Advertisement

Mycorrhiza

, Volume 28, Issue 4, pp 343–356 | Cite as

Impact of soil pedogenesis on the diversity and composition of fungal communities across the California soil chronosequence of Mendocino

  • P. E. Courty
  • M. Buée
  • J. J. T. Tech
  • D. Brulé
  • Y. Colin
  • J. H. J. Leveau
  • S. Uroz
Original Article

Abstract

Understanding how soil pedogenesis affects microbial communities and their in situ activities according to ecosystem functioning is a central issue in soil microbial ecology, as soils represent essential nutrient reservoirs and habitats for the biosphere. To address this question, soil chronosequences developed from a single, shared mineralogical parent material and having the same climate conditions are particularly useful, as they isolate the factor of time from other factors controlling the character of soils. In our study, we considered a natural succession of uplifted marine terraces in Mendocino, CA, ranging from highly fertile in the younger terrace (about 100,000 years old) to infertile in the older terraces (about 300,000 years old). Using ITS amplicon pyrosequencing, we analysed and compared the diversity and composition of the soil fungal communities across the first terraces (T1 to T3), with a specific focus in the forested terraces (T2 and T3) on soil samples collected below trees of the same species (Pinus muricata) and of the same age. While diversity and richness indices were highest in the grassland (youngest) terrace (T1), they were higher in the older forested terrace (T3) compared to the younger forested terrace (T2). Interestingly, the most abundant ectomycorrhizal (ECM) taxa that we found within these fungal communities showed high homology with ITS Sanger sequences obtained previously directly from ECM root tips from trees in the same study site, revealing a relative conservation of ECM diversity over time. Altogether, our results provide new information about the diversity and composition of the fungal communities as well as on the dominant ECM species in the soil chronosequence of Mendocino in relation to soil age and ecosystem development.

Keywords

Soil chronosequence ITS-based pyrosequencing Fungi Ectomycorrhizal fungi Soil nutrients Soil horizons pH 

Notes

Funding information

This work was funded by a France-Berkeley Fund grant, the ANR JCJC SVSE7 “BACTOWEATHER,” and the Labex ARBRE “INABACT” projects. The authors thank Renee Pasquinelli for their help during sampling and helpful discussions. The authors thank Drs. HV Moeller, MP Turpault, and A. Cébron for helpful discussions. Y. Colin is a postdoctoral scientist supported by grants from ANR, ANDRA, and Lorraine Region. The UMR1136 is supported by the French Agency through the Laboratory of Excellence Arbre (ANR-11-LABX-0002-01).

Supplementary material

572_2018_829_MOESM1_ESM.pdf (1.6 mb)
ESM 1 (PDF 1682 kb)

References

  1. Agerer R (2001) Exploration types of ectomycorrhizae. Mycorrhiza 11:107–114CrossRefGoogle Scholar
  2. Albornoz FE, Teste FP, Lambers H, Bunce M, Murray DC, White NE, Laliberté E (2016) Changes in ectomycorrhizal fungal community composition and declining diversity along a 2-million-year soil chronosequence. Mol Ecol 25:4919–4929CrossRefPubMedGoogle Scholar
  3. Allison VJ, Condron LM, Peltzer DA, Richardson SJ, Turner BL (2007) Changes in enzyme activities and soil microbial community composition along carbon and nutrient gradients at the Franz Josef chronosequence, New Zealand. Soil Biol Biochem 39:1770–1781CrossRefGoogle Scholar
  4. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic Local Alignment Search Tool. J Mol Biol 21:403–410CrossRefGoogle Scholar
  5. Blaalid R, Carlsen TOR, Kumar S, Halvorsen R, Ugland KI, Fontana G, Kauserud H (2012) Changes in the root-associated fungal communities along a primary succession gradient analysed by 454 pyrosequencing. Mol Ecol 21:1897–1908CrossRefPubMedGoogle Scholar
  6. Bokhorst S, Kardol P, Bellingham PJ, Kooyman RM, Richardson SJ, Schmidt S, Wardle DA (2017) Responses of communities of soil organisms and plants to soil aging at two contrasting long-term chronosequences. Soil Biol Biochem 106:69–79CrossRefGoogle Scholar
  7. Bonito G, Reynolds H, Robeson MS, Nelson J, Hodkinson BP, Tuskan G, Schadt CW, Vilgalys R (2014) Plant host and soil origin influence fungal and bacterial assemblages in the roots of woody plants. Mol Ecol 23:3356–3370CrossRefPubMedGoogle Scholar
  8. Bonito G, Hameed K, Ventura R, Krishnan J, Schadt CW, Vilgalys R (2016) Isolating a functionally relevant guild of fungi from the root microbiome of Populus. Fungal Ecol 22:35–42CrossRefGoogle Scholar
  9. Buée M, Courty PE, Mignot D, Garbaye J (2007) Soil niche effect on species diversity and catabolic activities in an ectomycorrhizal fungal community. Soil Biol and Biochem 39:1947–1955CrossRefGoogle Scholar
  10. Buée 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 184:449–456CrossRefPubMedGoogle Scholar
  11. Calvaruso C, Turpault MP, Leclerc E, Ranger J, Garbaye J, Uroz S, Frey-Klett P (2010) Forest trees influence distribution of the mineral weathering bacterial communities from the Scleroderma citrinum mycorrhizosphere. Appl Environ Microbiol 76:4780–4787CrossRefPubMedPubMedCentralGoogle Scholar
  12. Chapin FS (1980) The mineral nutrition of wild plants. An Rev Ecol System 11:233–260CrossRefGoogle Scholar
  13. Clemmensen KE, Finlay RD, Dahlberg A, Stenlid J, Wardle DA, Lindahl BD (2015) Carbon sequestration is related to mycorrhizal fungal community shifts during long-term succession in boreal forests. New Phytol 205:1525–1536CrossRefPubMedGoogle Scholar
  14. Coince A, Caël O, Bach C, Lengellé J, Cruaud C, Gavory F, Morin E, Murat C, Marcais B, Buée M (2013) Below-ground fine-scale distribution and soil versus fine root detection of fungal and soil oomycete communities in a French beech forest. Fungl Ecol 6:223–235CrossRefGoogle Scholar
  15. Courty PE, Buée M, Diedhiou AG, Frey-Klett P, Le Tacon F, Rineau F, Turpault MP, Uroz S, Garbaye J (2010) The role of ectomycorrhizal communities in forest ecosystem processes: new perspectives and emerging concepts. Soil Biol Biochem 42:679–698CrossRefGoogle Scholar
  16. Courty PE, Munoz F, Selosse MA, Duchemin M, Criquet S, Ziarelli F, Buée M, Plassard C, Taudière A, Garbaye J, Richard F (2016) Into the functional ecology of ectomycorrhizal communities: environmental filtering of enzymatic activities. J Ecol 104:1585–1598CrossRefGoogle Scholar
  17. Dickie IA, Xu B, Koide RT (2002) Vertical niche differentiation of ectomycorrhizal hyphae in soil as shown by T-RFLP analysis. New Phytol 156:527–535CrossRefGoogle Scholar
  18. Dickie IA, Martínez-García LB, Koele N, Grelet GA, Tylianakis JM, Peltzer DA, Richardson SJ (2013) Mycorrhizas and mycorrhizal fungal communities throughout ecosystem development. Plant Soil 367:11–39CrossRefGoogle Scholar
  19. Duchaufour P, Bonneau M (1959) Une méthode nouvelle de dosage du phosphore assimilable dans les sols forestiers. Bul AFES 4:193–198Google Scholar
  20. Eckert AJ, Shahi H, Datwyler L, Neale DB (2012) Spatially variable natural selection and the divergence between parapatric supspecies of lodgepole pine (Pinus contorta, pinaceae). American J Bot 99:1323–1334CrossRefGoogle Scholar
  21. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature meth 10:996–998CrossRefGoogle Scholar
  22. Fernandez CW, Kennedy PG (2016) Revisiting the ‘Gadgil effect’: do interguild fungal interactions control carbon cycling in forest soils? New Phytol 209:1382–1394CrossRefPubMedGoogle Scholar
  23. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes‐application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118Google Scholar
  24. Huggett RJ (1998) Soil chronosequences, soil development, and soil evolution: a critical review. Catena 32:155–172CrossRefGoogle Scholar
  25. Ishida TA, Nara K, Hogetsu T (2007) Host effects on ectomycorrhizal fungal communities: insight from eight host species in mixed conifer–broadleaf forests. New Phytol 174:430–440CrossRefPubMedGoogle Scholar
  26. Izquierdo JE, Houlton BZ, van Huysen TL (2013) Evidence for progressive phosphorus limitation over long-term ecosystem development: examination of a biogeochemical paradigm. Plant Soil 367:135–147CrossRefGoogle Scholar
  27. Jangid K, Whitman WB, Condron LM, Turner BL, Williams MA (2013) Soil bacterial community succession during long-term ecosystem development. Mol Ecol 22:3415–3424CrossRefPubMedGoogle Scholar
  28. Jany JL, Martin F, Garbaye J (2003) Respiration activity of ectomycorrhizas from Cenococcum geophilum and Lactarius sp. in relation to soil water potential in five beech forests. Plant Soil 255:487–494CrossRefGoogle Scholar
  29. Jeanbille M, Buée M, Bach C, Cébron A, Frey-Klett P, Turpault MP, Uroz S (2016) Soil parameters drive the structure, diversity and metabolic potentials of the bacterial communities across temperate beech forest soil sequences. Microb Ecol 71:482–493Google Scholar
  30. Jenny H, Arkley RJ, Schultz AM (1969) The pygmy forest-podzol ecosystem and its dune associates of the Mendocino coast. Madrono 20:60–74Google Scholar
  31. Jenny H (1973) Pygmy forest ecological staircase: a description and interpretation. 58 p. Privately publishedGoogle Scholar
  32. Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM, Douglas B, Drenkhan T, Eberhardt U, Dueñas M, Grebenc T, Griffith GW, Hartmann M, Kirk PM, Kohout P, Larsson E, Lindahl BD, Lücking R, Martín MP, Matheny PB, Nguyen NH, Niskanen T, Oja J, Peay KG, Peintner U, Peterson M, Põldmaa K, Saag L, Saar I, Schüßler A, Scott JA, Senés C, Smith ME, Suija A, Taylor DL, Telleria MT, Weiss M, Larsson KH (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277CrossRefPubMedGoogle Scholar
  33. Kuramae E, Gamper H, van Veen J, Kowalchuk G (2011) Soil and plant factors driving the community of soil-borne microorganisms across chronosequences of secondary succession of chalk grasslands with a neutral pH. FEMS Microbiol Ecol 77:285–294CrossRefPubMedGoogle Scholar
  34. Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103CrossRefPubMedGoogle Scholar
  35. Landeweert R, Hoffland E, Finlay RD, Kuyper TW, van Breemen N (2001) Linking plants to rocks: ectomycorrhizal fungi mobilize nutrients from minerals. Trends Ecol Evol 16:248–254CrossRefPubMedGoogle Scholar
  36. Landeweert R, Leeflang P, Kuyper TW, Hoffland E, Rosling A, Wernars K, Smit E (2003) Molecular identification of ectomycorrhizal mycelium in soil horizons. Appl Environ Microbiol 69:327–333CrossRefPubMedPubMedCentralGoogle Scholar
  37. Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40:2407–2415CrossRefGoogle Scholar
  38. Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120CrossRefPubMedPubMedCentralGoogle Scholar
  39. Lilleskov EA, Fahey TJ, Horton TR, Lovett GM (2002) Belowground ectomycorrhizal fungal community change over a nitrogen deposition gradient in Alaska. Ecology 83:104–115CrossRefGoogle Scholar
  40. Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Högberg P, Stenlid J, Finlay RD (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol 173:611–620CrossRefPubMedGoogle Scholar
  41. Lindahl BD, Tunlid A (2015) Ectomycorrhizal fungi–potential organic matter decomposers, yet not saprotrophs. New Phytol 205:1443–1447CrossRefPubMedGoogle Scholar
  42. Marschner P, Crowley DE, Yang CH (2004) Development of specific rhizosphere bacterial communities in relation to plant species, nutrition and soil type. Plant Soil 261:199–208CrossRefGoogle Scholar
  43. Martin FM, Uroz S, Barker DG (2017). Ancestral alliances: plant mutualistic symbioses with fungi and bacteria. Science 356: eaad4501Google Scholar
  44. Martínez-García LB, Richardson SJ, Tylianakis JM, Peltzer DA, Dickie IA (2015) Host identity is a dominant driver of mycorrhizal fungal community composition during ecosystem development. New Phytol 205:1565–1576CrossRefPubMedGoogle Scholar
  45. Merritts DJ, Chadwick OA, Hendricks DM (1991) Rates and processes of soil evolution on uplifted marine terraces, northern California. Geoderma 51:241–275CrossRefGoogle Scholar
  46. Metson AJ (1956) Methods of chemical analysis for soil survey samples. NZ Soil Bur Bull n°12Google Scholar
  47. Moeller HV, Peay KG, Fukami T (2014) Ectomycorrhizal fungal traits reflect environmental conditions along a coastal California edaphic gradient. FEMS Microbiol Ecol 87:797–806CrossRefPubMedGoogle Scholar
  48. Moore J, Macalady JL, Schulz MS, White AE, Brantley SL (2010) Shifting microbial community structure across a marine terrace grassland chronosequence, Santa Cruz, California. Soil Biol Biochem 42:21–31CrossRefGoogle Scholar
  49. Morriën E, Hannula SE, Snoek LB, Helmsing NR, Zweers H, De Hollander M et al (2017) Soil networks become more connected and take up more carbon as nature restoration progresses. Nature Comm 8:14349CrossRefGoogle Scholar
  50. Nilsson RH, Kristiansson E, Ryberg M, Hallenberg N, Larsson KH (2008) Intraspecific ITS variability in the Kingdom Fungi as expressed in the international sequence databases and its implications for molecular species identification. Evolution bioinform online 4:193CrossRefGoogle Scholar
  51. Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248CrossRefGoogle Scholar
  52. Nygren CM, Edqvist J, Elfstrand M, Heller G, Taylor AFS (2007) Detection of extracellular protease activity in different species and genera of ectomycorrhizal fungi. Mycorrhiza 17:241–248CrossRefPubMedGoogle Scholar
  53. Northup RR, Yu Z, Dahlgren RA, Vogt KA (1995a) Polyphenol control of nitrogen release from pine litter. Nature 377:227–229CrossRefGoogle Scholar
  54. Northup RR, Dahlgren RA, Yu Z (1995b) Intraspecific variation of conifer phenolic concentration on a marine terrace soil acidity gradient; a new interpretation. Plant Soil 171:255–262CrossRefGoogle Scholar
  55. Northup RR, Dahlgren RA, McColl JG (1998) Polyphenols as regulators of plant-litter-soil interactions in northern California’s pygmy forest: a positive feedback? In: Plant-induced soil changes: processes and feedbacks. Springer, Dordrecht, pp 189–220CrossRefGoogle Scholar
  56. Obase K, Cha JY, Lee JK, Lee SY, Lee JH, Chun KW (2009) Ectomycorrhizal fungal communities associated with Pinus thunbergii in the eastern coastal pine forests of Korea. Mycorrhiza 20:39–49CrossRefPubMedGoogle Scholar
  57. Peltzer DA, Wardle DA, Allison VJ, Baisden WT, Bardgett RD, Chadwick OA, Condron LM, Parfitt RL, Porder S, Richardson SJ, Turner BL, Vitousek PM, Walker J, Walker LR (2010) Understanding ecosystem retrogression. Ecol Monogr 80:509–529CrossRefGoogle Scholar
  58. Peter M, Kohler A, Ohm RA, Kuo A, Krützmann J, Morin E, Arend M, Barry KW, Binder M, Choi C, Clum A, Copeland A, Grisel N, Haridas S, Kipfer T, LaButti K, Lindquist E, Lipzen A, Maire R, Meier B, Mihaltcheva S, Molinier V, Murat C, Pöggeler S, Quandt CA, Sperisen C, Tritt A, Tisserant E, Crous PW, Henrissat B, Nehls U, Egli S, Spatafora JW, Grigoriev IV, Martin FM (2016) Ectomycorrhizal ecology is imprinted in the genome of the dominant symbiotic fungus Cenococcum geophilum. Nature Comm 7:12662CrossRefGoogle Scholar
  59. Philippot L, Tscherko D, Bru D, Kandeler E (2011) Distribution of high bacterial taxa across the chronosequence of two alpine glacier forelands. Microb Ecol 61:303–312CrossRefPubMedGoogle Scholar
  60. Phillips LA, Ward V, Jones MD (2014) Ectomycorrhizal fungi contribute to soil organic matter cycling in sub-boreal forests. ISME J 8:699–713CrossRefPubMedGoogle Scholar
  61. Pigott CD (1982) Survival of mycorrhizas formed by Cenococcum geophilum Fr. in dry soils. New Phytol 92:513–517CrossRefGoogle Scholar
  62. Rajala T, Peltoniemi M, Pennanen T, Mäkipää R (2012) Fungal community dynamics in relation to substrate quality of decaying Norway spruce (Picea abies [L.] Karst.) logs in boreal forests. FEMS Microbiol Ecol 81:494–505CrossRefPubMedGoogle Scholar
  63. Rengel Z, Marschner P (2005) Nutrient availability and management in the rhizosphere: exploiting genotypic differences. New Phytol 168:305–312CrossRefPubMedGoogle Scholar
  64. Rincón A, Santamaría-Pérez B, Rabasa SG, Coince A, Marçais B, Buée M (2015) Compartmentalized and contrasted response of ectomycorrhizal and soil fungal communities of Scots pine forests along elevation gradients in France and Spain. Environ Microbiol 17:3009–3024CrossRefPubMedGoogle Scholar
  65. Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK (2015) Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res 3:e47CrossRefGoogle Scholar
  66. Rosling A, Landeweert R, Lindahl BD, Larsson KH, Kuyper TW, AFS T, Finlay RD (2003) Vertical distribution of ectomycorrhizal fungal taxa in a podzol soil profile. New Phytol 159:775–783CrossRefGoogle Scholar
  67. Rousk J, Baath E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacteria and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351CrossRefPubMedGoogle Scholar
  68. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541CrossRefPubMedPubMedCentralGoogle Scholar
  69. Shah F, Nicolás C, Bentzer J, Ellström M, Smits M, Rineau Fet al (2016) Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors. New Phytol 209: 1705–1719Google Scholar
  70. Sterkenburg E, Bahr A, Brandström Durling M, Clemmensen KE, Lindahl BD (2015) Changes in fungal communities along a boreal forest soil fertility gradient. New Phytol 207:1145–1158CrossRefPubMedGoogle Scholar
  71. Tedersoo L, Kõljalg U, Hallenberg N, Larsson KH (2003) Fine scale distribution of ectomycorrhizal fungi and roots across substrate layers including coarse woody debris in a mixed forest. New Phytol 159:153–165CrossRefGoogle Scholar
  72. Tedersoo L, Suvi T, Larsson E, Koljalg U (2006) Diversity and community structure of ectomycorrhizal fungi in a wooded meadow. Mycol Res 110:734–748CrossRefPubMedGoogle Scholar
  73. Tedersoo L, Bahram M, Põlme S, Kõljalg U, Yorou NS, Wijesundera R, Smith ME (2014) Global diversity and geography of soil fungi. Science 346:1256688CrossRefPubMedGoogle Scholar
  74. Thompson CH (1981) Podzol chronosequences on coastal dunes of eastern Australia. Nature 291:59–61CrossRefGoogle Scholar
  75. Uroz S, Calvaruso C, Turpault MP, Frey-Klett P (2009) The microbial weathering of soil minerals, ecology, actors and mechanisms. Trends Microbiol 17:378–387CrossRefPubMedGoogle Scholar
  76. Uroz S, Tech JJ, Sawaya NA, Frey-Klett P, Leveau JHJ (2014) Structure and function of bacterial communities in ageing soils: insights from the Mendocino ecological staircase. Soil Biol Biochem 69:265–274CrossRefGoogle Scholar
  77. Uroz S, Buée M, Deveau A, Mieszkin S, Martin F (2016a) Ecology of the forest microbiome: highlights of temperate and boreal ecosystems. Soil Biol Biochem 103:471–488CrossRefGoogle Scholar
  78. Uroz S, Oger P, Tisserand E, Cébron A, Turpault MP, Buée M, De Boer W, Leveau JHJ, Frey-Klett P (2016b) Specific impacts of beech and Norway spruce on the structure and diversity of the rhizosphere and soil microbial communities. Sci Rep 6:27756CrossRefPubMedPubMedCentralGoogle Scholar
  79. Walker TW, Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderma 15:1–19CrossRefGoogle Scholar
  80. Wardle DA, Walker LR, Bardgett RD (2004) Ecosystem properties and forest decline in contrasting long-term chronosequences. Science 305:509–513CrossRefPubMedGoogle Scholar
  81. Westman WE, Whittaker RH (1975) The pygmy forest region of northern California: studies on biomass and primary productivity. J Ecol 63:493–520CrossRefGoogle Scholar
  82. Westman WE (1978) Patterns of nutrient flow in the pygmy forest region of northern California. Vegetatio 36:1–15CrossRefGoogle Scholar
  83. White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols: A Guide to Methods and Applications. New York: Academic Press Inc, pp 315–322Google Scholar
  84. White AF, Schlz MS, Vivit DV, Blum AE, Stonestrom DA, Anderson SP (2008) Chemical weathering of a marine terrace chronosequence, Santa Cruz, California I: interpreting rates and controls based on soil concentration-depth profiles. Geochem Cosmo Acta 72:36–68CrossRefGoogle Scholar
  85. Wurzbuger N, Bledsoe CS (2001) Comparison of ericoid and ectomycorrhizal colonization and ectomycorrhizal morphotypes in mixed conifer and pygmy forests on the northern California coast. Can J Bot 79:1202–1210Google Scholar
  86. Wurzbuger N, Bidartondo MI, Bledsoe CS (2001) Characterization of Pinus ectomycorrhizas from mixed conifer and pygmy forests using morphotyping and molecular methods. Can J Bot 79:1211–1216Google Scholar
  87. Yu Z, Dahlgren RA, Northup RR (1999) Evolution of soil properties and plant communities along an extreme edaphic gradient. European J Soil Biol 35:31–38CrossRefGoogle Scholar
  88. Yu Z, Kraus TEC, Dahlgren RA, Horwath WR, Zasoski RJ (2003) Mineral and dissolved organic nitrogen dynamics along a soil acidity-fertility gradient. Soil Sci Society American J 6:878–888CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Agroécologie, AgroSup Dijon, CNRS, INRAUniv. Bourgogne Franche-ComtéDijonFrance
  2. 2.INRA, UMR 1136 INRA, Université de Lorraine “Interactions Arbres Micro-organismes”Centre INRA de NancyChampenouxFrance
  3. 3.Department of Plant PathologyUniversity of CaliforniaDavisUSA
  4. 4.INRA UR 1138 “Biogéochimie des Ecosystèmes Forestiers”Centre INRA de NancyChampenouxFrance

Personalised recommendations