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
9 figures and 3 tables

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 …

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 …

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 …

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 …

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 …

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

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 …

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 …

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 …

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.

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