Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Plant nutrient acquisition and utilisation in a high carbon dioxide world

T. R. Cavagnaro A C , R. M. Gleadow A and R. E. Miller A B

A School of Biological Sciences, Monash University, Clayton, Vic. 3800, Australia.

B The Australian Centre for Biodiversity, Monash University, Clayton, Vic. 3800, Australia.

C Corresponding author. Email: timothy.cavagnaro@monash.edu

Functional Plant Biology 38(2) 87-96 http://dx.doi.org/10.1071/FP10124
Submitted: 4 June 2010  Accepted: 18 November 2010   Published: 1 February 2011

Abstract

Producing enough food to meet the needs of an increasing global population is one of the greatest challenges we currently face. The issue of food security is further complicated by impacts of elevated CO2 and climate change. In this viewpoint article, we begin to explore the impacts of elevated CO2 on two specific aspects of plant nutrition and resource allocation that have traditionally been considered separately. First, we focus on arbuscular mycorrhizas, which play a major role in plant nutrient acquisition. We then turn our attention to the allocation of resources (specifically N and C) in planta, with an emphasis on the secondary metabolites involved in plant defence against herbivores. In doing so, we seek to encourage a more integrated approach to investigation of all aspects of plant responses to eCO2.

Additional keywords: arbuscular mycorrhizas, cyanogenesis, elevated CO2, food security, nitrogen, secondary metabolism.


References

Agrawal AA, Fishbein M (2006) Plant defense syndromes. Ecology 87, S132–S149.
Plant defense syndromes.CrossRef | 16922309PubMed | open url image1

Agrell J, Anderson P, Oleszek W, Stochmal A, Agrell C (2006) Elevated CO2 levels and herbivore damage alter host plant preferences. Oikos 112, 63–72.
Elevated CO2 levels and herbivore damage alter host plant preferences.CrossRef | open url image1

Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytologist 165, 351–372.
What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2.CrossRef | 15720649PubMed | open url image1

Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant Cell and Environment 30, 258–270.
The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions.CrossRef | 1:CAS:528:DC%2BD2sXjtlemu78%3D&md5=fc6e69de59f8e214d1072da0476afc98CAS | open url image1

Alberton O, Kuyper TW, Gorissn A (2005) Taking mycocentrism seriously: mycorrhizal fungal and plant responses to elevated CO2. New Phytologist 167, 859–868.
Taking mycocentrism seriously: mycorrhizal fungal and plant responses to elevated CO2.CrossRef | 1:CAS:528:DC%2BD2MXhtVGitr7E&md5=5ac0efc8b42b36337b4f79ddee79798cCAS | 16101922PubMed | open url image1

Allen MF, Swenson W, Querejeta JI, Egerton-Warburton LM, Treseder KK (2003) Ecology of mycorrhizae: a conceptual framework for complex interactions among plants and fungi. Annual Review of Phytopathology 41, 271–303.
Ecology of mycorrhizae: a conceptual framework for complex interactions among plants and fungi.CrossRef | 1:CAS:528:DC%2BD3sXptFWlsLc%3D&md5=d4e09feabf49b8962b1b09465b776ecaCAS | 12730396PubMed | open url image1

Ames RN, Reid CPP, Porter LK, Cambardella C (1983) Hyphal uptake and transport of nitrogen from two 15N-labelled sources by Glomus mosseae, a vesicular arbuscular mycorrhizal fungus. New Phytologist 95, 381–396.
Hyphal uptake and transport of nitrogen from two 15N-labelled sources by Glomus mosseae, a vesicular arbuscular mycorrhizal fungus.CrossRef | open url image1

Bago B, Azcón-Aguilar C, Goulet A, Piché Y (1998) Branched adsorbing structures (BAS): a feature of the extraradical mycelium of symbiotic arbuscular mycorrhizal fungi. New Phytologist 139, 375–388.
Branched adsorbing structures (BAS): a feature of the extraradical mycelium of symbiotic arbuscular mycorrhizal fungi.CrossRef | open url image1

Bazin A, Goverde M, Erhardt A, Shykoff JA (2002) Influence of atmospheric carbon dioxide enrichment on induced response and growth compensation after herbivore damage in Lotus corniculatus. Ecological Entomology 27, 271–278.
Influence of atmospheric carbon dioxide enrichment on induced response and growth compensation after herbivore damage in Lotus corniculatus.CrossRef | open url image1

Bennett AE, Alers-Garcia J, Bever JD (2006) Three-way interactions among mutualistic mycorrhizal fungi, plants, and plant enemies: hypotheses and synthesis. American Naturalist 167, 141–152.
Three-way interactions among mutualistic mycorrhizal fungi, plants, and plant enemies: hypotheses and synthesis.CrossRef | 16670976PubMed | open url image1

Bidart-Bouzat MG, Imeh-Nathaniel A (2008) Global change effects on plant chemical defenses against insect herbivores. Journal of Integrative Plant Biology 50, 1339–1354.
Global change effects on plant chemical defenses against insect herbivores.CrossRef | 1:CAS:528:DC%2BD1cXhsVyltLfE&md5=fa92d78ea9e9d0523987cd2d461f971bCAS | 19017122PubMed | open url image1

Bloom AJ, Burger M, Asensio JSR, Cousins AB (2010) Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis. Science 328, 899–903.
Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis.CrossRef | 1:CAS:528:DC%2BC3cXlvVeltrc%3D&md5=cb03118708274c3aedff05e7cc472474CAS | 20466933PubMed | open url image1

Boege K, Marquis RJ (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends in Ecology & Evolution 20, 441–448.
Facing herbivory as you grow up: the ontogeny of resistance in plants.CrossRef | open url image1

Campbell CD, Sage RF (2006) Interactions between the effects of atmospheric CO2 content and P nutrition on photosynthesis in white lupin (Lupinus alba L.) Plant, Cell & Environment 29, 844–853.
Interactions between the effects of atmospheric CO2 content and P nutrition on photosynthesis in white lupin (Lupinus alba L.)CrossRef | 1:CAS:528:DC%2BD28Xlt1Gku7k%3D&md5=1d409a2f10e16263d9617c3b94123d22CAS | 17087468PubMed | open url image1

Cardoso A, Ernesto M, Cliff J, Egan SV, Bradbury JH (1998) Cyanogenic potential of cassava flour: field trial in Mozambique of a simple kit. International Journal of Food Sciences and Nutrition 49, 93–99.
Cyanogenic potential of cassava flour: field trial in Mozambique of a simple kit.CrossRef | 1:STN:280:DyaK1cznvFajsw%3D%3D&md5=901f89beff90e465ecaf13b31c58198dCAS | 9713579PubMed | open url image1

Cavagnaro TR (2008) The role of arbuscular mycorrhizas in improving plant zinc nutrition under low soil zinc concentrations: a review. Plant and Soil 304, 315–325.
The role of arbuscular mycorrhizas in improving plant zinc nutrition under low soil zinc concentrations: a review.CrossRef | 1:CAS:528:DC%2BD1cXitVaqs7o%3D&md5=61bbcba38f784545db5ba200bfeca581CAS | open url image1

Cavagnaro TR, Smith FA, Lorimer MF, Haskard KA, Ayling SM, Smith SE (2001) Quantitative development of Paris-type arbuscular mycorrhizas formed between Asphodelus fistulosus and Glomus coronatum. New Phytologist 149, 105–113.
Quantitative development of Paris-type arbuscular mycorrhizas formed between Asphodelus fistulosus and Glomus coronatum.CrossRef | open url image1

Cavagnaro TR, Smith FA, Smith SE, Jakobsen I (2005) Functional diversity in arbuscular mycorrhizas: exploitation of soil patches with different phosphate enrichment differs among fungal species. Plant, Cell & Environment 164, 485–491.

Cavagnaro TR, Sokolow SK, Jackson LE (2007) Mycorrhizal effects on growth and nutrition of tomato under elevated atmospheric carbon dioxide. Functional Plant Biology 34, 730–736.
Mycorrhizal effects on growth and nutrition of tomato under elevated atmospheric carbon dioxide.CrossRef | 1:CAS:528:DC%2BD2sXos1Knt7Y%3D&md5=8aa40504eca03e210a083a2ba2b7d01fCAS | open url image1

Chen X, Tu C, Burton MG, Watson DM, Burkey KO, Hu S (2007) Plant nitrogen acquisition and interactions under elevated carbon dioxide: impact of endophytes and mycorrhizae. Global Change Biology 13, 1238–1249.
Plant nitrogen acquisition and interactions under elevated carbon dioxide: impact of endophytes and mycorrhizae.CrossRef | open url image1

Coley PD, Massa M, Lovelock CE, Winter K (2002) Effects of elevated CO2 on foliar chemistry of saplings of nine species of tropical tree. Oecologia 133, 62–69.
Effects of elevated CO2 on foliar chemistry of saplings of nine species of tropical tree.CrossRef | open url image1

Collins-Johnson N, Wolf J, Reyes MA, Panter A, Koch GW, Redman A (2005) Species of plants and associated arbuscular mycorrhizal fungi mediate mycorrhizal responses to CO2 enrichment. Global Change Biology 11, 1156–1166.
Species of plants and associated arbuscular mycorrhizal fungi mediate mycorrhizal responses to CO2 enrichment.CrossRef | open url image1

Conroy JP, Milham PJ, Barlow EWR (1992) Effect of nitrogen and phosphorus availability on the growth-response of Eucalyptus grandis to high CO2. Plant, Cell & Environment 15, 843–847.
Effect of nitrogen and phosphorus availability on the growth-response of Eucalyptus grandis to high CO2.CrossRef | 1:CAS:528:DyaK3sXjs1SgsQ%3D%3D&md5=bfdfa70ea4e434549c587f124b89936aCAS | open url image1

Cordell D, Drangert J-O, White S (2009) The story of phosphorus: global food security and food for thought. Global Environmental Change 19, 292–305.
The story of phosphorus: global food security and food for thought.CrossRef | open url image1

Cornelissen T, Fernandes GW, Vasconcellos-Neto J (2008) Size does matter: variation in herbivory between and within plants and the plant vigor hypothesis. Oikos 117, 1121–1130.
Size does matter: variation in herbivory between and within plants and the plant vigor hypothesis.CrossRef | open url image1

Cotrufo MF, Ineson P, Scott A (1998) Elevated CO2 reduces the nitrogen concentration of plant tissues. Global Change Biology 4, 43–54.
Elevated CO2 reduces the nitrogen concentration of plant tissues.CrossRef | open url image1

Daepp M, Nösberger J, Lüscher A (2001) Nitrogen fertilization and developmental stage alter the response of Lolium perenne to elevated CO2. New Phytologist 150, 347–358.
Nitrogen fertilization and developmental stage alter the response of Lolium perenne to elevated CO2.CrossRef | 1:CAS:528:DC%2BD3MXjvVegsrg%3D&md5=4d4b892369e2bcb79f687ff3f5c45506CAS | open url image1

de Graaff MA, van Groeningen KJ, Six J, Hungate BA, van Kessel C (2006) Interactions between plant growth and nutrient dynamics under elevated CO2: a meta analysis. Global Change Biology 12, 2077–2091.
Interactions between plant growth and nutrient dynamics under elevated CO2: a meta analysis.CrossRef | open url image1

Dickson S (2004) The Arum–Paris continuum of mycorrhizal symbioses. New Phytologist 163, 187–200.
The Arum–Paris continuum of mycorrhizal symbioses.CrossRef | open url image1

Dickson S, Kolesik P (1999) Visualisation of mycorrhizal fungal structures and quantification of their surface area and volume using laser scanning confocal microscopy. Mycorrhiza 9, 205–213.
Visualisation of mycorrhizal fungal structures and quantification of their surface area and volume using laser scanning confocal microscopy.CrossRef | open url image1

Dickson S, Smith SE (2001) Cross walls in arbuscular trunk hyphae form after loss of metabolic activity. New Phytologist 151, 735–742.
Cross walls in arbuscular trunk hyphae form after loss of metabolic activity.CrossRef | open url image1

Dijkstra FA, Blumenthal D, Morgan JA, LeCain DR, Follett RF (2010) Elevated CO2 effects on semi-arid grassland plants in relation to water availability and competition. Functional Ecology 24, 1152–1161.
Elevated CO2 effects on semi-arid grassland plants in relation to water availability and competition.CrossRef | open url image1

Drake BG, Gonzàlez-Meler MA, Long SP (1997) More efficient plants: a consequence of rising atmospheric CO2? Annual Review of Plant Physiology and Plant Molecular Biology 48, 609–639.
More efficient plants: a consequence of rising atmospheric CO2?CrossRef | 1:CAS:528:DyaK2sXjs1eltbY%3D&md5=294307b103c53ccadd6753093f7c1fa9CAS | 15012276PubMed | open url image1

Edwards EJ, McCaffery S, Evans JR (2005) Phosphorus status determines biomass response to elevated CO2 in a legume: C4 grass community. Global Change Biology 11, 1968–1981.

Erbs M, Manderscheid R, Jansen G, Seddig S, Pacholski A, Weigel H-J (2010) Effects of free-air CO2 enrichment and nitrogen supply on grain quality parameters and elemental composition of wheat and barley grown in a crop rotation. Agriculture Ecosystems & Environment 136, 59–68.
Effects of free-air CO2 enrichment and nitrogen supply on grain quality parameters and elemental composition of wheat and barley grown in a crop rotation.CrossRef | 1:CAS:528:DC%2BC3cXhtVGrsr8%3D&md5=8cedef89e1969aabac0b39181a183f3fCAS | open url image1

Gamper H, Peter M, Jansa J, Luscher A, Hartwig UA, Leuchtmann A (2004) Arbuscular mycorrhizal fungi benefit from 7 years of free air CO2 enrichment in well-fertilized grass and legume monocultures. Global Change Biology 10, 189–199.
Arbuscular mycorrhizal fungi benefit from 7 years of free air CO2 enrichment in well-fertilized grass and legume monocultures.CrossRef | open url image1

Gamper H, Hartwig UA, Leuchtmann A (2005) Mycorrhizas improve nitrogen nutrition of Trifolium repens after 8 yr of selection under elevated atmospheric CO2 partial pressure. New Phytologist 167, 531–542.
Mycorrhizas improve nitrogen nutrition of Trifolium repens after 8 yr of selection under elevated atmospheric CO2 partial pressure.CrossRef | 1:CAS:528:DC%2BD2MXpt1ertr4%3D&md5=94e90c21fe1bf4455fb9415675fe9858CAS | 15998404PubMed | open url image1

Gange AC, West HM (1994) Interactions between arbuscular mycorrhizal fungi and foliar-feeding insects in Plantago lanceolata L. New Phytologist 128, 79–87.
Interactions between arbuscular mycorrhizal fungi and foliar-feeding insects in Plantago lanceolata L.CrossRef | open url image1

Garcia MO, Ovasapyan T, Greas M, Treseder KK (2008) Mycorrhizal dynamics under elevated CO2 and nitrogen fertilization in a warm temperate forest. Plant and Soil 303, 301–310.
Mycorrhizal dynamics under elevated CO2 and nitrogen fertilization in a warm temperate forest.CrossRef | 1:CAS:528:DC%2BD1cXht1ShtLg%3D&md5=2a6169873f65c389c9c96539bf8c8849CAS | open url image1

Gavito ME, Bruhn D, Jakobsen I (2002) P uptake by arbuscular mycorrhizal hyphae does not increase when the host plant grows under atmospheric CO2 enrichment. New Phytologist 154, 751–760.
P uptake by arbuscular mycorrhizal hyphae does not increase when the host plant grows under atmospheric CO2 enrichment.CrossRef | 1:CAS:528:DC%2BD38XkslWjtbw%3D&md5=48017616f6c8c4579bb74406baa4b5b3CAS | open url image1

Gavito ME, Schweiger P, Jakobsen I (2003) P uptake by arbuscular mycorrhizal hyphae: effect of soil temperature and atmospheric CO2 enrichment. Global Change Biology 9, 106–116.
P uptake by arbuscular mycorrhizal hyphae: effect of soil temperature and atmospheric CO2 enrichment.CrossRef | open url image1

Ghannoum O, von Caemmerer S, Barlow EWR, Conroy JP (1997) The effect of CO2 enrichment and irradiance on the growth, morphology and gas exchange of a C3 (Panicum laxum) and a C4 (Panicum antidotale) grass. Australian Journal of Plant Physiology 24, 227–237.
The effect of CO2 enrichment and irradiance on the growth, morphology and gas exchange of a C3 (Panicum laxum) and a C4 (Panicum antidotale) grass.CrossRef | 1:CAS:528:DyaK2sXjs1ajtL0%3D&md5=2091afb8c2893826217a5e43d88fd5c3CAS | open url image1

Glassop D, Smith SE, Smith FW (2005) Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake in roots. Planta 222, 688–698.
Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake in roots.CrossRef | 1:CAS:528:DC%2BD2MXhtFyntr%2FF&md5=0715461892fdee077d80c65f58e68647CAS | 16133217PubMed | open url image1

Gleadow RM, Woodrow IE (2000) Temporal and spatial variation in cyanogenic glycosides in Eucalyptus cladocalyx. Tree Physiology 20, 591–598.

Gleadow RM, Woodrow IE (2002) Constraints on effectiveness of cyanogenic glycosides in herbivore defense. Journal of Chemical Ecology 28, 1301–1313.
Constraints on effectiveness of cyanogenic glycosides in herbivore defense.CrossRef | 1:CAS:528:DC%2BD38XmsVGmsbs%3D&md5=47c096d7583136eb17f9e1db30095e0fCAS | 12199497PubMed | open url image1

Gleadow RM, Foley WJ, Woodrow IE (1998) Enhanced CO2 alters the relationship between photosynthesis and defence in cyanogenic Eucalyptus cladocalyx F. Muell. Plant, Cell & Environment 21, 12–22.
Enhanced CO2 alters the relationship between photosynthesis and defence in cyanogenic Eucalyptus cladocalyx F. Muell.CrossRef | 1:CAS:528:DyaK1cXitlCgsL0%3D&md5=b57b391f5b4f9d4aa91028c25bb4e6b3CAS | open url image1

Gleadow RM, Edwards E, Evans J (2009a) Changes in nutritional value of cyanogenic Trifolium repens at elevated CO2. Journal of Chemical Ecology 35, 476–478.
Changes in nutritional value of cyanogenic Trifolium repens at elevated CO2.CrossRef | 1:CAS:528:DC%2BD1MXlt1Kisrw%3D&md5=f761e8dc3bc3b95f8b1c3dd72387c9f1CAS | 19352773PubMed | open url image1

Gleadow RM, Evans J, McCaffrey S, Cavagnaro TR (2009b) Growth and nutritive value of cassava (Manihot esculenta Cranz.) are reduced when grown at elevated CO2. Plant Biology 11, 76–82.
Growth and nutritive value of cassava (Manihot esculenta Cranz.) are reduced when grown at elevated CO2.CrossRef | 1:CAS:528:DC%2BC3cXlslajsro%3D&md5=831e2d11af3c07b66c38b5122076c952CAS | 19778371PubMed | open url image1

Gleadow R, Cavagnaro T, O’Donnell N, Evans J, Neale A, Blomstedt C, Hamill J (2009c) Unbalancing global resources: will plants be edible in a high CO2 world? Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 153, s225
Unbalancing global resources: will plants be edible in a high CO2 world?CrossRef | open url image1

González-Guerrero M, Azcón-Aguilar C, Mooney M, Valderas A, MacDiarmid CW, Eide DJ, Ferrol N (2005) Characterization of a Glomus intraradices gene encoding a putative Zn transporter of the cation diffusion facilitator family. Fungal Genetics and Biology 42, 130–140.
Characterization of a Glomus intraradices gene encoding a putative Zn transporter of the cation diffusion facilitator family.CrossRef | 15670711PubMed | open url image1

González-Guerrero M, Cano C, Azcón-Aguilar C, Ferrol N (2007) GintMT1 encodes a functional metallothionein in Glomus intraradices that responds to oxidative stress. Mycorrhiza 17, 327–335.
GintMT1 encodes a functional metallothionein in Glomus intraradices that responds to oxidative stress.CrossRef | 17277942PubMed | open url image1

Gregory PJ, Johnson SN, Newton AC, Ingram JSI (2009) Integrating pests and pathogens into the climate change/food security debate. Journal of Experimental Botany 60, 2827–2838.
Integrating pests and pathogens into the climate change/food security debate.CrossRef | 1:CAS:528:DC%2BD1MXosFWjtb4%3D&md5=1283be9c879fe0f91d0f968cd60edea4CAS | 19380424PubMed | open url image1

Grünzweig JM, Körner C (2003) Differential phosphorus and nitrogen effects drive species and community responses to elevated CO2 in semi-arid grassland. Functional Ecology 17, 766–777.
Differential phosphorus and nitrogen effects drive species and community responses to elevated CO2 in semi-arid grassland.CrossRef | open url image1

Hartwig UA, Wittmann P, Braun R, Hartwig-Räz B, Jansa J, Mozafar A, Lüscher A, Leuchtmann A, Frossard E, Nösberger J (2002) Arbuscular mycorrhiza infection enhances the growth response of Lolium perenne to elevated atmospheric pCO2. Journal of Experimental Botany 53, 1207–1213.
Arbuscular mycorrhiza infection enhances the growth response of Lolium perenne to elevated atmospheric pCO2.CrossRef | 1:CAS:528:DC%2BD38XjsFans78%3D&md5=18af550cd21d7f36deb5f8b3401154c3CAS | 11971931PubMed | open url image1

Haugen R, Steffes L, Wolf J, Brown P, Matzner S, Siemens DH (2008) Evolution of drought tolerance and defense: dependence of tradeoffs on mechanism, environment and defense switching. Oikos 117, 231–244.
Evolution of drought tolerance and defense: dependence of tradeoffs on mechanism, environment and defense switching.CrossRef | open url image1

Högy P, Fangmeier A (2008) Effects of elevated atmospheric CO2 on grain quality of wheat. Journal of Cereal Science 48, 580–591.
Effects of elevated atmospheric CO2 on grain quality of wheat.CrossRef | open url image1

Högy P, Wieser H, Köhler P, Schwadorf K, Breuer J, Franzaring J, Muntifering R, Fangmeier A (2009) Effects of elevated CO2 on grain yield and quality of wheat: results from a 3-year free-air CO2 enrichment experiment. Plant Biology 11, 60–69.
Effects of elevated CO2 on grain yield and quality of wheat: results from a 3-year free-air CO2 enrichment experiment.CrossRef | 19778369PubMed | open url image1

Högy P, Franzaring J, Schwadorf K, Breuer J, Schultze W, Fangmeier A (2010) Effects of free-air CO2 enrichment on energy traits and seed quality of oilseed rape. Agriculture Ecosystems & Environment 139, 239–244.
Effects of free-air CO2 enrichment on energy traits and seed quality of oilseed rape.CrossRef | open url image1

Hu S, Tu C, Chen X, Gruver JB (2006) Progressive N limitation of plant response to elevated CO2: a microbiological perspective. Plant and Soil 289, 47–58.
Progressive N limitation of plant response to elevated CO2: a microbiological perspective.CrossRef | 1:CAS:528:DC%2BD28Xht1WnsrrM&md5=0cd18c3dc595012696c271b4e4fad7fbCAS | open url image1

IPCC (2007) Technical summary. In ‘Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change’. pp. 19–91. (Cambridge University Press: Cambridge)

Jackson LE, Burger M, Cavagnaro TR (2008) Roots, nitrogen transformations, and ecosystem services. Annual Review of Plant Biology 59, 341–363.
Roots, nitrogen transformations, and ecosystem services.CrossRef | 1:CAS:528:DC%2BD1cXntFaqsb4%3D&md5=ed85a45f25561fd3bc7dd99916e90dc7CAS | 18444903PubMed | open url image1

Jifon JL, Graham JH, Drouillard DL, Syvertsen JP (2002) Growth depression of mycorrhizal Citrus seedlings grown at high phosphorus supply is mitigated by elevated CO2. New Phytologist 153, 133–142.
Growth depression of mycorrhizal Citrus seedlings grown at high phosphorus supply is mitigated by elevated CO2.CrossRef | open url image1

Johansen A, Jakobsen I, Jensen ES (1993) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum. 3. Hyphal transport of 32P and 15N. New Phytologist 124, 61–68.
External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum. 3. Hyphal transport of 32P and 15N.CrossRef | 1:CAS:528:DyaK3sXmsVGitLc%3D&md5=d8b4b6db75d8d8b05cfc3fe6b3d37770CAS | open url image1

Jones DA (1998) Why are so many food plants cyanogenic? Phytochemistry 47, 155–162.
Why are so many food plants cyanogenic?CrossRef | 1:CAS:528:DyaK1cXislChtg%3D%3D&md5=8aaf6bb84be5ce2ff98baf716ed21b33CAS | 9431670PubMed | open url image1

Kimball BA, Morris CE, Pinter PJ, Wall GW, Hunsaker DJ, Adamsen FJ, LaMorte RL, Leavitt SW, Thompson TL, Matthias AD, Brooks TJ (2001) Elevated CO2, drought and soil nitrogen effects on wheat grain quality. New Phytologist 150, 295–303.
Elevated CO2, drought and soil nitrogen effects on wheat grain quality.CrossRef | 1:CAS:528:DC%2BD3MXjvVegsro%3D&md5=c6902a26dc56a3c11150bd9af9bdbb2cCAS | open url image1

Klironomos JN, Ursic M, Rillig M, Allen MF (1998) Interspecific differences in the response of arbuscular mycorrhizal fungi to Artemisia tridentata grown under elevated atmospheric CO2. New Phytologist 138, 599–605.
Interspecific differences in the response of arbuscular mycorrhizal fungi to Artemisia tridentata grown under elevated atmospheric CO2.CrossRef | open url image1

Lambers H (1993) Rising CO2, secondary plant metabolism, plant–herbivore interactions and litter decomposition: theoretical considerations. Vegetation 104–105, 263–271.
Rising CO2, secondary plant metabolism, plant–herbivore interactions and litter decomposition: theoretical considerations.CrossRef | open url image1

Lawler IR, Foley WJ, Woodrow IE, Cork SJ (1997) The effects of elevated CO2 atmospheres on the nutritional quality of Eucalyptus foliage and its interaction with soil nutrient and light availability. Oecologia 109, 59–68.
The effects of elevated CO2 atmospheres on the nutritional quality of Eucalyptus foliage and its interaction with soil nutrient and light availability.CrossRef | open url image1

Lincoln DE, Fajer ED, Johnson RH (1993) Plant insect herbivore interactions in elevated CO2 environments. Trends in Ecology & Evolution 8, 64–68.
Plant insect herbivore interactions in elevated CO2 environments.CrossRef | 1:STN:280:DC%2BC3M7itVygug%3D%3D&md5=85b7da349a43e8b287f4aa4dc9ce9bddCAS | open url image1

Lindroth RL (2010) Impacts of elevated atmospheric CO2 and O3 on forests: phytochemistry, trophic interactions and ecosystem dynamics. Journal of Chemical Ecology 36, 2–21.
Impacts of elevated atmospheric CO2 and O3 on forests: phytochemistry, trophic interactions and ecosystem dynamics.CrossRef | 1:CAS:528:DC%2BC3cXhs1amsL0%3D&md5=e2b79ec311e1404494bbe972f2bdbdbbCAS | open url image1

Lindroth RL, Kinney KK, Platz CL (1993) Responses of deciduous trees to elevated atmospheric CO2: productivity, phytochemistry and insect performance. Ecology 74, 763–777.
Responses of deciduous trees to elevated atmospheric CO2: productivity, phytochemistry and insect performance.CrossRef | 1:CAS:528:DyaK3sXltlGrtr0%3D&md5=de5cb3fc4b716401d843e65f9057b7a2CAS | open url image1

Loladze I (2002) Rising atmospheric CO2 and human nutrition: toward globally imbalanced plant stoichiometery. Trends in Ecology & Evolution 17, 457–461.
Rising atmospheric CO2 and human nutrition: toward globally imbalanced plant stoichiometery.CrossRef | open url image1

Lovelock C, Kyllo D, Popp M, Isopp H, Virgo A, Winter K (1997) Symbiotic vesicular arbuscular mycorrhizae influence maximum rates of photosynthesis in tropical tree seedlings grown under elevated CO2. Australian Journal of Plant Physiology 24, 185–194.
Symbiotic vesicular arbuscular mycorrhizae influence maximum rates of photosynthesis in tropical tree seedlings grown under elevated CO2.CrossRef | 1:CAS:528:DyaK2sXjs1ajsLo%3D&md5=fc49ba75c309df1c3f7cb53e2e38ffacCAS | open url image1

Lukac M, Calfapietra C, Godbold DL (2003) Production, turnover and mycorrhizal colonization of root systems of three Populus species grown under elevated CO2 (POPFACE). Global Change Biology 9, 838–848.
Production, turnover and mycorrhizal colonization of root systems of three Populus species grown under elevated CO2 (POPFACE).CrossRef | open url image1

Lukac M, Calfapietra C, Lagomarsino A, Loreto F (2010) Global climate change and tree nutrition: effects of elevated CO2 and temperature. Tree Physiology 30, 1209–1220.
Global climate change and tree nutrition: effects of elevated CO2 and temperature.CrossRef | 1:CAS:528:DC%2BC3cXhtFKhtLfK&md5=5d626fbbaf7f91d16e5737edba4cdd6bCAS | 20571150PubMed | open url image1

Martre P, Porter JR, Jamieson PD, Triboi E (2003) Modeling grain nitrogen accumulation and protein composition to understand the sink/source regulations of nitrogen remobilization for wheat. Plant Physiology 133, 1959–1967.
Modeling grain nitrogen accumulation and protein composition to understand the sink/source regulations of nitrogen remobilization for wheat.CrossRef | 1:CAS:528:DC%2BD2cXhvFKm&md5=08d61d7915efd40a260ea2277dd47d88CAS | 14630962PubMed | open url image1

Matros A, Amme S, Kettig B, Buck-Sorlin GH, Sonnewald U, Mock HP (2006) Growth at elevated CO2 concentrations leads to modified profiles of secondary metabolites in tobacco cv. SamsunNN and to increased resistance against infection with potato virus Y. Plant, Cell & Environment 29, 126–137.
Growth at elevated CO2 concentrations leads to modified profiles of secondary metabolites in tobacco cv. SamsunNN and to increased resistance against infection with potato virus Y.CrossRef | 1:CAS:528:DC%2BD28XitFWisb8%3D&md5=6f6db110f1ded35289b6234cf900102bCAS | 17086759PubMed | open url image1

Nowak RS, Ellsworth DS, Smith SD (2004) Functional responses of plants to elevated atmospheric CO2 – do photosynthetic and productivity data from FACE experiments support early predictions? New Phytologist 162, 253–280.
Functional responses of plants to elevated atmospheric CO2 – do photosynthetic and productivity data from FACE experiments support early predictions?CrossRef | open url image1

Olesniewicz KS, Thomas RB (1999) Effects of mycorrhizal colonization on biomass prodution and nitrogen fixation of black locust (Robinia pseudoacacia) seedlings grown under elevated atmospheric carbon dioxide. New Phytologist 142, 133–140.
Effects of mycorrhizal colonization on biomass prodution and nitrogen fixation of black locust (Robinia pseudoacacia) seedlings grown under elevated atmospheric carbon dioxide.CrossRef | open url image1

Olsrud M, Carlsson BA, Svensson BM, Michelsen A, Melillo JM (2010) Responses of fungal root colonization, plant cover and leaf nutrients to long-term exposure to elevated atmospheric CO2 and warming in a subarctic birch forest understorey. Global Change Biology 16, 1820–1829.
Responses of fungal root colonization, plant cover and leaf nutrients to long-term exposure to elevated atmospheric CO2 and warming in a subarctic birch forest understorey.CrossRef | open url image1

Peñuelas J, Estiarte M (1998) Can elevated CO2 affect secondary metabolism and ecosystem function? Trends in Ecology & Evolution 13, 20–24.
Can elevated CO2 affect secondary metabolism and ecosystem function?CrossRef | open url image1

Reich PB, Hobbie SE, Lee TD, Ellsworth DS, West JB, Timan D, Knops JMH, Naeem S, Trost J (2006) Nitrogen limitation constraints sustainability of ecosystem response to CO2. Nature 440, 922–925.
Nitrogen limitation constraints sustainability of ecosystem response to CO2.CrossRef | 1:CAS:528:DC%2BD28XjsVWktLk%3D&md5=b94d3e4dc75ee15adbf43382a77c3b48CAS | 16612381PubMed | open url image1

Rhoades DF (1979) ‘Evolution of chemical defence against herbivores.’ (Academic Press: New York)

Rillig MC (2004) Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecology Letters 7, 740–754.
Arbuscular mycorrhizae and terrestrial ecosystem processes.CrossRef | open url image1

Rillig MC, Allen MF (1999) What is the role of arbuscular mycorrhizal fungi in plant-to-ecosystem responses to elevated atmospheric CO2? Mycorrhiza 9, 1–8.
What is the role of arbuscular mycorrhizal fungi in plant-to-ecosystem responses to elevated atmospheric CO2?CrossRef | open url image1

Rillig MC, Allen MF, Klironomos JN, Field CB (1998) Arbuscular mycorrhizal percent infection and infection intensity of Bromus hordeaceus grown in elevated atmospheric CO2. Mycologia 90, 199–205.
Arbuscular mycorrhizal percent infection and infection intensity of Bromus hordeaceus grown in elevated atmospheric CO2.CrossRef | open url image1

Rogers A, Ainsworth EA, Leakey ADB (2009) Will elevated carbon dioxide concentration amplify the benefits of nitrogen fixation in legumes? Plant Physiology 151, 1009–1016.
Will elevated carbon dioxide concentration amplify the benefits of nitrogen fixation in legumes?CrossRef | 1:CAS:528:DC%2BD1MXhsVCjsb3F&md5=bad9949d385db961a3e3688b202aaba7CAS | 19755541PubMed | open url image1

Rosegrant MW, Cline SA (2003) Global food security: challenges and policies. Science 302, 1917–1919.
Global food security: challenges and policies.CrossRef | 1:CAS:528:DC%2BD3sXps1amsb4%3D&md5=8f2cf744cd375947233f0acf1ebdf23bCAS | 14671289PubMed | open url image1

Rouhier H, Read DJ (1998) The role of mycorrhiza in determining the response of Plantago lanceolata to CO2 enrichment. New Phytologist 139, 367–373.
The role of mycorrhiza in determining the response of Plantago lanceolata to CO2 enrichment.CrossRef | open url image1

Sanders IR, Streitwolf-Engel R, van der Heijden MGA, Boller T, Wiemken A (1998) Increased allocation to external hyphae of arbuscular mycorrhizal fungi under CO2 enrichment. Oecologia 117, 496–503.
Increased allocation to external hyphae of arbuscular mycorrhizal fungi under CO2 enrichment.CrossRef | open url image1

Schädler M, Roeder M, Brandl R, Matthies D (2007) Interacting effects of elevated CO2, nutrient availability and plant species on a generalist invertebrate herbivore. Global Change Biology 13, 1005–1015.
Interacting effects of elevated CO2, nutrient availability and plant species on a generalist invertebrate herbivore.CrossRef | open url image1

Smith SE, Read DJ (2008) ‘Mycorrhizal symbiosis.’ (Academic Press Ltd: Cambridge, UK)

Smith SE, St John BJ, Smith FA, Nicholas DJD (1985) Activity of glutamine synthetase and glutamate dehydrogenase in Trifolium subterraneum L. and Allium cepa L.: effects of mycorrhizal infection and phosphate nutrition. New Phytologist 99, 211–227.
Activity of glutamine synthetase and glutamate dehydrogenase in Trifolium subterraneum L. and Allium cepa L.: effects of mycorrhizal infection and phosphate nutrition.CrossRef | 1:CAS:528:DyaL2MXhs1Grur8%3D&md5=0e870fbccb54e6b6be132a0ca04a96deCAS | open url image1

Smith SE, Smith FA, Jakobsen I (2004) Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytologist 162, 511–524.
Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake.CrossRef | open url image1

Staddon PL, Fitter AH, Graves JD (1999) Effect of elevated atmospheric CO2 on mycorrhizal colonisation, external hyphal production and phosphorus inflow in Plantago lanceolata and Trifolium repens in association with the arbuscular mycorrhizal afungus Glomus mosseae. Global Change Biology 5, 347–358.
Effect of elevated atmospheric CO2 on mycorrhizal colonisation, external hyphal production and phosphorus inflow in Plantago lanceolata and Trifolium repens in association with the arbuscular mycorrhizal afungus Glomus mosseae.CrossRef | open url image1

Staddon PL, Gregersen R, Jakobsen I (2004) The response of two Glomus mycorrhizal fungi and a fine endophyte to elevated atmospheric CO2, soil warming and drought. Global Change Biology 10, 1909–1921.
The response of two Glomus mycorrhizal fungi and a fine endophyte to elevated atmospheric CO2, soil warming and drought.CrossRef | open url image1

Stiling P, Cornelissen T (2007) How does elevated carbon dioxide (CO2) affect plant–herbivore interactions? A field experiment and meta-analysis of CO2-mediated changes on plant chemistry and herbivore performance. Global Change Biology 13, 1823–1842.
How does elevated carbon dioxide (CO2) affect plant–herbivore interactions? A field experiment and meta-analysis of CO2-mediated changes on plant chemistry and herbivore performance.CrossRef | open url image1

Stitt M, Krapp A (1999) The molecular physiological basis for the interaction between elevated carbon dioxide and nutrients. Plant, Cell & Environment 22, 583–621.
The molecular physiological basis for the interaction between elevated carbon dioxide and nutrients.CrossRef | 1:CAS:528:DyaK1MXksVartLo%3D&md5=6f5e295cd4463750b3aa2b367e201b6bCAS | open url image1

Stöcklin J, Schweizer K, Körner C (1998) Effects of elevated CO2 and phosphorus addition on productivity and community composition of intact monoliths from calcareous grassland. Oecologia 116, 50–56.
Effects of elevated CO2 and phosphorus addition on productivity and community composition of intact monoliths from calcareous grassland.CrossRef | open url image1

Syvertsen JP, Graham JH (1999) Phosphorus supply and arbuscular mycorrhizas increase growth and net gas exchange response of two Citrus spp. grown at elevated [CO2]. Plant and Soil 208, 209–219.
Phosphorus supply and arbuscular mycorrhizas increase growth and net gas exchange response of two Citrus spp. grown at elevated [CO2].CrossRef | 1:CAS:528:DyaK1MXltFCrsbk%3D&md5=35dfc368c1c385fbf267220cdc191564CAS | open url image1

Tanaka Y, Yano K (2005) Nitrogen delivery to maize via mycorrhizal hyphae depends on the form of N supplied. Plant, Cell & Environment 28, 1247–1254.
Nitrogen delivery to maize via mycorrhizal hyphae depends on the form of N supplied.CrossRef | 1:CAS:528:DC%2BD2MXhtFGitbnF&md5=caea4d61d5ab3204807a21307675d333CAS | open url image1

Taub DR, Miller B, Allen H (2008) Effects of elevated CO2 on the protein concentration of food crops: a meta-analysis. Global Change Biology 14, 565–575.
Effects of elevated CO2 on the protein concentration of food crops: a meta-analysis.CrossRef | open url image1

Tobar R, Azcón R, Barea JM (1994) Improved nitrogen uptake and transport from 15N-labelled nitrate by external hyphae of arbuscular mycorrhiz under water-stressed conditions. New Phytologist 126, 119–122.
Improved nitrogen uptake and transport from 15N-labelled nitrate by external hyphae of arbuscular mycorrhiz under water-stressed conditions.CrossRef | open url image1

Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phophorus, and atmospheric CO2 in field studies. New Phytologist 164, 347–355.
A meta-analysis of mycorrhizal responses to nitrogen, phophorus, and atmospheric CO2 in field studies.CrossRef | open url image1

Treseder KK, Allen MF (2000) Mycorrhizal fungi have a potential role in soil carbon storage under elevated CO2 and nitrogen deposition. New Phytologist 147, 189–200.
Mycorrhizal fungi have a potential role in soil carbon storage under elevated CO2 and nitrogen deposition.CrossRef | 1:CAS:528:DC%2BD3cXms1yltLo%3D&md5=9e0ed0949334777ba16754e908625446CAS | open url image1

van Aarle IM, Cavagnaro TR, Smith SE, Smith FA, Dickson S (2005) Metabolic activity of Glomus intraradices in Arum- and Paris-type arbuscular mycorrhiza colonization. New Phytologist 166, 611–618.
Metabolic activity of Glomus intraradices in Arum- and Paris-type arbuscular mycorrhiza colonization.CrossRef | 15819923PubMed | open url image1

Veteli TO, Kuokkanen K, Julkenen-Tiitto R, Roininen H, Tahvanainen J (2002) Effects of elevated CO2 and temperature on plant growth and defensive chemistry. Global Change Biology 8, 1240–1252.
Effects of elevated CO2 and temperature on plant growth and defensive chemistry.CrossRef | open url image1

Wand SJE, Midgley GF, Jones MH, Curtis PS (1999) Responses of wild C4 and C3 grass (Poaceae) species to elevated atmospheric CO2 concentration: a meta-analytic test of current theories and perceptions. Global Change Biology 5, 723–741.
Responses of wild C4 and C3 grass (Poaceae) species to elevated atmospheric CO2 concentration: a meta-analytic test of current theories and perceptions.CrossRef | open url image1

Westley J (1988) Mammalian cyanide detoxification with sulfane sulfur. Ciba Foundation Symposium 140, 201–218.

Wieser H, Manderscheid R, Erbs M, Weigel H-J (2008) Effects of elevated atmospheric CO2 concentrations on the quantitative protein composition of wheat grain. Journal of Agricultural and Food Chemistry 56, 6531–6535.
Effects of elevated atmospheric CO2 concentrations on the quantitative protein composition of wheat grain.CrossRef | 1:CAS:528:DC%2BD1cXotFGqtb8%3D&md5=6cf732be55263f1462e2b70a451f4e7cCAS | 18598044PubMed | open url image1

Zagrobelny M, Bak S, Møller BL (2008) Cyanogenesis in plants and arthropods. Phytochemistry 69, 1457–1468.
Cyanogenesis in plants and arthropods.CrossRef | 1:CAS:528:DC%2BD1cXkvVOlsrY%3D&md5=3bd36fde5e1428814cf9cb40402dd053CAS | 18353406PubMed | open url image1

Ziska LH, Emche SD, Johnson EL, George K, Reed DR, Sicher RC (2005) Alterations in the production and concentration of selected alkaloids as a function of rising atmospheric carbon dioxide and air temperature: implications for ethno-pharmacology. Global Change Biology 11, 1798–1807.
Alterations in the production and concentration of selected alkaloids as a function of rising atmospheric carbon dioxide and air temperature: implications for ethno-pharmacology.CrossRef | open url image1



Export Citation Cited By (25)