1. Ecology
  2. Epidemiology and Global Health
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Hidden shift of the ionome of plants exposed to elevated CO2 depletes minerals at the base of human nutrition

  1. Irakli Loladze  Is a corresponding author
  1. The Catholic University of Daegu, Republic of Korea
Research Article
Cite this article as: eLife 2014;3:e02245 doi: 10.7554/eLife.02245
9 figures, 3 tables and 1 data set

Figures

Statistical power and the effect of CO2 on the plant ionome.

The effect of elevated atmospheric CO2 concentrations (eCO2) on the mean concentration of minerals in plants plotted (with the respective 95% confidence intervals [CI]) against the power of statistical analysis. The figure reflects data on 25 minerals in edible and foliar tissues of 125 C3 plant species and cultivars. The true CO2 effect is hidden in the very low and the low power regions. As the statistical power increases, the true effect becomes progressively clearer: the systemic shift of the plant ionome.

https://doi.org/10.7554/eLife.02245.003
The effect of CO2 on individual chemical elements in plants.

Change (%) in the mean concentration of chemical elements in plants grown in eCO2 relative to those grown at ambient levels. Unless noted otherwise, all results in this and subsequent figures are for C3 plants. Average ambient and elevated CO2 levels across all the studies are 368 ppm and 689 ppm respectively. The results reflect the plant data (foliar and edible tissues, FACE and non-FACE studies) from four continents. Error bars represent the standard error of the mean (calculated using the number of mean observations for each element). The number of mean and total (with all the replicates) observations for each element is as follows: C(35/169), N(140/696), P(152/836), K(128/605), Ca(139/739), S(67/373), Mg(123/650), Fe(125/639), Zn(123/702), Cu(124/612), and Mn(101/493). An element is shown individually if the statistical power for a 5% effect size for the element is >0.40. The ‘ionome’ bar reflects all the data on 25 minerals (all the elements in the dataset except of C and N). All the data are available at Dryad depository and at GitHub. Copies of all the original sources for the data are available upon request.

https://doi.org/10.7554/eLife.02245.004
The effect of CO2 on foliar tissues.

Change (%) in the mean concentration of chemical elements in foliar tissues grown in eCO2 relative to those grown at ambient levels. Average ambient and eCO2 levels across all the foliar studies are 364 ppm and 699 ppm respectively. Error bars represent 95% CI. For each element, the number of independent mean observations, m, is shown with the respective statistical power. For each plant group, m equals the sum of mean observations over all the minerals (not including C and N) for that group. Elements and plant groups for which the statistical power is >0.40 (for a 5% effect size) are shown.

https://doi.org/10.7554/eLife.02245.005
The effect of CO2 on edible tissues.

Change (%) in the mean concentration of chemical elements in edible parts of crops grown in eCO2 relative to those grown at ambient levels. Average ambient and elevated CO2 levels across all the crop edible studies are 373 ppm and 674 ppm respectively. Other details are in the legends for Figures 2 and 3.

https://doi.org/10.7554/eLife.02245.006
The effect of CO2 in artificial enclosures.

Change (%) in the mean concentration of chemical elements of plants grown in chambers, greenhouses, and other artificial enclosures under eCO2 relative to those grown at ambient levels. Average ambient and eCO2 levels across all the non-FACE studies are 365 ppm and 732 ppm respectively. Other details are in the legends for Figures 2 and 3.

https://doi.org/10.7554/eLife.02245.007
The effect of CO2 at FACE centers.

Change (%) in the mean concentration of chemical elements of plants grown in Free-Air Carbon dioxide Enrichments (FACE) centers relative to those grown at ambient levels. Average ambient and eCO2 levels across all the FACE studies are 376 ppm and 560 ppm respectively. Other details are in the legends for Figures 2 and 3.

https://doi.org/10.7554/eLife.02245.008
The effect of CO2 at various locations and latitudes.

Locations of the FACE and Open Top Chamber (OTC) centers, which report concentrations of minerals in foliar or edible tissues, are shown as white dots inside colored circles. The area of a circle is proportional to the total number of observations (counting replicates) generated by the center. If the mean change is negative (decline in mineral content), the respective circle is blue; otherwise, it is red. The figure reflects data on 21 minerals in 57 plant species and cultivars. The shaded region (between 35 N and S latitudes) represents tropics and subtropics.

https://doi.org/10.7554/eLife.02245.009
The systemic aspect of the CO2 effect.

Change (%) in the mean concentration of minerals in plants grown in eCO2 relative to those grown at ambient levels. All the results in the figure reflect the combined data for the foliar and the edible tissues. The number of total mean observations (m) for all the measured minerals across all the studies for each crop/plant group, experiment type, country, or region is shown with the respective statistical power. Country specific and regional results reflect all the FACE and Open Top Chamber (OTC) studies carried in any given country/region. The number of total observations (with replicates) for all the minerals (not counting C and N) for each country is as follows: Australia (926), China (193), Finland (144), Germany (908), and USA (1156). Other details are in the legends for Figures 2 and 3.

https://doi.org/10.7554/eLife.02245.010
Testing for publication bias.

A funnel plot of the effect size (the natural log of the response ratio) plotted against the number of replicates/sample sizes (n) for each study and each mineral in the dataset for C3 plants. The plot provides a simple visual evaluation of the distribution of effect sizes. The blue line represents the mean effect size of eCO2 on mineral concentrations: the decline of 8.39% (yielding the decline of 8.04% when back transferred from the log-form). The symmetrical funnel shape of the plot around the mean effect size indicates the publication bias in the dataset is insignificant (Egger et al., 1997).

https://doi.org/10.7554/eLife.02245.011

Tables

Table 1

Comparing the effects of CO2 on two plant quality indicators.

https://doi.org/10.7554/eLife.02245.012
Study/speciesC:N (%)TNC:protein (%)Reference
Arabidopsis thaliana25125Teng et al. (2006)
Bromus erectus626Roumet et al. (1999)*
Dactylis glomerata1753Roumet et al. (1999)*
wheat grain (low N)−1047Porteaus et al. (2009)
wheat grain (high N)−187Porteaus et al. (2009)
wheat grain96Högy et al. (2009)
27 C3 species2890Poorter et al. (1997)
meta-analysis2554Robinson et al. (2012)
meta-analysis2739Stiling and Cornelissen (2007)
  1. CO2-induced changes (%) in C:N (a quality indicator often used in CO2 studies) and in TNC:protein (a rarely used but nutritionally important indicator) for wheat grains and for foliar tissues of various plants. The results shows that in the same plant tissue, eCO2 can increase TNC:protein up to several-fold > C:N. Significant CO2-induced shifts in the ratio of major macronutrients are probable. Hence, it is important for CO2 studies to start accessing and reporting changes in TNC:protein.

  2. *

    in lieu of protein, N content is used.

Table 2

Comparing the effect of CO2 to the effect of adding ‘a spoonful of sugars.’

https://doi.org/10.7554/eLife.02245.013
Plant quality indicatorEffect of adding 5g of TNC (%)Effect of elevated CO2 (%)
Grains and tubers:
TNC2.61 to 15
TNC:protein76 to 47
TNC:minerals76 to 28
protein−4.8−14 to −9
minerals−4.8−10 to −5
Foliar tissues:
TNC2715 to 75
TNC:protein3326 to 125
TNC:minerals3324 to 98
protein−4.8−19 to −14
minerals−4.8−12 to −5
  1. Changes (%) in various plant quality indicators caused by: (1) Adding a teaspoon of TNC (∼5g of starch-and-sugars mixture) per 100g of dry mass (DM) of plant tissue, an:d (2) growing plants in twice-ambient CO2 atmosphere. Changes due to the addition of TNC are calculated assuming:the baseline TNC content of 65% for grains and tubers, and 15% for foliar tissues. The C content is assumed to be ∼42% for plant tissues and TNC.

Table 3

Studies covered in the meta-analysis of CO2 effects on the plant ionome.

https://doi.org/10.7554/eLife.02245.014
SpeciesCommon nameCrop+CO2CountryReference
Acer pseudoplatanusmaple treeNo260Overdieck, 1993
Acer rubrumred maple treeNo200USAFinzi et al., 2001
Agrostis capillarisgrassNo340UKBaxter et al., 1994
Agrostis capillarisgrassNo250Newbery et al., 1995
Alnus glutinosaalder treeNo350UKTemperton et al., 2003
Alphitonia petrieirainforest treeNo440Kanowski, 2001
Ambrosia dumosashrubNo180USAHousman et al., 2012
Arabidopsis thalianathale cressNo450Niu et al., 2013
Arabidopsis thalianathale cressNo330Teng et al., 2006
Betula pendula 'Roth'birch treeNo349FinlandOksanen et al., 2005
Bouteloua curtipendulagrassNo230Polley et al., 2011
Bromus tectorumcheatgrassNo150Blank et al., 2006
Bromus tectorumcheatgrassNo150Blank et al., 2011
Calluna vulgarisheather shrubNo200Woodin et al., 1992
Cercis canadensisred bud treeNo200USAFinzi et al., 2001
Chrysanthemum morifoliumchrysanthNo325Kuehny et al., 1991
Cornus floridadogwood treeNo200USAFinzi et al., 2001
Fagus sylvaticabeech treeNo260Overdieck, 1993
Fagus sylvaticabeech treeNo300Rodenkirchen et al., 2009
Festuca pratensismeadow fescueNo320Overdieck, 1993
Festuca viviparagrassNo340UKBaxter et al., 1994
Flindersia brayleyanarainforest treeNo440Kanowski, 2001
Galactia elliottiiElliott's milkpeaNo325USAHungate et al., 2004
Larix kaempferilarch treeNo335JapanShinano et al., 2007
Lepidium latifoliumpeppergrassNo339Blank and Derner, 2004
Liquidambar styracifluasweetgum treeNo200USAFinzi et al., 2001
Liquidambar styracifluasweetgum treeNo167USAJohnson et al., 2004
Liquidambar styracifluasweetgum treeNo156–200USANatali et al., 2009
Liriodendron tulipiferatulip treeNo325O’Neill et al., 1987
Lolium perennegrassNo320Overdieck, 1993
Lolium perennegrassNo290GermanySchenk et al., 1997
Lupinus albuswhite lupinNo550Campbell and Sage, 2002
Lycium pallidumshrubNo180USAHousman et al., 2012
Nephrolepis exaltatafernNo650Nowak et al., 2002
Pelargonium x hortorum 'Maverick White'geraniumNo330Mishra et al., 2011
Picea abies 'Karst.'spruce treeNo350Pfirrmann et al., 1996
Picea abies 'Karst.'spruce treeNo300Rodenkirchen et al., 2009
Picea abies 'Karst.'spruce treeNo300Weigt et al., 2011
Picea rubensspruce treeNo350Shipley et al., 1992
Pinus ponderosapine treeNo346USAWalker et al., 2000
Pinus ponderosa 'Laws.'pine treeNo350USAJohnson et al., 1997
Pinus sylvestrispine treeNo331Luomala et al., 2005
Pinus sylvestrispine treeNo225FinlandUtriainen et al., 2000
Pinus taedaloblolly pine treeNo200USAFinzi et al., 2001
Pinus taedapine treeNo200USANatali et al., 2009
Poa alpinagrassNo340UKBaxter et al., 1994
Poa alpinagrassNo340UKBaxter et al., 1997
Pteridium aquilinumfernNo320Zheng et al., 2008
Pteridium revolutumfernNo320Zheng et al., 2008
Pteris vittatafernNo320Zheng et al., 2008
Quercus chapmaniioak treeNo350USANatali et al., 2009
Quercus geminataoak treeNo350USAJohnson et al., 2003
Quercus geminataoak treeNo350USANatali et al., 2009
Quercus myrtifoliaoak treeNo350USAJohnson et al., 2003
Quercus myrtifoliaoak treeNo350USANatali et al., 2009
Quercus subercork oak treeNo350Niinemets et al., 1999
Schizachyrium scopariumgrassNo230Polley et al., 2011
Sorghastrum nutansgrassNo230Polley et al., 2011
Sporobolus kentrophyllusgrassNo330Wilsey et al., 1994
Trifolium alexandrinum 'Pusa Jayant'berseem cloverNo250IndiaPal et al., 2004
Trifolium pratensered cloverNo320Overdieck, 1993
Trifolium repenswhite cloverNo320Overdieck, 1993
Trifolium repenswhite cloverNo290GermanySchenk et al., 1997
Trifolium repenswhite cloverNo615Tian et al., 2014
Trifolium repens 'Regal'white cloverNo330Heagle et al., 1993
Vallisneria spinulosamacrophyteNo610Yan et al., 2006
Apium graveolensceleryYes670Tremblay et al., 1988
Brassica juncea 'Czern'mustardYes500IndiaSingh et al., 2013
Brassica napus 'Qinyou 8'rapeseedYes615Tian et al., 2014
Brassica napus 'Rongyou 10'rapeseedYes615Tian et al., 2014
Brassica napus 'Zhongyouza 12'rapeseedYes615Tian et al., 2014
Brassica napus 'Campino'oilseed rapeYes106GermanyHögy et al., 2010
Brassica rapa 'Grabe'turnipYes600Azam et al., 2013
Citrus aurantiumorange treeYes300USAPenuelas et al., 1997
Citrus madurensiscitrus treeYes600Keutgen and Chen, 2001
Cucumis sativuscucumberYes650Peet et al., 1986
Daucus carota 'T-1-111'carrotYes600Azam et al., 2013
Fragaria x ananassastrawberryYes600Keutgen et al., 1997
Glycine max 'Merr.'soybeanYes360USAPrior et al., 2008
Glycine max 'Merr.'soybeanYes200Rodriguez et al., 2011
Gossypium hirsutum 'Deltapine 77'cottonYes180USAHuluka et al., 1994
Hordeum vulgarebarleyYes175GermanyErbs et al., 2010
Hordeum vulgare 'Alexis'barleyYes334GermanyManderscheid et al., 1995
Hordeum vulgare 'Arena'barleyYes334GermanyManderscheid et al., 1995
Hordeum vulgare 'Europa'barleyYes400Haase et al., 2008
Hordeum vulgare 'Iranis'barleyYes350Pérez-López et al., 2014
Hordeum vulgare 'Theresa'barleyYes170GermanyWroblewitz et al., 2013
Lactuca sativa 'BRM'lettuceYes308Baslam et al., 2012
Lactuca sativa 'Mantilla'lettuceYes350Chagvardieff et al., 1994
Lactuca sativa 'MV'lettuceYes308Baslam et al., 2012
Lactuca sativa 'Waldmann's Green'lettuceYes600McKeehen et al., 1996
Lycopersicon esculentum 'Astra'tomatoYes600Khan et al., 2013
Lycopersicon esculentum 'Eureka'tomatoYes600Khan et al., 2013
Lycopersicon esculentum 'Mill.'tomatoYes360Li et al., 2007
Lycopersicon esculentum 'Zheza 809'tomatoYes450Jin et al., 2009
Mangifera indica 'Kensington'mango treeYes350Schaffer and Whiley, 1997
Mangifera indica 'Tommy Atkins'mango treeYes350Schaffer and Whiley, 1997
Medicago sativaalfalfaYes615Tian et al., 2014
Medicago sativa 'Victor'alfalfaYes100UKAl-Rawahy et al., 2013
Oryza sativariceYes200ChinaPang et al., 2005
Oryza sativa 'Akitakomachi'riceYes205–260JapanLieffering et al., 2004
Oryza sativa 'Akitakomachi'riceYes250JapanYamakawa et al., 2004
Oryza sativa 'BRRIdhan 39'riceYes210BangladeshRazzaque et al., 2009
Oryza sativa 'Gui Nnong Zhan'riceYes500Li et al., 2010
Oryza sativa 'IR 72'riceYes296PhilippinesZiska et al., 1997
Oryza sativa 'Japonica'riceYes200ChinaJia et al., 2007
Oryza sativa 'Jarrah'riceYes350Seneweera and Conroy, 1997
Oryza sativa 'Khaskani'riceYes210BangladeshRazzaque et al., 2009
Oryza sativa 'Rong You 398'riceYes500Li et al., 2010
Oryza sativa 'Shakkorkhora'riceYes210BangladeshRazzaque et al., 2009
Oryza sativa 'Shan You 428'riceYes500Li et al., 2010
Oryza sativa 'Tian You 390'riceYes500Li et al., 2010
Oryza sativa 'Wu Xiang jing'riceYes200ChinaGuo et al., 2011
Oryza sativa 'Wuxiangjing 14'riceYes200ChinaMa et al., 2007
Oryza sativa 'Wuxiangjing 14'riceYes200ChinaYang et al., 2007
Oryza sativa 'Yin Jing Ruan Zhan'riceYes500Li et al., 2010
Oryza sativa 'Yue Za 889'riceYes500Li et al., 2010
Phaseolus vulgaris 'Contender'beanYes340Mjwara et al., 1996
Phaseolus vulgaris 'Seafarer'beanYes870Porter and Grodzinski, 1984
Raphanus sativus 'Mino'radishYes600Azam et al., 2013
Raphanus sativus 'Cherry Belle'radishYes380Barnes and Pfirrmann, 1992
Raphanus sativus 'Giant White Globe'radishYes600McKeehen et al., 1996
Rumex patientia x R. Tianschanicus 'Rumex K-1'buckwheatYes615Tian et al., 2014
Secale cereale 'Wintergrazer-70'ryeYes615Tian et al., 2014
Solanum lycopersicum '76R MYC+'tomatoYes590Cavagnaro et al., 2007
Solanum lycopersicum 'rmc'tomatoYes590Cavagnaro et al., 2007
Solanum tuberosumpotatoYes500Cao and Tibbitts, 1997
Solanum tuberosum 'Bintje'potatoYes170GermanyHögy and Fangmeier, 2009
Solanum tuberosum 'Bintje'potatoYes278-281SwedenPiikki et al., 2007
Solanum tuberosum 'Bintje'potatoYes305-320EuropeFangmeier et al., 2002
Solanum tuberosum 'Dark Red Norland'potatoYes345USAHeagle et al., 2003
Solanum tuberosum 'Superior'potatoYes345USAHeagle et al., 2003
Sorghum bicolorsorghumYes360USAPrior et al., 2008
Spinacia oleraceaspinachYes250IndiaJain et al., 2007
Trigonella foenum-graecumfenugreekYes250IndiaJain et al., 2007
Triticum aestivumwheatYes175GermanyErbs et al., 2010
Triticum aestivum 'Ningmai 9'wheatYes200ChinaMa et al., 2007
Triticum aestivum 'Triso'wheatYes150GermanyHögy et al., 2009
Triticum aestivum 'Triso'wheatYes150GermanyHögy et al., 2013
Triticum aestivum 'Alcazar'wheatYes350de la Puente et al., 2000
Triticum aestivum 'Batis'wheatYes170GermanyWroblewitz et al., 2013
Triticum aestivum 'Dragon'wheatYes305-320SwedenPleijel and Danielsson, 2009
Triticum aestivum 'HD-2285'wheatYes250IndiaPal et al., 2003
Triticum aestivum 'Janz'wheatYes166AustraliaFernando et al., 2014
Triticum aestivum 'Jinnong 4'wheatYes615Tian et al., 2014
Triticum aestivum 'Minaret'wheatYes278GermanyFangmeier et al., 1997
Triticum aestivum 'Minaret'wheatYes300EuropeFangmeier et al., 1999
Triticum aestivum 'Rinconada'wheatYes350de la Puente et al., 2000
Triticum aestivum 'Star'wheatYes334GermanyManderscheid et al., 1995
Triticum aestivum 'Turbo'wheatYes334GermanyManderscheid et al., 1995
Triticum aestivum 'Turbo'wheatYes350Wu et al., 2004
Triticum aestivum 'Veery 10'wheatYes410Carlisle et al., 2012
Triticum aestivum 'Yangmai'wheatYes200ChinaGuo et al., 2011
Triticum aestivum 'Yitpi'wheatYes166AustraliaFernando et al., 2012a
Triticum aestivum 'Yitpi'wheatYes166AustraliaFernando et al., 2012b
Triticum aestivum 'Yitpi'wheatYes166AustraliaFernando et al., 2012c
Triticum aestivum 'Yitpi'wheatYes166AustraliaFernando et al., 2014
  1. The table provides species name, common name, the type of experimental set up, the level of CO2 enrichment, and indicates whether the species is a crop. Countries are listed only for FACE and OTC type experiments with ‘Europe’ accounting for combined data from Belgium, Denmark, Finland, Germany, Sweden, and the UK.

Data availability

The following data sets were generated
  1. 1
    CO2 Dataset (CSV format); CO2 Dataset (XLSX format); R Code for the CO2 dataset
    1. I Loladze
    (2014)
    Available at Dryad Digital Repository under a CC0 Public Domain Dedication.

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