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Is plant genetic control of ectomycorrhizal fungal communities an untapped source of stable soil carbon in managed forests?

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Abstract

Background

Ectomycorrhizal (ECM) fungi provide one of the main pathways for carbon (C) to move from trees into soils, where these fungi make significant contributions to microbial biomass and soil respiration.

Scope

ECM fungal species vary significantly in traits that likely influence C sequestration, such that forest C sequestration potential may be driven in part by the existing community composition of ECM fungi. Moreover, accumulating experimental data show that tree genotypes differ in their compatibility with particular ECM fungal species, i.e. mycorrhizal traits of forest trees are heritable. Those traits are genetically correlated with other traits for which tree breeders commonly select, suggesting that selection for traits of interest, such as disease resistance or growth rate, could lead to indirect selection for or against particular mycorrhizal traits of trees in forest plantations.

Conclusions

Altogether, these observations suggest that selection of particular tree genotypes could alter the community composition of symbiotic ECM fungi in managed forests, with cascading effects on soil functioning and soil C sequestration.

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References

  • 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 

  • Allen MF (1991) The ecology of mycorrhizae. Cambridge University Press, Cambridge, 184

    Google Scholar 

  • Bardgett RD, Wardle DA (2010) Aboveground-belowground linkages: biotic interactions, ecosystem processes, and global change. Oxford University Press, Oxford

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Buee M, Courty PE, Mignot D, Garbaye J (2007) Soil niche effect on species diversity and catabolic activities in an ectomycorrhizal fungal community. Soil Biol Biochem 39:1947–1955

    Article  CAS  Google Scholar 

  • Buee M, Reich M, Murat C, Morin E, Nilsson RH, Uroz S, Martin F (2009) 454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol 184:449–456

    Article  PubMed  CAS  Google Scholar 

  • Chapela IH, Osher LJ, Horton TR, Henn MR (2001) Ectomycorrhizal fungi introduced with exotic pine plantations induce soil carbon depletion. Soil Biol Biochem 33:1733–1740

    Article  CAS  Google Scholar 

  • Courty PE, Franc A, Garbaye J (2010) Temporal and functional pattern of secreted enzyme activities in an ectomycorrhizal community. Soil Biol Biochem 42:2022–2025

    Article  CAS  Google Scholar 

  • Courty PE, Labbe J, Kohler A, Marcais B, Bastien C, Churin JL, Garbaye J, Le Tacon F (2011) Effect of poplar genotypes on mycorrhizal infection and secreted enzyme activities in mycorrhizal and non-mycorrhizal roots. J Exp Bot 62:249–260

    Article  PubMed  CAS  Google Scholar 

  • Dixon RK, Garrett HE, Stelzer HE (1987) Growth and ectomycorrhizal development of loblolly pine progenies inoculated with 3 isolates of Pisolithus tinctorius. Silvae Genetica 36:240–245

    Google Scholar 

  • Drake JE, Gallet-Budynek A, Hofmockel KS, Bernhardt ES, Billings SA, Jackson RB, Johnsen KS, Lichter J, McCarthy HR, McCormack ML, Moore DJP, Oren R, Palmroth S, Phillips RP, Pippen JS, Pritchard SG, Treseder KK, Schlesinger WH, DeLucia EH, Finzi AC (2011) Increases in the flux of carbon belowground stimulate nitrogen uptake and sustain the long-term enhancement of forest productivity under elevated CO(2). Ecol Lett 14:349–357

    Article  PubMed  Google Scholar 

  • Gadgil RL, Gadgil PD (1971) Mycorrhiza and litter decomposition. Nature 233:133

    Article  PubMed  CAS  Google Scholar 

  • Galik CS, Jackson RB (2009) Risks to forest carbon offset projects in a changing climate. For Ecol Manage 257:2209–2216

    Article  Google Scholar 

  • Gardes M, Bruns TD (1996) Community structure of ectomycorrhizal fungi in a Pinus muricata forest: above- and below-ground views. Can J Bot 74:1572–1583

    Article  Google Scholar 

  • Garten CT, Wullschleger SD, Classen AT (2011) Review and model-based analysis of factors influencing soil carbon sequestration under hybrid poplar. Biomass Bioenergy 35:214–226

    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 

  • Goodale CL, Apps MJ, Birdsey RA, Field CB, Heath LS, Houghton RA, Jenkins JC, Kohlmaier GH, Kurz W, Liu SR, Nabuurs GJ, Nilsson S, Shvidenko AZ (2002) Forest carbon sinks in the Northern Hemisphere. Ecol Appl 12:891–899

    Article  Google Scholar 

  • Heinemeyer A, Hartley IP, Evans SP, De la Fuente JAC, Ineson P (2007) Forest soil CO2 flux: uncovering the contribution and environmental responses of ectomycorrhizas. Glob Chang Biol 13:1786–1797

    Article  Google Scholar 

  • Hobbie EA (2006) Carbon allocation to ectomycorrhizal fungi correlates with belowground allocation in culture studies. Ecology 87:563–569

    Article  PubMed  Google Scholar 

  • Hobbie EA, Agerer R (2010) Nitrogen isotopes in ectomycorrhizal sporocarps correspond to belowground exploration types. Plant Soil 327:71–83

    Article  CAS  Google Scholar 

  • Hoeksema JD, Thompson JN (2007) Geographic structure in a widespread plant–mycorrhizal interaction: pines and false truffles. J Evol Biol 20:1148–1163

    Article  PubMed  CAS  Google Scholar 

  • Hoeksema JD, Piculell B, Thompson JN (2009) Within-population genetic variability in mycorrhizal interactions. Communicative and Integrative Biology 2:110–112

    PubMed  CAS  Google Scholar 

  • Hogberg MN, Hogberg 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  CAS  Google Scholar 

  • Horton TR, Bruns TD (2001) The molecular revolution in ectomycorrhizal ecology: peeking into the black box. Mol Ecol 10:1855–1871

    Article  PubMed  CAS  Google Scholar 

  • Jackson RB, Schlesinger WH (2004) Curbing the US carbon deficit. Proc Natl Acad Sci U S A 101:15827–15829

    Article  PubMed  CAS  Google Scholar 

  • Johnsen KH, Wear D, Oren R, Teskey RO, Sanchez F, Will R, Butnor J, Markewitz D, Richter D, Rials T, Allen HL, Seiler J, Ellsworth D, Maier C, Katul G, Dougherty PM (2001) Carbon sequestration and southern pine forests. J For 99:14–21

    Google Scholar 

  • Jones MD, Twieg BD, Ward V, Barker J, Durall DM, Simard SW (2010) Functional complementarity of Douglas-fir ectomycorrhizas for extracellular enzyme activity after wildfire or clearcut logging. Funct Ecol 24:1139–1151

    Article  Google Scholar 

  • Joyce L, Aber J, McNulty S, Dale V, Hansen A, Irland L, Neilson R, Skog K (2001) Potential consequences of climate variability and change for the forests of the United States. In Climate Change Impacts on the United States. Cambridge University Press, Cambridge, pp 489–523

  • Karlinski L, Rudawska M, Kieliszewska-Rokicka B, Leski T (2010) Relationship between genotype and soil environment during colonization of poplar roots by mycorrhizal and endophytic fungi. Mycorrhiza 20:315–324

    Article  PubMed  Google Scholar 

  • Kiers ET, Hutton MG, Denison RF (2007) Human selection and the relaxation of legume defences against ineffective rhizobia. Proc R Soc B Biol Sci 274:3119–3126

    Article  CAS  Google Scholar 

  • Koide RT, Malcolm GM (2009) N concentration controls decomposition rates of different strains of ectomycorrhizal fungi. Fungal Ecol 2:197–202

    Article  Google Scholar 

  • Korkama T, Pakkanen A, Pennanen T (2006) Ectomycorrhizal community structure varies among Norway spruce (Picea abies) clones. New Phytol 171:815–824

    Article  PubMed  CAS  Google Scholar 

  • Labbe J, Jorge V, Kohler A, Vion P, Marcais B, Bastien C, Tuskan GA, Martin F, Le Tacon F (2011) Identification of quantitative trait loci affecting ectomycorrhizal symbiosis in an interspecific F(1) poplar cross and differential expression of genes in ectomycorrhizas of the two parents: Populus deltoides and Populus trichocarpa. Tree Genetics & Genomes 7:617–627

    Article  Google Scholar 

  • Lal R (2004) Soil carbon sequestration to mitigate climate change. Geoderma 123:1–22

    Article  CAS  Google Scholar 

  • Langley JA, Chapman SK, Hungate BA (2006) Ectomycorrhizal colonization slows root decomposition: the post-mortem fungal legacy. Ecol Lett 9:955–959

    Article  PubMed  Google Scholar 

  • Leake JR, Donnelly DP, Boddy L (2002) Interactions between ectomycorrhizal and saprotrophic fungi. In: Van der Heijden MGA, Sanders IR (eds) Mycorrhizal Ecology. Springer-Verlag, Berlin, pp 345–372

    Google Scholar 

  • Leake JR, Johnson D, Donnelly DP, Muckle GE, Boddy L, Read DJ (2004) Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Canadian Journal of Botany-Revue Canadienne De Botanique 82:1016–1045

    Article  Google Scholar 

  • Leski T, Aucina A, Skridaila A, Pietras M, Riepsas E, Rudawska M (2010) Ectomycorrhizal community structure of different genotypes of Scots pine under forest nursery conditions. Mycorrhiza 20:473–481

    Article  PubMed  Google Scholar 

  • Lilleskov EALEA, Hobbie EA, Horton TR (2011) Conservation of ectomycorrhizal fungi: exploring the linkages between functional and taxonomic responses to anthropogenic N deposition. Fungal Ecol 4:174–183

    Article  Google Scholar 

  • Lindahl BD, de Boer W, Finlay RD (2010) Disruption of root carbon transport into forest humus stimulates fungal opportunists at the expense of mycorrhizal fungi. ISME J 4:872–881

    Article  PubMed  Google Scholar 

  • Lukac M, Calfapietra C, Godbold DL (2003) Production, turnover and mycorrhizal colonization of root systems of three Populus species grown under elevated CO2 (POPFACE). Glob Chang Biol 9:838–848

    Article  Google Scholar 

  • Malajczuk N (1987) Ecology and management of ectomycorrhizal fungi in regenerating forest ecosystems in Australia. In: Sylvia DM, Hung LL, Graham JH (eds) Mycorrhizae in the Next Decade: Practical Applications and Research Priorities. University of Florida, Gainesville, pp 118–120

    Google Scholar 

  • Orwin KH, Kirschbaum MUF, St John MG, Dickie IA (2011) Organic nutrient uptake by mycorrhizal fungi enhances ecosystem carbon storage: a model-based assessment. Ecol Lett 14:493–502

    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 

  • Piculell BJ, Hoeksema JD, Thompson JN (2008) Interactions of biotic and abiotic environmental factors in an ectomycorrhizal symbiosis, and the potential for selection mosaics. BMC Biol 6:23 (11 pages)

    Article  PubMed  Google Scholar 

  • Prestemon JP, Abt RC (2002) The Southern timber market to 2040. J For 100:16–22

    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 14:1252–1264

    Article  Google Scholar 

  • Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53

    Article  PubMed  CAS  Google Scholar 

  • Rooney DC, Killham K, Bending GD, Baggs E, Weih M, Hodge A (2009) Mycorrhizas and biomass crops: opportunities for future sustainable development. Trends Plant Sci 14:542–549

    Article  PubMed  CAS  Google Scholar 

  • Schafer KVR, Oren R, Ellsworth DS, Lai CT, Herrick JD, Finzi AC, Richter DD, Katul GG (2003) Exposure to an enriched CO2 atmosphere alters carbon assimilation and allocation in a pine forest ecosystem. Glob Chang Biol 9:1378–1400

    Article  Google Scholar 

  • Schroter D, Brussaard L, De Deyn G, Poveda K, Brown VK, Berg MP, Wardle DA, Moore J, Wall DH (2004) Trophic interactions in a changing world: modelling aboveground-belowground interactions. Basic Appl Ecol 5:515–528

    Article  Google Scholar 

  • Singh LP, Gill SS, Tuteja N (2011) Unraveling the role of fungal symbionts in plant abiotic stress tolerance. Plant Signal Behav 6:175–191

    Article  PubMed  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, Amsterdam, 787

    Google Scholar 

  • Sthultz CM, Whitham TG, Kennedy K, Deckert R, Gehring CA (2009) Genetically based susceptibility to herbivory influences the ectomycorrhizal fungal communities of a foundation tree species. New Phytol 184:657–667

    Article  PubMed  CAS  Google Scholar 

  • Tagu D, Bastien C, Faivre-Rampant P, Garbaye J, Vion P, Villar M, Martin F (2005) Genetic analysis of phenotypic variation for ectomycorrhiza formation in an interspecific F1 poplar full-sib family. Mycorrhiza 15:87–91

    Article  PubMed  CAS  Google Scholar 

  • Taylor AFS, Gebauer G, Read DJ (2004) Uptake of nitrogen and carbon from double-labelled (N-15 and C-13) glycine by mycorrhizal pine seedlings. New Phytol 164:383–388

    Article  CAS  Google Scholar 

  • Tedersoo L, Nilsson RH, Abarenkov K, Jairus T, Sadam A, Saar I, Bahram M, Bechem E, Chuyong G, Koljag U (2010) 454 Pyrosequencing and Sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases. New Phytologist 188:291-301

    Google Scholar 

  • Toth R, Toth D, Starke D, Smith DR (1990) Vesicular-arbuscular mycorrhizal colonization in Zea mays affected by breeding for resistance to fungal pathogens. Canadian Journal of Botany-Revue Canadienne De Botanique 68:1039–1044

    Article  Google Scholar 

  • Treseder KK, Allen MF (2000) Mycorrhizal fungi have a potential role in soil carbon storage under elevated CO2 and nitrogen deposition. New Phytol 147:189–200

    Article  CAS  Google Scholar 

  • Treseder KK, Masiello CA, Lansing JL, Allen MF (2004) Species-specific measurements of ectomycorrhizal turnover under N-fertilization: combining isotopic and genetic approaches. Oecologia 138:419–425

    Article  PubMed  Google Scholar 

  • Trocha LK, Mucha J, Eissenstat DM, Reich PB, Oleksyn J (2010) Ectomycorrhizal identity determines respiration and concentrations of nitrogen and non-structural carbohydrates in root tips: a test using Pinus sylvestris and Quercus robur saplings. Tree Physiol 30:648–654

    Article  PubMed  CAS  Google Scholar 

  • van der Putten WH, Bardgett RD, de Ruiter PC, Hol WHG, Meyer KM, Bezemer TM, Bradford MA, Christensen S, Eppinga MB, Fukami T, Hemerik L, Molofsky J, Schadler M, Scherber C, Strauss SY, Vos M, Wardle DA (2009) Empirical and theoretical challenges in aboveground-belowground ecology. Oecologia 161:1–14

    Article  PubMed  Google Scholar 

  • Wallander H, Massicotte HB, Nylund JE (1997) Seasonal variation in protein, ergosterol and chitin in five morphotypes of Pinus sylvestris L ectomycorrhizae in a mature Swedish forest. Soil Biol Biochem 29:45–53

    Article  CAS  Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, Setala H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633

    Article  PubMed  CAS  Google Scholar 

  • Whitham TG, Bailey JK, Schweitzer JA, Shuster SM, Bangert RK, Leroy CJ, Lonsdorf EV, Allan GJ, DiFazio SP, Potts BM, Fischer DG, Gehring CA, Lindroth RL, Marks JC, Hart SC, Wimp GM, Wooley SC (2006) A framework for community and ecosystem genetics: from genes to ecosystems. Nat Rev Genet 7:510–523

    Article  PubMed  CAS  Google Scholar 

  • Zhu YG, Smith SE, Barritt AR, Smith FA (2001) Phosphorus (P) efficiencies and mycorrhizal responsiveness of old and modern wheat cultivars. Plant Soil 237:249–255

    Article  CAS  Google Scholar 

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Correspondence to Jason D. Hoeksema.

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Hoeksema, J.D., Classen, A.T. Is plant genetic control of ectomycorrhizal fungal communities an untapped source of stable soil carbon in managed forests?. Plant Soil 359, 197–204 (2012). https://doi.org/10.1007/s11104-012-1201-z

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