Skip to main content

Advertisement

Log in

Mycorrhizal and rhizospheric fungal community assembly differs during subalpine forest restoration on the eastern Qinghai-Tibetan Plateau

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

Mycorrhizosphere is the interface between roots and soil where a myriad of microorganisms mediate plant growth, nutrient acquisition and tolerance to biotic and abiotic stress, and result in driving ecosystem biogeochemical cycling. Understanding the complexity and dynamics of mycorrhizosphere and its ecology and evolution are critical to enhancing forest productivity and ecosystem functioning, especially in high latitude temperate or high altitude alpine forests. However, the fungal community compositions and their driving ecological mechanisms of mycorrhizosphere during forest restoration are poorly documented.

Methods

In this study, we simultaneously examined the ectomycorrhizal (EM) and rhizospheric fungal communities of two dominant host tree species (Abies faxoniana and Betula albosinensis) in subalpine forest communities with distinct forest restoration stages (30- vs. 60-year) after clear-cutting. Illumina MiSeq sequencing of internal transcribed spacer 2 (ITS2) sequences was adopted.

Results

A total of 1222 EM and 5880 rhizosphere fungal operational taxonomic units (OTUs) were obtained at a 97% sequence similarity level, which were mainly dominated by Basidiomycota. Host identity and forest restoration stage had no significant effects on fungal species richness of both EM and rhizospheric fungi. However, the community assembly of EM and rhizospheric fungi was significantly different during forest restoration, with opposite patterns shown on ectomycorrhizae and rhizosphere. The EM fungal community assembly was significantly affected by host identity, stand age and population dynamic, while the rhizosphere fungal community was significantly structured by combinations of host trees biomass, soil properties and spatial distance.

Conclusions

Our data provide important insights that community assembly of EM and rhizosphere fungi may respond idiosyncratically during forest restoration, which will help us deeper understanding forest succession, stability and ecosystem functioning on the Qinghai-Tibetan Plateau.

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

Similar content being viewed by others

References

  • Allison SD, Gartner TB, Mack MC et al (2010) Nitrogen alters carbon dynamics during early succession in boreal forest. Soil Biol Biochem 42:1157–1164

    CAS  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  • Bahram M, Põlme S, Kõljalg 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

    PubMed  Google Scholar 

  • Bais HP, Weir TL, Perry LG et al (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266

    CAS  PubMed  Google Scholar 

  • Baldrian P (2017) Forest microbiome: diversity, complexity and dynamics. FEMS Microbiol Rev 41:109–130

    CAS  PubMed  Google Scholar 

  • Bao SD (1999) Soil and agricultural chemistry analysis. China Agriculture Press, Beijing

    Google Scholar 

  • Barberán A, McGuire KL, Wolf JA, Jones FA, Wright SJ, Turner BL, Essene A, Hubbell SP, Faircloth BC, Fierer N (2015) Relating belowground microbial composition to the taxonomic, phylogenetic, and functional trait distributions of trees in a tropical forest. Ecol Lett 18:1397–1405

    PubMed  Google Scholar 

  • Bell C, Carrillo Y, Boot CM, Rocca JD, Pendall E, Wallenstein MD (2014) Rhizosphere stoichiometry: are C : N : P ratios of plants, soils, and enzymes conserved at the plant species-level? New Phytol 201:505–517

    CAS  PubMed  Google Scholar 

  • Bengtsson-Palme J, Ryberg M, Hartmann M et al (2013) Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods Ecol Evol 4:914–919

    Google Scholar 

  • Bennett JA, Klironomos J (2019) Mechanisms of plant–soil feedback: interactions among biotic and abiotic drivers. New Phytol 222:91–96

    PubMed  Google Scholar 

  • Buée M, Reich M, Murat C et al (2009) 454 pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol 184:449–456

    PubMed  Google Scholar 

  • Buscardo E, Rodríguez-Echeverría S, Freitas H et al (2014) Contrasting soil fungal communities in Mediterranean pine forests subjected to different wildfire frequencies. Fungal Divers 70:85–99

    Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335

    CAS  PubMed  PubMed Central  Google Scholar 

  • Castillo BT, Nave LE, Le Moine JM et al (2018) Impacts of experimentally accelerated forest succession on belowground plant and fungal communities. Soil Biol Biochem 125:44–53

    CAS  Google Scholar 

  • Chandrasekaran M, Kim K, Krishnamoorthy R et al (2016) Mycorrhizal symbiotic efficiency on C3 and C4 plants under salinity stress – a meta-analysis. Front Microbiol 7:1246

    PubMed  PubMed Central  Google Scholar 

  • Churchland C, Grayston SJ (2014) Specificity of plant-microbe interactions in the tree mycorrhizosphere biome and consequences for soil C cycling. Front Microbiol 5:261

    PubMed  PubMed Central  Google Scholar 

  • Clemmensen KE, Bahr A, Ovaskainen O, Dahlberg A, Ekblad A, Wallander H, Stenlid J, Finlay RD, Wardle DA, Lindahl BD (2013) Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339:1615–1618

    CAS  PubMed  Google Scholar 

  • Cui X, Song J (2007) Soil NH4 +/NO3 - nitrogen characteristics in primary forests and the adaptability of some coniferous species. Front For China 2:1–10

    Google Scholar 

  • Davison J, Opik M, Daniell TJ et al (2011) Arbuscular mycorrhizal fungal communities in plant roots are not random assemblages. FEMS Microbiol Ecol 78:103–115

    CAS  PubMed  Google Scholar 

  • Dickie IA, Koide RT, Steiner KC (2002) Influences of established trees on mycorrhizas, nutrition, and growth of Quercus rubra seedlings. Ecol Monogr 72:505–521

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gao C, Zhang Y, Shi N-N, Zheng Y, Chen L, Wubet T, Bruelheide H, Both S, Buscot F, Ding Q, Erfmeier A, Kühn P, Nadrowski K, Scholten T, Guo LD (2015) Community assembly of ectomycorrhizal fungi along a subtropical secondary forest succession. New Phytol 205:771–785

    PubMed  Google Scholar 

  • Gao C, Shi NN, Chen L, Ji NN, Wu BW, Wang YL, Xu Y, Zheng Y, Mi XC, Ma KP, Guo LD (2017) Relationships between soil fungal and woody plant assemblages differ between ridge and valley habitats in a subtropical mountain forest. New Phytol 213:1874–1885

    PubMed  Google Scholar 

  • Gao C, Montoya L, Xu L, Madera M, Hollingsworth J, Purdom E, Hutmacher RB, Dahlberg JA, Coleman-Derr D, Lemaux PG, Taylor JW (2019) Strong succession in arbuscular mycorrhizal fungal communities. ISME J 13:214–226

    PubMed  Google Scholar 

  • Gehring CA, Sthultz CM, Flores-Rentería L, Whipple AV, Whitham TG (2017) Tree genetics defines fungal partner communities that may confer drought tolerance. Proc Natl Acad Sci U S A 114:11169–11174

    CAS  PubMed  PubMed Central  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 26:6960–6973

    CAS  PubMed  Google Scholar 

  • Gómez-Aparicio L, Domínguez-Begines J, Kardol P et al (2017) Plant-soil feedbacks in declining forests: implications for species coexistence. Ecology 98:1908–1921

    PubMed  Google Scholar 

  • Henneron L, Chauvat M, Archaux F et al (2017) Plant interactions as biotic drivers of plasticity in leaf litter traits and decomposability of Quercus petraea. Ecol Monogr 87:321–340

    Google Scholar 

  • Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AF, 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 22:5271–5277

    PubMed  Google Scholar 

  • Legendre P (2007) Studying beta diversity: ecological variation partitioning by multiple regression and canonical analysis. J Plant Ecol 1:3–8

    Google Scholar 

  • Li ZS, Liu GH, Gong L et al (2015) Tree ring-based temperature reconstruction over the past 186 years for the Miyaluo natural reserve, western Sichuan Province of China. Theor Appl Climatol 120:495–506

    Google Scholar 

  • Luo TX, Zhang L, Zhu HZ et al (2009) Correlations between net primary productivity and foliar carbon isotope ratio across a Tibetan ecosystem transect. Ecography 32:526–538

    CAS  Google Scholar 

  • Luo YJ, Wang XK, Lu F (2015) Comprehensive database of biomass regression for China's tree species. China Forestry Publishing House, Beijing

    Google Scholar 

  • McPherson MR, Wang P, Marsh EL et al (2018) Isolation and analysis of microbial communities in soil, rhizosphere, and roots in perennial grassexperiments. J Visualized Exp (137): e57932

  • Miyamoto Y, Sakai A, Hattori M et al (2015) Strong effect of climate on ectomycorrhizal fungal composition: evidence from range overlap between two mountains. ISME J 9:1870–1879

    PubMed  PubMed Central  Google Scholar 

  • Nara K (2006) Ectomycorrhizal networks and seedling establishment during early primary succession. New Phytol 169:169–178

    CAS  PubMed  Google Scholar 

  • Nave LE, Nadelhoffer KJ, Le Moine JM et al (2013) Nitrogen uptake by trees and mycorrhizal fungi in a successional northern temperate forest: insights from multiple isotopic methods. Ecosystems 16:590–603

    CAS  Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M et al (2019) Vegan: community ecology package. R package version 2.5.4. https://CRAN.R-project.org/package=vegan. Accesed 10 September 2019

  • Ostonen I, Rosenvald K, Helmisaari H-S et al (2013) Morphological plasticity of ectomycorrhizal short roots in Betula sp and Picea abies forests across climate and forest succession gradients: its role in changing environments. Front Plant Sci 4:335

    PubMed  PubMed Central  Google Scholar 

  • Peay KG, Bruns TD (2014) Spore dispersal of basidiomycete fungi at the landscape scale is driven by stochastic and deterministic processes and generates variability in plant-fungal interactions. New Phytol 204:180–191

    PubMed  Google Scholar 

  • Peri PL, Ladd B, Pepper DA et al (2012) Carbon (δ13C) and nitrogen (δ15N) stable isotope composition in plant and soil in southern Patagonia's native forests. Glob Chang Biol 18:311–321

    Google Scholar 

  • Philippot L, Raaijmakers JM, Lemanceau P, van der Putten W (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799

    CAS  PubMed  Google Scholar 

  • R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Roberts DW (2016) Labdsv: ordination and multivariate analysis for ecology. R package version 1.8–0. https://cran.r-project.org/package=labdsv. Accessed 5 March 2019

  • Saravesi K, Aikio S, Wäli PR, Ruotsalainen AL, Kaukonen M, Huusko K, Suokas M, Brown SP, Jumpponen A, Tuomi J, Markkola A (2015) Moth outbreaks alter root-associated fungal communities in subarctic mountain birch forests. Microb Ecol 69:788–797

    CAS  PubMed  Google Scholar 

  • 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 D, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sergei P, Mohammad B, Takashi Y 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

    Google Scholar 

  • Shahzad T, Chenu C, Genet P et al (2015) Contribution of exudates, arbuscular mycorrhizal fungi and litter depositions to the rhizosphere priming effect induced by grassland species. Soil Biol Biochem 80:146–155

    CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, New York

    Google Scholar 

  • Smith JE, Molina R, Huso MM et al (2002) Species richness, abundance, and composition of hypogeous and epigeous ectomycorrhizal fungal sporocarps in young, rotation-age, and old-growth stands of Douglas-fir (Pseudotsuga menziesii) in the Cascade Range of Oregon, U.S.A. Can J Bot 80:186–204

    Google Scholar 

  • Taylor DL, Walters WA, Lennon NJ et al (2016) Accurate estimation of fungal diversity and abundance through improved lineage-specific primers optimized for Illumina amplicon sequencing. Appl Environ Microbiol 82:7217–7226

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tedersoo L, Smith ME (2013) Lineages of ectomycorrhizal fungi revisited: foraging strategies and novel lineages revealed by sequences from belowground. Fungal Biol Rev 27:83–99

    Google Scholar 

  • Tedersoo L, Bahram M, Põlme S et al (2014) Global diversity and geography of soil fungi. Science 346:1256688

    PubMed  Google Scholar 

  • Tedersoo L, Bahram M, Cajthaml T, Põlme S, Hiiesalu I, Anslan S, Harend H, Buegger F, Pritsch K, Koricheva J, Abarenkov K (2016) Tree diversity and species identity effects on soil fungi, protists and animals are context dependent. ISME J 10:346–362

    CAS  PubMed  Google Scholar 

  • Twieg BD, Durall DM, Simard SW (2007) Ectomycorrhizal fungal succession in mixed temperate forests. New Phytol 176:437–447

    PubMed  Google Scholar 

  • Uroz S, Buée M, Deveau A et al (2016) Ecology of the forest microbiome: highlights of temperate and boreal ecosystems. Soil Biol Biochem 103:471–488

    CAS  Google Scholar 

  • van der Heijden MGA, Martin FM, Selosse MA, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423

    PubMed  Google Scholar 

  • Wallander H (2000) Use of strontium isotopes and foliar K content to estimate weathering of biotite induced by pine seedlings colonised by ectomycorrhizal fungi from two different soils. Plant Soil 222:215–229

    CAS  Google Scholar 

  • Wobbrock JO, Findlater L, Gergle D et al (2011) The aligned rank transform for nonparametric factorial analyses using only anova procedures. Proceedings of the SIGCHI conference on human factors in computing systems. ACM, Vancouver

    Google Scholar 

  • Wu BW, Gao C, Chen L et al (2018) Host phylogeny is a major determinant of fagaceae-associated ectomycorrhizal fungal community assembly at a regional scale. Front Microbiol 9:2409

    PubMed  PubMed Central  Google Scholar 

  • Xiang X, Gibbons SM, Yang J et al (2015) Arbuscular mycorrhizal fungal communities show low resistance and high resilience to wildfire disturbance. Plant Soil 397:347–356

    CAS  Google Scholar 

  • Zachow C, Berg C, Müller H et al (2009) Fungal diversity in the rhizosphere of endemic plant species of Tenerife (Canary Islands): relationship to vegetation zones and environmental factors. ISME J 3:79–92

    CAS  PubMed  Google Scholar 

  • Zhang Z, Xiao J, Yuan Y et al (2018) Mycelium- and root-derived C inputs differ in their impacts on soil organic C pools and decomposition in forests. Soil Biol Biochem 123:257–265

    CAS  Google Scholar 

Download references

Acknowledgements

This study was funded by the Fundamental Research Funds of CAF (CAFYBB2018ZA003); the National Key R & D Program of China (2016YFC0502104; 2017YFC0505001). We greatly thank Liangdong Guo of the Institute of Microbiology, Chinese Academy of Sciences, Xiangzhen Li and Minjie Yao of Chengdu Institute of Biology, Chinese Academy of Sciences for providing insightful comments and constructive suggestions for revising an early draft of this article; and three anonymous reviewers for their valuable comments. We are also indebted to Pengpeng Lv, Hui Yao, Yonglong Wang and Maoping Li for assistance in bioinformation analysis and Dr. Ji Chen in grammatical correction. The study was prompted by the field assistance received from Xingliang Liu and Qiuhong Feng of Institute of Ecology, Sichuan Academy of Forestry and Peihao Peng of Chengdu University of Technology.

Author information

Authors and Affiliations

Authors

Contributions

Idea and study design: G.X., H.C. and Z.S.; data collection and analysis: H.C. and G.X. with support from S.L., X.C., M.Z., M.C., J.C., K.X., H.Y., G.Z.; writing of the manuscript: G.X., H.C. and Z.S., with all authors contributing substantially to revisions.

Corresponding author

Correspondence to Zuomin Shi.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible Editor: Felipe E. Albornoz.

Publisher’s note

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

Electronic supplementary material

ESM 1

(DOCX 216 kb)

ESM 2

(XLSX 901 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, G., Chen, H., Shi, Z. et al. Mycorrhizal and rhizospheric fungal community assembly differs during subalpine forest restoration on the eastern Qinghai-Tibetan Plateau. Plant Soil 458, 245–259 (2021). https://doi.org/10.1007/s11104-019-04400-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-019-04400-7

Keywords

Navigation