Skip to main content
Log in

Influence of the slope aspect on the ectomycorrhizal fungal community of Quercus variabilis Blume in the middle part of the Taihang Mountains, North China

  • Original Paper
  • Published:
Journal of Forestry Research Aims and scope Submit manuscript

Abstract

The slope aspect is one of the most critical topographic factors in mountainous areas. Little is known, however, about the effect of the aspect on the ectomycorrhizal (ECM) fungal community. Additionally, we know very little about the composition of ECM fungal communities associated with Quercus variabilis, which is widely distributed in East Asia. In this study, we compared the richness, community composition, and exploration types of ECM fungi associated with Q. variabilis between predominantly south- and north-facing slopes in the Taihang Mountain, North China for the first time. DNA was extracted from the root tips of Q. variabilis, and Illumina MiSeq sequencing was used to identify ECM fungi. In total, 168 operational taxonomic units belonging to 28 genera were detected, and the ECM community was found to be dominated by Russula, Inocybe, Tomentella, Scleroderma, and Cortinarius. Compared with the north-facing slopes, the ECM communities on the south-facing slopes had higher diversity. The community composition and exploration types were directly affected by the slope aspect. Also, the aspect-induced edaphic variables, such as total phosphorus, total nitrogen, total potassium, pH, and soil water content, were important sources of variation in ECM fungal richness and distributions of exploration types. Different genera tended to be distributed in various slope aspects. Cenococcum, Genea, and Clavulina were significantly enriched in north-facing slopes, while Geopora, Helvelosebacina, Scleroderma, Gyroporus, Astraeus, Boletus, Tricholoma, Hebeloma, Cortinarius and unclassified Thelephoraceae were more abundant in south-facing slopes. Hydrophobic ECM fungi were obviously enriched in the south-facing slope, but there was no statistical difference between hydrophilic among the south- and north-facing slopes. Our study deepened our knowledge of the aspect-driven variation in ECM fungal communities associated with Q. variabilis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Addison SL, Walbert K, Smaill SJ, Menkis A (2018) Edaphic properties related with changes in diversity and composition of fungal communities associated with Pinus radiata. Pedobiologia 66:43–51

    Article  Google Scholar 

  • Aerts R, Berendse F, Klerk NM, Bakker C (1989) Root production and root turnover in two dominant species of wet heathlands. Oecologia 81(3):374–378

    Article  CAS  PubMed  Google Scholar 

  • Agerer R (2001) Exploration types of ectomycorrhizae. Mycorrhiza 11(2):107–114

    Article  Google Scholar 

  • Agerer R (2006) Fungal relationships and structural identity of their ectomycorrhizae. Mycol Prog 5(2):67–107

    Article  Google Scholar 

  • Ai ZM, Zhang JY, Liu HF, Xue S, Liu GB (2018) Influence of slope aspect on the microbial properties of rhizospheric and non-rhizospheric soils on the Loess Plateau China. Solid Earth 9(5):1157–1168

    Article  CAS  Google Scholar 

  • Albanese D, Fontana P, De Filippo C, Cavalieri D, Donati C (2015) MICCA: a complete and accurate software for taxonomic profiling of metagenomic data. Sci Rep 5:9743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bahnmann B, Masinova T, Halvorsen R, Davey ML, Sedlak P, Tomgovsky M, Baldrian P (2018) Effects of oak, beech and spruce on the distribution and community structure of fungi in litter and soils across a temperate forest. Soil Biol Biochem 119:162–173

    Article  CAS  Google Scholar 

  • Bauman D, Raspe O, Meerts P, Degreef J, Muledi JI, Drouet T (2016) Multiscale assemblage of an ectomycorrhizal fungal community: the influence of host functional traits and soil properties in a 10-ha miombo forest. FEMS Microbiol Ecol 92(10):pii: fiw151

    Article  CAS  Google Scholar 

  • Bowman EA, Arnold AE (2018) Distributions of ectomycorrhizal and foliar endophytic fungal communities associated with Pinus ponderosa along a spatially constrained elevation gradient. Am J Bot 105(4):687–699

    Article  PubMed  Google Scholar 

  • 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(1–2):37–77

    Article  CAS  Google Scholar 

  • Bruns TD, Bidartondo MI, Taylor DL (2002) Host specificity in ectomycorrhizal communities: what do the exceptions tell us? Integr Comp Biol 42(2):352–359

    Article  PubMed  Google Scholar 

  • Buee M, Vairelles D, Garbaye J (2005) Year-round monitoring of diversity and potential metabolic activity of the ectomycorrhizal community in a beech (Fagus silvatica) forest subjected to two thinning regimes. Mycorrhiza 15(4):235–245

    Article  PubMed  Google Scholar 

  • Burke DJ (2015) Effects of annual and interannual environmental variability on soil fungi associated with an old-growth, temperate hardwood forest. FEMS Microbiol Ecol 91(6):pii: fiv053

    Article  CAS  Google Scholar 

  • Burke DJ, Lopez-Gutierrez JC, Smemo KA, Chan CR (2009) Vegetation and soil environment influence the spatial distribution of root-associated fungi in a mature beech-maple forest. Appl Environ Microbiol 75(24):7639–7648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chai YX, Jiang SJ, Guo WJ, Qin MS, Pan JB, Bahadur A, Shi GX, Luo JJ, Jin ZC, Liu YJ, Zhang Q, An LZ, Feng HY (2018) The effect of slope aspect on the phylogenetic structure of arbuscular mycorrhizal fungal communities in an alpine ecosystem. Soil Biol Biochem 126:103–113

    Article  CAS  Google Scholar 

  • Chen LZ, Huang JH (1997) The research of the structure and function of warm temperate forest ecosystem. Science Press, Beijing

    Google Scholar 

  • Chu HY, Xiang XJ, Yang J, Adams JM, Zhang KP, Li YT, Shi Y (2016) Effects of slope aspects on soil bacterial and arbuscular fungal communities in a boreal forest in China. Pedosphere 26(2):226–234

    Article  Google Scholar 

  • Coince A, Cael O, Bach C, Lengelle J, Cruaud C, Gavory F, Morin E, Murat C, Marcais B, Buee M (2013) Below-ground fine-scale distribution and soil versus fine root detection of fungal and soil oomycete communities in a French beech forest. Fungal Ecol 6(3):223–235

    Article  Google Scholar 

  • Colwell RK (2013) EstimateS: Statistical estimation of species richness and shared species from samples. Version 9. User's Guide and application. https://purl.oclc.org/estimates

  • Courty PE, Franc A, Pierrat JC, Garbaye J (2008) Temporal changes in the ectomycorrhizal community in two soil horizons of a temperate oak forest. Appl Environ Microbiol 74(18):5792–5801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Beeck MO, Lievens B, Busschaert P, Declerck S, Vangronsveld J, Colpaert JV (2014) Comparison and validation of some ITS primer pairs useful for fungal metabarcoding studies. Plos One 9(6):11

    Google Scholar 

  • De Witte LC, Rosenstock NP, van der Linde S, Braun S (2017) Nitrogen deposition changes ectomycorrhizal communities in Swiss beech forests. Sci Total Environ 605:1083–1096

    Article  PubMed  CAS  Google Scholar 

  • Delang CO, Yuan Z (2015) China’s reforestation and rural development programs. China’s grain for green program. Springer, New York, pp 19–35

    Google Scholar 

  • Dickie IA (2007) Host preference, niches and fungal diversity. New Phytol 174(2):230–233

    Article  PubMed  Google Scholar 

  • Dickie IA, Dentinger BTM, Avis PG, McLaughlin DJ, Reich PB (2009) Ectomycorrhizal fungal communities of oak savanna are distinct from forest communities. Mycologia 101(4):473–483

    Article  CAS  PubMed  Google Scholar 

  • Doyle JJ, Doyle JL (1990) Isolation ofplant DNA from fresh tissue. Focus 12(13):39–40

    Google Scholar 

  • Ebel BA (2012) Impacts of wildfire and slope aspect on soil temperature in a mountainous environment. Vadose Zone J 11(3):10

    Article  Google Scholar 

  • Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10(10):996

    Article  CAS  PubMed  Google Scholar 

  • Essene AL, Shek KL, Lewis JD, Peay KG, McGuire KL (2017) Soil type has a stronger role than dipterocarp host species in shaping the rctomycorrhizal fungal community in a Bornean lowland tropical rain forest. Front Plant Sci 8:10

    Article  Google Scholar 

  • Fan YX, Lin F, Yang LM, Zhong XJ, Wang MH, Zhou JC, Chen YM, Yang YS (2018) Decreased soil organic P fraction associated with ectomycorrhizal fungal activity to meet increased P demand under N application in a subtropical forest ecosystem. Biol Fertil Soils 54(1):149–161

    Article  CAS  Google Scholar 

  • Fang JY, Shen ZH, Cui HT (2004) Ecological characteristics of mountains and research issues of mountain ecology. Biodivers Sci 12(1):10–19

    Google Scholar 

  • Frank E, Harrell J (2018) Hmisc: Harrell Miscellaneous. R package version 4.1-1. https://CRAN.R-project.org/package=Hmisc

  • Franklin O, Nasholm T, Hogberg P, Hogberg MN (2014) Forests trapped in nitrogen limitation—an ecological market perspective on ectomycorrhizal symbiosis. New Phytol 203(2):657–666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frey B, Rime T, Phillips M, Stierli B, Hajdas I, Widmer F, Hartmann M (2016) Microbial diversity in European alpine permafrost and active layers. FEMS Microbiol Ecol 92(3):fiw018

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Guzman O, Garibay-Orijel R, Hernandez E, Arellano-Torres E, Oyama K (2017) Word-wide meta-analysis of Quercus forests ectomycorrhizal fungal diversity reveals southwestern Mexico as a hotspot. Mycorrhiza 27(8):811–822

    Article  CAS  PubMed  Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2(2):113–118

    Article  CAS  PubMed  Google Scholar 

  • Geml J (2019) Soil fungal communities reflect aspect-driven environmental structuring and vegetation types in a Pannonian forest landscape. Fungal Ecol 39:63–79

    Article  Google Scholar 

  • Geng R, Geng ZC, Huang J, He WX, Hou L, She D, Han QS, Long DF (2016) Diversity of ectomycorrhizal fungi associated with Quercus aliena in Xinjiashan forest region of Qinling Mountains. Mycosystema 35(3):1–15

    Google Scholar 

  • Glassman SI, Wang IJ, Bruns TD (2017) Environmental filtering by pH and soil nutrients drives community assembly in fungi at fine spatial scales. Mol Ecol 26(24):6960–6973

    Article  CAS  PubMed  Google Scholar 

  • Hammer Ø, Harper D, Ryan P (2001) PAST: Paleontological Statistics software package for education and data analysis. Palaeontol Electron 4(1):9

    Google Scholar 

  • He F, Yang BS, Wang H, Yan QL, Cao Y, He XH (2016) Changes in composition and diversity of fungal communities along Quercus mongolica forests developments in Northeast China. Appl Soil Ecol 100:162–171

    Article  Google Scholar 

  • Hoeksema JD (2010) Ongoing coevolution in mycorrhizal interactions. New Phytol 187(2):286–300

    Article  PubMed  Google Scholar 

  • Huang J, Nara K, Zong K, Wang J, Xue SG, Peng KJ, Shen ZG, Lian CL (2014) Ectomycorrhizal fungal communities associated with Masson pine (Pinus massoniana) and white oak (Quercus fabri) in a manganese mining region in Hunan Province, China. Fungal Ecol 9:1–10

    Article  Google Scholar 

  • Ishaq L, Barber PA, Hardy GESJ, Dell B (2018) Diversity of fungi associated with roots of Eucalyptus gomphocephala seedlings grown in soil from healthy and declining sites. Australas Plant Pathol 47(2):155–162

    Article  CAS  Google Scholar 

  • Jarvis SG, Woodward S, Alexander IJ, Taylor AFS (2013) Regional scale gradients of climate and nitrogen deposition drive variation in ectomycorrhizal fungal communities associated with native Scots pine. Global Change Biol 19(6):1688–1696

    Article  CAS  Google Scholar 

  • Jarvis SG, Woodward S, Taylor AFS (2015) Strong altitudinal partitioning in the distributions of ectomycorrhizal fungi along a short (300 m) elevation gradient. New Phytol 206(3):1145–1155

    Article  CAS  PubMed  Google Scholar 

  • Johnson D, Martin F, Cairney JWG, Anderson IC (2012) The importance of individuals: intraspecific diversity of mycorrhizal plants and fungi in ecosystems. New Phytol 194(3):614–628

    Article  PubMed  Google Scholar 

  • Jumpponen A, Jones KL, Mattox D, Yaege C (2010) Massively parallel 454-sequencing of fungal communities in Quercus spp. ectomycorrhizas indicates seasonal dynamics in urban and rural sites. Mol Ecol 19:41–53

    Article  PubMed  Google Scholar 

  • Kennedy PG (2010) Ectomycorrhizal fungi and interspecific competition: species interactions, community structure, coexistence mechanisms, and future research directions. New Phytol 187(4):895–910

    Article  PubMed  Google Scholar 

  • Kennedy PG, Mielke LA, Nguyen NH (2018) Ecological responses to forest age, habitat, and host vary by mycorrhizal type in boreal peatlands. Mycorrhiza 28(3):315–328

    Article  CAS  PubMed  Google Scholar 

  • Kjoller R, Nilsson LO, Hansen K, Schmidt IK, Vesterdal L, Gundersen P (2012) Dramatic changes in ectomycorrhizal community composition, root tip abundance and mycelial production along a stand-scale nitrogen deposition gradient. New Phytol 194(1):278–286

    Article  CAS  PubMed  Google Scholar 

  • Kumar J, Atri NS (2018) Studies on ectomycorrhiza: an appraisal. Bot Rev 84(2):108–155

    Article  Google Scholar 

  • Kummel M, Lostroh P (2011) Altering light availability to the plant host determined the identity of the dominant ectomycorrhizal fungal partners and mediated mycorrhizal effects on plant growth. Botany-Botanique 89(7):439–450

    Article  Google Scholar 

  • Lai JS (2019) rdacca.hp: Hierarchical partitioning for redundancy analysis and canonical correspondence analysis. R package version 0.1.0. https://github.com/laijiangshan/rdacca.hp

  • Lancellotti E, Franceschini A (2013) Studies on the ectomycorrhizal community in a declining Quercus suber L. stand. Mycorrhiza 23(7):533–542

    Article  PubMed  Google Scholar 

  • Leski T, Pietras M, Rudawska M (2010) Ectomycorrhizal fungal communities of pedunculate and sessile oak seedlings from bare-root forest nurseries. Mycorrhiza 20(3):179–190

    Article  PubMed  Google Scholar 

  • Lilleskov EA, Fahey TJ, Horton TR, Lovett GM (2002) Belowground ectomycorrhizal fungal community change over a nitrogen deposition gradient in Alaska. Ecology 83(1):104–115

    Article  Google Scholar 

  • Lilleskov EA, Kuyper TW, Bidartondo MI, Hobbie EA (2019) Atmospheric nitrogen deposition impacts on the structure and function of forest mycorrhizal communities: a review. Environ Pollut 246:148–162

    Article  CAS  PubMed  Google Scholar 

  • Lindberg K, Furze B, Staff M, Black R (1997) Ecotourism and other services derived from forests in the Asia-Pacific region: outlook to 2010. Asia-Pacific Forestry Towards 2010. Asia-Pacific Forestry Sector Outlook Study Working Paper Series (FAO)

  • Liu L, Hart MM, Zhang JL, Cai XB, Gai JP, Christie P, Li XL, Klironomos JN (2015) Altitudinal distribution patterns of AM fungal assemblages in a Tibetan alpine grassland. FEMS Microbiol Ecol 91(7):pii: fiv078

    Article  CAS  Google Scholar 

  • Liu M, Zheng R, Bai SL, Bai YE, Wang JG (2017) Slope aspect influences arbuscular mycorrhizal fungus communities in arid ecosystems of the Daqingshan Mountains, Inner Mongolia North China. Mycorrhiza 27(3):189–200

    Article  PubMed  Google Scholar 

  • Maghnia FZ, Abbas Y, Mahe F, Kerdouh B, Tournier E, Ouadji M, Tisseyre P, Prin Y, El Ghachtouli N, Yakhlef SEB, Duponnois R, Sanguin H (2017) Habitat- and soil-related drivers of the root-associated fungal community of Quercus suber in the Northern Moroccan forest. Plos One 12(11):17

    Article  CAS  Google Scholar 

  • Matsuoka S, Mori AS, Kawaguchi E, Hobara S, Osono T (2016) Disentangling the relative importance of host tree community, abiotic environment and spatial factors on ectomycorrhizal fungal assemblages along an elevation gradient. FEMS Microbiol Ecol 92(5):fiw044

    Article  PubMed  CAS  Google Scholar 

  • McCune B, Keon D (2002) Equations for potential annual direct incident radiation and heat load. J Veg Sci 13(4):603–606, 604

    Article  Google Scholar 

  • Mendez-Toribio M, Meave JA, Zermeno-Hernandez I, Ibarra-Manriquez G (2016) Effects of slope aspect and topographic position on environmental variables, disturbance regime and tree community attributes in a seasonal tropical dry forest. J Veg Sci 27(6):1094–1103

    Article  Google Scholar 

  • Morgado LN, Semenova TA, Welker JM, Walker MD, Smets E, Geml J (2015) Summer temperature increase has distinct effects on the ectomycorrhizal fungal communities of moist tussock and dry tundra in Arctic Alaska. Global Chang Biol 21(2):959–972

    Article  Google Scholar 

  • Morris MH, Smith ME, Rizzo DM, Rejmanek M, Bledsoe CS (2008) Contrasting ectomycorrhizal fungal communities on the roots of co-occurring oaks (Quercus spp.) in a California woodland. New Phytol 178(1):167–176

    Article  PubMed  Google Scholar 

  • Morris MH, Perez-Perez MA, Smith ME, Bledsoe CS (2009) Influence of host species on ectomycorrhizal communities associated with two co-occurring oaks (Quercus spp.) in a tropical cloud forest. FEMS Microbiol Ecol 69(2):274–287

    Article  CAS  PubMed  Google Scholar 

  • Moser AM, Frank JL, D'Allura JA, Southworth D (2009) Ectomycorrhizal communities of Quercus garryana are similar on serpentine and nonserpentine soils. Plant Soil 315(1–2):185–194

    Article  CAS  Google Scholar 

  • Mrak T, Kuehdorf K, Grebenc T, Straus I, Muenzenberger B, Kraigher H (2017) Scleroderma areolatum ectomycorrhiza on Fagus sylvatica L. Mycorrhiza 27(3):283–293

    Article  CAS  PubMed  Google Scholar 

  • 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(3):1174–1183

    Article  PubMed  Google Scholar 

  • Mundra S, Bahram M, Tedersoo L, Kauserud H, Halvorsen R, Eidesen PB (2015) Temporal variation of Bistorta vivipara-associated ectomycorrhizal fungal communities in the High Arctic. Mol Ecol 24(24):6289–6302

    Article  PubMed  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucl Acids Res 8(19):4321–4326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nelson DW, Sommers LE (1996) Total carbon, organic carbon, and organic matter. In: Sparks DL et al (eds) Methods of soil analysis part 3—chemical methods. Soil Science Society of America & American Society of Agronomy, Madison, pp 961–1010. https://doi.org/10.2136/sssabookser5.3.c34

    Chapter  Google Scholar 

  • Nguyen NH, Song ZW, 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 20:241–248

    Article  Google Scholar 

  • Nickel UT, Weikl F, Kerner R, Schaefer C, Kallenbach C, Munch JC, Pritsch K (2018) Quantitative losses vs. qualitative stability of ectomycorrhizal community responses to 3 years of experimental summer drought in a beech-spruce forest. Global Chang Biol 24(2):E560–E576

    Article  Google Scholar 

  • Nilsson RH, Larsson KH, Taylor AFS, Bengtsson-Palme J, Jeppesen TS, Schigel D, Kennedy P, Picard K, Glockner FO, Tedersoo L, Saar I, Koljalg U, Abarenkov K (2018) The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucl Acids Res 47(D1):D259–D264

    Article  CAS  PubMed Central  Google Scholar 

  • O'Hanlon R (2012) Below-ground ectomycorrhizal communities: the effect of small scale spatial and short term temporal variation. Symbiosis 57(2):57–71

    Article  Google Scholar 

  • Oksanen J, Guillaume Blanchet F, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MH, Szoecs E, Wagner HH (2017) vegan: community ecology package. R package version 2.5-2. https://CRAN.R-project.org/package=vegan.

  • Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. Circular 939. United States Department of Agriculture, Washington, DC, pp 1–17

  • Palmer JM, Jusino MA, Banik MT, Lindner DL (2018) Non-biological synthetic spike-in controls and the AMPtk software pipeline improve mycobiome data. Peerj 6:e4925

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Polme S, Bahram M, Yamanaka T, Nara K, Dai YC, Grebenc T, Kraigher H, Toivonen M, Wang PH, Matsuda Y, Naadel T, Kennedy PG, Koljalg U, Tedersoo L (2013) Biogeography of ectomycorrhizal fungi associated with alders (Alnus spp.) in relation to biotic and abiotic variables at the global scale. New Phytol 198(4):1239–1249

    Article  CAS  PubMed  Google Scholar 

  • Querejeta JI, Roldán A, Albaladejo J, Castillo V (1998) The role of mycorrhizae, site preparation, and organic amendment in the afforestation of a semi-arid Mediterranean site with Pinus halepensis. Forest Sci 44(2):203–211

    Google Scholar 

  • R Core Team (2018) R: a language and environment for statistical computing. Accessed 6 May 2018. https://www.R-project.org/

  • Reis F, Valdiviesso T, Varela C, Tavares RM, Baptista P, Lino-Neto T (2018) Ectomycorrhizal fungal diversity and community structure associated with cork oak in different landscapes. Mycorrhiza 28(4):357–368

    Article  PubMed  Google Scholar 

  • Reverchon F, Ortega-Larrocea MDP, Perez-Moreno J (2012) Soil factors influencing ectomycorrhizal sporome distribution in neotropical forests dominated by Pinus montezumae Mexico. Mycoscience 53(3):203–210

    Article  Google Scholar 

  • Roberts DW (1986) Ordination on the basis of fuzzy set theory. Vegetatio 66(3):123–131

    Article  Google Scholar 

  • Saitta A, Anslan S, Bahram M, Brocca L, Tedersoo L (2018) Tree species identity and diversity drive fungal richness and community composition along an elevational gradient in a Mediterranean ecosystem. Mycorrhiza 28(1):39–47

    Article  PubMed  Google Scholar 

  • Scattolin L, Montecchio L, Agerer R (2008) The ectomycorrhizal community structure in high mountain Norway spruce stands. Trees-Struct Funct 22(1):13–22

    Article  Google Scholar 

  • Scattolin L, Lancellotti E, Franceschini A, Montecchio L (2014) The ectomycorrhizal community in Mediterranean old-growth Quercus ilex forests along an altitudinal gradient. Plant Biosyst 148(1):74–82

    Article  Google Scholar 

  • Schlatter DC, Kahl K, Carlson B, Huggins DR, Paulitz T (2018) Fungal community composition and diversity vary with soil depth and landscape position in a no-till wheat-based cropping system. Fems Microbiol Ecol 94(7):15

    Article  CAS  Google Scholar 

  • Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12(6):18

    Article  Google Scholar 

  • Smith SE, Read D (2008) Mycorrhizal symbiosis. Academic Press, San Diego. https://doi.org/10.1016/b978-0-12-370526-6.x5001-6

    Book  Google Scholar 

  • 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(4):847–863

    Article  CAS  PubMed  Google Scholar 

  • Sternberg M, Shoshany M (2001) Influence of slope aspect on Mediterranean woody formations: comparison of a semiarid and an arid site in Israel. Ecol Res 16(2):335–345

    Article  Google Scholar 

  • Suz LM, Barsoum N, Benham S, Dietrich HP, Fetzer KD, Fischer R, Garcia P, Gehrman J, Kristofel F, Manninger M, Neagu S, Nicolas M, Oldenburger J, Raspe S, Sanchez G, Schrock HW, Schubert A, Verheyen K, Verstraeten A, Bidartondo MI (2014) Environmental drivers of ectomycorrhizal communities in Europe's temperate oak forests. Mol Ecol 23(22):5628–5644

    Article  CAS  PubMed  Google Scholar 

  • Suz LM, Kallow S, Reed K, Bidartondo MI, Barsoum N (2017) Pine mycorrhizal communities in pure and mixed pine-oak forests: abiotic environment trumps neighboring oak host effects. For Ecol Manag 406:370–380

    Article  Google Scholar 

  • Tedersoo L, Koljalg 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(1):153–165

    Article  CAS  PubMed  Google Scholar 

  • Tedersoo L, Bahram M, Toots M, Diedhiou AG, Henkel TW, Kjoller R, Morris MH, Nara K, Nouhra E, Peay KG, Polme S, Ryberg M, Smith ME, Koljalg U (2012) Towards global patterns in the diversity and community structure of ectomycorrhizal fungi. Mol Ecol 21(17):4160–4170

    Article  PubMed  Google Scholar 

  • Tedersoo L, Bahram M, Polme S, Koljalg U, Yorou NS, Wijesundera R, Ruiz LV, Vasco-Palacios AM, Thu PQ, Suija A, Smith ME, Sharp C, Saluveer E, Saitta A, Rosas M, Riit T, Ratkowsky D, Pritsch K, Poldmaa K, Piepenbring M, Phosri C, Peterson M, Parts K, Partel K, Otsing E, Nouhra E, Njouonkou AL, Nilsson RH, Morgado LN, Mayor J, May TW, Majuakim L, Lodge DJ, Lee SS, Larsson KH, Kohout P, Hosaka K, Hiiesalu I, Henkel TW, Harend H, Guo LD, Greslebin A, Grelet G, Geml J, Gates G, Dunstan W, Dunk C, Drenkhan R, Dearnaley J, De Kesel A, Dang T, Chen X, Buegger F, Brearley FQ, Bonito G, Anslan S, Abell S, Abarenkov K (2014) Global diversity and geography of soil fungi. Science 346(6213):1078

    Article  CAS  Google Scholar 

  • Teste FP, Laliberte E, Lambers H, Auer Y, Kramer S, Kandeler E (2016) Mycorrhizal fungal biomass and scavenging declines in phosphorus-impoverished soils during ecosystem retrogression. Soil Biol Biochem 92:119–132

    Article  CAS  Google Scholar 

  • Toju H, Yamamoto S, Sato H, Tanabe AS, Gilbert GS, Kadowaki K (2013) Community composition of root-associated fungi in a Quercus-dominated temperate forest: "codominance" of mycorrhizal and root-endophytic fungi. Ecol Evol 3(5):1281–1293

    Article  PubMed  PubMed Central  Google Scholar 

  • Trocha LK, Kalucka I, Stasinska M, Nowak W, Dabert M, Leski T, Rudawska M, Oleksyn J (2012) Ectomycorrhizal fungal communities of native and non-native Pinus and Quercus species in a common garden of 35-year-old trees. Mycorrhiza 22(2):121–134

    Article  PubMed  Google Scholar 

  • Twieg BD, Durall DM, Simard SW, Jones MD (2009) Influence of soil nutrients on ectomycorrhizal communities in a chronosequence of mixed temperate forests. Mycorrhiza 19(5):305–316

    Article  PubMed  Google Scholar 

  • Van Geel M, Yu K, Ceulemans T, Peeters G, van Acker K, Geerts W, Ramos MA, Serafim C, Kastendeuch P, Najjar G, Ameglio T, Ngao J, Saudreau M, Waud M, Lievens B, Castro PML, Somers B, Honnay O (2018) Variation in ectomycorrhizal fungal communities associated with Silver linden (Tilia tomentosa) within and across urban areas. FEMS Microbiol Ecol 94(12):fiy207

    CAS  Google Scholar 

  • Van Strien AJ, Boomsluiter M, Noordeloos ME, Verweij RJT, Kuyper TW (2018) Woodland ectomycorrhizal fungi benefit from large-scale reduction in nitrogen deposition in the Netherlands. J Appl Ecol 55(1):290–298

    Article  CAS  Google Scholar 

  • Veach AM, Stokes CE, Knoepp J, Jumpponen A, Baird R (2018) Fungal communities and functional guilds shift along an elevational gradient in the southern Appalachian Mountains. Microb Ecol 76(1):156–168

    Article  CAS  PubMed  Google Scholar 

  • Voriskova J, Brabcova V, Cajthaml T, Baldrian P (2014) Seasonal dynamics of fungal communities in a temperate oak forest soil. New Phytol 201(1):269–278

    Article  CAS  PubMed  Google Scholar 

  • 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(6):461–470

    Article  PubMed  Google Scholar 

  • Wang XN, Agathokleous E, Qu LY, Fujita S, Watanabe M, Tamai Y, Mao QZ, Koyama A, Koike T (2018) Effects of simulated nitrogen deposition on ectomycorrhizae community structure in hybrid larch and its parents grown in volcanic ash soil: the role of phosphorous. Sci Total Environ 618:905–915

    Article  CAS  PubMed  Google Scholar 

  • Wei SP, Song YJ, Jia LM, Yuan Z (2018) Diversity of ectomycorrhizal fungi associated with Quercus variabilis in gneissose area of Taihang Mountains. Mycosystema 37(4):422–433

    Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protoc Guide Methods Appl 18(1):315–322

    Google Scholar 

  • Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, Heidelberg

    Book  Google Scholar 

  • Xu SQ, Zhang JF, Luo SS, Zhou X, Shi SH, Tian CJ (2018) Similar soil microbial community structure across different environments after long-term succession: evidence from volcanoes of different ages. J Basic Microbiol 58(8):704–711

    Article  PubMed  Google Scholar 

  • Xue R, Yang Q, Miao FH, Wang XZ, Shen YY (2018) Slope aspect influences plant biomass, soil properties and microbial composition in alpine meadow on the Qinghai-Tibetan Plateau. J Soil Sci Plant Nutr 18(1):1–12

    CAS  Google Scholar 

  • Yang JG, Wang GX, Hua WS, Song CS, Chen YF, Chen ZS (1993) Evaluation of site quality and suitability of trees in the Taihang mountains. Chinese Forest Press, Beijing

    Google Scholar 

  • Yang YH, Watanabe M, Li FD, Zhang JQ, Zhang WJ, Zhai JW (2006) Factors affecting forest growth and possible effects of climate change in the Taihang Mountains, northern China. Forestry 79(1):135–147

    Article  Google Scholar 

  • Zavisic A, Yang N, Marhan S, Kandeler E, Polle A (2018) Forest soil phosphorus resources and fertilization affect ectomycorrhizal community composition, beech P uptake efficiency, and photosynthesis. Front Plant Sci 9:13

    Article  Google Scholar 

  • Zhang Y, Zhou DQ, Zhao Q, Zhou TX, Hyde KD (2010) Diversity and ecological distribution of macrofungi in the Laojun Mountain region, southwestern China. Biodivers Conserv 19(12):3545–3563

    Article  Google Scholar 

  • Zhang J, Taniguchi T, Tateno R, Xu M, Du S, Liu GB, 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(2):297–305

    Article  Google Scholar 

  • Zhang J, Taniguchi T, Xu M, Du S, Liu GB, Yamanaka N (2014) Ectomycorrhizal fungal communities of Quercus liaotungensis along different successional stands on the Loess Plateau China. J For Res 19(4):395–403

    Article  CAS  Google Scholar 

  • Zumsteg A, Baath E, Stierli B, Zeyer J, Frey B (2013) Bacterial and fungal community responses to reciprocal soil transfer along a temperature and soil moisture gradient in a glacier forefield. Soil Biol Biochem 61:121–132

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to Shanghai Majorbio Bio-pharm Technology Co., Ltd for providing the free online platform of Majorbio I-Sanger Cloud Platform for us to perform some data processing. And we thank American Journal Experts (AJE) for English language editing.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Liming Jia.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Project funding: The work was supported by the National Key Technology Research and Development Program of the Ministry of Science and Technology of China (2015BAD07B02).

The online version is available at http://www.springerlink.com

Corresponding editor: Lei Yu

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 30 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wei, S., Song, Y. & Jia, L. Influence of the slope aspect on the ectomycorrhizal fungal community of Quercus variabilis Blume in the middle part of the Taihang Mountains, North China. J. For. Res. 32, 385–400 (2021). https://doi.org/10.1007/s11676-019-01083-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11676-019-01083-9

Keywords

Navigation