selection analysis approach devel-oped by
Lande & Arnold [97]. This approach usesmultiple regression to
account for correlations amongtraits. As a result, it can
differentiate between traitsthat are directly associated with
fitness versustraits that are indirectly associated with fitness
due tocorrelations with other phenotypic traits. It should benoted,
however, that there are several statistical andbiological
challenges to be dealt with when applyingthis approach (summarized
by Mitchell-Olds & Shaw[98]), including issues with identifying
traits directlyunder selection due to correlations between
measuredtraits and unmeasured traits that are under selection.In
the selection analyses in ambient [CO2] versus
Phil. Trans. R. Soc. B (2012)
elevated [CO2] environments conducted to date, how-ever, there
is little evidence suggesting that differenttraits are associated
with high fitness in ambient[CO2] versus elevated [CO2] [64]. It is
important tonote, however, that most such studies focus ongrowth or
phenological traits rather than on physio-logical traits.
Similarly, comparisons amongrecombinant inbred lines (as suggested
by Zhanget al. [95]), mutant-wild-type comparisons [99]
andexperimental manipulations of phenotypic traits[100] also may
effectively identify traits involved inCO2 response because focal
traits segregate indepen-dently of genetic background.
Alternatively,modelling approaches [101] can be used to
predictwhich traits are important to fitness/yields in
futureenvironments, identifying focal traits for further
inves-tigation in empirical studies.
Similar approaches can be applied to interspeci-fic comparisons
[102]. While previous interspecificcomparisons were largely limited
to coarse-scale com-parisons among functional groups or to studies
onfew species in a single clade, the advent of new traitdatabases,
which include physiological, as well as mor-phological and
phenological traits, such as TRY [103],may allow for robust
multi-trait analyses on the hun-dreds of species for which [CO2]
responses have beenmeasured. Although such trait-based approaches
havenot yet been used to investigate traits underlying[CO2]
response, they have been employed to predictchanges in community
composition in responseto other anthropogenic environmental changes
(e.g.habitat fragmentation [104]).
A challenge to all studies focused on finding traits orgenes
underlying adaptation to elevated [CO2] is thatmultiple traits are
probably involved. For example,interspecific variation in
photosynthetic efficiency isnot due to one trait, but is instead a
result of severalphysiological traits each with relatively small
effects[105]. Moreover, these traits are often correlated andmay
have synergistic effects [72]. For example, hypothe-tically, having
low Amass and high Nmass is expected toyield very unfit genotypes
because the high cost of main-taining Rubisco would exceed carbon
gains [72]. Manysuch correlations are probably maintained by
selection,suggesting that the correlations may change in responseto
novel environmental conditions. Although it wouldrequire large
sample sizes and many trait measurements,in the quantitative
genetics framework, correlatio-nal selection studies could be used
to identify how theadaptive value of one trait depends on other
traitvalues. Similar approaches could be applied to inter-specific
trait datasets. Alternatively, cluster analyses
ofmorpho-physiological diversity may be used to identifysuites of
correlated traits underlying adaptation [102].Cluster analyses have
been used to identify traits andpotential diversity for improved
agronomic breeding tonovel stressors, such as drought tolerance
[106].
The trait-based approaches described earlier may bepowerful
tools for identifying individual traits and suitesof correlated
traits underlying high fitness in future[CO2]. Ultimately, suites
of traits with synergisticinteractions are likely to contribute to
high fitness innovel environments. As a result, large datasets
consist-ing of many traits for each of many genotypes or
http://rstb.royalsocietypublishing.org/
-
Review. Plant adaptation to atmospheric [CO2] A. D. B. Leakey
& J. A. Lau 621
on June 3, 2018http://rstb.royalsocietypublishing.org/Downloaded
from
species are necessary. Prior palaeoecological studieson
evolutionary responses to variation in [CO2] con-centration have
identified several potential traits thatmay be involved in [CO2]
responses, and modellingapproaches may identify many more.
Improvements inboth the number of traits and number of taxa
includedin existing trait datasets, as well as identification
oflikely adaptive traits through modelling or knowledgeof
physiological responses, may allow for rapid advancesin identifying
the physiological, phenological and mor-phological traits that may
lead to increased growthand fitness in future, elevated [CO2]
environments.Moreover, crosses between distinct genotypes
thatdiffer in entire suites of traits may yield novel genotypesand
trait combinations that could contribute to fitnessand yield
improvement in ambient [CO2] versuselevated [CO2].
6. QUESTION 5: HOW DOES EVOLUTIONARYHISTORY IMPACT AND INFORM
EFFORTSTO ENGINEER CROPS FOR IMPROVEDPERFORMANCE IN PRESENT
ANDFUTURE [CO2]?Circumventing the limitations of current low [CO2]
tophotosynthesis in many of our main crop plants is akey target for
biotechnological efforts to improvecrop productivity [107110]. In
addition, there isemerging recognition that intervention to adapt
cropsby breeding or biotechnology for optimal performancein
elevated [CO2] is needed [111]. In response, targetsfor selection
are beginning to be identified [1], andapproaches that account for
the challenges of geneticand trait-based approaches described
earlier (Ques-tions 3 and 4) have been proposed [62]. Here,
wereview present targets for crop improvement relatedto present and
future [CO2].
The enzyme responsible for photosynthetic fixationof CO2 in all
plants, Rubisco (RibUlose-1,5-BISpho-sphate Carboxylase Oxygenase),
is fundamentallyinefficient. This stems from a relatively low CO2
affi-nity and low carboxylation reaction catalytic rate,which
plants compensate for by synthesizing verylarge quantities of the
enzyme, at the expense of avery large fraction of their leaf
nitrogen. In addition,a significant fraction of reactions catalysed
by Rubiscoresult in oxygenation rather than carboxylation ofRuBP
(RibUlose-1,5-BisPhosphate). Recycling of thetoxic 2PG
(2-PhosphoGlycolate) that is one of theproducts of the oxygenation
reaction is achieved bythe photorespiratory pathway, but at the
expense ofenergy, carbon and nitrogen [109]. Efforts to circum-vent
these inefficiencies fall into three categories. First,engineering
of the Rubisco to improve its enzymaticperformance. Second,
engineering of CO2 concentrat-ing mechanisms to saturate the
carboxylation reactionand suppress the oxygenation reaction. Third,
modifi-cations to the photorespiratory pathway that reducelosses of
carbon, nitrogen and energy.
There has been considerable selective pressure forthe evolution
of more efficient Rubisco throughout thehistory of land plants.
During the periods of sub-saturating [CO2], whichat a
minimuminclude50 Myr in the Carboniferous/Permian and the last
Phil. Trans. R. Soc. B (2012)
30 Myr (figure 1a), modifications leading to greater[CO2]
specificity, greater catalytic rate or impairedoxygenation without
deleterious side-effects couldhave increased photosynthetic
efficiency [110]. Duringperiods of saturating [CO2], modifications
leading togreater catalytic rate without deleterious
side-effectscould have increased photosynthetic efficiency. In
eachcase, greater photosynthetic efficiency would resultin greater
carbon gain for the same investment inresources, or equivalent
carbon gain but with greaterwater-use efficiency and nitrogen-use
efficiency. Never-theless, it appears that evolution of Rubisco has
beenconstrained in a fundamental manner as it remains thelimiting
step in metabolism for most modern C3plants in many growing
conditions.
The factors that have constrained the evolution andengineering
of improved Rubisco up until now arebecoming better understood
[110]. There are threedifferent clades of Rubisco [112]. Clade 1
includesall vascular plants along with cyanobacteria andsome algae
and proteobacteria. Clade 2 is found inchemoautotrophs,
dinoflagellate algae and some pro-teobacteria. Clade 3 is exclusive
to the archaea. Theyall probably share a common ancestor, which was
amethanogenic archaea [112]. Even with considerablevariation in
amino acid sequence and biological func-tion, key active site
residues are conserved across thethree clades [113]. This has
resulted in a shared acti-vation process and catalytic chemistry
that suggeststhat there are considerable constraints upon
modifi-cation of enzyme function [114]. One fundamentalissue may be
that CO2 directly binds to the RuBPenediol, rather than forming a
Michaelis complexwith Rubisco, which reduces the capacity for
discri-mination against O2 binding [115]. An importanttrade-off
exists in which Rubiscos with greater speci-ficity for CO2 relative
to O2 have lower catalytic rates(figure 3) [116,117]. Modelling the
effects of variationin Rubisco specificity on canopy photosynthesis
whileaccounting for the constraints of this relationship indi-cated
that the Rubisco specificity and catalytic rate ofmodern C3 plants
is optimal for [CO2] of approxi-mately 200 ppm [116]. This may
reflect adaptationof Rubisco for optimal carbon gain at the
average[CO2] of the last 400 000 years. If so, Rubisco evol-ution
has not kept pace with anthropogenic [CO2]rise, and will become
increasingly maladapted overthe course of this century. In
addition, the evolution-ary changes that have occurred could be
consideredfine-scale tuning of Rubisco without solving its
morefundamental inefficiencies. Transgenic Rubiscos havebeen
produced that break the trade-off between speci-ficity and
catalytic rate, but typically the results havebeen reduced rather
than improved enzyme perform-ance [116]. However, the modelling
analysis doesemphasize that among the natural diversity of
Rubisco,there are enzymes with more favourable characteristicsthan
currently found in C3 plants. Improved under-standing of the
expression and assembly of Rubiscois necessary to allow the
expression of non-nativeRubisco in higher plants. The process is
complicatedbecause Rubisco in higher plants is a complex offour
dimers of a large subunit encoded in the plastidgenome plus eight
small subunits encoded in the nuclear
http://rstb.royalsocietypublishing.org/
-
100
100 200 300
CO2 concentration (mmol mol1)
C2C1
2
1
400 500 600 700
90
80
70
60
50
optim
al s
peci
fici
ty f
acto
r,
Figure 3. Assuming a fixed number of Rubisco active sites
per unit leaf area and the dependence of catalytic rate
peractive site kcc on specificity described for different
photo-synthetic organisms by Zhu et al. [116], the line shows,
forany given atmospheric [CO2], the specificity (t) that willgive
the highest light-saturated rate of leaf photosynthetic
CO2 uptake (Asat). The average t for terrestrial C3 cropplants
(92.5) is indicated (t1) together with the interpolatedatmospheric
[CO2] at which it would yield the maximumAsat (C1). Point t2 is the
specificity that would yield the high-est Asat at the current [CO2]
of the atmosphere (C2). At C2,decrease in t from present average
(t1) to the optimum forcurrent [CO2] (t2) can increase
light-saturated leaf photo-synthetic carbon uptake by 12%.
Reproduced withpermission from Zhu et al. [116].
622 A. D. B. Leakey & J. A. Lau Review. Plant adaptation to
atmospheric [CO2]
on June 3, 2018http://rstb.royalsocietypublishing.org/Downloaded
from
genome [110]. Progress has been made in using plas-tome
transformation to replace tobacco Rubisco withbacterial and
archaeal Rubiscos [118,119]. However,attempts to express more
efficient red algal andsunflower Rubiscos in tobacco have failed
owing todifferences in their requirements for protein foldingand
assembly [110]. An additional molecular constraintto the
modification of Rubisco is the need for sugar-phosphate inhibitors
bound to its active site to beremoved during an interaction with
Rubisco activase.The identity of residues required for successful
inter-action with Rubisco activase has been proposed [120],but
awaits experimental confirmation [110]. Theabsence of regulation by
Rubisco activase and colocaliza-tion of genes for both Rubisco
subunits and chaperoneproteins on the plastome may explain why
evolution ofRubisco appears to have progressed further in redalgae
than in higher plants [121].
While Rubisco engineering attempts to overcomethe limitations of
natural evolution, an alternative strat-egy is derived from
knowledge of successful naturalevolutionary responses in which a
CO2 concentratingmechanism overcomes the CO2-limitation of
photosyn-thesis. Higher plants with C4 and CAM photosynthesis,as
well as cyanobacteria with carboxysomes and algaewith pyrenoids,
all achieve efficient photosynthesis byconcentrating CO2 around
Rubisco in order to stimu-late carboxylation and inhibit
oxygenation. Effortshave begun to engineer these traits in C3
plants as ameans to increase productivity and yield.
C4 photosynthesis is thought to have evolved asan adaptation to
limit photorespiration at times ofsub-saturating [CO2] [42].
Successful conversion ofrice from a C3 plant to a C4 plant would
likely increase
Phil. Trans. R. Soc. B (2012)
A, water-use efficiency and nitrogen-use efficiency,especially
in hotter and drier environments [107].Achieving this goal will be
challenging because C4photosynthesis is a highly polygenic trait.
Accordingly,it will require not just the expression of genes
encodingthe enzymes of the CO2 concentrating mechanism, butalso
engineering Kranz anatomy and transporters sup-porting flux between
mesophyll and bundle sheathcompartments [122]. This is reflected in
a proposedevolutionary scheme involving a series of steps in
theevolution from C3 to C4 photosynthesis: (i)
generalpreconditioning, i.e. gene duplication; (ii)
anatomicalpreconditioning, i.e. close veins; (iii) enhancement
ofbundle sheath organelles; (iv) addition of photore-spiratory
pump, including localization of glycinedecarboxylase to the bundle
sheath; (v) enhancementof Phosphoenol pyruvate carboxylase
activity;(vi) integration of components; and (vii) optimizationof
components [42]. Linked to this knowledge, signi-ficant effort has
recently focused on determiningthe transcriptional control of C4
leaf structural andmetabolic development [123]. The fact that C4
photo-synthesis has independently evolved in many
geneticbackgrounds on different occasions increases the like-lihood
that successful engineering can be achieved[107]. Specific evidence
for this assertion includesthat: (i) independent lineages of C4
species sharecommon mechanisms controlling the localization ofkey
enzymes for C4 photosynthesis in bundle sheathcells; and (ii)
specific localization of enzymes in C4leaves to bundle sheath
versus mesophyll cells can beachieved by modification of
trans-factors without achange in existing cis-regulation of C3
species [124].
An effort is also beginning to engineer tobaccoplants with
carboxysomes from cyanobacteria
(http://www.nsf.gov/news/news_summ.jsp?cntn_id=119017).This could
also enhance carbon gain, water-use effi-ciency and nitrogen-use
efficiency. Carboxysomes arestructures where photosynthetic enzymes
are localized,creating high [CO2]. Engineering carboxysomes
intochloroplasts of crop plants would effectively create
anevolutionary flashback to when cyanobacteria weresymbiotically
recruited into host cells as the precursorsof chloroplasts. While
the strategy requires conglom-eration of traits from now distantly
related species,it benefits from being limited to manipulation
ofmetabolism within individual cells.
An alternative in preventing photorespiratory lossesby the
development of CO2 concentrating mecha-nisms is direct manipulation
of the photorespiratorypathway in order to prevent or reduce the
typicallosses of carbon, nitrogen and energy once the oxygen-tion
reaction has produced 2PG [109]. Twoindependent approaches in
achieving this goal haveinserted multi-enzyme pathways into plant
chloro-lasts. The first fully oxidizes glycolate in thechloroplast
into CO2 [125]. The second inserts a bac-terial pathway into the
chloroplast that convertsglycolate into glycerate (producing some
CO2 as aby-product), which can then be phosphorylated
andre-incorporated into the Calvin cycle [126]. Bothmodifications
are beneficial because they: (i) releaseCO2 in the chloroplast that
can be refixed by Rubisco,potentially at higher concentrations;
(ii) avoid release
http://www.nsf.gov/news/news_summ.jsp?cntn_id=119017http://www.nsf.gov/news/news_summ.jsp?cntn_id=119017http://www.nsf.gov/news/news_summ.jsp?cntn_id=119017http://rstb.royalsocietypublishing.org/
-
Review. Plant adaptation to atmospheric [CO2] A. D. B. Leakey
& J. A. Lau 623
on June 3, 2018http://rstb.royalsocietypublishing.org/Downloaded
from
of ammonia and the energetic cost usually associatedwith its
reassimilation; and (iii) produce additionalreducing equivalents in
the chloroplast [109].Expression of the bacterial pathway in
Arabidopsis ledto a 30 per cent stimulation of biomass
production[127]. One potential problem that remains to betested is
whether excess reducing equivalents will beproduced under high
light conditions, as photorespira-tion can play an important role
as an alternativeelectron sink during periods of stress that
impairphotosynthetic quenching [109,128].
All of the approaches to enhancing photosynthesisdescribed above
tackle the limitation to photosynthe-sis by current [CO2]. They
address the urgent needto boost crop production in the face of
growing foodinsecurity. However, looking further into the
future,the continuing rise of [CO2] will gradually diminishthis
limitation to photosynthesis and optimization ofcrop productivity
will present a modified set of chal-lenges. The speed of
anthropogenically driven [CO2]rise means forward thinking is
particularly necessaryto optimize crops to their growth [CO2].
Based onthe evidence reviewed earlier, natural selection
forimproved performance in elevated [CO2] is weak andthere is
unlikely to have been incidental breedingfor improved performance
at elevated [CO2] to date(Questions 2 and 3). However,
understanding ofplant cellular, physiological and agronomic
responsesto elevated [CO2] has allowed preliminary identifi-cation
of targets for biotechnological improvement [1].
Future, elevated [CO2] will favour replacement ofRubisco in C3
crops with Rubisco that has lowerspecificity and greater catalytic
rate (derived from C4species or algae) even more so than under
presentconditions [116]. Some organisms are capable ofexpressing
different Rubiscos whose characteristicsare tailored to variation
in growth conditions [127].Engineering such a regulatory system
into cropscould provide additional benefits, such as
expressingdifferent Rubiscos in sun and shade leaves [116].
At elevated [CO2], A becomes limited by the capacityfor
regeneration of RuBp [129]. Modelling suggeststhat allocation of
greater nitrogen resources to enzy-mes involved in RuBp
regeneration in the Calvincycle will stimulate photosynthesis at
elevated [CO2][130]. Transgenic tobacco overexpressing one of
theseenzymes, sedoheptulose-1,7-bisphosphatase, achievesenhanced
photosynthesis and productivity [131].
C3 plants grown at elevated [CO2] consistentlyaccumulate
substantially larger pools of carbohydratesin leaves and other
tissues, even when grown withunlimited rooting volume in the field
[132]. The pri-mary molecular response of soybean to growth
atelevated [CO2] is transcriptional reprogramming of therespiratory
pathway, allowing greater use of theadditional available assimilate
[133]. Even though soy-bean undergoes this metabolic rewiring and
is able tomatch greater C fixation with enhanced N
assimilation[134], there is still significant accumulation of
leafstarch for much of the growing season [133,135]. Thisimplies
that greater enhancement of productivity at elev-ated [CO2] might
be achieved by increasing utilizationof photoassimilate. Despite
improved understanding ofhow carbohydrate status drives
productivity [136,137],
Phil. Trans. R. Soc. B (2012)
further work is needed to determine how C utilizationis
controlled by interactions among sink metabolism,photoassimilate
transport capacity and energy demandfor photoassimilate export from
source leaves [133,138141]. Given the projected increases in
tempera-ture, drought and disease stress that crops willexperience
due to global environmental change, greaterallocation of carbon
resources to metabolites associatedwith stress tolerance could have
multiple advantages [1].For example, greater production of
osmolytes, such aspinotol, mannitol and raffinose, can provide
protectionfrom dehydration under high temperature and
droughtstress, while antioxidant metabolites, such as
ascorbate,reduce oxidative damage from elevated ozone anddrought
stress [142144]. Greater carbon resourcesare typically assumed to
allow plants to invest greatresources in defence [145]. However,
the changes inhormone signalling and secondary metabolism ofsoybean
grown under elevated [CO2] provide an inter-esting exception to
this rule. When grown at elevated[CO2] in the field, the inducible
defence response ofsoybean to damage by Japanese beetle, induction
of aprotease inhibitor that hinders the beetles digestive pro-cess,
is impaired [146]. Changes in sugarhormoneinteractions are thought
to underpin the responseand may provide another target for
enhancing cropproduction in elevated [CO2].
Growth at elevated [CO2] increases nitrogen-useefficiency by
stimulating A per unit leaf N and byallowing photosynthetic
acclimation in which less Nis allocated to Rubisco, leaving greater
N resourcesavailable for other processes including growth[129,147].
Despite these physiological changes, Navailability strongly limits
the response of productivityto elevated [CO2] [132]. Legumes are
able to achievelarge increases in yield and maintain tissue C : N
ratiosunder elevated [CO2] because they can allocateadditional
carbon to N-fixing nodules, providedother nutrients are not
limiting [148150]. Engineer-ing other C3 crops with the capacity to
fix N throughsymbiotic relationships with nodule-forming or
endo-phytic microbes would allow them to benefit morefrom rising
[CO2] and would be favoured by con-ditions of greater C
availability. The biofuel crop,Miscanthus giganteus, shows the
potential of suchan approach, as it was recently shown to achieve
itsextremely high productivity by combining C4 photo-synthesis with
N fixation by endophytic microbes[151]. A potentially deleterious
coupling between inhi-bition of photorespiration at elevated [CO2]
andimpairment of leaf N assimilation in Arabidopsis hasalso
recently been proposed [152]. If this is the casein crop species
under field conditions, and theresponse is not counteracted by
greater root N assim-ilation, elucidation of the mechanism of
responsecould yield a further target for
biotechnologicalimprovement to optimize the coupling of carbon
andnitrogen metabolism and maximize productivity.
7. CONCLUSIONThere are several lines of evidence that periods of
fallingand low [CO2] in the palaeo-record created selectivepressure
for two major classes of adaptation: (i)
http://rstb.royalsocietypublishing.org/
-
624 A. D. B. Leakey & J. A. Lau Review. Plant adaptation to
atmospheric [CO2]
on June 3, 2018http://rstb.royalsocietypublishing.org/Downloaded
from
adaptations to acquire and use water in exchange for[CO2], which
were presumably restricted to plants exist-ing in mesic
environments and (ii) adaptations for CO2concentrating mechanisms
that increase photosyntheticefficiency and maximize water-use
efficiency, whichwere presumably favoured in hot and dry
environments.Nevertheless, while contemporary global
environmentalchange is impacting many elements of plant
biology,there is still no unequivocal evidence for plant
adaptationto contemporary increases in [CO2]. This includes
noevidence for incidental breeding of crop varieties toachieve
greater yield enhancement from future [CO2].The studies of
evolution in response to elevated [CO2]conducted to date applying
selection in controlledenvironments, quantitative genetics and
trait-basedapproaches suggest that the evolutionary responses
ofnatural plant populations to future [CO2] will not beconsistent
or strong relative to ecological and physio-logical responses. This
lack of evidence for strongevolutionary effects is surprising given
the large effectsof elevated [CO2] on plant phenotypes. Most
selectionand quantitative genetics studies to date, however,
havebeen conducted in relatively simplistic
environmentalconditions, where biotic and abiotic stresses
wereavoided. Under more stressful and complex fieldenvironments, it
is possible that the genetic changes inphysiological traits
observed in numerous studies maychange from conditionally neutral
to beneficial, therebyresulting in differential effects on growth
and fitness.Given that temperature and potentially drought
stresswill increase simultaneously with [CO2], such studiesare
needed to identify evolutionary effects and traitsunder selection
in future environments. Improvementsin both the number of traits
and number of taxa includedin existing trait datasets, as well as
identification of likelyadaptive traits through modelling or
knowledge of phys-iological responses, may allow for rapid advances
inidentifying the physiological, phenological and morpho-logical
traits that may lead to increased growth andfitness in future,
elevated [CO2] environments. Already,efforts are underway to
engineer plants to overcome pre-sent day [CO2] limitations to
photosynthesis and carbongain. These include efforts to tackle
those inefficienciesof Rubisco that natural selection has failed to
overcome,as well as attempts to mimic the evolutionary successesof
CO2 concentrating mechanisms and photorespiratoryshunts that allow
enhanced carbon gain and greaterresource-use efficiency in some
higher plants, algae andbacteria. Looking further into the future,
the continuingrise of [CO2] will gradually diminish this limitation
tophotosynthesis and optimization of crop productivitywill present
a modified set of challenges. Methods totackle this challenge are
available and fundamentalunderstanding of plant cellular and
physiologicalresponses is improving such that targets for
biotechnolo-gical optimization of crop performance under
future[CO2] are being proposed and should be tested.
We thank David Beerling for the invitation to participate inthe
workshop, CO2 and Plant Evolution, which wasfunded and hosted by
the Royal Society at the KavliCentre, and led to the development of
this manuscript. Wethank Dana Royer for providing a compilation
ofPhanerozoic [CO2] estimates from proxy analysis. We also
Phil. Trans. R. Soc. B (2012)
thank Dana Royer, Colin Osborne and an anonymousreviewer for
helpful comments and suggestions that greatlyimproved this
manuscript. This is KBS publication no. 1594.
REFERENCES1 Ainsworth, E. A., Rogers, A. & Leakey, A. D. B.
2008
Targets for crop biotechnology in a future high-CO2and high-O3
world. Plant Physiol. 147, 1319. (doi:10.1104/pp.108.117101)
2 Beerling, D. J. 2009 Coevolution of photosyntheticorganisms
and the environment. Geobiology 7,
9799.(doi:10.1111/j.1472-4669.2009.00196.x)
3 Ward, J. K. & Kelly, J. K. 2004 Scaling up
evolutionary
responses to elevated CO2: lessons from Arabidopsis.Ecol. Lett.
7, 427440. (doi:10.1111/j.1461-0248.2004.00589.x)
4 Ward, J. K. & Strain, B. R. 1999 Elevated CO2 studies:
past, present and future. Tree Physiol. 19,
211220.(doi:10.1093/treephys/19.4-5.211)
5 Ackerly, D. D. et al. 2000 The evolution of
plantecophysiological traits: recent advances and futuredirections.
BioScience 50, 979995.
(doi:10.1641/0006-3568(2000)050[0979:TEOPET]2.0.CO;2)
6 Ackerly, D. D. & Monson, R. K. 2003 Waking thesleeping
giant: the evolutionary foundations ofplant function. Int. J. Plant
Sci. 164, S1S6. (doi:10.1086/374729)
7 Reusch, T. B. H. & Wood, T. E. 2007 Molecular ecol-ogy of
global change. Mol. Ecol. 16,
39733992.(doi:10.1111/j.1365-294X.2007.03454.x)
8 Beerling, D. J. 2005 Leaf evolution: gases, genes
andgeochemistry. Ann. Bot. 96, 345352. (doi:10.1093/aob/mci186)
9 Edwards, E. J., Osborne, C. P., Stromberg, C. A. E.,Smith, S.
A. and C4 Grasses Consortium. 2010 Theorigins of C4 grasslands:
integrating evolutionary andecosystem science. Science 328, 587591.
(doi:10.1126/science.1177216)
10 Feild, T. S. & Arens, N. C. 2005 Form, function
andenvironments of the early angiosperms: mergingextant phylogeny
and ecophysiology with fossils. NewPhytol. 166, 383408.
(doi:10.1111/j.1469-8137.2005.01333.x)
11 Gerhart, L. M. & Ward, J. K. 2010 Plant responses tolow
[CO2] of the past. New Phytol. 188,
674695.(doi:10.1111/j.1469-8137.2010.03441.x)
12 Willis, K. J. & McElwain, J. C. 2002 The evolution
ofplants. Oxford, UK: Oxford University Press.
13 Berner, R. A. 2006 GEOCARBSULF: a combinedmodel for
Phanerozoic atmospheric O2 and CO2.Geochim. Cosmochim. Acta 70,
56535664. (doi:10.1016/j.gca.2005.11.032)
14 Royer, D. L. 2001 Stomatal density and stomatal indexas
indicators of paleoatmospheric CO2 concentration.Rev. Palaeobot.
Palynol. 114, 128. (doi:10.1016/S0034-6667(00)00074-9)
15 Cerling, T. E. 1991 Carbon dioxide in the atmosphere-evidence
from Cenozoic and Mesozoic paleosols.Am. J. Sci. 291, 377400.
(doi:10.2475/ajs.291.4.377)
16 Fletcher, B. J., Brentnall, S. J., Anderson, C. W.,
Berner, R. A. & Beerling, D. J. 2008 Atmosphericcarbon
dioxide linked with Mesozoic and early Ceno-zoic climate change.
Nat. Geosci. 1, 4348. (doi:10.1038/ngeo.2007.29)
17 Freeman, K. H. & Hayes, J. M. 1992 Fractionation of
carbon isolopes by phytoplankton and estimates ofancient carbon
dioxide levels. Glob. Biogeochem. Cycles6, 185198.
(doi:10.1029/92GB00190)
http://dx.doi.org/10.1104/pp.108.117101http://dx.doi.org/10.1104/pp.108.117101http://dx.doi.org/10.1111/j.1472-4669.2009.00196.xhttp://dx.doi.org/10.1111/j.1461-0248.2004.00589.xhttp://dx.doi.org/10.1111/j.1461-0248.2004.00589.xhttp://dx.doi.org/10.1093/treephys/19.4-5.211http://dx.doi.org/10.1641/0006-3568(2000)050[0979:TEOPET]2.0.CO;2http://dx.doi.org/10.1641/0006-3568(2000)050[0979:TEOPET]2.0.CO;2http://dx.doi.org/10.1086/374729http://dx.doi.org/10.1086/374729http://dx.doi.org/10.1111/j.1365-294X.2007.03454.xhttp://dx.doi.org/10.1093/aob/mci186http://dx.doi.org/10.1093/aob/mci186http://dx.doi.org/10.1126/science.1177216http://dx.doi.org/10.1126/science.1177216http://dx.doi.org/10.1111/j.1469-8137.2005.01333.xhttp://dx.doi.org/10.1111/j.1469-8137.2005.01333.xhttp://dx.doi.org/10.1111/j.1469-8137.2010.03441.xhttp://dx.doi.org/10.1016/j.gca.2005.11.032http://dx.doi.org/10.1016/j.gca.2005.11.032http://dx.doi.org/10.1016/S0034-6667(00)00074-9http://dx.doi.org/10.1016/S0034-6667(00)00074-9http://dx.doi.org/10.2475/ajs.291.4.377http://dx.doi.org/10.1038/ngeo.2007.29http://dx.doi.org/10.1038/ngeo.2007.29http://dx.doi.org/10.1029/92GB00190http://rstb.royalsocietypublishing.org/
-
Review. Plant adaptation to atmospheric [CO2] A. D. B. Leakey
& J. A. Lau 625
on June 3, 2018http://rstb.royalsocietypublishing.org/Downloaded
from
18 Pagani, M., Freeman, K. H. & Arthur, M. A. 1999
LateMiocene atmospheric CO2 concentrations and theexpansion of C4
grasses. Science 285, 876879.(doi:10.1126/science.285.5429.876)
19 Pagani, M., Zachos, J. C., Freeman, K. H., Tipple, B.
&Bohaty, S. 2005 Marked decline in atmospheric carbondioxide
concentrations during the Paleogene. Science309, 600603.
(doi:10.1126/science.1110063)
20 Royer, D. L., Berner, R. A. & Beerling, D. J. 2001
Phaner-ozoic atmospheric CO2 change: evaluating geochemicaland
paleobiological approaches. Earth Sci. Rev. 54,349392.
(doi:10.1016/S0012-8252(00)00042-8)
21 Royer, D. 2006 CO2-forced climate thresholds duringthe
Phanerozoic. Geochim. Cosmochim. Acta 70,56655675.
(doi:10.1016/j.gca.2005.11.031)
22 Wullschleger, S. D. 1993 Biochemical limitations tocarbon
assimilation in C3 plants: a retrospective analy-
sis of the A/Ci curves from 109 species. J. Exp. Bot. 44,907920.
(doi:10.1093/jxb/44.5.907)
23 Franks, P. J. & Beerling, D. J. 2009 CO2-forcedevolution
of plant gas exchange capacity and water-use efficiency over the
Phanerozoic. Geobiology 7,227236.
(doi:10.1111/j.1472-4669.2009.00193.x)
24 Knoll, A. H. & Niklas, K. J. 1987 Adaptation, plant
evol-ution, and the fossil record. Rev. Palaeobot. Palynol.
50,127149. (doi:10.1016/0034-6667(87)90043-1)
25 Osborne, C. P., Beerling, D. J., Lomax, B. H. &
Chaloner, W. G. 2004 Biophysical constraints on theorigin of
leaves inferred from the fossil record. Proc.Natl Acad. Sci. USA
101, 10 36010 362. (doi:10.1073/pnas.0402787101)
26 Brodribb, T. J. & Feild, T. S. 2010 Leaf
hydraulicevolution led a surge in leaf photosynthetic
capacityduring early angiosperm diversification. Ecol. Lett.
13,175183. (doi:10.1111/j.1461-0248.2009.01410.x)
27 Haworth, M., Elliott-Kingston, C. & McElwain, J. C.
2011 Stomatal control as a driver of plant evolution.J. Exp.
Bot. 62, 24192423. (doi:10.1093/jxb/err086)
28 Beerling, D. J., Osborne, C. P. & Chaloner, W. G.
2001Evolution of leaf-form in land plants linked to atmos-pheric
CO2 decline in the Late Palaeozoic era. Nature410, 352354.
(doi:10.1038/35066546)
29 Franks, P. J. & Beerling, D. J. 2009 Maximum
leafconductance driven by CO2 effects on stomatal size anddensity
over geologic time. Proc. Natl Acad. Sci. USA106, 10 34310 347.
(doi:10.1073/pnas.0904209106)
30 Woodward, W. I. 1998 Do plants really need stomata?J. Exp.
Bot. 49, 471480. (doi:10.1093/jexbot/49.suppl_1.471)
31 Boyce, C. K., Brodribb, T. J., Field, T. S. &
Zwienieki,
M. A. 2009 Angiosperm leaf vein evolution was physiologi-cally
and environmentally transformative. Proc. R. Soc. B276, 17711776.
(doi:10.1098/rspb.2008.1919)
32 Beerling, D. J. & Franks, P. J. 2010 The hidden cost
oftranspiration. Nature 464, 495496. (doi:10.1038/464495a)
33 McKown, A. D., Cochard, H. & Sack, L. 2010 Decodingleaf
hydraulics with a spatially explicit model: principlesof venation
architecture and implications for its evol-ution. Am. Nat. 175,
447460. (doi:10.1086/650721)
34 Sack, L. & Holbrook, N. M. 2006 Leaf hydraulics.Annu.
Rev. Plant Biol. 57, 361381.
(doi:10.1146/annurev.arplant.56.032604.144141)
35 Gould, S. J. & Vrba, E. S. 1982 Exaptation: a missingterm
in the science of form. Paleobiology 8, 415.
36 Anderson, L. J., Maherali, H., Johnson, H. B., Polley,H. W.
& Jackson, R. B. 2001 Gas exchange and photo-synthetic
acclimation over subambient to elevated CO2in a C3C4 grassland.
Global Change Biol. 7,
693707.(doi:10.1046/j.1354-1013.2001.00438.x)
Phil. Trans. R. Soc. B (2012)
37 Tholen, D. & Zhu, X. G. 2011 The mechanistic basis
ofinternal conductance: a theoretical analysis of meso-phyll cell
photosynthesis and CO2 diffusion. PlantPhysiol. 156, 90105.
(doi:10.1104/pp.111.172346)
38 Farquhar, G. D. & Sharkey, T. D. 1982 Stomatal
con-ductance and photosynthesis. Annu. Rev. Plant Phys.Plant Mol.
Biol. 33, 317345. (doi:10.1146/annurev.pp.33.060182.001533)
39 Niinemets, U., Flexas, J. & Penuelas, J. 2011
Evergreensfavored by higher responsiveness to increased CO2.
TrendsEcol. Evol. 26, 136142. (doi:10.1016/j.tree.2010.12.012)
40 Christin, P. A., Besnard, G., Samaritani, E., Duvall,
M. R., Hodkinson, T. R., Savolainen, V. & Salamin, N.2008
Oligocene CO2 decline promoted C4 photosyn-thesis in grasses. Curr.
Biol. 18, 3743. (doi:10.1016/j.cub.2007.11.058)
41 Ehleringer, J. R., Cerling, T. E. & Helliker, B. R.
1997
C4 photosynthesis, atmospheric CO2 and climate.Oecologia 112,
285299. (doi:10.1007/s004420050311)
42 Sage, R. F. 2004 The evolution of C4 photosynthesis.New
Phytol. 161, 341370. (doi:10.1111/j.1469-8137.2004.00974.x)
43 Urban, M. A., Nelson, D. M., Jimenez-Moreno, G.,Chateauneuf,
J. J., Pearson, A. & Hu, F. S. 2010 Isoto-pic evidence of C4
grasses in southwestern Europeduring the Early OligoceneMiddle
Miocene. Geology38, 10911094. (doi:10.1130/G31117.1)
44 Kuypers, M. M. M., Pancost, R. D. & Damste, J. S. S.1999
A large and abrupt fall in atmospheric CO2concentration during
Cretaceous times. Nature 399,342345. (doi:10.1038/20659)
45 Kuypers, M. M. M., Blokker, P., Erbacher, J., Kinkel,H.,
Pancost, R. D., Schouten, S. & Damste, J. S. S.2001 Massive
expanasion of marine archaea during amid-Cretaceous oceanic anoxic
event. Science 239,9294. (doi:10.1126/science.1058424)
46 Silvera, K., Santiago, L. S., Cushman, J. C. &Winter, K.
2009 Crassulacean acid metabolism andepiphytism linked to adaptive
radiations in the Orch-idaceae. Plant Physiol. 149, 18381847.
(doi:10.1104/pp.108.132555)
47 Arakaki, M., Christin, P.-A., Nyffeler, R., Lendel, A.,Eggli,
U., Ogburn, R. M., Spriggs, E., Moore, M. J. &Edwards, E. J.
2011 Contemporaneous and recent radi-ations of the worlds major
succulent plant lineages.Proc. Natl Acad. Sci. USA 108, 83798384.
(doi:10.1073/pnas.1100628108)
48 Ward, J. K., Harris, J. M., Cerling, T. E., Wiedenhoeft,A.,
Lott, M. J., Dearing, M. D., Coltrain, J. B. &Ehleringer, J. R.
2005 Carbon starvation in glacial
trees recovered from the La Brea tar pits, southernCalifornia.
Proc. Natl Acad. Sci. USA 102,
690694.(doi:10.1073/pnas.0408315102)
49 Geber, M. A. & Dawson, T. E. 1997 Genetic variation
instomatal and biochemical limitations to photosynthesis in
the annual plant, Polygonum arenastrum. Oecologia 109,535546.
(doi:10.1007/s004420050114)
50 Intergovernmental Panel on Climate Change. 2007 Cli-mate
Change 2007: The Physical Science BasisSummaryfor Policymakers, 18
pp. Cambridge, UK: CambridgeUniversity Press.
51 Lammertsma, E. I., de Boer, H. J., Dekker, S. C.,Dilcher, D.
L., Lotter, A. F. & Wagner-Cremer, F.2011 Global CO2 rise leads
to reduced maximum sto-matal conductance in Florida vegetation.
Proc. NatlAcad. Sci. USA 108, 40354040.
(doi:10.1073/pnas.1100371108)
52 Lobell, D. B., Schlenker, W. & Costa-Roberts, J.
2011Climate trends and global crop production since 1980.Science
333, 616620. (doi:10.1126/science.1204531)
http://dx.doi.org/10.1126/science.285.5429.876http://dx.doi.org/10.1126/science.1110063http://dx.doi.org/10.1016/S0012-8252(00)00042-8http://dx.doi.org/10.1016/j.gca.2005.11.031http://dx.doi.org/10.1093/jxb/44.5.907http://dx.doi.org/10.1111/j.1472-4669.2009.00193.xhttp://dx.doi.org/10.1016/0034-6667(87)90043-1http://dx.doi.org/10.1073/pnas.0402787101http://dx.doi.org/10.1073/pnas.0402787101http://dx.doi.org/10.1111/j.1461-0248.2009.01410.xhttp://dx.doi.org/10.1093/jxb/err086http://dx.doi.org/10.1038/35066546http://dx.doi.org/10.1073/pnas.0904209106http://dx.doi.org/10.1093/jexbot/49.suppl_1.471http://dx.doi.org/10.1093/jexbot/49.suppl_1.471http://dx.doi.org/10.1098/rspb.2008.1919http://dx.doi.org/10.1038/464495ahttp://dx.doi.org/10.1038/464495ahttp://dx.doi.org/10.1086/650721http://dx.doi.org/10.1146/annurev.arplant.56.032604.144141http://dx.doi.org/10.1146/annurev.arplant.56.032604.144141http://dx.doi.org/10.1046/j.1354-1013.2001.00438.xhttp://dx.doi.org/10.1104/pp.111.172346http://dx.doi.org/10.1146/annurev.pp.33.060182.001533http://dx.doi.org/10.1146/annurev.pp.33.060182.001533http://dx.doi.org/10.1016/j.tree.2010.12.012http://dx.doi.org/10.1016/j.cub.2007.11.058http://dx.doi.org/10.1016/j.cub.2007.11.058http://dx.doi.org/10.1007/s004420050311http://dx.doi.org/10.1111/j.1469-8137.2004.00974.xhttp://dx.doi.org/10.1111/j.1469-8137.2004.00974.xhttp://dx.doi.org/10.1130/G31117.1http://dx.doi.org/10.1038/20659http://dx.doi.org/10.1126/science.1058424http://dx.doi.org/10.1104/pp.108.132555http://dx.doi.org/10.1104/pp.108.132555http://dx.doi.org/10.1073/pnas.1100628108http://dx.doi.org/10.1073/pnas.1100628108http://dx.doi.org/10.1073/pnas.0408315102http://dx.doi.org/10.1007/s004420050114http://dx.doi.org/10.1073/pnas.1100371108http://dx.doi.org/10.1073/pnas.1100371108http://dx.doi.org/10.1126/science.1204531http://rstb.royalsocietypublishing.org/
-
626 A. D. B. Leakey & J. A. Lau Review. Plant adaptation to
atmospheric [CO2]
on June 3, 2018http://rstb.royalsocietypublishing.org/Downloaded
from
53 van Mantgem, P. J. et al. 2009 Widespread increase oftree
mortality rates in the Western United States. Science323, 521524.
(doi:10.1126/science.1165000)
54 Welch, J. R., Vincent, J. R., Auffhammer, M., Moya,P. F.,
Dobermann, A. & Dawe, D. 2010 Rice yields
intropical/subtropical Asia exhibit large but opposing
sen-sitivities to minimum and maximum temperatures. Proc.Natl Acad.
Sci. USA 107, 14 56214 567. (doi:10.1073/pnas.1001222107)
55 Barnes, J., Bender, J., Lyons, T. & Borland, A.
1999Natural and man-made selection for air pollution resist-ance.
J. Exp. Bot. 50, 14231435. (doi:10.1093/jexbot/50.338.1423)
56 Davison, A. W. & Reiling, K. 1995 A rapid change inozone
resistance of Plantago major after summers withhigh ozone
concentrations. New Phytol. 131,
337344.(doi:10.1111/j.1469-8137.1995.tb03069.x)
57 Franks, S. J., Sim, S. & Weis, A. E. 2007 Rapid
evol-ution of flowering time by an annual plant in responseto a
climate fluctuation. Proc. Natl Acad. Sci. USA104, 12781282.
(doi:10.1073/pnas.0608379104)
58 Pulido, F. & Berthold, P. 2010 Current selection for
lower migratory activity will drive the evolution of resi-dency
in a migratory bird population. Proc. Natl Acad.Sci. USA 107,
73417346. (doi:10.1073/pnas.0910361107)
59 Hoffmann, A. A. & Sgro, C. M. 2011 Climate change
and evolutionary adaptation. Nature 470,
479485.(doi:10.1038/nature09670)
60 Ziska, L. H., Morris, C. F. & Goins, E. W. 2004
Quan-titative and qualitative evaluation of selected wheat
varieties released since 1903 to increasing atmosphericcarbon
dioxide: can yield sensitivity to carbon dioxidebe a factor in
wheat performance? Global ChangeBiol. 10, 18101819.
(doi:10.1111/j.1365-2486.2004.00840.x)
61 Manderscheid, R. & Weigel, H. J. 1997 Photosyntheticand
growth responses of old and modern spring wheatcultivars to
atmospheric CO2 enrichment. Agric.Ecosyst. Environ. 64, 6573.
(doi:10.1016/S0167-8809(97)00020-0)
62 Ainsworth, E. A. et al. 2008 Next generation of elevated[CO2]
experiments with crops: a critical investmentfor feeding the future
world. Plant Cell Environ. 31,13171324.
(doi:10.1111/j.1365-3040.2008.01841.x)
63 Bazzaz, F. A., Jasienski, M., Thomas, S. C. & Wayne,
P.
1995 Microevolutionary responses in experimentalpopulations of
plants to CO2-enriched environments:parallel results from two model
systems. Proc. NatlAcad. Sci. USA 92, 81618165.
(doi:10.1073/pnas.92.18.8161)
64 Lau, J. A., Shaw, R. G., Reich, P. B., Shaw, F. H.
&Tiffin, P. 2007 Strong ecological but weak evolutionaryeffects
of elevated CO2 on a recombinant inbredpopulation of Arabidopsis
thaliana. New Phytol. 175,351362.
(doi:10.1111/j.1469-8137.2007.02108.x)
65 Lau, J. A., Shaw, R. G., Reich, P. B. & Tiffin, P.
2010Species interactions in a changing environment: elev-ated CO2
alters the ecological and potentialevolutionary consequences of
competition. Evol. Ecol.Res. 12, 435455.
66 Maxon-Smith, J. W. 1977 Selection for response to
CO2-enrichment in glasshouse lettuce. Hort. Res. 17, 1522.
67 Mycroft, E. E., Zhang, J. Y., Adams, G. & Reekie, E.2009
Elevated CO2 will not select for enhanced
growth in white spruce despite genotypic variation inresponse.
Basic Appl. Ecol. 10, 349357. (doi:10.1016/j.baae.2008.08.005)
68 Potvin, C. & Tousignant, D. 1996 Evolutionaryconsequences
of simulated global change: genetic
Phil. Trans. R. Soc. B (2012)
adaptation or adaptive phenotypic plasticity. Oecologia108,
683693. (doi:10.1007/BF00329043)
69 Steinger, T., Stephan, A. & Schmid, B. 2007
Predicting
adaptive evolution under elevated atmospheric CO2in the
perennial grass Bromus erectus. Global ChangeBiol. 13, 10281039.
(doi:10.1111/j.1365-2486.2007.01328.x)
70 Tonsor, S. J. & Scheiner, S. M. 2007 Plastic trait
inte-
gration across a CO2 gradient in Arabidopsis thaliana.Am. Nat.
169, E119E140. (doi:10.1086/513493)
71 Ward, J. K., Antonovics, J., Thomas, R. B. & Strain,B. R.
2000 Is atmospheric CO2 a selective agent on
model C3 annuals? Oecologia 123, 330341.
(doi:10.1007/s004420051019)
72 Donovan, L. A., Maherali, H., Caruso, C. M., Huber, H.&
de Kroon, H. 2011 The evolution of the worldwide leafeconomics
spectrum. Trends Ecol. Evol. 26,
8895.(doi:10.1016/j.tree.2010.11.011)
73 Gonzalez, J. A., Bruno, M., Valoy, M. & Prado, F. E.2011
Genotypic variation of gas exchange parametersand leaf stable
carbon and nitrogen isotopes in tenQuinoa cultivars grown under
drought. J. Agro