Crop Adaptation to Climate Change (Yadav/Crop Adaptation to Climate Change) || Plant Responses to Increased Carbon Dioxide

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Chapter 6

Plant Responses to Increased Carbon DioxideS. Seneweera and R.M. Norton

Introduction

Carbon dioxide (CO2) input to the atmospherefrom burning fossil fuels and other anthro-pogenic activities has seen concentrations in-crease from less than 300 μmol/mol beforethe industrial revolution to 387 μmol/mol in2009, increasing at 1.9 μmol/mol per year since2000 (Forster et al. 2007). The increase inatmospheric greenhouse gases CO2, methane,nitrous oxide, and halocarbons are likely tohave increased radiative forcing by 9% between1998 and 2007, leading to a warming of the at-mosphere (Forster et al. 2007).

The IPCC 2007 emissions scenario A1B in-dicates that atmospheric carbon dioxide con-centration ([CO2]) will reach 550 μmol/mol by2050 (Carter et al. 2007). The climatic pertur-bations that result from a changed atmosphereare expected to have strong regional effects, butgenerally it is likely that there will be warmertemperatures and more frequent droughts partic-ularly at the mid-latitudes (Carter et al. 2007).For example, in southern Australia, rainfall willdecline by 50–100 mm and annual mean surfacetemperatures will rise by 1–2 ◦C by 2050 (Moiseand Hudson 2008).

An understanding of the impact of climateon future crop production requires an apprecia-

tion of the general responses of a range of croptypes to elevated [CO2] (e[CO2]) and the waysin which those effects interact with temperatureand water supply. The literature on e[CO2] re-sponse is large, for example, by 2006, 87 reviewsand conceptual papers were reported in Korner(2006) and many more have been published sincethen. So, the objective of this chapter is to presentan overview of the responses to e[CO2] and theunderlying causes of those responses.

Methods to investigate cropresponses to CO2

The effects of higher [CO2] on plant growth andecosystem function have been investigated in anumber of ways. Early studies were done in con-trolled environments, laboratory glasshouses,and enclosed chambers, and later in open toppedchambers (OTC) and free air carbon dioxide en-richment (FACE) systems. Amthor (2001) com-pared the response of wheat grown for its wholelife cycle under these systems and found rea-sonable agreement to responses in controlledenvironments and in OTC (e.g., Amthor 1995;Drake et al. 1997; Wand et al. 1999). Enclosurestudies can cause artifacts in the plants studieddue to root restriction for container-grown plants(Arp 1991), changed radiation conditions due

Crop Adaptation to Climate Change, First Edition. Edited by Shyam S. Yadav, Robert J. Redden, Jerry L. Hatfield,Hermann Lotze-Campen and Anthony E. Hall.c© 2011 John Wiley & Sons, Ltd. Published 2011 by John Wiley & Sons, Ltd.

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PLANT RESPONSES TO INCREASED CARBON DIOXIDE 199

to the enclosure, and other “enclosure effects”(Ainsworth and Long 2005). It is also importantto grow the target species at e[CO2] for suffi-ciently long periods to enable the plants to ac-climate to altered growth conditions. To addresssome of these concerns, the FACE technique wasdeveloped to grow plants in communities in thefield in open atmospheres enriched with CO2 toinvestigate how crop (e.g., Kimball et al. 1995;Miglietta et al. 1997), forest (e.g., Hendrey et al.1999), and natural plant communities (Hovendenet al. 2006) will respond to e[CO2].

The FACE rings (often octagons) used vary indiameter from 1.5 m (Hovenden et al. 2006) to30 m (Hendrey et al. 1999). Some (e.g., Lewinet al. 1994) inject premixed air and CO2, whileothers inject pure CO2 over the area where thetarget plants are grown (e.g., Miglietta et al.1997; Mollah et al. 2009). Both premixed andpure CO2 fumigating systems are able to meettheir target [CO2], but the premixed system pro-vided better temporal and spatial uniformity anduse less CO2 (Lewin et al. 2009).

While all e[CO2] experimental systems haveartifacts, the FACE system produces an environ-ment similar to field conditions albeit with quitehigh spatial and temporal variation in e[CO2]in the test areas (Mollah et al. 2009). However,Long et al. (2006) and Ainsworth et al. (2008b)proposed that the yield responses reported inFACE experiments were around half of the re-sponse reported from enclosure studies. Otherauthors (Korner 2006; Tubiello et al. 2007; Ziskaand Bunce 2007; Hogy and Fangmeier 2009) ar-gued that the two methods produced essentiallysimilar results, while in a direct comparison ofOTC and FACE systems the relative responsesof the aboveground biomass and absolute growthrelative to e[CO2] were nearly identical (Kimballet al. 1997). Nowak et al. (2004) reviewed theresponses of plants growing in communities un-der FACE and concluded that the measured andexpected responses were in general agreement.Ainsworth et al. (2008b) showed 14% yield in-crease in FACE compared to a 31% increase fromenclosures when [CO2] was raised from ∼373 to

∼570 μmol/mol. While it is unclear if FACEis underestimating responses or OTC is overes-timating, the results of any studies need to beassessed in terms of the experimental manipula-tion methods used, which may have significantquantitative differences in response (Ainsworthet al. 2008b). Even so, the true magnitude of thepositive “fertilization” effect of e[CO2] is stilluncertain.

Overview of plant growthresponse to e[CO2]

The primary responses of plants to e[CO2] isan increase in photosynthetic rate (A) and a re-duction in stomatal conductance (gs) (e.g., Longet al. 2004; Gifford 2004; Ainsworth and Rogers2007). The increase in A occurs because Ribulosebisphosphate carboxlase/oxygenase (RuBisCO)is not saturated at ambient [CO2] in C3 plants(Drake et al. 1997). In the analysis of 12 large-scale FACE experiments, Ainsworth and Long(2005) reported that exposure to e[CO2] gavea 31% increase in light-saturated leaf A and a28% increase in diurnal photosynthetic carbonassimilation. Depending on plant types and Cassimilation pathway, the improved photosyn-thetic efficiency resulted in a change in growthand yield responses, termed a “fertilization” ef-fect. The majority of vascular plants use the C3

carbon assimilation pathway, about 2–3% are C4

such as maize (Zea mays), sorghum (Sorghumbicolor), and sugarcane (Saccharum spp.), while6–7% use crassulacean acid metabolism (CAM)(Drennan and Nobel 2000) and these three mech-anisms respond differently to e[CO2].

The present atmospheric [CO2] sets an up-per limit of A in C3 plants and presumably, thelower [CO2] in the past was even more limit-ing (Drake et al. 1997; Sage and Coleman 2001;Ainsworth and Rogers 2007). Indeed, the ki-netic properties of RuBisCO suggest that it oper-ates best at [CO2] of 200 μmol/mol, which sug-gests that these were the condition under whichit evolved (Ainsworth et al. 2008c). Increasingatmospheric [CO2] will undoubtedly increase the



200 CROP ADAPTATION TO CLIMATE CHANGE

A in C3 plants (Drake et al. 1997; Makino andMae 1999; Farquhar et al. 1980). In contrast, C4

plants are less responsive to e[CO2] as they haveevolved with a mechanism to concentrate CO2 inthe leaf mesophyll (Hatch and Slack 1968; Ziskaand Bunce 1997; Ghannoum 2009). However,the initial stimulation of C3 photosynthesis isnot always maintained when plants are exposedto e[CO2] for a longer period, and this adjust-ment is known as “photosynthetic acclimation”(Bowes 1991; Moore et al. 1998; Seneweera et al.2002), which accompanies morphological andbiochemical adjustments at the cellular to wholeplant level (Drake et al. 1997; Makino and Mae1999; Moore et al. 1999; Stitt 1999; Seneweeraet al. 2002). The short-term response to e[CO2]can be demonstrated by analysing RuBisCO ki-netics and gas exchange data and here we addressthose changes as well as other long-term adjust-ments reported.

Growth and morphological changes inC3 systems

Plant growth, development, and morphologicalchanges in response to e[CO2] are well docu-mented in both C3 and C4 species (Ghannoumet al. 2000; Ainsworth and Long 2005), al-though there is a great deal of interspecific vari-ation. Generally, e[CO2] increases the efficiencyof leaf photosynthesis, resulting in taller plantswith thicker stems and more branches and leaves(Ainsworth and Long 2005) and these plantsare almost always larger (Pritchard et al. 1999).The increased growth is often not uniform, withchanges in root to shoot ratios, increasing in 60%of species reviewed and decreasing or unchangedin the others (Rogers et al. 1997). Pritchard et al.(1999) indicated that root length, diameter, andbranching patterns all increased in e[CO2] al-though changes in the nature and distributioncan be a response to root or shoot limitationsoperating rather than an intrinsic allometric re-lationship between top and root growth (Huntand Nicholls 1986). Increased root growth couldbe a response to the need to acquire more nutri-

ents to match the increased C supplied (Rogerset al. 1997). The results of any root growthstudy would be strongly affected by plant de-velopment stage and soil conditions as well asatmospheric [CO2].

Changes occur in the shoot apices and vascu-lar cambium, giving taller, more branched plants.Such changes, especially in the number of api-cal meristems, have a large effect on the estab-lishment of future sink strength. As well as theexpected difference among species, there are in-traspecific differences in the responses, with themore determinate types responding less than lessdeterminate types in soybean (Ziska and Bunce2000; Ainsworth et al. 2002) and wheat (Ziska2008). The reasons for increased shoot, head, orpod numbers could be improved under e[CO2]through increased assimilate supply (e.g. Nakanoet al. 1997) although Seneweera et al. (2003)postulated that in rice, [CO2] may regulate mor-phology and development via its influence onchanges in plant hormonal balance (e.g., ethylenebiosynthesis). Irrespective of the mechanism, ayield response to e[CO2] requires a concomitantincrease in sink capacity to match the sourceactivity.

Leaf morphology shows considerable plas-ticity and various structural adaptations havetaken place in response to changing environ-ments (Pritchard et al. 1999), including lightand N supply (Gutierrez et al. 2009). Ainsworthand Long (2005) concluded that leaf number in-creases, but leaf area index did not change inC3 grasses grown under e[CO2] even though therate of leaf expansion may be higher early in leafgrowth (Pritchard et al. 1999; Seneweera andConroy 2005). Leaf mass per unit area (i.e., leafthickness) often increases due to changes in thenumber and size of mesophyll cells per leaf area(Gutierrez et al. 2009).

Historical evidence suggests that stomataldensity declines as [CO2] increased (Trickeret al. 2005) although the literature has exam-ples where density increases, decreases, or hasnot changed (e.g., Ainsworth and Rogers 2007).In their review of data from FACE experiments,




Ainsworth and Rogers (2007) reported an av-erage decline in stomatal density of 5%, whichwas not statistically significant. They suggestedthat density changes are generally small (±10%)and that there is little evidence for a significantdecrease in stomatal density, so any changes inleaf conductance are a consequence of changesin aperture rather than density.

The effects of e[CO2] on plant developmentand structure are many and varied, interactingwith both plant C assimilation and water rela-tions. Pritchard et al. (1999) concluded that themost significant direct effects of e[CO2] are anincrease in carbohydrate availability and a re-duction in water use and these together wouldstimulate cell proliferation, and phenological de-velopment, light, and nutrient availability wouldmoderate the response.

C3 photosynthesis at e[CO2]

Elevated [CO2] stimulates A in C3 plants becauseof the increased [CO2] gradient from the air tothe site of CO2 fixation. Stimulation of A to short-term [CO2] enrichment is well explained by us-ing RuBisCO kinetic data (Farquhar et al. 1980;von Caemmerer 2000). RuBisCO is the key en-zyme in the photosynthetic carbon reduction cy-cle (PCR) and it is also active in the Photorespi-ratory carbon oxidation cycle (PCO) or photores-piration (Bowes 1991; Lorimer 1981). WhenRubilose 1-5-bisphosphate (RuBP) is carboxy-lated by RuBisCO, it produces two moleculesof 3-phosphoglyceric acid (PGA). On the otherhand, when RuBP is oxygenated with RuBisCO,it forms one molecule each of PGA and 2-phosphoglycolate (PG). The PGA is further pro-cessed into carbohydrates and is used to regen-erate RuBP. Oxygenation of RuBP forms PG,which is a waste product that uses up a con-siderable amount of light energy derived fromthe photosynthetic light reaction. For example,at present atmospheric [O2] concentration of21 kPa and 380 μmol CO2 mol−1, the produc-tion of PG will result in the reduction in potentialphotosynthetic capacity by 20–50% depending

on temperature (Sharkey 1985). Doubling thecurrent atmospheric [CO2] will completely in-hibit C3 photorespiration, which will lead to anincrease in the photosynthetic efficiency of theplant (Bowes 1991; Sage and Kubien 2007).

Short-term [CO2] response can be evaluatedby measuring A as intercellular [CO2] (Ci) in-creases (Farquhar et al. 1980). Three major lim-itations for C3 photosynthesis have been iden-tified, giving the shape of the A/Ci curve inFig. 6.1, and they are:

1. The limitation of photosynthesis imposed byRuBisCO referred to as the limitation due tosupply and utilization of CO2.

2. The supply and utilization of light, which lim-its the rate of electron transport for regenera-tion of RuBP.

3. The utilization of triose phosphate, whichlimits the availability of inorganic phospho-rus (Pi) in the chloroplast for ATP synthesisto regenerate RuBP (Farquhar and Sharkey1982; Sharkey 1985).

The second and third limitations are com-monly identified under e[CO2] conditions(Sharkey 1985; Makino and Mae 1999). The sec-ond limitation can be caused by low photosyn-thetic photon flux densities or the inability toconvert light energy into chemical energy. Thethird limitation, triose phosphate limitation, oc-curs when there is a mismatch in carbohydratesynthesis and utilization (Paul and Foyer 2001;Sharkey 1985).

C4 photosynthesis at e[CO2]

Plants with C4 photosynthesis concentrate CO2

in the mesophyll [CO2] to ∼2000 μmol/mol,which completely represses the oxygenation re-action and saturates the carboxylating function(Hatch and Slack 1968; Poorter and Navas 2003).Because of this mechanism, A is not expected toincrease under e[CO2] in C4 plants (Fig. 6.1).However, there are many reports that C4 growthis accelerated at e[CO2] (Samarakoon and




60

50

40

30

20

CO

2 as

sim

ilatio

n ra

te (

A),

µm

ol m

−2 s

−1

Chloroplastic CO2, Ci, (µmo1 mol−1)

10

0200

−10

400 600 800

Phosphatelimited

1000

C4

C3

RuBP limite

d

RuBisC

O lim

ited

Fig. 6.1. Modeled photosynthetic rate as a function of CO2 assimilationrates against Ci in C3 and C4 plants. The data are adapted from von Caem-merer (2000) showing the three major limitations to photosynthetic flux inC3 plants. The C4 line is adapted from Leakey et al. (2009).

Gifford 1996; Seneweera et al. 1998; Ziska et al.1999; Leakey et al. 2006; Ghannoum 2009) andit seems that enhanced C4 growth at e[CO2] ispartly mediated through the adjustment in plantwater relations (Seneweera et al. 1998; Ziskaet al. 1999; Ghannoum et al. 2001; Seneweeraet al. 2001; Leakey et al. 2004). The positiveresponses of C4 plants to e[CO2] could alsobe the result of several other factors possiblysuch as CO2 leakiness in the bundle sheath cell,direct CO2 fixation in the bundle sheath, andthe presence of C3-like photosynthesis duringleaf expansion (Wand et al. 1999). In addition,diurnal variation in photosynthetic response toe[CO2] could be affected, although the literatureat present is not conclusive on the relative con-tributions of these factors to C gain and growthin C4 plants.

From a meta-analysis of C4 plant gs de-cline by 30% with e[CO2], which is similarto the response in C3 plants (Ghannoum et al.2000; Ainsworth and Rogers 2007). Even thoughthe mechanisms controlling stomatal aperture ate[CO2] have not been clearly elucidated, e[CO2]reduces gs, which in turn reduces the transpi-ration rate and leads to improved soil water

availability later in plant growth (Seneweeraet al. 1998; Leakey et al. 2004, 2006). Leakeyet al. (2006) reported that A in maize was notincreased under e[CO2] where there was nosoil water deficit during the growing season,but photosynthesis was greater in a year whereepisodic water stress occurred. Their conclusionwas that e[CO2] indirectly enhances C gain dur-ing drought.

Therefore, the increased growth in C4 plantsunder e[CO2] is not a direct photosynthetic re-sponse, but a consequence of reduced droughtstress as water use is lower, which reserves waterto extend the duration of photosynthesis (Sene-weera et al. 2002; Leakey et al. 2009).

CAM photosynthesis at e[CO2]

CAM is the modification seen in some vascu-lar plants such as pineapple (Ananas comosus),prickly pear (Opuntia stricta), and agave (Agavesalmania). As well, some species show C3-CAM intermediates, with low water availabil-ity inducing CAM expression (Luttge 1996). InCAM plants, CO2 fixation and CO2 metabolismare temporally separated. CO2 fixation occurs




at night and/or the early morning and/or lateafternoon with fixation catalyzed by the cytoso-lic enzyme phosphoenolpyruvate carboxylase(PEPCase) to form malate or aspartate, whichis stored in the vacuole. Decarboxylation occursduring the daytime and releases CO2 from themalic or aspartic acid, which is ultimately as-similated into carbohydrates (Winter and Smith1996). Typically, CAM plants have transpirationefficiencies three to five times higher than C3 orC4 plants (Nobel 1996) and often these speciesoccur in environments characterized by watershortage (Drennan and Nobel 2000).

Drennan and Nobel (2000) reported that adoubling of [CO2] increased both daytime andnighttime CO2 uptake with an average biomassincrease of about 35% for 10 species examined.Those authors proposed that CO2 fixation byRuBisCO increased in the late afternoon as wellas nocturnal CO2 fixation, although carboxyla-tion activities of both RuBisCO and PEPCase de-crease in response to e[CO2]. Nocturnal malatelevels increase with e[CO2] as do carbohydratecontents (Drennan and Nobel 2000). The de-crease in RuBisCO content in CAM species un-der e[CO2] is compensated by higher enzymeactivation, so that A is maintained. With littleevidence of acclimation to e[CO2], some CAMplants show higher CO2 assimilation (source ca-pacity), greater sucrose transport in the phloem,and stronger sink strength (Drennan and Nobel2000; Osmond et al. 2008). Because of theseadaptations, a greater understanding of the mech-anisms controlling C gain in CAM plants couldprovide new insights into the mechanisms thatmay help for genetic manipulation of C3 speciesfor C rich atmosphere.

Growth and yield responses to e[CO2]

There have been many reviews and meta-analyses of [CO2] enrichment studies and in gen-eral the responses reported show higher growthand yield under e[CO2] although there are im-portant interactions with N, water, and temper-ature. Poorter and Navas (2003) concluded that

fast-growing C3 species are the most responsivegroup of plants to e[CO2], although N-fixing di-cots respond well at low nutrient levels.

Ainsworth and Long (2005) performed ameta-analysis of data from 40 species across12 FACE sites and showed that growth andabove-ground biomass generally increased un-der e[CO2], with an average crop yield increaseof 17%. Figure 6.2 shows the responses of dif-ferent groups of plants to e[CO2]. Trees showedthe largest response in dry matter accumulation(28%) although the response in C3 grasses (10%)(Ainsworth and Long 2005) was substantiallylower than earlier reports (Wand et al. 1999).The trend of about 15% wheat grain yield in-crease is lower than other authors (Amthor 2001;Kimball et al. 2002). For example, wheat yieldsincreased on an average of 31% when [CO2] wasraised from 350 to 700 μmol/mol (Amthor 2001).Ainsworth and Long (2005) suggested that thesize of the response is a consequence of the in-teraction of the photosynthetic response and en-vironmental conditions. This may be well ex-plained that smaller responses they saw in FACEcompared to chamber experiments (Ainsworthet al. 2008b). Similar analyses have proposedyield increases of 23% for rice (Ainsworth 2008)and 24% for soybean (Ainsworth et al. 2002)with e[CO2].

Regulation of photosyntheticresponse to e[CO2]

The initial stimulation of photosynthesis oftendeclines when plants are grown under e[CO2]for periods of weeks, months, or years (Drakeet al. 1997; Bloom 2006; Ainsworth and Rogers2007). Acclimation of A to e[CO2] has been doc-umented in a number of species, and there isvariation among functional groups, species, andcultivars (Ainsworth and Long 2005; Ainsworthand Rogers 2007; Prasad et al. 2009).

The short-term photosynthetic data do not al-ways translate into the sorts of responses seenover the whole season in C3 plants. That dif-ference of A acclimation during ontogeny and




Height TreesShrubsC3 Crops

RiceWheatCottonSorghum

No StressDroughtLow N

Trees C3 Grasses

Trees C3 Grasses Legumes

C3 C4

LAI

DMP

Crop yield

–40 –20 0 20 40

Percentage change in elevated [CO2]

60 80 100

Fig. 6.2. Comparative responses to e[CO2] of different functional groups and ex-perimental conditions on growth and yield variables. Results from: ©, (Ainsworthand Long 2005); �, a meta-analysis of tree species (Curtis and Wang 1998); �, ameta-analysis of C4 grasses (Wand et al. 1999); �, comparative results from a meta-analysis of 79 crop and wild species (Jablonski et al. 2002). Number of species, FACEexperiments, and individual observations for each response are given in Ainsworth andLong 2005). (Reproduced from Ainsworth and Long 2005, with permission.)

understanding of the basis of the A acclimationcould help to translate it into a larger whole sea-son response. In this section, possible underlyingfactors that regulate the photosynthetic responseto long-term CO2 enrichment will be discussed.

Photosynthesis and leaf N at e[CO2]

Critical leaf N content is the nutrient concentra-tion at which 90% of the maximum growth orbiochemical reaction is achieved at a given time(Reuter and Robinson 1997). Interspecific andintraspecific differences in critical N concentra-tions have been identified although in general,C4 plants have a lower critical N concentrationthan C3 plants (Conroy 1992; Aben et al. 1999).Nitrogen deficiency reduces plant growth and al-

ters the allocation of biomass between the shootand root (Makino et al. 1997; Aben et al. 1999).

Under e[CO2], dry mass per unit of leaf Nincreases. For example, in rice, the critical Nconcentrations were 4.0% at the present atmo-spheric [CO2], but at doubled ambient [CO2],the critical level decreased to 2.8% (Aben et al.1999). Even though concentrations decline (30%in the above example), the “fertilizer” effect ofe[CO2] can increase the total N demand of thecrops.

Plant photosynthetic capacity is largely influ-enced by leaf N content, whereas light-saturatedA is linearly correlated with leaf N under a widevariety of conditions including e[CO2] when Ais measured under the same [CO2] concentra-tion (Evans 1989b; Makino et al. 1994; Nakano




et al. 1997; Aben et al. 1999). However, thisrelationship differs among plant functionalgroups (e.g., Evans 1989b; Sudo et al. 2003).A large amount of N is allocated to leaves, forexample in rice, about 65–70% of the total Nin the shoot is invested in the leaf blade (Sene-weera, unpublished) and approximately 80% ofthe total leaf N is allocated to the chloroplasts(Evans 1989a). Most of the N in the chloroplastis invested in photosynthetic proteins, includingRuBisCO and thylakoid protein (Evans 1989b;Makino and Osmond 1991).

The most striking feature at e[CO2] is the de-crease in N allocation to leaf blades (Conroy andHocking 1993; Nakano et al. 1997; Ghannoum2009; Leakey et al. 2009) and this is againsta rise in A, with the consequence that photo-synthetic N-use efficiency (PNUE) rises undere[CO2] (Nakano et al. 1997; Aben et al. 1999;Seneweera et al. 2002; Leakey et al. 2009). Forexample, in rice grown under e[CO2], whichshowed an increase in A, N uptake per plantremained the same or increased, N uptake onan area basis increased by 15%, but the N con-tent on leaf area basis was reduced by 12% atthe panicle initiation in rice (Kim et al. 2003).This decrease was found only after panicle initi-ation and the reason for these differences couldbe due to an increase in N demand for largerpanicles in plants grown at e[CO2] (Seneweeraet al. 2002). In contrast, reduced leaf N contentwas reported at various stages of plant develop-ment in wheat (Rogers et al. 1996; Seneweeraand Conroy 2005) and during early growth ofsoybean (Rogers et al. 2006).

The decline in leaf N could be a consequenceof reduced supply or transport capacity due tofaster growth (Stitt and Krapp 1999), sink lim-itation due to a finite N supply (Rogers et al.1996; Long et al. 2004), restricted root volumes(Stitt and Krapp 1999; Long et al. 2004), and/orreduced soil N supply due to progressive N lim-itation (Luo et al. 2004).

One of the common explanations for reduc-tion in leaf N content at e[CO2] is the dilutionof N due to excess carbohydrate accumulation

(Conroy 1992). This mechanism does not explainlow leaf N in wheat because concentrations werereduced by e[CO2] irrespective of whether N wasexpressed on a total dry mass or total structuraldry mass, or leaf area basis (Rogers et al. 1996).In addition, there was no change in the N concen-tration of leaf sheaths at e[CO2] despite the factthat a large amount of starch accumulated (Se-neweera et al. 1994; Aben et al. 1999; Zhu et al.2009). This carbohydrate feedback is proposedto cause a suppression of genes involved in pho-tosynthesis, including RuBisCO (Jang and Sheen1994; Gesch et al. 1998; Moore et al. 1999) be-cause 25% leaf N contributes to RuBisCO inC3 plants. However, an inverse relationship be-tween photosynthesis and soluble sugar contentwould be expected, but is not always been re-ported (Nakano et al. 2000; McCormick et al.2006).

Reduced transpiration could contribute tolower N concentration at e[CO2] because lowergs reduces the transpiration flow, thereby lower-ing the N uptake (McDonald et al. 2002). How-ever, nutrients other than N seem to be littlechanged in plants grown under e[CO2] and havesimilar mineral contents to those grown in ambi-ent [CO2], e.g., berseem clover leaves (Pal et al.2003), potato tubers (Pikki et al. 2007), wheatgrain (Hogy et al. 2009), wheat, and barley grains(Erbs et al. 2010). It is likely that if transpirationis the limiting factor for nutrient uptake, then theuptake of other nutrients, such as K, would alsobe lower, but the examples above do not clearlyshow that decline.

Taub et al. (2008) concluded that the best sup-ported of these theories for declining leaf N wasa decrease in transpiration drive mass flow ofN and a lower N demand due to improved effi-ciency, although they also indicated that root ar-chitecture, higher N loss through volatilization,and root exudates could also contribute. So, nosingle clear mechanism is entirely supported bythe present evidence.

PCR and NO3− photoassimilatory cycles

compete for electrons from light reaction of pho-tosynthesis (Smart et al. 1998; Bloom et al.




2002) with CO2 assimilation favored. Undere[CO2], electron partitioning toward PCR andaway from the NO3

− photoassimilatory cyclecould result in a slower N influx and then pos-sibly a reduction in the synthesis of protein.Under e[CO2], the growth response is higherwhere NH4+ is the N source (Geiger et al.1999), free NO3

− accumulation has been re-ported (Hocking and Meyer 1991; Smart et al.1998), and nitrate reductase (NR) activity isreduced in the leaf but not in other tissues(Bauer and Berntson 2001; Bloom et al. 2002).These observations support the hypothesis thatchanges in the photosynthetic electron flow be-tween PCR and NO3

− photoreduction is an-other possible cause of the decrease in leaf Ncontent and reduced protein synthesis includingRuBisCO, which could lead to photosyntheticacclimation to e[CO2]. As with reduction in plantNO3

− photoassimilation at e[CO2] (Bloom et al.2010), crops will become depleted of all or-ganic N compounds, including protein, leadingto lower protein quality and quantity in food.Management of NO3

− and NH4+ are suggested

to be the best alternative to overcome this issue,but it will require sophisticated technology todeliver appropriate fertilizer products to crops inthe preferred form. An improved understandingof plant NH4

+ and NO3− assimilation is critical

to overcome the grain quality changes suggestedunder future climate.

Effect of e[CO2] on RuBisCO content

RuBisCO is the rate-limiting enzyme in photo-synthesis and constitutes about 56% of all solu-ble protein and 26% of total leaf N in C3 plants(Mae et al. 1983; Evans 1989b; Makino andOsmond 1991). The RuBisCO enzyme has aheteromeric structure of eight large and eightsmall subunits of polypeptides, resulting in a na-tive molecular mass of 520 kDa (Lorimer 1981).The amount of RuBisCO in the leaves is theresult of the balance between its synthesis anddegradation (Mae et al. 1983). RuBisCO syn-thesis is controlled by transcriptional, posttran-

scriptional, and translational processes (Mooreet al. 1999; Stitt and Krapp 1999). It is rapidlysynthesized during leaf expansion followed by agradual degradation as leaf ontogeny progresses(Suzuki et al. 2001).

Environmental factors such as light intensity,soil nitrogen, atmospheric [CO2], and [O3] allinfluence RuBisCO synthesis and degradation.It is possible that the change in leaf N statusat e[CO2] is strongly related to the decline inRuBisCO content and A acclimation to e[CO2].Makino et al. (2000) found that 30% of RuBisCOis lost before RuBisCO limits photosynthesis ate[CO2].

Suppression of RuBisCO synthesis occurs ate[CO2] when there is an imbalance between sup-ply and utilization of carbohydrates (Moore et al.1998; Moore et al. 1999). In the case of cereals,about 80–90% of RuBisCO is synthesized justprior to the full expansion of leaf blades (Suzukiet al. 2001; Feller et al. 2008). Similarly, rbcSand rbcL mRNA increases during leaf expansionand reach maxima a few days before full expan-sion; after full expansion, very little RuBisCO issynthesized (Fig. 6.3; Table 6.1). Our researchfindings clearly demonstrate that RuBisCO

RuBisCO

2

1

0

0 20

Days after leaf emergence

RuB

isC

O(m

g le

af b

lade

−1)

40 60

Fig. 6.3. Changes in the amount of RuBisCO content inthe flag leaf blades of rice from emergence to senescence.Each data point is the mean of four replicates. (Seneweera,unpublished.)




Table 6.1. Leaf photosynthesis (measured at 590 μmol m−2 s−1), RuBisCO, and N concentrationin flag leaf blade. Measurements were made 76–80 days after transplanting.

Growth [CO2] Flag leaf

Photosynthesis (at 590 μmol m−2 s−1) Ambient (FACE) 29.09 (20.43∗∗∗)RuBisco (g m−2) Ambient (FACE) 1.79 (1.25∗∗∗)N (g m−2) Ambient (FACE) 1.73 (1.44∗∗∗)

Source: Data adopted from Seneweera et al. 2002.Values are the mean of four replicates. The significant differences between CO2 treatments areshown and they are ∗∗∗ p ≤ 0.001

synthesis is suppressed during leaf expansionwhile RuBisCO degradation accelerated duringleaf senescence at e[CO2] (Fig. 6.3). However,repression of photosynthetic genes at e[CO2] isapparent only in senescing leaves and no rela-tionship was found between gene transcript andsoluble sugar (Ludewig and Sonnewald 2000).

In monocots, RuBisCO degradation is alwayspredominant after full expansion of the leaf bladeand leads to a rapid decline in RuBisCO content.RuBisCO degradation is accelerated at e[CO2]during leaf senescence in flag leaf blade of therice (Fig. 6.3). This could be an adaptive salvagemechanism in terms of nutrient remobilizationfor sink development as RuBisCO represents asignificant N store as well as its metabolic role.However, the mechanism by which e[CO2] ac-celerates RuBisCO degradation is not well un-derstood.

At e[CO2], the activity of antioxidative de-fense enzymes like superoxide dismutase, per-oxidase, catalase, ascorbate peroxidase, and glu-tathione peroxidase is lower (Schwanz et al.1996; Pritchard et al. 2000; Vurro et al. 2009).These enzymes are known to detoxify highly re-active oxygen species, possibly decreasing theenzyme activities leading to increases in the re-active oxygen concentration in the chloroplast,which could contribute to RuBisCO degradationat e[CO2].

Effect of e[CO2] on RuBisCO activity

As RuBisCO is the primary enzyme involved infunneling CO2 into the PCR, understanding itsregulation is important in developing strategies

to adapt crops to growing in e[CO2] environ-ments. RuBisCO has an extremely low catalyticcapacity compared to other enzymes and its invivo activity is regulated through a range of in-teractive mechanisms (Stitt and Schulze 1994).

RuBisCO activity is regulated through a re-versible carbamylation of a lycine residue of theenzyme and binding of Mg2+ (Lorimer 1981;Cleland et al. 1998). RuBisCO activation de-pends on the presence of the catalytic chaper-one and RuBisCO activase, which promotes theATP-dependent dissociation of inhibitory sugarphosphates, thereby promoting the carbamyla-tion reaction (Lorimer 1981). However, the roleof ATP-dependent RuBisCO activase on car-bomylation reaction is not well understood. Fur-ther, high concentrations of a RuBisCO inhibitor,2-carboxyarabintol-1-phosphate, have been re-ported in plants grown at e[CO2] (Allen at al.2000; Hrstka et al. 2007). In low light, RuBisCOis deactivated, and with increasing irradiance, theactivation state of RuBisCO increases and it isfully activated under e[CO2] when light levelsare over 1000 μmol m−2 s−1 (Bowes et al. 1991;Hrstka et al. 2007). However, when RuBisCOactivity is estimated from in vivo measurementsand compared with actual A at 1000 μmol CO2

mol−1, enzyme activity is 1.5- to 2.0-fold greater,suggesting that the efficiency of CO2 saturatedphotosynthesis is only 50–70% of potential A(Makino et al. 2000).

Deactivation of RuBisCO has been reportedwhen plants are exposed to e[CO2] for ex-tended periods (Sage et al. 1988; Theobaldet al. 1998). It has been suggested that a reduc-tion in RuBisCO content at e[CO2] is always




Vc,max

RuBisCO content (mass/unit area)

N (mass/unit area)

N (mass/unit mass)

Chlorophyll (mass/unit area)

Percentage change in elevated [CO2]

−40

Chlorophyll (mass/unit mass)

Sugar (mass/unit area)

Starch (mass/unit area)

Jmax

Vc,max:Jmax

−20 0 20 40 60 80 100

Fig. 6.4. Mean response of maximum carboxylation rate (Vc,max), maxi-mum rate of electron transport (Jmax), ratio of Vc,max : Jmax, RuBisCo content(mass/unit area), nitrogen content reported on both area and mass basis, chloro-phyll content reported on both area and mass basis, sugar and starch contentsreported on area basis, and ±95% CI. Number of species, FACE experiments,and individual observations for each response are given in Ainsworth and Long(2005). (Reproduced with permission).

associated with an increase in RuBisCO activ-ity (Fig 6.4; Cheng and Fuchigama 2000). Thishypothesis was supported by antisense rice with40% wild type RuBisCO, which when grownunder e[CO2], achieved a 100% enzyme activa-tion, suggesting that deactivation of this enzymeis an optimizing response to e[CO2]. Activationand deactivation of the enzyme during ontogenyhas also been reported (Seneweera et al. 2002).It has been suggested that the deactivation oractivation of RuBisCO under e[CO2] is a sec-ondary response to maintain the balance betweenRuBisCO and other processes that limit photo-synthesis (Seneweera et al. 2002).

Source and sink balance

While the capacity for C acquisition and uti-lization is a key to understanding how plantsrespond to e[CO2] (Paul and Foyer 2001), hav-ing appropriate sinks for the added C is equallyimportant in achieving that potential plant pro-duction. Grain yield may be limited by the rate

of supply (source) of photosynthate, the move-ment from source to sink and/or the sink activ-ity, and the present understanding is that sinkactivity is the main limit on grain filling incereals (Fischer 2007). Under e[CO2], specieswith the highest biomass growth response tendto have the largest sinks (Poorters and Navas2003).

If the assimilated C is not being utilized, therewould be an accumulation of assimilates in theleaves, resulting in the end-product inhibitionof photosynthesis (Neales and Incoll 1968; Pauland Foyer 2001). To overcome this constraint, ahigher metabolic or storage capacity is requiredto match high A at e[CO2]. Soluble carbohydrateand starch content increased by 52% and 160%on an average at e[CO2], across 32 experiments(Long et al. 1992). The extent to which starchand soluble sugars accumulate at e[CO2] variesamong species. For example, cotton preferen-tially accumulates starch, while fructans and su-crose are mainly accumulated by wheat and rice,respectively.




Variation in carbohydrate concentration in re-sponse to e[CO2] could be because carbohydratesynthesis is far in excess of that required forgrowth and utilization. Accumulation of sugarsand starch in leaves and stems causes feedbackinhibition of photosynthesis at e[CO2]. Improve-ment in biochemical efficiency of C utilization,so reducing this inhibition, is a key target forcrop improvement at e[CO2].

Two reports (Ziska et al. 2004; Ziska 2008)present comparative responses to e[CO2] amongearly and late 20th century wheat cultivars. [CO2]had a significant effect on all vegetative char-acteristics among cultivars, including increas-ing tiller number. Under e[CO2], tiller forma-tion was greater for earlier released cultivarsthan for later ones, so that the relative yieldincreases were greater for the earlier releasedcultivars. Ziska (2008) concludes that yield re-sponse to e[CO2] is still sink limited and that ad-dressing vegetative growth responses and the de-velopment of reproductive sink capacity amongcultivars may offer significant opportunities todevelop cultivars more responsive to e[CO2].This responsiveness to e[CO2] could be related to“indeterminacy,” which is the ability to set addedheads/seed sites in wheat (Ziska 2008) and soy-bean (Ziska and Bunce 2000). Ainsworth et al.(2004) compared soybean isolines differing indeterminacy and found that the less determinatetypes did respond more to e[CO2] although ge-netic differences in the amount of determinacyaffected the response.

Responses of N fixers to e[CO2]

Given the importance of N in determining thelikely response of plants to e[CO2], legumesshould be more responsive than nonlegumes astheir N supply is enhanced because they ex-change C for N with symbiotic partners. In cropsystems, legumes tend to be more responsivethan non-N fixers (Ainsworth and Long 2005).The photosynthetic stimulation of N-fixing soy-beans at e[CO2] was three times the stimula-tion of nonnodulated cultivars (Ainsworth et al.

2002). These changes are in accord with the gen-eral view that e[CO2] leads to lower leaf N con-tents in N-limited plants, but not necessarily inwell-fertilized or well-nodulated legumes.

The responses of legumes to e[CO2] do varyamong species (Lee et al. 2003; West et al. 2005)and may reflect different levels of determinancy,or the impact of nutrient limitations other than Nas growth is stimulated. Phosphorus and molyb-denum have been implicated in particular situa-tions as limiting e[CO2] responses although thiscould be considered a general limitation that ismade worse when C and N supplies increase(Rogers et al. 2009).

Effect of e[CO2] on product quality

In C3 plants, the decline in plant N concentra-tion associated with higher [CO2] is largely theresult of more carbohydrate, less RuBisCO (al-beit with higher activity), and lower N uptake.Most of the N that ends up in grain as proteinis remobilzed from vegetative organs. As a con-sequence, grain protein concentration (GPC) isgenerally decreased under e[CO2] (Kimball et al.2002; Hogy and Fangmeier 2009). The responsesof GPC to e[CO2] reported in the literature arevariable and are affected by N supply and en-vironmental factors such as water supply andtemperature, as well as rooting volume restric-tions (Hogy and Fangmeier 2009). Lower prod-uct quality under e[CO2] has also been reportedfor forage species (Milchunas et al. 2005), pota-toes (Hogy and Fangmeier 2009), and peanut(Burkey et al. 2007), and changed fatty acid com-position in soybean (Heagle et al. 1998).

Erbs et al. (2010) showed significant GPC de-clines in wheat and barley under e[CO2] as wellas lower grain S, Zn, and Ca concentrations.Wheat GPC decreased by 7.4% under e[CO2]and amino acid composition of the protein alsoaltered, which could also have affected flour rhe-ological properties (Hogy et al. 2009). These dataindicate that cereals grown under e[CO2], espe-cially where N is limited, will have lower grainquality.




Interactions of e[CO2] withclimate factors

In future agricultural systems with e[CO2], it isexpected that the climate will also be relativelydryer and warmer, especially at the mid-latitudes(Moise and Hudson 2008). While the general re-sponse to e[CO2] indicate improved water-useefficiency as more C is exchanged for less or thesame amount of water, the interaction with theseother climatic factors is very important to assessclimate change impacts. Asseng et al. (2004) in-vestigated the trade-off between the CO2 fertil-ization effect against reduced water supply andhigher temperatures in a cropping systems mod-eling study. They showed that e[CO2] increasedyield as long as N was not limiting growth. In-creased temperature and reduced water supplyreduced yields and the yield response to N supplyunder ambient and e[CO2]. Linking ecosystemscale modeling and FACE experimentation be-comes more important as leaf and plant responsemodels need to be able to realistically upscale ane[CO2] response to crop and ecosystem levels,and need to include temperature and water in-teractions to account for the other environmentalchanges expected.

Interaction with temperature

Photosynthesis, photorespiration, respiration,and transpiration are all directly or indirectlyregulated by temperature (Morison and Lawlor1999; Sage and Kubien 2007). In C3 plants,the optimum temperature for growth increasesunder e[CO2] (McMurtrie et al. 1992). This re-sponse to temperature and e[CO2] is largely me-diated through changes in the kinetic proper-ties of RuBisCO (von Caemmerer and Farquhar1981; Sage and Kubien 2007). At current at-mospheric [CO2], the specificity of RuBisCOfor CO2 is reduced over O2, which leads to in-creases in photorespiration at higher tempera-tures (Bowes 1991). Suppression of photores-piration at e[CO2] is widely reported and thiscould partly contribute to increases in the opti-

mum temperatures for C3 photosynthesis (Bowes1991; Sage and Kubien 2007). Accelerated plantdevelopment at e[CO2] is well documented andthis response can increase further at higher tem-perature (Jitla et al. 1997; Ghannoum et al. 2010).

Despite the significance of the interaction be-tween long-term CO2 enrichment and high tem-perature on plant growth and photosynthesis, ithas been scarcely investigated mainly becauseof the difficulty of raising temperatures withoutartifacts, such as changed vapor pressure deficit.

Interaction with water supply

The growth response to e[CO2] is usually main-tained or even increased under mild water stress(Samarakoon and Gifford 1996; Seneweera et al.2001), but under severe drought, the response ismuch smaller (Seneweera et al. 2001). In gen-eral, relative water content and leaf water po-tential decrease under water-limited conditions,which is linked to a reduction in photosyntheticcapacity (Lawlor and Cornic 2002). The reduc-tion in gs and lower transpiration rates are welldocumented at e[CO2], reserving water for pho-tosynthesis and growth (Ghannoum et al. 2001;Seneweera et al. 2001).

Other interactions

Korner (2006) suggests that there is a consen-sus in the literature that the nutrient cycle setsthe ultimate limit to a carbon-driven, long-termstimulation of plant production and an impor-tant aspect of this is the demand and supply ofN through the soil and plant system. Luo et al.(2004) provide evidence of progressive N limi-tation in a range of ecosystems, where mineral Ndeclines over time at e[CO2], if there is no new Ninput or decreases in N losses. The mechanismsleading to N limitation are complex but residueswith higher C:N ratios, increased rhizodeposi-tion stimulating mineralization of N from recal-citrant soil organic matter pools (de Graaf et al.2009) or changes in microbial populations couldall contribute. Even though PNUE increases




under e[CO2], further investigations on N dy-namics are warranted in both natural and man-aged ecosystems.

As well as [CO2] rising, ozone (O3) is also ris-ing, particularly in industrialized countries. Thepollutant O3 reduces both plant growth and yieldfor a range of species (Morgan et al. 2003), andthis suppression could counteract the stimulationof the higher [CO2]. Pikki et al. (2008) demon-strated that O3 and CO2 affected spring wheatgrain yield but in different directions and by dif-ferent means. O3 decreased grain size, while CO2

increased grain number per unit ground area.Those authors concluded that because they act indifferent ways, the negative effects of O3 wouldnot necessarily be balanced by e[CO2].

At an ecosystem level, e[CO2] is likely tocause changes in plant diseases (Chakrabortyet al. 2008; Lake and Wade 2009), tolerance toinsect herbivory by pests (Lau and Tiffin 2009),changes in defense signaling (Zavala et al. 2008),and plant–plant competitiveness (Brooker 2006).These interactions will lead to dynamic changesin both natural and managed ecosystems andwill require interdisciplinary approaches to man-aging these systems and implementing adaptivestrategies particularly to ensure food and ecosys-tem services security in the future.

Summary and future directions

There is now adequate evidence that the CO2

fertilization effect is occurring due to improvedphotosynthetic efficiency and will continue forC3 plants at least until the [CO2] reaches750 μmol/mol (Fig. 6.1). C4 plants are less likelyto respond, but in C3 plant, radiation, water andN use efficiencies all are expected to increasewith the outcome as increased growth and yield,and ultimately food security. The final outcomewill be moderated by water, temperature, andN supply as well as O3 and various ecosys-tem level impacts that are now starting to beunderstood.

It is apparent that current breeding strategiesare not necessarily selecting genotypes that are

responsive to e[CO2] (Ziska et al. 2004), so afresh approach will be needed using the rapidlyadvancing capabilities in functional genomics,genetic transformation, and synthetic biology,targeting traits that will provide cultivars ableto exploit what was—in evolutionary terms—scarce atmospheric carbon. Ainsworth et al.(2008c) and Sun et al. (2009) identified targettraits and genes that show promise for improv-ing photosynthesis. Therefore, the developmentof crop plants with high photosynthetic capac-ity low photorespiration and less sink limitationideotype is proposed. Strategic traits identifiedby Ainsworth et al. (2008c) include reengineer-ing the catalytic properties of RuBisCO and im-proving the rate at which RuBP is regenerated inthe Calvin cycle. They also proposed reducingthe sugar feedback inhibition by increasing sinkcapacity particularly through increasing biomassproduction, the number of reproductive sinks andtherefore seed/grain yield can be increased. Ex-ploiting the improved RuBisCO activity alreadyseen at e[CO2] could release N that can be de-ployed elsewhere in the plant such as in grainprotein.

The challenge to develop new cultivars willrequire a revised strategy evaluating hundreds orthousands of genotypes rather than the current4 or 5. This evaluation should consider theseresponses across a broad range of environmen-tal conditions, in experiments designed to testinteractions between e[CO2] and other factorssuch as temperature, water, and O3. Ainsworthet al. (2008a) proposed a new generation of largeFACE experiments that would contribute to thechallenge of understanding, and then adapting tothe challenges of a carbon-rich future.

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Crop Adaptation to Climate Change (Yadav/Crop Adaptation to Climate Change) || Plant Responses to Increased Carbon Dioxide