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Effects of twice-ambient carbon dioxide and nitrogen amendment on biomass, nutrient contents and carbon costs of Norway spruce seedlings as influenced by mycorrhization with Piloderma croceum and Tomentellopsis submollis

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Abstract

Elevated tropospheric CO2 concentrations may increase plant carbon fixation. In ectomycorrhizal trees, a considerable portion of the synthesized carbohydrates can be used to support the mutualistic fungal root partner which in turn can benefit the tree by increased nutrient supply. In this study, Norway spruce seedlings were inoculated with either Piloderma croceum (medium distance “fringe” exploration type) or Tomentellopsis submollis (medium distance “smooth” exploration type). We studied the impact of either species regarding fungal biomass production, seedling biomass, nutrient status and nutrient use efficiency in rhizotrons under ambient and twice-ambient CO2 concentrations. A subset was amended with ammonium nitrate to prevent nitrogen imbalances expected under growth promotion by elevated CO2. The two fungal species exhibited considerably different influences on growth, biomass allocation as well as nutrient uptake of spruce seedlings. P. croceum increased nutrient supply and promoted plant growth more strongly than T. submollis despite considerably higher carbon costs. In contrast, seedlings with T. submollis showed higher nutrient use efficiency, i.e. produced plant biomass per received unit of nutrient, particularly for P, K and Mg, thereby promoting shoot growth and reducing the root/shoot ratio. Under the given low soil nutrient availability, P. croceum proved to be a more favourable fungal partner for seedling development than T. submollis. Additionally, plant internal allocation of nutrients was differently influenced by the two ECM fungal species, particularly evident for P in shoots and for Ca in roots. Despite slightly increased ECM length and biomass production, neither of the two species had increased its capacity of nutrient uptake in proportion to the rise of CO2. This lead to imbalances in nutritional status with reduced nutrient concentrations, particularly in seedlings with P. croceum. The beneficial effect of P. croceum thus diminished, although the nutrient status of its host plants was still above that of plants with T. submollis. We conclude that the imbalances of nutrient status in response to elevated CO2 at early stages of plant development are likely to prove particularly severe at nutrient-poor soils as the increased growth of ECM cannot cover the enhanced nutrient demand. Hyphal length and biomass per unit of ectomycorrhizal length as determined for the first time for P. croceum amounted to 6.9 m cm−1 and 6.0 μg cm−1, respectively, across all treatments.

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References

  • Agerer R (1987–2008) Colour atlas of ectomycorrhizae. 1st–14th del. Einhorn, Schwäbisch Gmünd

  • Agerer R (1998) Tomentellopsis submollis. In: Agerer R (ed) Colour atlas of ectomycorrhizae, plate 138. Einhorn, Schwäbisch Gmünd

    Google Scholar 

  • Agerer R (1999) Never change a functionally successful principle: the evolution of Boletales s. l. (Hymenomycetes, Basidiomycota) as seen from below-ground features. Sendtnera 6:5–91

    Google Scholar 

  • Agerer R (2001) Exploration types of ectomycorrhizae. A proposal to classify ectomycorrhizal mycelial systems according to their patterns of differentiation and putative ecological importance. Mycorrhiza 11:107–114

    Article  Google Scholar 

  • Agerer R (2007) Diversity of ectomycorrhizae as seen from below and above ground: the exploration types. Z Mykol 73:61–88

    Google Scholar 

  • Agerer R, Rambold G (1998) DEEMY, a DELTA-based information system for characterization and determination of ectomtcorrhizae, version 1.1. Mycology Section, Institute for Systematic Botany, University of München, München

  • Agerer R, Göttlein A (2003) Correlations between projection area of ectomycorrhizae and H2O extractable nutrients in organic soil layers. Mycol Prog 2:45–52

    Article  Google Scholar 

  • Agerer R, Raidl S (2004) Distance related half-quantitative estimation of the emanating ectomycorrhizal mycelia of Cortinarius obtusus and Tylospora asterophora. Mycological Progress 3:57–64

    Article  Google Scholar 

  • Agerer R, Rambold G (2004–2009 [first posted on 2004-06-01; most recent update: 2009-01-26]). DEEMY—an information system for characterization and determination of ectomycorrhizae. München

  • Alberton O, Kuyper TW (2009) Ectomycorrhizal fungi associated with Pinus sylvestris seedlings respond differently to increased carbon and nitrogen availability: implications for ecosystem responses to global change. Glob Chang Biol 15(1):166–175

    Article  Google Scholar 

  • Alberton O, Kuyper TW, Gorissen A (2005) Taking mycocentrism seriously: mycorrhizal fungal and plant responses to elevated CO2. New Phytol 167:859–868

    Article  CAS  PubMed  Google Scholar 

  • Alberton O, Kuyper TW, Gorisson A (2007) Competition for nitrogen between Pinus sylvestris and ectomycorrhizal fungi generates potential for negative feedback under elevated CO2. Plant Soil 296:159–172

    Article  CAS  Google Scholar 

  • Alexander IJ, Fairley RJ (1983) Effects of N fertilization on populations of fine roots and mycorrhizas in spruce humus. Plant Soil 71:49–54

    Article  CAS  Google Scholar 

  • Allen MF (1991) The ecology of mycorrhizae. Cambridge University Press, Cambridge

    Google Scholar 

  • Anderson IC, Cairney JWG (2007) Ectomycorrhizal fungi: exploring the mycelial frontier. FEMS Microbiol Rev 31(4):388–406

    Article  CAS  PubMed  Google Scholar 

  • Arnebrant K, Söderström B (1992) Effects of fertilizer treatments on ectomycorrhizal colonization potential in two Scots pine forests in Sweden. For Ecol Manag 53:77–89

    Article  Google Scholar 

  • Arocena JM, Glowa KR, Masicotte HB (2001) Calcium-rich hypha encrustations on Piloderma. Mycorrhiza 10:209–215

    Article  CAS  Google Scholar 

  • Bååth E, Söderström B (1979) Fungal biomass and fungal immobilization of plant nutrients in Swedish coniferous forest soils. Rev Ecol Biol Soil 16:477–489

    Google Scholar 

  • Bakken LR, Olsen RA (1983) Buoyant densities and dry-matter contents of microorganisms: conversion of a measured biovolume into biomass. Appl Environ Microbiol 45:1188–1195

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bidartondo MI, Ek H, Wallander H, Söderström B (2001) Do nutrient additions alter carbon sink strength of ectomycorrhizal fungi? New Phytol 151:543–550

    Article  CAS  Google Scholar 

  • BMVEL (2005) Handbuch Forstliche Analytik. Bundesministerium f. Verbraucherschutz, Ernährung und Landwirtschaft, Bonn

  • Brand F (1991a) Ektomykorrhizen an Fagus sylvatica. Charakterisierung und Identifizierung, ökologische Kennzeichnung und unsterile Kultivierung. Libri botanici vol 2, IHW, Eching, pp 1–229

  • Brand F (1991b) Piloderma croceum. In: Agerer R (ed) Colour atlas of ectomycorrhizae, plate 62. Einhorn, Schwäbisch Gmünd

    Google Scholar 

  • Bücking H, Heyser W (1999) Elemental composition and function of polyphosphates in ectomycorrhizal fungi—an X-ray microanalytical study. Mycol Res 103:31–39

    Article  Google Scholar 

  • Cairney JWG, Jennings DH, Agerer R (1991) The nomenclature of fungal multi-hyphal linear aggregates. Cryptogam Bot 2(3):246–251

    Google Scholar 

  • Chapin FS III (1980) The mineral nutrition of wild plants. Ann Rev Ecol Syst 11:233–260

    Article  CAS  Google Scholar 

  • Colpaert JV, van Tichelen KK (1996) Mycorrhizas and environmental stress. In: Frankland JC, Magan N, Gadd GM (eds) Fungi and environmental change. Symposium of the British Mycological Society. Cambridge University Press, Cambridge, pp 109–128

  • Colpaert JV, van Assche JA, Luijtens K (1992) The growth of the extramatrical mycelium of ectomycorrhizal fungi and the growth responses of Pinus sylvestris L. New Phytol 120:127–135

    Article  Google Scholar 

  • Conroy JP, Milham PJ, Bevege DI, Barlow EWR (1990) Influence of phosphorus deficiency on the growth response of four families of Pinus radiata seedlings to CO2-enriched atmospheres. For Ecol Manag 30:175–188

    Article  Google Scholar 

  • Duddridge JA, Malibari A, Read DJ (1980) Structure and function of mycorrhizal rhizomorphs with special reference to their role in water transport. Nature (London) 287:834–836

    Article  Google Scholar 

  • Ek H (1997) The influence of nitrogen fertilization on the carbon economy of Paxillus inolutus in ectomycorrhizal association with Betula pendula. New Phytol 135:133–142

    Article  CAS  Google Scholar 

  • Ericsson T (1995) Growth and shoot: root ratio of seedlings in relation to nutrient availability. Plant Soil 168–169:205–214

    Article  Google Scholar 

  • Frankland JC, Lindley AK, Swift MJ (1978) A comparison of two methods for the estimation of mycelial biomass in leaf litter. Soil Biol Biochem 10:323–333

    Article  CAS  Google Scholar 

  • Fransson PMA, Taylor AFS, Finlay RD (2000) Effects of continuous optimal fertilization on belowground ectomycorrhizal community structure in a Norway spruce forest. Tree Physiol 20:599–606

    Article  PubMed  Google Scholar 

  • Fransson PM, Taylor AF, Finlay RD (2005) Mycelial production, spread and root colonisation by the ectomycorrhizal fungi Hebeloma crustuliniforme and Paxillus involutus under elevated atmospheric CO2. Mycorrhiza 15:25–31

    Article  PubMed  Google Scholar 

  • Franz F (1994) Ektomykorrhizen der Fichte: Identifizierung, Ultrastruktur und Miroelementanalyse (EELS, ESI). Diss Univ Bayreuth

  • Garcia MO, Ovasapyan T, Greas M, Treseder KK (2008) Mycorrhizal dynamics under elevated CO2 and nitrogen fertilization in a warm temperate forest. Plant Soil 303:301–310

    Article  CAS  Google Scholar 

  • Godbold DL, Berntson GM (1997) Elevated atmospheric CO2 concentration changes ectomycorrhizal morphotype assemblages in Betula papyrifera. Tree Physiol 17:347–350

    Article  CAS  PubMed  Google Scholar 

  • Godbold DL, Berntson GM, Bazzaz FA (1997) Growth and mycorrhizal colonization of three North American tree species under elevated CO2. New Phytol 137:433–440

    Article  CAS  Google Scholar 

  • Godbold DL, Hoosbeek MR, Lukac M, Cotrufo MF, Janssens IA, Ceulemans R, Polle A, Velthorst EJ, Scarascia-Mugnozza G, De Angelis P, Miglietta F, Peressotti A (2006) Mycorrhizal hyphal turnover as a dominant process for carbon input into soil organic matter. Plant Soil 281:15–24

    Article  CAS  Google Scholar 

  • Gorissen A, Kuyper TW (2000) Fungal species-specific responses of ectomycorrhizal Scots pine (Pinus sylvestris) to elevated CO2. New Phytol 146:163–168

    Article  CAS  Google Scholar 

  • Handa T, Hagedorn F, Hättenschwiler S (2008) No stimulation in root production in response to 4 years of in situ CO2 enrichment at the Swiss treeline. Funct Ecol 22:348–358

    Article  Google Scholar 

  • Haug I, Pritsch K (1992) Ectomycorrhizal types of spruce (Picea abies (L.) Karst.) in the Black Forest. A microscopical atlas. Kernforschungszentrum Karlsruhe, PEF-Ber, pp 1–89

  • Högberg MN, Högberg P (2002) Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil. New Phytol 154:791–795

    Article  Google Scholar 

  • Holmgren PK, Holmgren NH, Barnett LC (1990) Index herbariorum. Part I. Herbaria of the world. 8th edn. [Regnum Vegetabile No. 120] New York Botanical Garden, New York (http://www.nybg.org/bsci/ih/ih.html)

  • Ineichen K, Wiemken V, Wiemken A (1995) Shoots, roots and ectomycorrhiza formation of pine seedlings at elevated atmospheric carbon dioxide. Plant Cell Environ 18:703–707

    Article  Google Scholar 

  • IPCC (2007) Zusammenfassung für politische Entscheidungsträger. In: Klimaänderung 2007: Wissenschaftliche Grundlagen. Beitrag der Arbeitsgruppe I zum Vierten Sachstandsbericht des Zwischenstaatlichen Ausschusses für Klimaänderung (IPCC), Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL, eds, Cambridge University Press, Cambridge, United Kingdom und New York, NY, USA. Deutsche Übersetzung durch ProClim-, österreichisches Umweltbundesamt, deutsche IPCC-Koordinationsstelle, Bern/Wien/Berlin, 2007

  • Iversen CM (2010) Digging deeper: fine-root responses to rising atmospheric [CO2] concentration in forest ecosystems. New Phytol 186:346–357

    Article  PubMed  Google Scholar 

  • Janssens I, Crookshanks M, Taylor G, Ceulemans R (1998) Elevated atmospheric CO2 increases fine root production, respiration, rhizosphere respiration and soil CO2 efflux in Scots pine seedlings. Glob Chang Biol 4:871–878

    Article  Google Scholar 

  • Jentschke G, Brandes B, Kuhn AJ, Schröder WH, Godbold DL (2001) Interdependence of phosphorus, nitrogen, potassium and magnesium translocation by the ectomycorrhizal fungus Paxillus involutus. New Phytol 149:327–337

    Article  CAS  Google Scholar 

  • Johnson DW, Ball T, Walker RF (1995) Effects of elevated CO2 and nitrogen on nutrient uptake in ponderosa pine seedlings. Plant Soil 168(169):535–545

    Article  Google Scholar 

  • Johnson MG, Rygiewicz PT, Tingey DT, Phillips DL (2006) Elevated CO2 and elavated temerature have no effect on Douglas-fir fine-root dynamics in nitrogen-poor soil. New Phytol 170:345–356

    Article  CAS  PubMed  Google Scholar 

  • Jones MD, Durall DM, Tinker PB (1990) Phosphorus relationship and production of extramatrical hyphae by two types of willow ectomycorrhizas at different soil phosphorus levels. New Phytol 115(2):259–268

    Article  CAS  Google Scholar 

  • Jones MD, Durall DM, Tinker PB (1991) Fluxes of carbon and phosphorus between symbionts in willow ectomycorrhizas and their changes with time. New Phytol 119:99–106

    Article  CAS  Google Scholar 

  • Kammerbauer H, Agerer R, Sandermann H (1989) Studies on ectomycorrhiza XXII. Mycorrhizal rhizomorphs of Thelephora terrestris and Pisolithus tinctorius in association with Norway spruce (Picea abies): formation in vitro and translocation of phosphate. Trees 3:78–84

    Article  Google Scholar 

  • Kasurinen A, Helmisaari H-S, Holopainen T (1999) The influence of elevated CO2 and O3 on fine roots and mycorrhizas of naturally growing young Scots pine trees during three exposure years. Glob Chang Biol 5:771–780

    Article  Google Scholar 

  • King JS, Hanson PJ, Bernhardt E, DeAngelis P, Norby RJ, Pregitzer KS (2004) A multiyear synthesis of soil respiration responses to elevated atmospheric CO2 from four forest FACE experiments. Glob Chang Biol 10:1027–1042

    Article  Google Scholar 

  • Koch N, Andersen CP, Raidl S, Agerer R, Matyssek R, Grams TEE (2007) Temperature–respiration relationships differ in mycorrhizal and non-mycorrhizal root systems of Picea abies (L.) Karst. Plant Biol 9:545–549

    Article  CAS  PubMed  Google Scholar 

  • Köljalg U, Tammi H, Timonen S, Agerer R, Sen R (2001) ITS rDNA sequence-based positioning of pink-type ectomycorrhizas and Tomentellopsis species from boreal and temperate forests. Mycol Progr 1:81–92

    Article  Google Scholar 

  • Kunzweiler K, Kottke I (1986) Quantifizierung von Mycel im Boden. In: Einsele G (ed) Das landschaftsökologische Forschungsprojekt Naturpark Schönbuch, DFG-Forschungsbericht, VHV Weinheim, pp 429–441

  • Leake J, Johnson D, Donelly D, Muckle G, Boddy L, Read D (2004) Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystems. Can J Bot 82:1016–1045

    Article  Google Scholar 

  • Lewis JD, Strain BR (1996) The role of mycorrhizas in the response of Pinus taeda seedlings to elevated CO2. New Phytol 133:431–443

    Article  Google Scholar 

  • Lewis JD, Thomas RB, Strain BR (1994) Effect of elevated CO2 on mycorrhizal colonization of loblolly pine (Pinus taeda L.) seedlings. Plant and Soil 165:81–88

    Article  CAS  Google Scholar 

  • Marschner H, Kirkby E, Cakmak I (1996) Effect of mineral nutritional status on shoot–root partitioning of photoassimilates and cycling of mineral nutrients. J Exp Bot 47:1255–1263

    Article  CAS  PubMed  Google Scholar 

  • Marx DH (1969) The influence of ectotrophic mycorrhizal fungi on the resistance of pine roots to pathogenic infections: I. Antagonism of mycorrhizal fungi to root pathogenic fungi and soil bacteria. Phytopathology 59:153–163

    Google Scholar 

  • Matuszkiewicz W (1962) Zur Systematik der natürlichen Kiefernwälder des mittel- und osteuropäischen Flachlandes. Mitt. flor.-soz. Arbeitsgem., Stolzenau/Weser, N.F 9:145–186

    Google Scholar 

  • McCarthy HR, Oren R, Johnsen KH, Gallet-Budynek A, Pritchard SG, Cook CW, LaDeau SL, Jackson RB, Finzi AC (2010) Re-assessment of plant carbon dynamics at the Duke free-air CO2 enrichment site: interactions of atmospheric [CO2] with nitrogen and water availability over stand development. New Phytol 185:514–528

    Article  CAS  PubMed  Google Scholar 

  • Millard P, Sommerkorn M, Grelet GA (2007) Environmental change and carbon limitation in trees: a biochemical, ecophysiological and ecosystem appraisal. New Phytol 175:11–28

    Article  CAS  PubMed  Google Scholar 

  • Moorhead DL, Linkins AE (1997) Elevated CO2 alters belowground exoenzyme activities in tussock tundra. Plant Soil 189:321–329

    Article  CAS  Google Scholar 

  • Mousseau M, Saugier B (1992) The direct effect of increased CO2 on gas exchange and growth of forest tree species. J Exp Bot 43:1121–1130

    Article  Google Scholar 

  • Nakayama FS, Hulukab G, Kimballa BA, Lewinc KF, Nagyc J, Hendrey GR (1994) Soil carbon dioxide fluxes in natural and CO2-enriched systems. Agric For Meteorol 70:131–140

    Article  Google Scholar 

  • Nilsson LO (2004) External mycelia of mycorrhizal fungi. Ph.D. thesis, Department of Ecology, Lund University, Sweden

  • Norby JN, O’Neill EG, Luxmoore RJ (1986) Effects of atmospheric CO2 enrichment on the growth and mineral nutrition of Quercus alba seedlings in nutrient-poor soil. Plant Physiol 82:83–89

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Norby RJ, O’Neill EG, Hood WG, Luxmoore RJ (1987) Carbon allocation, root exudation and mycorrhizal colonization of Pinus echinata seedlings grown under CO2 enrichment. Tree Physiol 3:203–210

    Article  CAS  PubMed  Google Scholar 

  • Norby RJ, Ledford J, Reilly CD, Miller NE, O’Neill EG (2004) Fine-root production dominates response of a deciduous forest to atmospheric CO2 enrichment. Proc Natl Acad Sci 101:9689–9693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Neill EG (1994) Responses of soil biota to elevated atmospheric carbon dioxide. Plant Soil 165:55–65

    Article  Google Scholar 

  • O’Neill EG, Luxmoore RJ, Norby RJ (1987) Increases in mycorrhizal colonization and seedling growth in Pinus echinata and Quercus alba in an enriched CO2 atmosphere. Can J For Res 17:878–883

    Article  Google Scholar 

  • Parrent JL, Vilgalys R (2007) Biomass and compositional responses of ectomycorrhizal fungal hyphae to elevated CO2 and nitrogen fertilization. New Phytol 176:164–174

    Article  PubMed  Google Scholar 

  • Parrent JL, Morris WF, Vilgalys R (2006) CO2-enrichment and nutrient availability alter ectomycorrhizal fungal communities. Ecology 87:2278–2287

    Article  PubMed  Google Scholar 

  • Plassard C, Guérin-Laguette A, Véry A-A, Casarin V, Thibaud J-B (2002) Local measurements of nitrate and potassium fluxes along roots of maritime pine. Effects of ectomycorrhizal symbiosis. Plant Cell Environ 25:75–84

    Article  Google Scholar 

  • Pregitzer KS, Zak DR, Maziasz J, DeForest J, Curtis PS, Lussenhop J (2000) Interactive effects of atmospheric CO2 and soil-N availability on fine roots of Populus tremuloides. Ecol Appl 10:18–33

    Google Scholar 

  • Pritchard SG, Rogers HH, Davis M, van Santen E, Prior SA, Schlesinger WH (2001) The influence of elevated atmosphereic CO2 on fine root dynamics in an intact temperate forest. Glob Chang Biol 7:829–837

    Article  Google Scholar 

  • Pritchard SG, Strand AE, McCormack ML, Davis MA, Oren R (2008) Mycorrhizal and rhizomorph dynamics in a loblolly pine forest during 5 years of free-air-CO2-enrichment. Glob Chang Biol 14:1–13

    Google Scholar 

  • Raidl S (1997) Studien zur Ontogenie an Rhizomorphen von Ektomykorrhizen. Bibliotheca Mycologica, vol 169, Cramer, Braunschweig, pp 1–184

  • Read DJ (1992) The mycorrhizal mycelium. In: Allen MF (ed) Mycorrhizal functioning. An integrative plant–fungal process. Chapman & Hall, New York, pp 102–133

    Google Scholar 

  • Rey A, Jarvis PG (1997) Growth response of young birch trees (Betula pendula Roth.) after four and a half years of CO2 exposure. Ann Bot 80:809–816

    Article  Google Scholar 

  • Rogers HH, Peterson CM, McCrimmon JN, Cure JD (1992) Response of plant roots to elevated atmospheric carbon dioxide. Plant Cell Environ 15:749–752

    Article  CAS  Google Scholar 

  • Rouhier H, Read DJ (1999) Plant and fungal responses to elevated atmospheric CO2 in mycorrhizal seedlings of Betula pendula. Environ Exp Bot 42:231–241

    Article  Google Scholar 

  • Rousseau JV, Sylvia DM, Fox AJ (1994) Contribution of ectomycorrhiza to the potential nutrient-absorbing surface of pine. New Phytol 128:639–644

    Article  Google Scholar 

  • Runion GB, Mitchell RJ, Rogers HH, Prior SA, Counts TK (1997) Effects of nitrogen and water limitation and elevated CO2 on ectomycorrhiza of longleaf pine. New Phytol 137:681–689

    Article  Google Scholar 

  • Rygiewicz PT, Andersen CP (1994) Mycorrhiza alter quality and quantity of carbon allocated below ground. Nature (London) 369:58–60

    Article  Google Scholar 

  • Rygiewicz PT, Johnson MG, Ganio LM, Tingey DT, Storm MJ (1997) Lifetime and temporal occurrence of ectomycorrhizae on ponderosa pine (Pinus ponderosa Laws.) seedlings grown under varied atmospheric CO2 and nitrogen levels. Plant Soil 189:275–287

    Article  CAS  Google Scholar 

  • Schlesinger WH, Andrews JA (2000) Soil respiration and the global carbon cycle. Biogeochemistry 48:7–20

    Article  CAS  Google Scholar 

  • Schubert R, Raidl S, Funk R, Bahnweg G, Müller-Starck G, Agerer R (2003) Quantitative detection of agar-cultivated and rhizotron-grown Piloderma croceum Erikss. & Hjortst. by ITS-based fluorescent PCR. Mycorrhiza 13:159–165

    Article  CAS  PubMed  Google Scholar 

  • Segmüller S, Rennenberg H (1994) Interactive effects of mycorrhization and elevated carbon dioxide on growth of young pedunculate oak (Quercus pedunculata L.) trees. Plant Soil 167:325–329

    Article  Google Scholar 

  • Simard SW, Durall DM, Jones MD (2002) Carbon and nutrient fluxes within and between mycorrhizal plants. In: van der Heijden MGA, Sanders IR (eds) Mycorrhizal ecology. Ecological studies 157. Springer, Berlin, pp 33–74

  • Sittig U (1999) Zur saisonalen Dynamik von Ektomykorrhizen der Buche (Fagus sylvatica L.). Ber Forsch Waldökosyst 162:1–119

    Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, San Diego

    Google Scholar 

  • Söderström B, Read DJ (1987) Respiratory activity of intact and excised ectomycorrhizal mycelial systems growing in unsterilized soil. Soil Biol Biochem 19:231–236

    Article  Google Scholar 

  • Stalpers JA (1993) The aphyllophoraceous fungi I: kerys to the species of the Thelephorales. Studies in Mycology 35:1–168

    Google Scholar 

  • Thomas SM, Whitehead D, Reid JB, Cook FJ, Adams JA, Leckie AC (1999) Growth, loss, and vertical distribution of Pinus radiata fine roots growing at ambient and elevated CO2 concentration. Glob Chang Biol 5:07–121

    Article  Google Scholar 

  • Tingey DT, Phillips DL, Johnson MG (2000) Elevated CO2 and conifer roots: effects on growth, life span and turnover. New Phytol 147:87–103

    Article  CAS  Google Scholar 

  • Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347–355

    Article  Google Scholar 

  • Turnau K, Berger A, Loewe A, Einig W, Hampp R, Chalot M, Dizengremel P, Kottke I (2001) Carbon dioxide concentration and nitrogen input affect the C and N storage pools in Amanita muscaria–Picea abies mycorrhizae. Tree Physiol 21:93–99

    Article  CAS  PubMed  Google Scholar 

  • Walker RF, Geisinger DR, Johnson DW, Ball JT (1995) Interactive effects of atmospheric CO2 enrichment and soil N on growth and ectomycorrhizal colonization of ponderosa pine seedlings. Forest Sci 41:491–500

    Google Scholar 

  • Wang YP, Rey A, Jarvis PG (1998) Carbon balance of young birch trees grown in ambient and elevated atmospheric CO2 concentrations. Glob Chang Biol 4:797–807

    Article  Google Scholar 

  • Wiemken V, Laczko E, Ineichen K, Boller T (2001) Effects of elevated carbon dioxide and nitrogen fertilization on mycorrhizal fine roots and the soil microbial community in beech–spruce ecosystems on siliceous and calcareous soil. Microb Ecol 42:126–135

    CAS  PubMed  Google Scholar 

  • Zak DR, Pregitzer KS, King JS, Holmes WE (2000) Elevated atmospheric CO2, fine roots and the response of soil microorganisms: a review and hypothesis. New Phytol 147:201–222

    Article  CAS  Google Scholar 

  • Zhu Y-G, Miller RM (2003) Carbon cycling by arbuscular mycorrhizal fungi in soil plant systems. Trends Plant Sci 8:407–409

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was funded by the German Research Foundation (DFG) as part of the interdisciplinary research program “SFB 607—Growth and Parasite Defense” (sub-projects B7 and B10). We appreciate very much the help provided by our technicians E. Marksteiner and C. Bubenzer-Hange. The Department of Environmental Engineering at the German Research Center for Environmental Health is kindly acknowledged for providing the greenhouse facilities.

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  1. Department of Biology I and GeoBio-Center (LMU), Division of Organismic Biology: Mycology, Ludwig-Maximilians-Universität München, Menzinger Str. 67, 80638, Munich, Germany

    Rosemarie Barbara Weigt, Stefan Raidl, Rita Verma & Reinhard Agerer

  2. Department of Ecology and Ecosystem Management, Forest Nutrition and Water Resources, Technische Universität München, Hans-Carl-von-Carlowitz-Platz 2, 85350, Freising, Germany

    Hermann Rodenkirchen & Axel Göttlein

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Weigt, R.B., Raidl, S., Verma, R. et al. Effects of twice-ambient carbon dioxide and nitrogen amendment on biomass, nutrient contents and carbon costs of Norway spruce seedlings as influenced by mycorrhization with Piloderma croceum and Tomentellopsis submollis . Mycorrhiza 21, 375–391 (2011). https://doi.org/10.1007/s00572-010-0343-1

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  • DOI: https://doi.org/10.1007/s00572-010-0343-1

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