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Ectomycorrhizal fungal communities of Quercus liaotungensis along local slopes in the temperate oak forests on the Loess Plateau, China

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Ecological Research

Abstract

Topographic factors strongly affect the diversity of plants and local environmental conditions, yet little is known about their effects on the distribution of ectomycorrhizal fungi (EMF). By combining morphological and molecular identification methods, we investigated the relationship between EMF communities of Quercus liaotungensis and topographic factors along local slopes in the temperate oak forest on the Loess Plateau of northwest China. ITS-RFLP analysis revealed a high diversity of EMF taxa (135 taxa) associated with Q. liaotungensis along three local slopes. EMF communities among slope sites or slope positions, tended to share major common EMF species, which accounted for more than 80 % of the total EMF abundance, and showed a diverse distribution, which mainly related to rare species. Ordination analyses showed that EMF taxa distribution was significantly correlated with several environmental variables (slope site, slope position, slope gradient, and soil C:N). Topography-mediated changes of environmental conditions may be important determinants of the distribution of EMF taxa along local slopes (slope position and slope site) in the central Loess Plateau.

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References

  • Akema T, Futai K (2005) Ectomycorrhizal development in a Pinus thunbergii stand in relation to location on a slope and effect on tree mortality from pine wilt disease. J Forest Res 10(2):93–99. doi:10.1007/s10310-004-0101-3

    Article  Google Scholar 

  • Al Omary A (2011) Effects of aspect and slope position on growth and nutritional status of planted Aleppo pine (Pinus halepensis Mill.) in a degraded land semi-arid areas of Jordan. New Forest 42(3):285–300. doi:10.1007/s11056-011-9251-2

    Article  Google Scholar 

  • Aponte C, Garcia LV, Maranon T, Gardes M (2010) Indirect host effect on ectomycorrhizal fungi: leaf fall and litter quality explain changes in fungal communities on the roots of co-occurring Mediterranean oaks. Soil Biol Biochem 42(5):788–796. doi:10.1016/j.soilbio.2010.01.014

    Article  CAS  Google Scholar 

  • Avis PG, McLaughlin DJ, Dentinger BC, Reich PB (2003) Long-term increase in nitrogen supply alters above- and below-ground ectomycorrhizal communities and increases the dominance of Russula spp. in a temperate oak savanna. New Phytol 160(1):239–253. doi:10.1046/j.1469-8137.2003.00865.x

  • Avis PG, Mueller GM, Lussenhop J (2008) Ectomycorrhizal fungal communities in two North American oak forests respond to nitrogen addition. New Phytol 179(2):472–483. doi:10.1111/j.1469-8137.2008.02491.x

    Article  CAS  Google Scholar 

  • 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(2):465–473. doi:10.1111/j.1469-8137.2011.03927.x

    Article  Google Scholar 

  • Bai YR, Wang YK (2011) Spatial variability of soil chemical properties in a Jujube slope on the Loess Plateau of China. Soil Sci 176(10):550–558. doi:10.1097/SS.0b013e3182285cfd

    Article  CAS  Google Scholar 

  • Benucci GMN, Raggi L, Albertini E, Grebenc T, Bencivenga M, Falcinelli M, Di Massimo G (2011) Ectomycorrhizal communities in a productive Tuber aestivum Vittad. orchard: composition, host influence and species replacement. FEMS Microbiol Ecol 76(1):170–184. doi:10.1111/j.1574-6941.2010.01039.x

    Google Scholar 

  • Casper BB, Goldman R, Lkhagva A, Helliker BR, Plante AF, Spence LA, Liancourt P, Boldgiv B, Petraitis PS (2012) Legumes mitigate ecological consequences of a topographic gradient in a northern Mongolian steppe. Oecologia 169(1):85–94. doi:10.1007/s00442-011-2183-x

    Article  Google Scholar 

  • Cavender-Bares J, Izzo A, Robinson R, Lovelock CE (2009) Changes in ectomycorrhizal community structure on two containerized oak hosts across an experimental hydrologic gradient. Mycorrhiza 19(3):133–142. doi:10.1007/s00572-008-0220-3

    Article  CAS  Google Scholar 

  • Colwell RK (2009) EstimateS: statistical estimation of species richness and shared species from samples. Version 8.2. User’s guide and application. http://purl.oclc.org/estimates

  • Du S, Yamanaka N, Yamamoto F, Otsuki K, Wang SQ, Hou QC (2007) The effect of climate on radial growth of Quercus liaotungensis forest trees in Loess Plateau, China. Dendrochronologia 25(1):29–36. doi:10.1016/j.dendro.2007.01.005

    Article  Google Scholar 

  • Du S, Wang YL, Kume T, Zhang JG, Otsuki K, Yamanaka N, Liu GB (2011) Sapflow characteristics and climatic responses in three forest species in the semiarid Loess Plateau region of China. Agric For Meteorol 151(1):1–10. doi:10.1016/j.agrformet.2010.08.011

    Article  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. doi:10.1111/j.1365-294X.1993.tb00005.x

    Article  CAS  Google Scholar 

  • 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(2):430–440. doi:10.1111/j.1469-8137.2007.02016.x

    Article  CAS  Google Scholar 

  • Ishida TA, Nara K, Ma SR, Takano T, Liu SK (2009) Ectomycorrhizal fungal community in alkaline–saline soil in northeastern China. Mycorrhiza 19(5):329–335. doi:10.1007/s00572-008-0219-9

    Article  Google Scholar 

  • Jiao JY, Tzanopoulos J, Xofis P, Mitchley J (2008) Factors affecting distribution of vegetation types on abandoned cropland in the hilly-gullied Loess Plateau region of China. Pedosphere 18(1):24–33. doi:10.1016/s1002-0160(07)60099-x

    Article  Google Scholar 

  • Kennedy P (2010) Ectomycorrhizal fungi and interspecific competition: species interactions, community structure, coexistence mechanisms, and future research directions. New Phytol 187(4):895–910. doi:10.1111/j.1469-8137.2010.03399.x

    Article  Google Scholar 

  • Kernaghan G, Hambling B, Fung M, Khasa D (2002) In vitro selection of boreal ectomycorrhizal fungi for use in reclamation of saline-alkaline habitats. Restor Ecol 10(1):43–51. doi:10.1046/j.1526-100X.2002.10105.x

    Article  Google Scholar 

  • Kranabetter JM, Durall DM, MacKenzie WH (2009) Diversity and species distribution of ectomycorrhizal fungi along productivity gradients of a southern boreal forest. Mycorrhiza 19(2):99–111. doi:10.1007/s00572-008-0208-z

    Article  CAS  Google Scholar 

  • Landeweert R, Leeflang P, Smit E, Kuyper T (2005) Diversity of an ectomycorrhizal fungal community studied by a root tip and total soil DNA approach. Mycorrhiza 15:1–6. doi:10.1007/s00572-003-0284-z

    Article  Google Scholar 

  • Lilleskov EK, Bruns TD (2001) Nitrogen and ectomycorrhizal fungal communities: what we know, what we need to know. New Phytol 149(2):156–158. doi:10.1046/j.1469-8137.2001.00042-2.x

    Article  Google Scholar 

  • Lilleskov EA, Parrent JL (2007) Can we develop general predictive models of mycorrhizal fungal community–environment relationships? New Phytol 174(2):250–256. doi:10.1111/j.1469-8137.2007.02023.x

    Article  CAS  Google Scholar 

  • Lilleskov EA, Bruns TD, Horton TR, Taylor DL, Grogan P (2004) Detection of forest stand-level spatial structure in ectomycorrhizal fungal communities. FEMS Microbiol Ecol 49(2):319–332. doi:10.1016/j.femsec.2004.04.004

    Article  CAS  Google Scholar 

  • Liu SL, Guo XD, Fu BJ, Lian G, Wang J (2007) The effect of environmental variables on soil characteristics at different scales in the transition zone of the Loess Plateau in China. Soil Use Manag 23(1):92–99. doi:10.1111/j.1475-2743.2006.00064.x

    Article  Google Scholar 

  • Matsuda Y, Hijii N (1999) Characterization and identification of Strobilomyces confusus ectomycorrhizas on Momi fir by RFLP analysis of the PCR-amplified ITS region of the rDNA. J Forest Res 4:145–150. doi:10.1007/BF02762239

    Article  Google Scholar 

  • McCune B, Mefford MJ (1995–2002) PC-ORD. Multivariate analysis of ecological data, Version 4. MJM Software Design, Gleneden Beach

  • 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. doi:10.1111/j.1469-8137.2007.02348.x

    Google Scholar 

  • Nilsson LO, Wallander H (2003) Production of external mycelium by ectomycorrhizal fungi in a Norway spruce forest was reduced in response to nitrogen fertilization. New Phytol 158(2):409–416. doi:10.1046/j.1469-8137.2003.00728.x

    Article  Google Scholar 

  • Nippert JB, Ocheltree TW, Skibbe AM, Kangas LC, Ham JM, Arnold KBS, Brunsell NA (2011) Linking plant growth responses across topographic gradients in tallgrass prairie. Oecologia 166(4):1131–1142. doi:10.1007/s00442-011-1948-6

    Article  Google Scholar 

  • Ostonen I, Helmisaari HS, Borken W, Tedersoo L, Kukumagi M, Bahram M, Lindroos AJ, Nojd P, Uri V, Merila P, Asi E, Lohmus K (2011) Fine root foraging strategies in Norway spruce forests across a European climate gradient. Glob Change Biol 17(12):3620–3632. doi:10.1111/j.1365-2486.2011.02501.x

    Article  Google Scholar 

  • 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(6):470–480. doi:10.1111/j.1461-0248.2007.01035.x

    Article  Google Scholar 

  • Peay KG, Schubert MG, Nguyen NH, Bruns TD (2012) Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules. Mol Ecol 21(16):4122–4136. doi:10.1111/j.1365-294X.2012.05666.x

    Article  Google Scholar 

  • Pena R, Offermann C, Simon J, Naumann PS, Gessler A, Holst J, Dannenmann M, Mayer H, Kogel-Knabner I, Rennenberg H, Polle A (2010) Girdling affects ectomycorrhizal fungal (EMF) diversity and reveals functional differences in EMF community composition in a beech forest. Appl Environ Microbiol 76(6):1831–1841. doi:10.1128/aem.01703-09

    Article  CAS  Google Scholar 

  • Qiu Y, Fu BJ, Wang J, Chen LD (2001) Soil moisture variation in relation to topography and land use in a hillslope catchment of the Loess Plateau. China J Hydrol 240(3–4):243–263. doi:10.1016/s0022-1694(00)00362-0

    Article  Google Scholar 

  • Richard F, Millot S, Gardes M, Selosse MA (2005) Diversity and specificity of ectomycorrhizal fungi retrieved from an old-growth Mediterranean forest dominated by Quercus ilex. New Phytol 166(3):1011–1023. doi:10.1111/j.1469-8137.2005.01382.x

    Article  CAS  Google Scholar 

  • Rincón A, Pueyo JJ (2010) Effect of fire severity and site slope on diversity and structure of the ectomycorrhizal fungal community associated with post-fire regenerated Pinus pinaster Ait. seedlings. For Ecol Manag 260 (3):361–369. doi:10.1016/j.foreco.2010.04.028

  • Sariyildiz T, Anderson JM, Kucuk M (2005) Effects of tree species and topography on soil chemistry, litter quality, and decomposition in Northeast Turkey. Soil Biol Biochem 37(9):1695–1706. doi:10.1016/j.soilbio.2005.02.004

    Article  CAS  Google Scholar 

  • Shi LB, Guttenberger M, Kottke I, Hampp R (2002) The effect of drought on mycorrhizas of beech (Fagus sylvatica L.): changes in community structure, and the content of carbohydrates and nitrogen storage bodies of the fungi. Mycorrhiza 12(6):303–311. doi:10.1007/s00572-002-0197-2

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, San Diego

    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. doi:10.1111/j.1469-8137.2007.02040.x

    Article  CAS  Google Scholar 

  • Srinivasan M, Natarajan K, Nagarajan G (2000) Growth optimization of an ectomycorrhizal fungus with respect to pH and temperature in vitro, using design of Experiments. Bioproc Eng 22(3):267–273. doi:10.1007/s004490050731

    Article  CAS  Google Scholar 

  • Suggitt AJ, Gillingham PK, Hill JK, Huntley B, Kunin WE, Roy DB, Thomas CD (2011) Habitat microclimates drive fine-scale variation in extreme temperatures. Oikos 120(1):1–8. doi:10.1111/j.1600-0706.2010.18270.x

    Article  Google Scholar 

  • Takyu M, Aiba SI, Kitayama K (2002) Effects of topography on tropical lower montane forests under different geological conditions on Mount Kinabalu, Borneo. Plant Ecol 159(1):35–49. doi:10.1023/a:1015512400074

    Article  Google Scholar 

  • Tang GA, Li FY, Liu XJ, Long Y, Yang X (2008) Research on the slope spectrum of the Loess Plateau. Sci China Ser E Technol Sci 51:175–185. doi:10.1007/s11431-008-5002-9

    Google Scholar 

  • Toljander JF, Eberhardt U, Toljander YK, Paul LR, Taylor AFS (2006) Species composition of an ectomycorrhizal fungal community along a local nutrient gradient in a boreal forest. New Phytol 170(4):873–883. doi:10.1111/j.1469-8137.2006.01718.x

    Article  CAS  Google Scholar 

  • Trudell SA, Edmonds RL (2004) Macrofungus communities correlate with moisture and nitrogen abundance in two old-growth conifer forests, Olympic National Park, Washington, USA. Can J Bot 82(6):781–800. doi:10.1139/b04-057

    Article  CAS  Google Scholar 

  • Tsui CC, Chen ZS, Hsieh CF (2004) Relationships between soil properties and slope position in a lowland rain forest of southern Taiwan. Geoderma 123(1–2):131–142. doi:10.1016/j.geoderma.2004.01.031

    Article  Google Scholar 

  • Tsujino R, Sato H, Imamura A, Yumoto T (2009) Topography-specific emergence of fungal fruiting bodies in warm temperate evergreen broad-leaved forests on Yakushima Island, Japan. Mycoscience 50(5):388–399. doi:10.1007/s10267-009-0494-0

    Article  Google Scholar 

  • Twieg BD, Durall DM, Simard SW (2007) Ectomycorrhizal fungal succession in mixed temperate forests. New Phytol 176(2):437–447. doi:10.1111/j.1469-8137.2007.02173.x

    Article  Google Scholar 

  • Visser S (1995) Ectomycorrhizal fungal succession in jack pine stands following wildfire. New Phytol 129(3):389–401. doi:10.1111/j.1469-8137.1995.tb04309.x

    Article  Google Scholar 

  • Wang J, Fu BJ, Qiu Y, Chen LD (2003) Analysis on soil nutrient characteristics for sustainable land use in Danangou catchment of the Loess Plateau, China. Catena 54(1–2):17–29. doi:10.1016/s0341-8162(03)00054-7

    Article  CAS  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. doi:10.1007/s00572-011-0423-x

    Article  Google Scholar 

  • Wezel A, Steinmuller N, Friederichsen JR (2002) Slope position effects on soil fertility and crop productivity and implications for soil conservation in upland northwest Vietnam. Agric Ecosyst Environ 91(1–3):113–126. doi:10.1016/s0167-8809(01)00242-0

    Article  Google Scholar 

  • White TJ, Bruns TD, Lee S, Taylor J (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. Academic Press, New York

    Google Scholar 

  • Wu QX, Yang WZ (1998) Forest and grassland vegetation construction and its sustainable development in Loess Plateau. Science Press, Beijing

    Google Scholar 

  • Yamanaka T (2003) The effect of pH on the growth of saprotrophic and ectomycorrhizal ammonia fungi in vitro. Mycologia 95(4):584–589. doi:10.2307/3761934

    Article  Google Scholar 

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Acknowledgments

This study was supported by the Japan Society for the Promotion of Science through the Core University Program and the Global COE Program: Global Center of Excellence for Dryland Science. We are grateful to the Institute of Soil and Water Conservation, CAS for valuable assistance, Kouhei Sugita for help in the field, and the two anonymous referees who gave valuable comments on early versions of the manuscript.

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Authors and Affiliations

  1. Arid Land Research Center, Tottori University, Tottori, 680-0001, Japan

    Jian Zhang, Takeshi Taniguchi & Norikazu Yamanaka

  2. Institute of Soil and Water Conservation, Chinese Academy of Sciences and Ministry of Water Resources, Yangling, Shaanxi, 712100, China

    Jian Zhang, Ming Xu, Sheng Du & Guo-Bin Liu

  3. Field Science Education and Research Center, Kyoto University, Kyoto, 606-8502, Japan

    Ryunosuke Tateno

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  1. Jian Zhang
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  2. Takeshi Taniguchi
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  3. Ryunosuke Tateno
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  4. Ming Xu
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  7. Norikazu Yamanaka
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Correspondence to Jian Zhang.

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Zhang, J., Taniguchi, T., Tateno, R. et al. Ectomycorrhizal fungal communities of Quercus liaotungensis along local slopes in the temperate oak forests on the Loess Plateau, China. Ecol Res 28, 297–305 (2013). https://doi.org/10.1007/s11284-012-1017-6

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