Abstract
Quercus liaotungensis is a major tree species in deciduous broad-leaved forests in northern China. In this study, we investigated ectomycorrhizal (ECM) communities associated with Q. liaotungensis from five typical habitats across northern China. We used internal transcribed spacer-polymerase chain reaction and DNA sequencing to identify ECM fungi, and we detected 220 operational taxonomic units. In general, at the regional scale, the dominant ECM lineages were /tomentella-thelephora, /cenococcum, /russula-lactarius, and /inocybe. Analysis of variance demonstrated significant differences in alpha diversity among these ECM communities, and the ECM fungal richness was positively correlated with elevation and soil organic matter. Analysis of similarity and a nonmetric multidimensional scaling analysis revealed that there were significant differences in community composition, and the geographical distance was correlated with the ECM fungal communities. Among the environmental factors we studied, soil parameters and climate factors were the primary direct driving factors of the ECM fungal communities. Our study primarily advances our understanding of environmental factors affecting ECM fungal communities at regional scale.
Similar content being viewed by others
References
Abarenkov K, Tedersoo L, Nilsson RH et al (2010) PlutoF—a web based workbench for ecological and taxonomic research, with an online implementation for fungal ITS sequences. Evol Bioinform Online 6:189–196. doi:10.4137/EBO.S6271
Bahram M, Koljalg U, Kohout P, Mirshahvaladi S, Tedersoo L (2013) Ectomycorrhizal fungi of exotic pine plantations in relation to native host trees in Iran: evidence of host range expansion by local symbionts to distantly related host taxa. Mycorrhiza 23:11–19. doi:10.1007/s00572-012-0445-z
Bahram M, Polme S, Koljalg U, Zarre S, Tedersoo L (2012) Regional and local patterns of ectomycorrhizal fungal diversity and community structure along an altitudinal gradient in the Hyrcanian forests of northern Iran. New Phytol 193:465–473. doi:10.1111/j.1469-8137.2011.03927.x
Baldrian P (2009) Ectomycorrhizal fungi and their enzymes in soils: is there enough evidence for their role as facultative soil saprotrophs? Oecologia 161:657–660. doi:10.1007/s00442-009-1433-7
Benedict JB (2011) Sclerotia as indicators of mid-Holocene tree-limit altitude, Colorado Front Range, USA. The Holocene 21:1021–1023. doi:10.1177/0959683610395078
Borcard D, Legendre P (2002) All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices. Ecol Model 153:51–68. doi:10.1016/S0304-3800(01)00501-4
Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77. doi:10.1007/s11104-008-9877-9
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 Biochem 39:1947–1955. doi:10.1016/j.soilbio.2007.02.016
Colwell RK, Elsensohn JE (2014) EstimateS turns 20: statistical estimation of species richness and shared species from samples, with non-parametric extrapolation. Ecography 37:609–613. doi:10.1111/ecog.00814
Erlandson SR, Savage JA, Cavender-Bares JM, Peay KG (2016) Soil moisture and chemistry influence diversity of ectomycorrhizal fungal communities associating with willow along an hydrologic gradient. FEMS Microbiol Ecol 92. doi:10.1093/femsec/fiv148
Gómez-Hernández M, Williams-Linera G, Guevara R, Lodge DJ (2011) Patterns of macromycete community assemblage along an elevation gradient: options for fungal gradient and metacommunity analyse. Biodivers Conserv 21:2247–2268. doi:10.1007/s10531-011-0180-3
Huang J, Nara K, Lian C, Zong K, Peng K, Xue S, Shen Z (2012) Ectomycorrhizal fungal communities associated with Masson pine (Pinus massoniana lamb.) in Pb-Zn mine sites of central south China. Mycorrhiza 22:589–602. doi:10.1007/s00572-012-0436-0
Jansa J, Bukovska P, Gryndler M (2013) Mycorrhizal hyphae as ecological niche for highly specialized hypersymbionts—or just soil free-riders? Front Plant Sci 4:134. doi:10.3389/fpls.2013.00134
Jany J-L, 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 255:487–494. doi:10.1023/A:1026092714340
Jarvis SG, Woodward S, Taylor AF (2015) Strong altitudinal partitioning in the distributions of ectomycorrhizal fungi along a short (300 m) elevation gradient. New Phytol 206:1145–1155. doi:10.1111/nph.13315
Jumpponen A, Jones KL, David Mattox J, Yaege C (2010) Massively parallel 454-sequencing of fungal communities in Quercus spp. ectomycorrhizas indicates seasonal dynamics in urban and rural sites. Mol Ecol 19(Suppl 1):41–53. doi:10.1111/j.1365-294X.2009.04483.x
Kivlin SN, Winston GC, Goulden ML, Treseder KK (2014) Environmental filtering affects soil fungal community composition more than dispersal limitation at regional scales. Fungal Ecol 12:14–25. doi:10.1016/j.funeco.2014.04.004
Kranabetter JM, Durall DM, MacKenzie WH (2009) Diversity and species distribution of ectomycorrhizal fungi along productivity gradients of a southern boreal forest. Mycorrhiza 19:99–111. doi:10.1007/s00572-008-0208-z
Lavergne S, Mouquet N, Thuiller W, Ronce O (2010) Biodiversity and climate change: integrating evolutionary and ecological responses of species and communities. Annu Rev Ecol Evol S 41:321–350. doi:10.1146/annurev-ecolsys-102209-144628
Long D, Liu J, Han Q, Wang X, Huang J (2016) Ectomycorrhizal fungal communities associated with Populus simonii and Pinus tabuliformis in the hilly-gully region of the Loess Plateau, China. Sci Rep 6:24336. doi:10.1038/srep24336
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 205:1565–1576. doi:10.1111/nph.13226
Miyamoto Y, Nakano T, Hattori M, Nara K (2014) The mid-domain effect in ectomycorrhizal fungi: range overlap along an elevation gradient on Mount Fuji, Japan. ISME J 8:1739–1746. doi:10.1038/ismej.2014.34
Miyamoto Y, Sakai A, Hattori M, Nara K (2015) Strong effect of climate on ectomycorrhizal fungal composition: evidence from range overlap between two mountains. ISME J 9:1870–1879. doi:10.1038/ismej.2015.8
Mujic AB, Durall DM, Spatafora JW, Kennedy PG (2016) Competitive avoidance not edaphic specialization drives vertical niche partitioning among sister species of ectomycorrhizal fungi. New Phytol 209:1174–1183. doi:10.1111/nph.13677
Park S, Seo Y-S, Hegeman AD (2014) Plant metabolomics for plant chemical responses to belowground community change by climate change. J Plant Biol 57:137–149. doi:10.1007/s12374-014-0110-5
Parrent JL, Morris WF, Vilgalys R (2006) CO2-enrichment and nutrient availability alter ectomycorrhizal fungal communities. Ecology 87:2278–2287. doi:10.1890/0012-9658(2006)87[2278:CANAAE]2.0.CO;2
Peay KG, Bruns TD, Kennedy PG, Bergemann SE, Garbelotto M (2007) A strong species-area relationship for eukaryotic soil microbes: island size matters for ectomycorrhizal fungi. Ecol Lett 10:470–480. doi:10.1111/j.1461-0248.2007.01035.x
Polme S et al (2013) Biogeography of ectomycorrhizal fungi associated with alders (Alnus spp.) in relation to biotic and abiotic variables at the global scale. New Phytol 198:1239–1249. doi:10.1111/nph.12170
Rahbek C (2005) The role of spatial scale and the perception of large-scale species-richness patterns. Ecol Lett 8:224–239. doi:10.1111/j.1461-0248.2004.00701.x
Roy M, Rochet J, Manzi S, Jargeat P, Gryta H, Moreau PA, Gardes M (2013) What determines Alnus-associated ectomycorrhizal community diversity and specificity? A comparison of host and habitat effects at a regional scale. New Phytol 198:1228–1238. doi:10.1111/nph.12212
Smith ME, Douhan GW, Rizzo DM (2007) Ectomycorrhizal community structure in a xeric Quercus woodland based on rDNA sequence analysis of sporocarps and pooled roots. New Phytol 174:847–863. doi:10.1111/j.1469-8137.2007.02040.x
Smith SE, Read DJ (2008) Mycorrhizal Symbiosis. 3rd edn. Academic Press, London
Sommers LE, Nelson DW (1972) Determination of Total phosphorus in soils: a rapid perchloric acid digestion procedure. Soil Sci Soc Am J 36:902–904. doi:10.2136/sssaj1972.03615995003600060020x
Suz LM, Barsoum N, Benham S, Dietrich HP et al (2014) Environmental drivers of ectomycorrhizal communities in Europe’s temperate oak forests. Mol Ecol 23:5628–5644. doi:10.1111/mec.12947
Swaty RL, Gehring CA, Van Ert M, Theimer TC, Keim P, Whitham TG (1998) Temporal variation in temperature and rainfall differentially affects ectomycorrhizal colonization at two contrasting sites. New Phytol 139:733–739. doi:10.1046/j.1469-8137.1998.00234.x
Talbot JM, Bruns TD, Taylor JW et al (2014) Endemism and functional convergence across the North American soil mycobiome. Proc Natl Acad Sci U S A 111:6341–6346. doi:10.1073/pnas.1402584111
Tedersoo L, Bahram M, Toots M et al (2012) Towards global patterns in the diversity and community structure of ectomycorrhizal fungi. Mol Ecol 21:4160–4170. doi:10.1111/j.1365-294X.2012.05602.x
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 159:153–165. doi:10.1046/j.1469-8137.2003.00792.x
Tedersoo L, May TW, Smith ME (2010) Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20:217–263. doi:10.1007/s00572-009-0274-x
Tibbett M, Sanders F, Cairney J (1998) The effect of temperature and inorganic phosphorus supply on growth and acid phosphatase production in arctic and temperate strains of ectomycorrhizal Hebeloma spp. in axenic culture. Mycol Res 102:129–135
Wang Q, He XH, Guo LD (2012) Ectomycorrhizal fungus communities of Quercus liaotungensis Koidz of different ages in a northern China temperate forest. Mycorrhiza 22:461–470. doi:10.1007/s00572-011-0423-x
Zhang J, Taniguchi T, Tateno R, Xu M, Du S, Liu G-B, Yamanaka N (2013) Ectomycorrhizal fungal communities of Quercus liaotungensis along local slopes in the temperate oak forests on the Loess Plateau, China. Ecol Res 28:297–305. doi:10.1007/s11284-012-1017-6
Zhang J, Taniguchi T, Xu M, Du S, Liu G-B, Yamanaka N (2014) Ectomycorrhizal fungal communities of Quercus liaotungensis along different successional stands on the Loess Plateau, China. J For Res 19:395–403. doi:10.1007/s10310-013-0433-y
Acknowledgements
This research was supported in part by the National Science-Technology Support Project (2015BAD07B02). The work was mainly performed in the Key Comprehensive Laboratory of Forest for Shaanxi Province.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Wang, X., Liu, J., Long, D. et al. The ectomycorrhizal fungal communities associated with Quercus liaotungensis in different habitats across northern China. Mycorrhiza 27, 441–449 (2017). https://doi.org/10.1007/s00572-017-0762-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00572-017-0762-3