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Physiologia Plantarum 133: 705–. 2008 Copyright ª Physiologia Plantarum 2008, ISSN 0031-9317 REVIEW Impact of climate change on crop nutrient and water use efficiencies Sylvie M. Brouder* and Jeffrey J. Volenec Department of Agronomy, Lilly Hall of Life Sciences, Purdue University, 915 W. State Street, West Lafayette, IN 47907-2054, USA Correspondence *Corresponding author, e-mail: [email protected] Received 15 November 2007; revised 1 May 2008 doi: 10.1111/j.1399-3054.2008.01136.x Implicit in discussions of plant nutrition and climate change is the assumption that we know what to do relative to nutrient management here and now but that these strategies might not apply in a changed climate. We review existing knowledge on interactive influences of atmospheric carbon dioxide concen- tration, temperature and soil moisture on plant growth, development and yield as well as on plant water use efficiency (WUE) and physiological and up- take efficiencies of soil-immobile nutrients. Elevated atmospheric CO 2 will increase leaf and canopy photosynthesis, especially in C3 plants, with minor changes in dark respiration. Additional CO 2 will increase biomass without marked alteration in dry matter partitioning, reduce transpiration of most plants and improve WUE. However, spatiotemporal variation in these attributes will impact agronomic performance and crop water use in a site-specific manner. Nutrient acquisition is closely associated with overall biomass and strongly influenced by root surface area. When climate change alters soil factors to restrict root growth, nutrient stress will occur. Plant size may also change but nutrient concentration will remain relatively unchanged; therefore, nutrient removal will scale with growth. Changes in regional nutrient requirements will be most remarkable where we alter cropping systems to accommodate shifts in ecozones or alter farming systems to capture new uses from existing systems. For regions and systems where we currently do an adequate job managing nutrients, we stand a good chance of continued optimization under a changed climate. If we can and should do better, climate change will not help us. Introduction Climate change variables including precipitation (amount and distribution), temperature and atmospheric CO 2 con- centrations are expected to alter agricultural productivity patterns worldwide. Carbon dioxide is a plant nutrient, and atmospheric enrichment has the potential to enhance plant productivity. Schimel (2006) observed that, at least in some regions, agriculture may be one of the bright spots, ‘the silver lining in the climate change cloud’. But higher global temperatures and altered precipitation patterns are expected to accompany the higher CO 2 levels, and these factors may lessen or negate any pro- duction increases or even depress production below current levels. The myriad of modeling studies attempting to project the short- and long-term impacts of climate change on agriculture are consistent only in highlighting that the nature of the productivity change itself will vary. Realized yield changes will reflect differences in local environments as well as differences in access to seed and management technologies that may offset negative climate change impacts. Regardless, with any potential changes in agricultural productivity comes a potential for associated changes in crop nutrient use. Local potential yield levels are Abbreviations – AE, agronomic efficiency; FACE, free-air concentration enrichment; PE, physiological efficiency; Ps, net photosynthesis; Rd, dark respiration; UE, uptake efficiency; WUE, water use efficiency. Physiol. Plant. 133, 2008 705

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  • Physiologia Plantarum 133: 705–. 2008 Copyright ª Physiologia Plantarum 2008, ISSN 0031-9317

    REVIEW

    Impact of climate change on crop nutrient and water useefficienciesSylvie M. Brouder* and Jeffrey J. Volenec

    Department of Agronomy, Lilly Hall of Life Sciences, Purdue University, 915 W. State Street, West Lafayette, IN 47907-2054, USA

    Correspondence

    *Corresponding author,

    e-mail: [email protected]

    Received 15 November 2007; revised 1

    May 2008

    doi: 10.1111/j.1399-3054.2008.01136.x

    Implicit in discussions of plant nutrition and climate change is the assumption

    thatwe knowwhat to do relative to nutrientmanagement here and nowbut that

    these strategies might not apply in a changed climate. We review existingknowledge on interactive influences of atmospheric carbon dioxide concen-

    tration, temperature and soil moisture on plant growth, development and yield

    as well as on plant water use efficiency (WUE) and physiological and up-

    take efficiencies of soil-immobile nutrients. Elevated atmospheric CO2 will

    increase leaf and canopy photosynthesis, especially in C3 plants, with minor

    changes in dark respiration. Additional CO2 will increase biomass without

    marked alteration in drymatter partitioning, reduce transpiration ofmost plants

    and improve WUE. However, spatiotemporal variation in these attributes willimpact agronomic performance and crop water use in a site-specific manner.

    Nutrient acquisition is closely associated with overall biomass and strongly

    influenced by root surface area. When climate change alters soil factors to

    restrict root growth, nutrient stress will occur. Plant size may also change but

    nutrient concentration will remain relatively unchanged; therefore, nutrient

    removal will scale with growth. Changes in regional nutrient requirementswill

    bemost remarkable where we alter cropping systems to accommodate shifts in

    ecozones or alter farming systems to capture new uses from existing systems.For regions and systems where we currently do an adequate job managing

    nutrients, we stand a good chance of continued optimization under a changed

    climate. If we can and should do better, climate change will not help us.

    Introduction

    Climate change variables including precipitation (amount

    and distribution), temperature and atmospheric CO2 con-centrations are expected to alter agricultural productivity

    patterns worldwide. Carbon dioxide is a plant nutrient,

    and atmospheric enrichment has the potential to enhance

    plant productivity. Schimel (2006) observed that, at least

    in some regions, agriculture may be one of the bright

    spots, ‘the silver lining in the climate change cloud’. But

    higher global temperatures and altered precipitation

    patterns are expected to accompany the higher CO2levels, and these factors may lessen or negate any pro-

    duction increases or even depress production below

    current levels. Themyriad of modeling studies attempting

    to project the short- and long-term impacts of climatechange on agriculture are consistent only in highlighting

    that the nature of the productivity change itself will vary.

    Realized yield changes will reflect differences in local

    environments as well as differences in access to seed

    and management technologies that may offset negative

    climate change impacts.

    Regardless, with any potential changes in agricultural

    productivity comes a potential for associated changes incrop nutrient use. Local potential yield levels are

    Abbreviations – AE, agronomic efficiency; FACE, free-air concentration enrichment; PE, physiological efficiency; Ps, net

    photosynthesis; Rd, dark respiration; UE, uptake efficiency; WUE, water use efficiency.

    Physiol. Plant. 133, 2008 705

  • determined by prevailing climate, ambient CO2 and crop

    characteristics, but these yields are almost always limited

    by root zone resources such as nutrients and water and

    further reduced by pests and diseases (Goudriaan and

    Zadoks 1995). The interactive effects of soil moisture

    and nutrient availability are two key edaphic factorsthat determine crop yield (Ziska and Bunce 2007). The

    questionwe address here is whether such changeswill be

    ones we cannot anticipate based on our existing

    knowledge of plant mineral nutrition and soil fertility

    management. In other words, current nutrient manage-

    ment recommendations are based on an understanding of

    crop-specific needs for achieving expected yields and

    soil-specific nutrient supply characteristics. To whatextent does our existing knowledge remain useful under

    a changed climate? Addressing this question requires an

    assessment of the potential for global climate change

    factors to influence the physiological efficiency (PE) of

    nutrient usewithin the plant and to alter the availability of

    nutrients in soil and their transport through soil and across

    root membranes. In this review, we conduct an integrated

    analysis of whole-plant responses to global climatechange and couple this information to a mechanistic

    evaluation of root growth, nutrient availability in soil and

    ion movement and uptake at the root surface. It is

    important to note that the objective of this review is to be

    illustrative in addressing concepts and theory and not

    necessarily comprehensive. Our objective is to provide

    a conceptual framework useful for understanding how

    plant nutrient uptake may change in response to globalclimate change. Our focus is on agroecosystems where,

    when feasible, attempts are made to fertilize and remove

    nutrient constraints to production and where long-term

    sustainability requires replacement of nutrients removed

    in harvests. Studies on global climate change andmineral

    nutrition remain relatively sparse, with nitrogen being the

    primary focus of previous research. Several existing

    literature reviews have examined N and climate changeemphasizing key topics such as soil biodiversity (Chapin

    2003, Swift et al. 1998), water cycling (Pendall et al.

    2004), uptake kinetics (BassiriRad 2000) and soil C/N

    cycling in extreme environments (Hobbie et al. 2002).

    Thus, our focus is on potassium, and, to a certain extent,

    phosphorus and magnesium, the most commonly limit-

    ing macronutrients in agroecosystems other than N.

    Greenhouse gases and climate change

    Consent appears to be solidifying among even the most

    recalcitrant public and private sectors that our climate is

    changing. From the end of the last glaciation until about

    1750, ambient CO2 concentrations were approximately

    278 mmol mol21; currently, atmospheric concentrations

    are >370 mmol mol21 with a rate of increase of approx-

    imately 1 mmol mol21 year21 (Intergovernmental Panel

    on Climate Change 2007). Concomitant increases in the

    biogenic gasses methane and nitrous oxide have also

    been observed. Several factors including our insatiable

    appetite for fossil fuel, industrialization, vegetation de-struction and CO2 release from disturbed soils are

    considered critical contributors to elevated CO2. The

    current concentrations of greenhouse gasses are believed

    bymany to have already altered global climate, and there

    is some evidence that warming has already negatively

    impacted yields. Temperature records from the Northern

    Hemisphere show a temperature rise of approximately

    0.6�C within a 150-year period that is in sharp contrastto relatively constant temperatures of the preceding

    450 years (Mann et al. 1998). Across Europe, average

    wheat (Triticum aestivum L.) yields have increased mark-

    edly since the early 1960s, but rates of increase have

    been slower in more southern countries (e.g. Portugal

    and Spain) when compared with the UK and France;

    Schär et al. (2004) conclude that these yield trend dif-

    ferences reflect a regional, differential impact of thewarming since the early 1990s.

    The rate of increase in ambient greenhouse gas con-

    centrations is expected to accelerate, and CO2 concen-

    trations of 550 mmol mol21 are expected by 2050 (Raven

    and Karley 2006). Likewise, rate of increase in temper-

    aturewithin the next century are expected to bemarkedly

    higher than the changes occurring in the preceding

    century. For example, Schlenker et al. (2006) estimatedthat, relative to current conditions, US growing season

    temperatures will increase between 2.0 and 2.4�Cbetween 2020 and 2049, whereas dramatic increases

    (from 3.6 to 7.4�C) are expected to occur between 2070and 2099. Themean annual global surface temperature is

    projected to increase by 1–3.5�C by 2100 (Southworthet al. 2000), but, unlike CO2, the magnitude of temper-

    ature increase will vary regionally and be accompaniedby altered precipitation patterns. For the conterminous

    United States, Izaurralde et al. (2003) estimated average

    temperature increases over current ambient temperatures

    of up to 4.5�C by 2095, with marked differences amongagriculturally important regions. Climate change effects

    will be more intense in the Southern Great Plains than in

    the Cornbelt region (Table 1). Greater increases in both

    the maximum and the minimum temperatures arepredicted for the Southern Great Plains. Precipitation

    will increase at both locations but to a greater extent in

    the Cornbelt where runoff losses will also be higher.

    Evapotranspiration will increase in proportion to pre-

    cipitation in both regions.Water use efficiencies (WUEs),

    an estimate of plant growth per unit of water, are expected

    to decline to between 83% (Southern Great Plains) and

    706 Physiol. Plant. 133, 2008

  • 88% (Cornbelt) of current values by 2095.Models predictonly modest changes in water stress days per year at both

    locations, whereas increases in temperature stress days

    per year are expected to be pronounced, especially in the

    Southern Great Plains. These results agree in general with

    those of Schlenker et al. (2006)whoalso predicted greater

    growing season precipitation by 2099 but cautioned that

    site-specific water and temperature stress will occur,

    especially, in the Southern United States.

    Crop responses to climate change

    The extent to which these expected changes in ambient

    CO2 concentration, temperature and precipitation will

    influence agriculture is the subject of intense scientificstudy and debate. Because we are only on the cusp of

    climate change or in the earliest years of what is antic-

    ipated to be radical change in both mean and extreme

    conditions, crop models have been major tools for

    studying climate change scenarios. Crop growth, devel-

    opment and yield responses to climatic variability are

    a mixture of linear and non-linear functions. Changes in

    the mean, variability and rate of occurrence of extremesin temperature all affect crop processes but not necessar-

    ily the same processes (Porter and Semenov 2005).

    Photosynthesis and respiration can change continuously

    and non-linearly in response to incremental increases in

    temperature, but short periods of high temperatures can

    do disproportionate damage when coinciding with

    flowering or pollination. Likewise, mild water stress has

    a different effect than prolonged drought or flooding.Application of the Epic agroecosystems model to US

    climate change scenarios produced by the Hadley

    Climate Change model (Table 2) illustrates the differen-

    tial impact that climate change may have on crop

    productivity. Temperatures and rainfall increases coupled

    with ambient CO2 of 560 mmol mol21 are expected to

    improve general conditions for growth of all major crops

    in the US Cornbelt (Izaurralde et al. 2003; Fig. 1). Winterwheat production is predicted to be particularly bene-

    fited, presumably from better overwintering in more

    northerly regions. A companion study on yield variabilityof selected crops suggests that increased rainfall will

    reduce year-to-year variation in Cornbelt maize (Zea

    mays L.) yields (Reilly et al. 2003). In contrast, in the

    Southern Plains, alfalfa (Medicago sativa L.) is the only

    crop projected to benefit significantly from climate

    change (Izaurralde et al. 2003). For Southern Plains

    maize and wheat, fertilization benefits of increased CO2are canceled out by yield losses because of increasedtemperature and water stress; for soybean (Glycine max

    L. Merril), yields are expected to be reduced by more

    than 20%.

    As is often acknowledged by authors, results from

    climate change – yield impact modeling – vary widely.

    Izaurralde et al. (2003) remark that their results for US

    wheat and maize are more favorable than the earlier

    projections of Brown and Rosenberg (1999) who foundonly small increases in yield with a temperature increase

    of 2.5�C and large decreases in yield with a temperatureincrease of 5�C. The relative merits of the different resultscan be difficult to discern. Changes in assumptions

    pertaining to critical drivers such as the interannual

    variability of precipitation (intensity and occurrence) and

    temperature (extremes and their duration) can drastically

    alter model outcomes (Porter and Semenov 2005). Someregions of the world such as the central United States

    appear predisposed to respond more beneficially than

    others. Furthermore, the extent to which a given agricul-

    tural region is vulnerable to negative impacts of climate

    change reflects social and economic variables; projec-

    tions vary according to assumptions about levels of

    available technology and market forces (Reilly and

    Schimmelpfennig 1999). For example, Darwin et al.(1995) predict a 20–30% reduction in global cereal

    production without technology and market factors, but

    a 0.2–1.2% increase with these factors optimized. In

    a similar study, Rosenzweig and Parry (1994) specifically

    highlight the effect of differential access to technology in

    developing countries where available technologies may

    not overcome the negative impacts on global climate

    change. Finally, new results from free-air concentration

    Table 1. Present-day and future (2095) regional temperatures, precipitation and associated crop production-influencing factors as estimated by the

    Hadley Centermodel. Adapted from Izaurralde et al. (2003). aUS Cornbelt states areOhio, Indiana, Illinois, Iowa, andMissouri; U.S. Southern Plains states

    are Texas and Oklahoma. bWUE is plant or crop WUE.

    US regiona

    Maximum

    temperature

    (�C)

    Minimum

    temperature

    (�C)Precipitation

    (mm year21)

    Runoff

    (mm year21)

    Evapotranspiration

    (mm year21)

    WUEb

    (kg ha21 mm21)

    H2O stress days

    (days year21)

    Temperature

    stress days

    (days year21)

    Cornbelt Present 16.4 4.5 941 156 581 10.4 6.1 16.1

    2095 18.4 7.7 1195 194 774 9.2 5.6 18.2

    Southern

    Plains

    Present 24.7 10.5 727 86 568 9.8 19.4 13.6

    2095 27.8 14.2 815 85 642 8.1 19.8 17.4

    Physiol. Plant. 133, 2008 707

  • Table

    2.Im

    pactofelevated

    CO2onmajorplantprocesses

    andtheircomponen

    ts.

    Process

    Influen

    tialcomponen

    tRem

    arks

    regardingelevated

    CO2

    Referen

    ces

    Photosynthesis

    C3

    Single-leafrate

    Averageincrease

    of14%;individualincreasesas

    highas

    50%

    Longet

    al.(2006),New

    man

    etal.(2003),So

    ussan

    aan

    dLuscher

    (2007)

    Can

    opy

    Averageincrease

    of20%;individualincreasesas

    highas

    100%

    primarily

    asaresultofgreater

    single-leafrate

    andad

    ditionalleaf

    area

    per

    plant.Leaf

    angle,opticalp

    roperties

    ofleaves,plantheightan

    d

    verticalleaf

    distributionin

    thecanopywerenotalteredbyhighCO2

    Bunce

    (1995),Hillet

    al.(2007),Longet

    al.(2006),

    Soussan

    aan

    dLuscher

    (2007),Teughelset

    al.(1995)

    C4

    Single-leafrate

    Averageincrease

    of10%;individualincreasesas

    highas

    25%

    Longet

    al.(2006),So

    ussan

    aan

    dLuscher

    (2007)

    Can

    opy

    Averageincrease

    of6%;individualincreasesas

    highas

    30%

    Longet

    al.(2006),So

    ussan

    aan

    dLuscher

    (2007)

    Rd

    Tissuemassbasis

    Responsesrangefrom

    noinfluen

    ceofelevated

    CO2upto

    a

    40%

    reductionat

    elevated

    CO2

    Atkin

    etal.(2005),ElKohen

    andMousseau(1994),

    Hillet

    al.(2007),Zh

    aoet

    al.(2004)

    Can

    opybasis

    Noeffect;greater

    Rdbecau

    seofgreater

    totalb

    iomasswas

    offsetby

    increasedcanopyphotosynthesisat

    elevated

    CO2

    Dunnet

    al.(2007)

    Growth

    Biomass

    Averageincrease

    inyieldof17%;upto

    a66%

    increase

    inyield

    ofC3plants.Nobiomassresponse

    forC4plants

    Derner

    etal.(2003),Hillet

    al.(2007),New

    man

    etal.(2003),

    Soussan

    aan

    dLuscher

    (2007)

    Harvestindex

    Noeffect

    inC3plants;reducedslightlyin

    C4

    Longet

    al.(2006)

    Leaf:stem

    Noeffect

    tomodestincrease

    Barrettan

    dGifford

    (1995),Gueh

    letal.(1994)

    Root:shoot

    Effectsvary

    dep

    endingonspeciesan

    dman

    agem

    ent

    Barrettan

    dGifford

    (1995),Derner

    etal.(2003),Gueh

    letal.(1994),Hillet

    al.

    (2007),Maestre

    andReynolds(2006),So

    ussan

    aan

    dLuscher

    (2007)

    Storedreserves

    Tran

    sien

    tstorage

    inleaves

    Leaf

    sugar

    andstarch

    concentrationsincrease

    atelevated

    CO2

    ElKohen

    andMousseau(1994),Vuet

    al.(2002),Zh

    aoet

    al.(2004)

    Long-term

    storagein

    peren

    niatingorgan

    s

    Increasedconcentrationsin

    storageroots,

    rhizomes,stolonsan

    dstem

    bases

    Casellaan

    dSo

    ussan

    a(1997)

    708 Physiol. Plant. 133, 2008

  • enrichment (FACE) studies suggest that the beneficial

    effects of CO2 fertilization may be far less than had been

    suggested by previous experimentation with less sophis-

    ticated techniques – resultswhich have been used inmostmodeling studies to date (Long et al. 2006).

    In sum, climate will change but details regarding

    impact on agriculture remain vague. Mineral stressors on

    crop production are one of the many biotic and abiotic

    uncertainties that contribute to our inability to predict

    future food supply. Lynch and St Clair (2004) identified

    this as a critical gap in climate change studies, noting that

    most plant systems, natural and agricultural, havingsuboptimal nutrient availability and mineral stress inter-

    actions with global climate change variables are likely to

    be important but remain understudied. For agriculture,

    the obvious and practical question is whether nutrient

    inputs will need to increase or change to optimize

    productivity responses to climate change and to maintain

    or improve the overall use efficiency or agronomic

    efficiency (AE) of fertilizer nutrients. The AE of a unit offertilizer is the product of PE and uptake efficiency (UE)

    where internal nutrient use efficiency can be quantified

    by simple expressions that relate a plant’s productivity

    to its nutrient content. Gerloff and Gabelman (1983)

    proposed a general nutrient efficiency ratio that was

    a function of units of yield and units of nutrient. In

    managed systems, PE can be couched in terms of fertilizer

    units such that

    PE ¼ ðDyield; kgÞ=ðDtissue element content; kgÞ ð1Þ

    and

    UE ¼ ðDtissue element content; kgÞ=ðfertilizer increment; kgÞ ð2Þ

    In the absence of a large body of experimentation on

    the interactive effects of global climate change variableswith plant nutrition variables, existing knowledge regard-

    ing temperature and moisture impacts on UE and PE can

    be reevaluated within the specific context of anticipated

    physiological changes related to enhanced CO2 levels.

    While detailed mechanistic models exist for crop

    plants, for example, Hybrid Maize (Yang et al. 2004) or

    CERES-Maize (Jones and Kiniry 1986), for simplicity, we

    will describe the impact of CO2 on four processes: netphotosynthesis (Ps, gross photosynthesis minus photores-

    piration), dark respiration (Rd), growth and accumula-

    tion/use of stored organic reserves (primarily starches and

    fructans) that serve to buffer changes in photosynthesis.

    These components can be related to one another as

    follows:

    Net Ps2Rd ¼ growth 1 stored reserves ð3Þ

    The left side of Equation 3 (Net Ps 2 Rd) represents thenet carbohydrate that is produced by the plant and is thesource of 90–95% of plant dry mass. The remaining 5–

    10% comes from soil nutrients. The right side of Equation

    3 represents two alternative sinks for the net carbohy-

    drate: plants can use the carbon for irreversible growth or

    they can store the carbon for later use when demand for

    carbohydrate exceeds that supplied through photosyn-

    thesis (e.g. in darkness). While single-factor climate

    change experiments may reveal striking effects on plantperformance when supplied alone, when multiple global

    change factors are imposed simultaneously, adjustments

    in plant growth and physiological processes often dam-

    pen the overall response (Dermody, 2006). An integrated

    understanding of the responses of model components

    in Equation 3 to elevated CO2 will provide key insight

    into how important agronomic traits like yield, nutrient

    uptake and water use will respond to and interact withclimate change.

    Net photosynthesis

    Two distinct photosynthetic mechanisms occur in crops,

    C3 and C4, named for the number of carbon atoms in the

    initial organic molecules fixed by the plant. These plants

    are also referred to as having the Calvin–Benson cycle

    (C3) and the Hatch–Slack cycle (C4), and the contrasting

    Fig. 1. Projected percentage change in crop yields in 2095 for the US

    Cornbelt (Ohio, Indiana, Illinois, Iowa and Missouri) and Southern Plains

    (Texas and Oklahoma). Projections based on application of the Epic

    agroecosystems model to climate change scenarios produced by the

    Hadley Center model and assumes ambient CO2 concentrations of

    560 mmol mol21. Asterisk (*) identifies changes from current yields are

    significant (P � 0.10). Data adapted from Izaurralde et al. (2003).

    Physiol. Plant. 133, 2008 709

  • response of plants with these different photosynthetic

    mechanisms to environment including temperature and

    CO2 is one of the hallmark traits distinguishing one group

    from the other. The C4 plants generally have higher

    photosynthetic rates but are sensitive to cool temper-

    atures and as such are often referred to as ‘warm-season’plants. Representative agronomic species include maize,

    sorghum (Sorghum bicolor L. Moench), sugarcane

    (Saccharum officinarum L.) and bermudagrass (Cynodon

    dactylon L.). By comparison, C3 plants are well adapted

    to cool temperatures (referred to as ‘cool-season plants’)

    but have lower photosynthetic rates than C4 plants.

    Representative C3 species include soybean, cereals like

    wheat and rice (Oryza sativa L.), clover (Trifolium spp.),alfalfa and the cool-season grasses like ryegrass (Lolium

    perenne L.).

    There is general agreement that both single-leaf and

    canopy photosynthesis of C3 plants will increase more

    than that of C4 plants as atmospheric CO2 concentrations

    increase (Table 2). This is in part because of competitive

    inhibition of photorespiration by CO2 in C3 plants,

    a process that does not impact photosynthesis of C4plants. Results frommost FACE studies reveal that canopy

    photosynthesis of C3 plants increased primarily as a result

    of greater single-leaf photosynthetic rate and additional

    leaf area per plant (Table 2). However, exceptions to

    these general observations can be found in unique

    environments. Cook et al. (1998) compared growth of

    ecotypes ofNardus strictus that had grown for more than

    100 years at 790 mmol CO2 mol21 because of their

    proximity to naturally emitting CO2 springs in Iceland

    to that of ecotypes of this species growing in an adjacent

    area upwind where CO2 concentrations were 360 mmol

    mol21. They were surprised to find that ecotypes growing

    in elevated CO2 exhibited a 25% reduction in photosyn-

    thesis that was associated with less Chl and had lower

    amounts of key photosynthetic proteins when compared

    with the ecotypes grown upwind from the springs. Lessinvestment of resources into the photosynthetic mecha-

    nism may reflect the enhanced photosynthetic efficiency

    of the process at high CO2 that has occurred during

    100 years of adaptation to high CO2. If similar changes

    were to occur in other species in response to high CO2,

    higher PE of nutrient usewould result because less N,Mg,

    Fe, S and other nutrients directly involved in photosyn-

    thesis would be needed.

    Dark respiration

    Unlike photosynthesis, no fundamental differences in Rd

    exist between C3 and C4 plants. In general, Rd per unit

    tissue mass is unaffected or declines in plants exposed to

    elevated CO2 (Table 2). For example, Hill et al. (2007)

    reported that Rd of perennial ryegrass grown in a FACE

    systemwas reduced 26% at 600 mmol CO2 mol21 when

    compared with ambient CO2. However, Rd on a soil

    surface or canopy basis is often greater at elevated CO2because of greater biomass accumulation in response to

    high CO2, especially in C3 plants. Dunn et al. (2007)found that increased seasonal respiration because of

    higher biomass in a boreal forest ecosystem is offset by

    increased CO2 assimilation through photosynthesis and

    resulted in no net effect on season-long CO2 balance.

    Temperature is generally considered a key environ-

    mental factor influencingRd rate and one that is predicted

    to increase significantly with the accumulation of

    greenhouse gases (Table 1). The commonly held assump-tion is that Rd rate doubles for each 10�C increase intemperature. This concept has been recently challenged

    by Atkin et al. (2005) who reported no consistent change

    in respiration when tree species were allowed to

    acclimate to warmer temperatures prior to respiration

    measurement. Working with tall fescue [Lolium arundi-

    naceum (Schreb.) S.J. Darbyshire], we also observed

    acclimation of leaf Rd rate for plants acclimated to a 5�Cincrease in temperature prior to measurement (Volenec

    et al. 1984). The homeostatic nature of Rd with modest

    temperature increase (2–5�C) simplifies our prediction ofthe impact of greenhouse gases on components of our

    model (Equation 3) to focus primarily on the direct effect

    of CO2.

    Summarizing the effects of CO2 on Ps and Rd, this

    model predicts a modest increase in net carbohydratefixation (left side of Equation 3) in C4 plants because of

    their limited increase in photosynthesis and no or a slight

    decline in Rd in response to elevated CO2. By compar-

    ison, Ps of C3 plants is expected to increase, in some

    cases markedly, in response to elevated CO2. The in-

    crease in Ps, along with a decline in Rd, would result in

    greater net carbohydrate fixation in these species, carbon

    that can be used for growth and/or be stored (right side ofEquation 3).

    Growth

    The right side of Equation 3 provides two sinks for fixed

    carbon, growth and stored reserves. Because the effect of

    increased CO2 on Ps differs between C3 and C4 plants

    and because 90% or more of plant dry weight is derivedfrom this process, it is not surprising that growth responses

    of C3 and C4 plants also differ in response to elevated

    CO2 (Table 2). Growth of aboveground biomass of C3

    plants is often increased significantly by elevated CO2.

    Long et al. (2006) summarized biomass and yield data

    from several FACE studies and reported that C3 species

    produced an average of 16% more biomass and 13%

    710 Physiol. Plant. 133, 2008

  • greater grain yield at 550 mmol CO2 mol21 when

    compared with ambient CO2 concentrations. Neither

    biomass nor grain yield of C4 species was responsive to

    elevated CO2 in these studies. Responses of specific C3

    species can often be substantially greater. For example,

    Newman et al. (2003) grew tall fescue in a FACE systemand observed a 50–60% increase in dry matter pro-

    duction that was associated with a doubling of tiller

    production. Increased vegetative growth such as this

    often translates into greater grain yield because of

    a relatively constant harvest index (seed mass/total

    aboveground biomass) (Table 2). Jackson et al. (1995)

    reported greater biomass of Avena barbata in response to

    highCO2 andwith this a proportional increase in seed dryweight.

    Partitioning of dry matter among leaves, stems and

    roots also is an important consideration because greater

    aboveground biomass without a concomitant increase in

    root biomass could alter key processes like water and

    nutrient uptake and could lead to greater incidence of

    lodging. In addition, the nutrient composition of leaves,

    stems and roots differs considerably and so changingthe relative abundance of these organs will alter plant

    nutrient needs. Elevated CO2 does not alter or may

    slightly increase the leaf:stem weight ratio of plants

    whose growth is enhanced by CO2. For example, Guehl

    et al. (1994) observed increased growth of Quercus and

    Pinus species at 700 mmol CO2 mol21, but partitioning

    of dry matter between leaves, stems and roots was largely

    unaffected. By comparison, Barrett and Gifford (1995)reported that leaf:stem ratio of cotton (Gossypium

    hirsutum L.) increased with elevated CO2 and that this

    coincided with a decline in root:shoot ratio. However,

    most studies, including other research with cotton

    (Derner et al. 2003), have found little impact of elevated

    CO2 on root:shoot ratio. For example, Hill et al. (2007)

    grew perennial ryegrass in a FACE system and reported

    a 66% increase in shoot mass that was accompanied byan 83% increase in root biomass, resulting in no signi-

    ficant change in root:shoot biomass ratio. Thus, changes

    in plant biomass in response to elevated CO2, and

    not large changes in dry matter partitioning, are expected

    to drive changes in nutrient needs as climate change

    occurs.

    Stored reserves

    Several studies have examined the impact of elevated

    CO2 on transient accumulation of carbohydrate in leaves,

    and most have found that sugars and starches are often

    higher in leaves of plants grown at elevated CO2(Table 2). For example, Vu et al. (2002) reported higher

    single-leaf photosynthetic rates, lower transpiration rates

    and greater WUE in ‘Ambersweet’ orange [Citrus

    reticulata Blanco � (Citrus paradise Macf. � C. reticu-lata)] at 720 mmol CO2 mol

    21 when compared with

    360 mmol CO2 mol21. Starch accumulated to higher

    concentrations in late afternoon in leaves of plants in

    elevated CO2. Similar results were reported for cotton(Zhao et al. 2004) and chestnut (Castanea sativa L.) (El

    Kohen andMousseau 1994). Accumulation of these non-

    structural carbohydrates reflects the imbalance between

    photosynthesis and translocation that can occur when

    elevated CO2 increases net carbohydrate synthesis

    (Equation 1, left side).

    Less is known regarding the impact of elevated CO2 on

    accumulation of long-term carbohydrate reserves instorage organs. These reserves serve to buffer growth

    and Rd against reductions in photosynthesis and are

    particularly important in perennial plants. Likewise,

    when carbohydrate supply from photosynthesis exceeds

    growth and respiratory needs, as might happen in C3

    plants grown at elevated CO2, the additional carbohy-

    drate can accumulate in storage organs. For example,

    Casella and Soussana (1997) reported a 40% increase infructan accumulation in the pseudostem of wheat at

    700 mmol CO2 mol21 when compared with plants

    grown at 350 mmol CO2 mol21. A 3�C increase in

    temperature as might be expected to result from global

    warming exerted the same influence on fructan accumu-

    lation at 700 mmol CO2 mol21 in this species.

    In summary, plant growth responses to elevated CO2will be species dependent, with C3 plants being moreresponsive than C4 plants. Positive responseswill include

    higher photosynthetic rates, greater growth and higher

    yields.None of these changes are likely to requiremarked

    changes in tissue nutrient concentrations, and major

    changes in dry matter partitioning among organs (roots,

    stems and leaves) and harvest index are not expected.

    Therefore, overall PE for a given nutrient will likely

    remain unchanged. Nevertheless, larger plants withgreater yield may influence total water and nutrient

    uptake and could impact how plants will ultimately

    respond to global climate change.

    Water use efficiency

    Root-nutrient contact occurs primarily as a result of two

    processes: mass flow and ion diffusion. Water is a keycommon denominator in these processes, and bothmight

    be altered should plant water relations change markedly

    with climate change. In addition, transpiration from leaf

    surfaces consumes large quantities of energy through

    latent heat of vaporization, which serves to cool foli-

    age up to 5�C below prevailing ambient air tempera-tures. Changes in plant water use or reductions in water

    Physiol. Plant. 133, 2008 711

  • availability may significantly alter nutrient uptake and

    possibly increase tissue temperatures.

    One measure of whole-plant water use is WUE. WUE

    is calculated as the ratio of plant yield to water use

    [(kg ha21)/mm]. Species differ, with WUE of C4 plants

    often being twice that of C3 plants. This species differenceis primarily because of the advantage C4 plants have

    over C3 plants in rate of Ps. Another factor that increases

    WUE is partial stomatal closure, which generally reduces

    water loss out of a leaf more than it reduces CO2 uptake

    into the leaf, thus increasing dry matter accumulation

    per unit of water transpired. However, factors that alter

    transpiration will have a direct impact on mass flow of

    water to the root surface, and with it, alter the mech-anism of ion transport and possibly nutrient uptake

    (see below).

    Elevated CO2 alters yield in a species-specific manner

    as discussed above (Table 2) and also reduces stomatal

    conductance in many species. Bunce (1995) reported

    that leaf conductance was reduced in the high CO2 en-

    vironment to 77–86% of values found in ambient CO2conditions. However, Samarakoon and Gifford (1995)reported species differences in the effect of elevated

    CO2 on transpiration. For cotton, both transpiration and

    growth of cotton were increased at high CO2. In contrast,

    transpiration of maize was reduced at high CO2, and

    these plants exhibited only a modest increase in plant

    biomass. Wheat transpiration was not consistently

    affected by high CO2 even though plant growth was

    much greater under high CO2. Regardless of stomatalresponse,WUE of all species was greater at elevated CO2and total water use was reduced when compared with

    ambient CO2. Such shifts in water use might alter mass

    flow of nutrients to the root surface, change soil moisture

    patterns and increase foliage temperatures that could

    reduce photosynthesis. Chartzoulakis and Psarras (2005)

    suggested that, although high CO2 may improve plant

    WUE, reductions in precipitation and increased evapo-transpiration will reduce soil moisture in some parts of

    southern Europe. They predicted that this will reduce

    photosynthesis and alter soil fertility, including soil

    organic matter decomposition and nitrate leaching.

    However, Manderscheid and Weigel (2007) showed that

    the effect of drought was negated somewhat by elevated

    CO2 (550 mmol mol21). When compared with ambient

    CO2 conditions, high CO2 increasedWUE by 20% underwell-watered conditions but WUE increased by 42% in

    response to high CO2 under drought conditions. These

    authors concluded that the negative effects of climate

    change-induced drought will be mitigated by high CO2.

    Clearly, elevated CO2 will result in site-specific changes

    inwater availability, but increases inWUEand reductions

    in total water use are expected to influence key plant

    functions including root-nutrient contact and plant

    growth that, in turn, will alter total nutrient needs.

    Influence of climate change on nutrientavailability and acquisition

    Increases in air temperature and changes in precipitation

    will significantly impact prevailing root zone temperature

    and moisture regimes. The nature and extent of the

    change in these two parameters will be site- and soil-

    specific, reflecting meteorological conditions, soil phys-

    ical factors and other surface characteristics including

    leaf area index and ground litter stores (Kang et al. 2000).

    The primary function of roots is acquisition of nutrientsand water, and the successful root system is one that

    is adapted to the local conditions to optimize these

    functions. UE reflects a suite of physical, chemical and

    biological processes that determine whether a nutrient

    ion in the soil is in a form that is available to the root and

    whether the plant-available ion is actually acquired by

    a root. As reviewed by Jungk (2002), plant availability

    of nutrients in the soil is a function of soil chemicalproperties aswell as location of the ion relative to the root

    surface and the length of the pathway the nutrient must

    travel in the soil to reach the root surface; nutrient

    acquisition by the plant reflects an array of physiological

    phenomena that govern nutrient transport to and into

    roots and can alter aspects of both chemical and posi-

    tional nutrient availability in the soil. Given that soil

    moisture and temperature are primary determinants ofnutrient availability and root growth and development

    and that carbon allocation to roots governs nutrient ac-

    quisition, it is reasonable to expect that process outcomes

    will be reflective of the changed climate. Furthermore,

    there is a significant body of work that suggests the

    hypothesis that climate change impacts on nutrient UE

    will be primarily affected through direct impacts on root

    surface area. The foundation of this hypothesis is the largebody of crop modeling work conducted with process-

    based models such as the Barber family of single root

    models (Barber and Cushman 1981, Claassen and Barber

    1976, Cushman 1979, 1980, Itoh and Barber 1983).

    Plants accumulate nutrients from the soil solution pool,

    and nutrients must be in solution to be mobile in the soil.

    In the absence of roots, steady-state solution-phase

    concentrations of nutrient ions are controlled by adsorp-tion–precipitation and desorption–dissolution reactions

    between nutrients and the surface complex of soil,

    mineralization and immobilization for solutes of organic

    origin and additions from fertilizer (Table 3). Given the

    importance of C and N cycling to both agricultural

    productivity and sustainability, the preponderance of

    belowground climate change studies have focused on

    712 Physiol. Plant. 133, 2008

  • Table

    3.Im

    pactofclim

    atechan

    geonprocesses

    andparam

    eterscontrollingnutrientavailability.Forin-dep

    thdescriptionofparam

    eters,seeBarber

    (1995).

    Nutrient

    availability/acquisition

    attribute

    Soil/plantcontrols

    Controllerparam

    eters

    Rem

    arks

    regardingglobalclim

    atechan

    ge

    Presen

    ceofnutrients

    insoilsolution

    Adsorption/desorption

    Buffer

    power

    (b),Temperature

    (T),pH,soilmoisture

    (u)

    andsolutionionicstrength

    (m)

    IncreasedTmay

    increase

    process

    rates;increasedCO2

    may

    enhan

    cerootexudates

    that

    alterb,

    enhan

    cefinerootgrowth

    andturnover;chan

    ges

    inu

    causedbychan

    ges

    inrainfallpatternsmay

    enhan

    ce

    ordep

    ress

    processes.IncreasedTmay

    enhan

    cevolatilization

    ofsurface-ap

    pliedNfertilizers;chan

    ges

    inrainfallpatterns

    may

    enhan

    ceordep

    ress

    volatilizationan

    dleaching

    losses

    ofnutrients

    Mineralization/im

    mobilization

    u,T,organ

    icmatterquality/quan

    tity

    andmicrobialactivity

    Fertilization

    Source,

    timing,rate

    andplacemen

    t

    Nutrientmovemen

    tMassflow

    u,soilphysicalproperties

    includingbulkden

    sity

    andhydraulic

    conductivity,soilsolutionconcentration(C

    l)

    andwater

    influxrate

    into

    roots(v0)

    IncreasedCO2may

    reduce

    tran

    spiration,dep

    ressing

    nutrientmovemen

    tto

    therootthroughmassflow

    butmay

    increase

    rootexudationan

    dfinerootgrowth

    enhan

    cingb,

    Clan

    dnutrientmovemen

    tthroughdiffusion.Increased

    Twillalso

    enhan

    cenutrientdiffusion;chan

    ges

    inucausedby

    chan

    ges

    inrainfallpatternsmay

    enhan

    ceordep

    ress

    mass

    flow

    and/ordiffusion

    Diffusion

    u,tortuosity

    (interactivew/u

    andphysicalproperties),

    T,ban

    dnutrientuptake

    Nutrientuptake

    Morphologyan

    darchitecture

    Length,diameter,surfacearea,branchingan

    dspatial

    distribution,distance

    betweenroots,roothairsan

    d

    specialized

    structures

    Elevated

    CO2may

    enhan

    cefinerootdevelopmen

    t.IfT

    issuboptimal,increasedTwillen

    han

    cerootsurfacearea

    developmen

    t;chan

    ges

    inucausedbychan

    ges

    inrainfall

    patternsmay

    enhan

    ceordep

    ress

    massflow

    and/ordiffusion.

    Intheo

    ry,elevated

    CO2should

    makemore

    carbohydrate

    availableforactive

    uptake

    Kinetics

    Tran

    sporter

    capacity(I m

    ax,maxim

    um

    uptake

    rate),affinity

    (Km,theMichaelis–M

    entonconstan

    t)an

    defficien

    cy

    (Cmin,minim

    um

    soilsolutionconcentrationat

    which

    net

    uptake

    canstilloccur)

    Physiol. Plant. 133, 2008 713

  • microbiology. Biological transformation betweenorganic

    and inorganic pools is strongly influenced by moisture

    and temperature, and thus, global climate change may

    strongly influence solution concentrations of N as well as

    S. Some have speculated that soil C pool size will not

    change as increased soil respiration and decompositioncaused by soil warming will be moderated by the

    increased C supply belowground (Kirschbaum 2000).

    Others, however, note that interactive and indirect effects

    of water and soil nutrient availability may lead to

    unexpected outcomes as uncertainties abound in our

    understanding of key feedback processes (Pendall et al.

    2004). For example, many expect elevated CO2 to in-

    crease belowground C that will, in turn, enrich micro-bial C, but Zak et al. (2000) reviewed the literature

    on microbial C and N responses to elevated CO2 and

    found reports of increases, decreases and no change. For

    N, the review of Pendall et al. (2004) suggests that

    increased CO2may not exert a significant direct effect on

    N mineralization per se but associated warming can

    cause increased N mineralization, leading to increased

    solution-phase N. While few, if any, studies have ex-amined impacts of elevated CO2 on solution-phase

    concentrations of nutrients such as K whose availability

    is not strongly controlled by biological activity, theory

    suggests that any impacts will also be indirectly mediated

    by temperature and moisture changes. Rates of adsorp-

    tion/desorption reactions will accelerate with increased

    temperature, and changes in soil moisture may further

    modify reactions by altering the ionic strength of the soilsolution. However, uncertainties surrounding the magni-

    tude of temperature increases coupled with the spatial

    and temporal variation in soil moisture make it challeng-

    ing to predict how climate change will impact plant K

    availability.

    Almost 50 years ago, Barber proposed that nutrient

    transport through the soil matrix toward roots occurred

    by two simultaneous processes: mass flow and diffusion(Barber 1962). As a plant transpires, solution-phase nutri-

    ents are transported in the convective movement of water

    in the bulk soil toward root surfaces. Quantitatively, mass

    flow contributions to a nutrient’s acquisition are the

    product of the volume of water transpired (v0) and the

    mean solution-phase concentration (Cl, Table 3). For

    nutrients that are highly buffered and maintained at low

    solution-phase concentrations, mass flow does notdeliver sufficient quantities to the root surface. Therefore,

    in the presence of a growing root, concentrations of these

    nutrients in the solution immediately adjacent to the root

    surface will be depleted. Movement by diffusion is

    a function of an ion’s diffusivity in water, the water

    content of the soil, the tortuous nature of the pathway an

    ionmust travel to reach the root, the buffer power and the

    concentration gradient created by root uptake (Table 3).

    Barber models and other, similar single- and multi-root

    models integrate equations for mass flow and diffusive

    flux with equations that characterize development of the

    root system and transport across the root membrane, the

    latter often based on Michaelis–Menton kinetics tocharacterize plant uptake as a function of ion concentra-

    tion at the root surface (see Silberbush 2002 for a brief

    review of models and their features).

    Root surface area and diffusive flux

    Previously and again today, as we consider the impacts of

    climate change, the value of these models is that theyallow us to explore specific aspects of UE, factors and

    processes that are complex, concomitant and non-linear

    and that are time consuming, expensive and extremely

    difficult to assess with direct experimentation. Indeed,

    questions of the impacts of temperature and moisture on

    nutrient availability are not new, even if the specific

    condition of elevated CO2 has yet to be explicitly

    addressed. Ching and Barber (1979) examined the effectof increasing root zone temperature from 15 to 30�C onavailability and uptake of K by maize seedlings. Raising

    root zone temperature increased nutrient uptake in both

    fertilized and unfertilized treatments (Fig. 2A). They also

    observed a positive impact on both availability and

    uptake factors. At 30�C, root surface area was increasedapproximately 70% at high and low K fertility; K diffusive

    flux increased 160 and 50% in low- and high-fertilitytreatments, respectively. Mackay and Barber (1984)

    observed a similar effect on maize P accumulation with

    a more moderate temperature comparison (19 vs 25�C;Fig. 2B). Again, marked increases in root surface area at

    both high- and low-fertility levels accompanied one- to

    two-fold increases in nutrient uptake. Temperature

    impacts on diffusive flux were again apparent, although

    much smaller in magnitude than the changes in rootsurface area. While changes in temperature with global

    climate change are expected to be substantially smaller

    than the experimental treatments used in these studies,

    there is no reason to expect responses to be different other

    than in magnitude. Mackay and Barber (1985) also

    examined the effect of drought on P uptake and avail-

    ability and found reduced nutrient uptake, root surface

    area and ion diffusivity with moisture stress for bothhigh and low fertility (Fig. 2C). In this study, the mois-

    ture treatments are directly meaningful in the context

    of climate change scenarios.

    For many, the observation that increasing soil moisture

    and temperature from suboptimal to optimal conditions

    increases nutrient diffusion and root growth will

    seem obvious. Following the Stokes–Einstein equation,

    714 Physiol. Plant. 133, 2008

  • diffusion of an ion in water is a direct function of both

    temperature and viscosity; viscosity itself is a function oftemperature (Barber 1995). At 15�C, the rate of diffusionis only 78% of the rate at 25�C (Weast 1982). Ion dif-fusivity rates in soil are a direct function of ion diffusiv-

    ity inwater and soilmoisture content. At low soilmoisture

    content, the diffusion pathway becomes longer as ions

    must travel around expanded air pockets. Likewise, cell

    expansion requires adequate water, and species-specific

    temperature optimums for root growth have beenextensively documented (for a review, see McMichael

    and Burke 2002). However, moving beyond the obvious

    effects of temperature and moisture on availability and

    acquisition, the more difficult and relevant question

    concerns the extent to which a specific factor or suite of

    factors contributes to observed reductions in nutrient

    uptake. In their study on soil moisture and P, Mackay and

    Barber (1984) reported a strong, linear relationship(r2 ¼ 0.96) between root surface area and P uptakeacross three soils and three moisture levels. They did not

    report the relationship between diffusive flux and P

    uptake but plotting their tabular data finds amuchweaker

    relationship (r2 ¼ 0.36, P ¼ 0.053; data not shown),suggesting that root surface area reductions may be more

    directly important for P uptake. Separate sensitivity

    analysis for model performance in predicting both P andK uptake supports this conclusion (Silberbush and Barber

    1983a, 1983b). For both nutrients, varying one model

    parameter while holding all others constant identified

    root growth rate as the single most influential factor

    governing nutrient uptake. Increasing diffusivity did not

    greatly increase uptake but, within the parameter ranges

    explored, proportional decreases in diffusivity reduced

    uptake as much as corresponding changes in root surface

    area.Certainly, such sensitivity analyses have their short-

    comings. In its most simple form, the approach overlooks

    parameter interdependence, and not all parameters

    are equally amenable to change. But a more thoughtful

    tinkering with parameters coupled with targeted exper-

    imentation over widely varied plant–soil systems can

    produce solid working hypotheses. As reviewed by

    Brouder (1999), investigations of K accumulation byflooded rice (Teo et al. 1992), slash pine seedlings grown

    alone and in combination with other species (Van Rees

    et al. 1990) and cotton grown in a range of soil conditions

    (Brouder and Cassman 1994a) also identified root geo-

    metry (length and diameter) as highly sensitive and a

    potentially dominating parameter controlling K accumu-

    lation. Direct evaluations of genotypic differences in root

    geometry and K acquisition efficiency of soybean (Silber-bush and Barber 1984), corn (Schenk and Barber 1980)

    and cotton (Brouder and Cassman 1990, 1994b) serve to

    further substantiate the relative importance of root growth

    when compared with other nutrient availability and

    acquisition factors for uptake of relatively immobile

    nutrients.

    These observations on the importance of root explora-

    tion of the soil by enhanced root surface areamay seem tobode well for a changed climate where CO2 fertilization

    could increase C available for building additional fine

    roots. If root:shoot ratios remain constant but the overall

    plant is bigger (as discussed above), there may be more

    potential for an enlarged root system to capture the

    relatively immobile nutrients. The environment of the

    root system is extremely heterogeneous in time and

    Fig. 2. The effect of temperature or moisture on nutrient uptake of maize and on selected soil availability and root acquisition parameters. Data are

    shown as percentage change from the baseline condition. Data are adapted from experiments where (A) root zone temperatures were increased from15

    to 29�C in an unfertilized soil and a soil receiving 500 mg K g21 soil (Ching and Barber 1979), (B) root zone temperatureswere increased from18 to 25�Cin a low- and high-P fertility soil (Mackay and Barber 1984) and (C) root zone soil moisture was reduced in soil water potential from233 to2170 kPa in

    a low- and high-P fertility soil (Mackay and Barber 1985).

    Physiol. Plant. 133, 2008 715

  • space; the adaptation of extreme phenotypic plasticity to

    exploit such an environment is a key attribute of success

    (Fitter 2002). Crop plants are expected to be particularly

    plastic in response to patchy nutrient availability as such

    plants were initially not only adapted to but also

    improved in their ability to be strongly responsive toenhanced nutrient supply. As documented in classic

    experiments by Drew, fine roots proliferate in zones

    enriched with nutrients, particularly NH14 , NO23 and P

    (Drew 1975, Drew and Saker 1975, 1978, Drew et al.

    1973). This phenomenon has been repeatedly shown

    both in controlled environment and in the field for many

    major crop species [e.g. sorghum-sudangrass (Pothuluri

    et al. 1986), winter wheat (Newman and Andrews 1973),corn (Zhang and Barber 1993) and cotton (Brouder and

    Cassman 1994b)]. As summarized in several reports

    (Lynch and St Clair 2004, Pendall et al. 2004), a few

    studies have suggested that root architecturemay respond

    to elevated CO2. For example, Pritchard and Rogers

    (2000) proposed that elevated CO2 would stimulate

    lateral branching, particularly in surface horizons. But

    such responses and/or their benefits may be conditionalupon other climate change variables and the quantity and

    distribution of nutrients. Some studies have suggested that

    elevated CO2 may help negate the impact of increased

    temperatures that exceed the optimum for root growth

    (Bassow et al. 1994, Wan et al. 2004). In studies of

    amodel grassland,Maestre and Reynolds (2006) reported

    that belowground biomass increased in response to high

    CO2 but only if high levels of nutrients were provided;root proliferation into nutrient patches increased with

    increasing nutrient availability but was not influenced by

    ambient CO2. As can readily be seen with modeling

    studies, root proliferation is of no benefit if roots are

    competing with each other. Thus, we may be headed

    toward a not too surprising conclusion that growing

    a bigger plant with CO2 fertilization may require en-

    hanced nutrient inputs.

    Water influx and mass flow

    In general, model simulations for immobile nutrients

    have not been very sensitive to changes in the rate of

    water influx into the root (Silberbush and Barber 1983a,

    1983b), a point relevant to discussions of the positive

    influence of CO2 fertilization on plant WUE. Underconditions of reduced transpiration, some have theorized

    that acquisition of nutrients that travel frombulk soil to the

    root surface primarily by mass flow will be negatively

    affected, resulting in nutrient deficiency (Lynch and St

    Clair 2004). Nutrients long considered to be delivered

    primarily bymass flow include soil-mobile nutrients such

    as nitrate and sulfate and soil-exchangeable nutrients

    such asMg andCa that are abundant in the solution phase

    but required in relatively small quantities by the plant

    (Barber 1995). However, reducing mass flow to a point

    where it restricts nutrient delivery but does not cause

    a more direct effect of water stress (e.g. reduced root

    growth) seems unlikely. Diffusion and mass flow are notmutually exclusive deliverymechanisms; the process that

    dominates is not an attribute of the nutrient itself but

    a reflection of root zone conditions. When the product of

    water uptake per unit root surface area (v0) and ion

    concentration in the soil solution (Cl) are equivalent to the

    plants needs (Imax, Table 3), mass flow will clearly be

    the dominant mode of solute transport to the root (in the

    context of the Cushman–Barber model, v0Cl ¼ Imax), butwhen v0Cl < Imax, diffusion contributes to nutrient trans-

    port. The Ching and Barber (1979) study discussed above

    can be used to illustrate this point. Adding 500 mg K g21

    soil increased v0Cl from 3.2 � 1028 to 4.8 � 1026 mmolcm22 s21, while Imax remained constant at 5.6 � 1027mmol cm22 s21, switching the dominant transport pro-

    cess from diffusion to mass flow (at 15�C, calculatedfrom Ching and Barber 1979). Rerunning the model(Version 1.1, Oates and Barber 1987) and reducing v0to 1 � 1027 cm s21, a >85% reduction does not effectsimulated K uptake for either fertility treatment (

  • root acquisition of P from low P soils. BassiriRad (2000)

    proposed that altering nutrient uptake to meet plant needs

    in a changing environment would be best accomplished

    by focusing on high-affinity nutrient transporters and their

    kinetic parameters. In theory, elevated CO2 should permit

    upregulation of transporters as there would be a higheravailability of carbohydrates to meet transporter energy

    requirements (Bielenberg andBassiriRad2005).However,

    the effectiveness of molecular engineering the kinetic

    aspects of nutrient uptake to negate the consequences of

    global change has not been critically evaluated.

    The advent of molecular techniques has made it

    possible to examine the importance of gene expression

    for regulation of nutrient uptake across the cell mem-brane. We explored the impact of expression of high-

    affinity P transporters on tobacco (Nicotiana tabacum L.)

    growth and P uptake (A.S. Berg, 2004, Thesis, Purdue

    University, West Lafayette, IN, USA). Expression of high-

    affinity P transporter genes from yeast and Arabidopsis,

    driven by a constitutive promoter and measured as

    transcript abundance, was very high in both root and

    shoot tissues. Two control groups were included: trans-genic plants containing the transformation vectorwithout

    a P transporter insert and a commercial tobacco cultivar,

    W-38. Plants were grown for 7 weeks in soils that had

    either low or high soil test P concentrations, and dry

    weights and plant P content were measured 4, 5, 6 and

    7 weeks after transplanting. As expected, plant growth

    andP uptakeweremuchgreater in the high-P soil than the

    low-P soil (Fig. 3). Growth and P uptake of the transgenicplants containing the high-affinity P transporters were

    similar to the transgenic control plants without the P

    transporter insert in both soils. At week 4 in high-P soil,

    growth of the commercial cultivar W-38 was less than

    both plants transformed with P transporters, and P uptake

    of W-38 was reduced when compared with the trans-

    formed control plants. However, by week 7, P uptake of

    W-38 in the high-P soil was greater than that of the otherplants. There was no influence of overexpression of either

    yeast or Arabidopsis P transporter gene on P uptake and

    plant growth in the low-P soil.

    To date, our study is one of only a very limited number

    of studies where transgenic approaches to improve

    nutrient uptake have been examined in soils. Recently,

    Park et al. (2007) have reported that constitutive ex-

    pression of a high-affinity P transporter from tobaccocould increase tissue P concentrations of rice. Although

    these authors observed higher instantaneous uptake rates

    of 32P in transgenic plants compared with untransformed

    control plants, total P uptake was not reported because

    tissue mass data were not assessed. Therefore, the re-

    ported growth reductions (qualitative results only) were

    possibly confounded with observations of higher tissue P

    concentrations. Surprisingly, a comprehensive survey of

    the literature revealed no published reports focusing on

    upregulation of K transporters and its impact on K uptake

    from soil. Numerous studies have reported induction of

    K transporters in roots exposed to low media (not soil) K

    concentrations (Ashley et al. 2006 and references cited

    therein) and imply that these changes are essential to

    maintain rapid K uptake as solution K concentrationsdecline. However, Garciadeblas et al. (2007) recently

    suggested that K transporters may have broader functions

    in plants including high-affinity K uptake, K efflux into the

    media to reduce tissue K concentrations and as a link

    between K nutrition and root morphogenesis. This sug-

    gests that the roles of K transporters may go beyond

    merely facilitating K uptake across the plasmamembrane

    at low K concentrations. Clearly, even without climatechange as an additional variable, we posses only a rudi-

    mentary understanding of the role of transporters in

    nutrient uptake from soil.

    Fig. 3. Trends in total biomass and plant P uptake of tobacco lines grown

    in high- and low-P soils during weeks 4–7 posttransplanting. Two lines

    contained constitutively expressed high-affinity P transporter genes from

    yeast and Arabidopsis, one control line was transformed with the vector

    alonewithout a P transporter gene and the fourth linewas the commercial

    cultivar W-38. Asterisks indicate dates where significant differences

    between W-38 and the other lines occurred (see text for details).

    Physiol. Plant. 133, 2008 717

  • Under P-limited conditions, upregulation of P trans-

    porters is just one of several known physiological mech-

    anisms plants can use to enhance P uptake. A key

    additional physiological mechanism is the secretion of

    organic acids (Sánchez-Calderón et al. 2006), also an

    important factor for mobilizing other, relatively insol-uble nutrients including Fe (Lynch and St Clair 2004).

    Theoretically, enhanced allocation of C belowground as

    a result of global climate change could alter the quantity

    and quality of exudates that may benefit nutrient uptake

    in soils where acidity or alkalinity limit nutrient solubility.

    As reviewed by Lynch and St Clair (2004), only a few

    studies have critically examined this hypothesis, and

    results to date have been mixed; Norby et al. (1987),Hodge (1996) and Uselman et al. (2000) found no effect

    of elevated CO2 on exudates, while Hodge and col-

    leagues observed reduction in volume and changes in

    composition of exudates (Hodge and Millard 1998,

    Hodge et al. 1998). As repeatedly remarked in the liter-

    ature, the area of root uptake responses to global climate

    change are understudied and requiremuchmore intensive

    study (BassiriRad 2000, Lynch and St Clair 2004, Pendallet al. 2004).

    Conclusions: managing plant nutrition ina changed climate

    What are the practical implications of the above

    discussions? First and foremost is the concept that crop

    plants may be bigger, smaller or similar in size whencompared with today’s specimens, but their nutrient

    content and PE will be scaled according to size. To date,

    experimentation on crop plants has not found conclusive

    evidence that PE is altered in high CO2 environments

    (Long et al. 2006). The observation of Schimel (2006) that

    ‘Some set of biological processes appears to operate to

    reduce the impact of CO2 on realized gains in biomass

    and yield below that expected from the effects ofphotosynthesis.’ can be viewed as a simple restatementof the Law of the Minimum within the context of global

    climate change. Clearly, nutrient stress has the potential

    to reduce growth stimulation by elevated CO2 (Campbell

    and Sage 2006, Lynch and St Clair 2004). Modest, crop-

    specific benefits in agricultural yieldsmay be realized but

    only where nutrient availability can be optimized and

    where climate change increases temperatures to a spe-cies-specific optimum and changes precipitation patterns

    to reduce water stress (drought or flooding) days. C3

    species may also accrue a direct benefit from CO2fertilization. Nutrient recommendations for a changed

    climate will operate on the same premise as current

    recommendations – an understanding of the PE that is

    specific to the crop and of the UE that is specific to the

    unique combination of crop and soil. Simple, empirical

    models will continue to be used to translate this in-

    formation from theory into practice. We anticipate that

    major portions of today’s soil fertility/plant nutrition

    recommendations will remain viable irrespective of

    climate change.

    Implications for nutrient management

    Nutrient replacement is a core tenet of many existing

    recommendations for sustainable management of rela-

    tively immobile nutrients. If plants produced under

    elevated CO2 are simply bigger, but otherwise the same

    in their gross nutrient content per unit biomass, thenpresent-day nutrient balance calculations for fertilizer

    recommendationswill remain applicable. In crop species

    that have been extensively improved for agriculture,

    nutrient concentrations, especially in grain, can be

    relatively constant when yields are not limited by other

    factors. Dobermann et al. (1996a) examined irrigated rice

    yields and grain composition in the Philippines, Indo-

    nesia, Vietnam, China and India and determined that theK concentrations of modern rice varieties were fairly

    constant across environments. Fifty percent of all samples

    analyzed ranged from 2.5 to 3.3 mg kg21. In a 6-year

    study conducted at five locations on widely varying soils,

    we have also documented relatively constant nutrient

    concentrations in high-yieldingmaize and soybean grain.

    Across site-years, P, K and Mg concentrations in maize

    grain (yields >10 000 kg ha21) averaged 3.3, 3.9 and1.3 mg kg21, respectively; P, K andMg concentrations in

    soybean grain (yields>3500 kg ha21) averaged 5.5, 18.3

    and 2.4 mg kg21, respectively (Table 4). Standard devia-

    tions in nutrient concentrations were relatively similar

    between species, although coefficients of variation

    tended to be lower in soybean, reflecting its higher

    concentration values. When these average removal

    values are used to estimate actual crop removal over thefull range of yielding environments, the relationship

    between predicted and measured values is very strong.

    For example, the predicted:measured relationship for

    yearly K removal is close to unity for both crops (Table 4,

    Fig. 4A). The predicted:measured relationship for 6-year

    cumulative removal of a maize–soybean rotation has

    a 1:1 relationship across all locations (Fig. 4B).

    Therefore, provided we continue to pursue a nutrientreplacement philosophy, changes in regional input re-

    quirements will be most remarkable where we alter the

    cropping system to accommodate shifts in crop ecozones

    or alter the farming system to capture new uses from

    existing systems (e.g. use of whole-plant maize for bio-

    fuels). Climate change may disproportionately increase

    the risks of growing one crop species when compared

    718 Physiol. Plant. 133, 2008

  • with an acceptable alternative. Southworth et al. (2000)suggest that variation by 2050 may increase risks

    associated with growing maize in southern regions of

    the Cornbelt, and growers may elect to modulate risk by

    growing a different crop that is better suited to the

    emerging ecozone. These authors suggest that growers

    may benefit fromplanting indeterminant crop species like

    soybean in place of maize to deal with the greater

    potential risks associatedwith increased climate variationand, at the same time, derive benefit from increased CO2that occurs when growing a C3 crop species.

    Changes in demand for agricultural products may also

    cause dramatic changes in regional requirements for

    nutrient inputs. Shortages of fossil fuels and an aggressive

    bioenergy agenda shifted large areas of the US Cornbelt

    from a maize–soybean rotation to continuous maizeproduction in 2007. Despite lower grain concentrations

    of all nutrients (Table 4), maize’s higher yields and lack of

    N2 fixation will significantly increase input requirements

    for P and N, although K input requirements will be

    reduced. In grain crops where cellulosic biomass may

    eventually also be harvested, nutrients removed in

    residue will need to be replaced and this could require

    significant new inputs. For the 74 million ha of irrigatedrice in Asia, Dobermann et al. (1996a) estimate that

    harvesting straw for fuel will increase crop K removal

    at least five-fold from 0.9–1.2 million t year21 to 5–9

    million t year21. Furthermore, residue removal itself

    may reduce soil nutrient supply as residue return both

    protects against soil erosion loss and replenishes soil

    Table 4. Nutrient concentrations in high-yielding maize and soybean grown in Indiana, USA. For all observations, maize (n ¼ 358) and soybean(n ¼ 474) yields exceeded 10 and 3.5 Mg ha21, respectively. Regression relationship is for all observations in a 6-year, five location (60 plots location21)study ofmaize–soybean rotations. Predicted values are the product of yield andmean nutrient concentration; observed values are the product of yield and

    the measured concentration in subsamples from each plot-year. NS, P > 0.05.

    Nutrient

    Grain nutrient concentration Nutrient removal regression: observed vs predicted

    Mean (mg kg21) SD

    Coefficient of

    variation (%) Slope Intercept r2

    Maize Soy Maize Soy Maize Soy Maize Soy Maize Soy Maize Soy

    N 13.7 63.1 1.43 2.72 10.5 4.3 0.97 0.99 4.10 NS 0.81 0.96

    P 3.3 5.5 0.72 0.49 22.0 8.9 1.09 1.02 23.42 NS 0.62 0.85

    K 3.9 18.3 0.70 1.42 17.8 7.8 1.10 1.07 24.01 24.81 0.70 0.90

    Mg 1.3 2.4 0.29 0.30 22.8 12.7 1.05 1.00 21.09 NS 0.60 0.77

    S 1.1 3.5 0.18 0.41 16.4 11.8 0.93 1.07 0.66 21.04 0.69 0.82

    Ca 0.1 2.6 0.04 0.37 41.2 14.3 0.95 1.01 NS NS 0.30 0.71

    Fig. 4. Relationship between measured K removal by maize and soybean crops and predicted K removal based on crop yields and an assumed constant

    unit removal value (3.9 and 18.3 mg K kg21 grain dry weight for maize and soybean, respectively; Table 4). Data are from a 6-year, five location, 60 plots

    location21 study conducted in Indiana, United States. Data shown are for (A) annual crop removal in each experimental plot and (b) 6-year cumulative

    removal in each experimental plot by the maize–soybean rotation. Different symbols are used to identify crop (A) or experimental location (B).

    Physiol. Plant. 133, 2008 719

  • organic C. As discussed above, soil organic C is an im-

    portant source of nutrients such as N and helps retain

    availability of nutrients such as Fe that can form organic

    chelates. Limited research has shown that maize stover

    removal can lower grain and stover yields of subsequent

    crops and also soil C pools (Wilhelm et al. 1986). Whilethe dynamics of governing biomass conversion to soil

    organic C is not well understood and is a subject of

    intensive ongoing research (Wilhelm et al. 2007), residue

    removal drives changes in soil energy balance. Bare soils

    can be >5�C warmer with much higher surface evapo-transpiration than residue covered soils (reviewed by

    Wilhelm et al. 2004), resulting in altered rates of min-

    eralization and nutrient diffusion.For regions and systems where we currently do an

    adequate jobmanaging nutrients, we stand a good chance

    of continuing to optimize nutrient use under a changed

    climate. If we can and should do better, climate change

    will not help us. To this end, the irrigated rice study of

    Dobermann et al. (1996a, 1996b) not only serves

    a cautionary warning but also highlights a key aspect of

    nutrient management in need of improvement. Theyconclude that current recommendations for K fertilizer

    additions in most intensive irrigated rice domains do not

    replace the K removed in present-day yields; they remark

    that with either increased yields from technology or straw

    removal without any increase in yield, K removal will far

    exceed the present fertilizer levels and deplete soil K

    reserves, ultimately degrading the soil resource. Driving

    this imbalance is a lack of appreciation or perhapsknowledge of the K-supplying power of the soil, that

    specific combination of the crop and soil that governs UE

    (Dobermann et al. 1996b). Review of existing recom-

    mendations for the US Cornbelt suggests that this problem

    is not unique to Asian rice production. Despite extensive

    scientific study and available tools (e.g. high-resolution

    soil surveys and spatially and temporally intensive soil

    testing results), current recommendations are not welltailored to knownsoil- and crop-specific differences inUE.

    Long-term studies in Indiana suggest that additional rates

    of 7.5–20 kg ha21 are required to increase available K in

    actively farmed soils by 1 mg kg21 for a range of major

    agronomic soils (Li and Barber 1988 and ongoing studies)

    but recommendations call for only 4.5–7.5 kg ha21

    (Vitosh et al. 1995) to achieve this change. The reason

    for this clear disconnection between the recommenda-tions for K management and the observations of local soil

    responses has been difficult to discern. Thus, while the

    empirical model that addresses nutrient replacement is

    good, the empiricalmodel for soilmanagement appears to

    require significant improvements in at least a few major

    agronomic regions if we are to achieve optimum AE in

    both present and future production.

    Implications for crop improvement

    Finally, in our discussions of plant growth and nutrient

    needs in a changed climate, we should not overlook the

    combined forces of crop improvement and genetic

    variation/natural selection. To date, most experimenta-

    tion on the effects of elevated CO2 on plant production,

    including the elaborate FACE studies, has been con-

    ducted by imposing elevatedCO2 levels on plantmaterial

    adapted to current atmospheric composition. Genotypic

    variation in traits influencing phenotypic expression and

    plasticity in important plant attributes such as root

    architecture and exudation will allow continued drift

    toward form and function adapted to changed conditions.

    The Cook et al. (1998) study of evolution of N. strictus

    ecotypes under 790 mmol CO2 mol21 is a persistent re-

    minder that we should be cautious in drawing conclu-

    sions when skipping a 100 years of selection pressure.

    Crop improvement efforts will only hasten the process as

    suggested by a recent analysis of shifting agroecozones in

    the United States. In a study initially designed to examine

    the effect that climate change has had to date on cropping

    patterns, Reilly et al. (2003) analyzed the geographic

    centers of production for maize, soybean and wheat over

    the last 100 years. They found a significant north and

    westward shift in centroids for both maize and soybean

    production, and this shift was accompanied by a 4�Cdecrease in temperature despite an estimated US warm-

    ing trend of 0.6�C. This shift reflects management andgenetic technologies including development of new

    varieties of soybean that are adapted to longer photo-

    periods and earlier maturing maize hybrids that

    decreased risk because of early frost. The authors remark

    that in the last 100 years, we have seen adaptation to the

    magnitude of temperature change that we expect for the

    coming century, albeit in the opposite direction.

    As noted in the beginning of the paper, pursuit of

    adaptive technologies will certainly mitigate negative

    impacts and enhance advantages for future plant growth.

    While the promise of enhanced nutrient uptake through

    transgenic manipulation of transports has yet to be

    realized and more research is needed, morphological

    traits may be as or more promising crop improvement

    targets. As summarized by Lynch (2007), these include

    greater root biomass, greater root surface area, longer/

    denser root hairs, more adventitious, smaller diameter

    roots and shallower basal roots in surface soils and an

    architecture that features more dispersed laterals. Other

    desirable features are enhanced exudation and mycor-

    rhizal symbiosis. For emerging crop species that do not

    have a long crop improvement history (e.g. canola;

    Svecnjak andRengel 2006), breeding to improvePE (yield

    as a function of tissue nutrient content) may afford

    720 Physiol. Plant. 133, 2008

  • significant opportunities as well. Irrespective of climate

    change impacts, improvedAEwill be increasingly critical

    as cost and availability of scarce resources – food and fuel

    – constrain their use. Access to and deployment of such

    technology will be as important a driver of realized

    changes in production patterns as the increased ambientCO2 and temperature and altered precipitation patterns.

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