Skip to main content
SpringerLink
Log in

Root fungal colonisations of the understory grass Deschampsia flexuosa after top-canopy harvesting

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

Abstract

Aims

Root fungal relationships in forest understory may be affected by tree harvesting. Deschampsia flexuosa forms a mutualistic symbiosis with arbuscular mycorrhizal (AM) fungi functioning in nutrient uptake, and a more loose association with dark septate endophytic (DSE) fungi. We asked how harvesting affects fungal colonisations and whether DSE is more prone to change than AM.

Methods

Deschampsia flexuosa plants were sampled close to a control or a cut tree after top-canopy harvesting in a primary successional site. Colonisations were studied using light microscopy. Shoot N%, vegetation cover and soil nutrients were determined.

Results

Tree harvesting did not affect vegetation and soil parameters, except potassium (K+) increasing near cut trees. AM colonisation did not change, while DSE increased. Shoot N% increased with increasing DSE near cut trees. Hyaline septate (HSE) hyphae and soil K+ and magnesium (Mg2+) were positively correlated near control trees. Lichen cover and HSE correlated negatively.

Conclusions

DSE colonisation increased but AM did not change after harvesting. Positive correlation of DSE with shoot N% near cut trees may suggest a role for DSE in favouring plant nitrogen uptake after disturbance in an open microsite. HSE may play a role in K+ and Mg2+ uptake.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Addy HD, Piercey MM, Currah RS (2005) Micro fungal endophytes in roots. Can J Bot 83:1–13. doi:10.1139/b04-171

    Article  Google Scholar 

  • Ahlich K, Sieber TN (1996) The profusion of dark septate endophytic fungi in non ectomycorrhizal fine roots of forest trees and shrubs. New Phytol 132:259–270. doi:10.1111/j.1469-8137.1996.tb01845.x

    Article  Google Scholar 

  • Ahonen-Jonnarth U, Göransson A, Finlay RD (2003) Growth and nutrient uptake of ectomycorrhizal Pinus sylvestris seedlings in a natural substrate treated with elevated Al concentrations. Tree Physiol 23:157–167. doi:10.1093/treephys/23.3.157

    Article  CAS  PubMed  Google Scholar 

  • Ahti T (1977) Lichens in the boreal coniferous zone. In: Seaward MRD (ed) Lichen ecology. Academic, London, pp 145–181

    Google Scholar 

  • Alaoja V (2013) The role of symbiotic arbuscular mycorrhizal fungi (Glomeromycota) in roots of the host plant Deschampsia flexuosa in vegetation succession of inland sand dunes in Finnish Lapland. Masters Thesis, University of Jyväskylä

  • Alestalo R (1979) Land uplift and development of the littoral and aeolian morphology on Hailuoto. PhD Dissertation, University of Oulu, Oulu, Finland, Finland

    Google Scholar 

  • Barrow JR (2003) Atypical morphology of dark septate fungal root endophytes of Bouteloua in arid southwestern USA rangelands. Mycorrhiza 13:239–247. doi:10.1007/s00572-003-0222-0

    Article  CAS  PubMed  Google Scholar 

  • Barrow J, Aaltonen R (2001) Evaluation of the internal colonization of Atriplex canescens (Pursh) Nutt. roots by dark septate fungi and the influence of host physiological activity. Mycorrhiza 11:199–205. doi:10.1007/s005720100111

    Article  Google Scholar 

  • Barrow JR, Osuna P (2002) Phosphorus solubilisation and uptake by dark septate fungi in fourwing saltbush, Atriplex canescens (Pursh) Nutt. J Arid Environ 51:449–459. doi:10.1006/jare.2001.0925

    Article  Google Scholar 

  • Bartholdy BA, Berreck M, Haselwandter K (2001) Hydroxamate siderophore synthesis by Phialocephala fortinii, a typical dark septate fungal root endophyte. Biol Met 14:33–42. doi:10.1023/A:1016687021803

    CAS  Google Scholar 

  • Brundrett MC (2006) Understanding the roles of multifunctional mycorrhizal and endophytic fungi. In: Schulz B, Boyle C, Sieber TN (eds) Microbial root endophytes. Springer, Berlin, pp 281–298

    Chapter  Google Scholar 

  • Caldwell BA, Jumpponen A, Trappe JM (2000) Utilization of major detrital substrates by dark-septate, root endophytes. Mycologia 230–232. doi:10.2307/3761555

  • Corkidi L, Rincón E (1997) Arbuscular mycorrhizae in a tropical sand dune ecosystem on the Gulf of Mexico. Mycorrhiza 7:17–23. doi:10.1007/s005720050158

    Article  Google Scholar 

  • Crawley MJ (2012) The R book, 2nd edn. Wiley, Chichester

    Book  Google Scholar 

  • Crush JR (1973) Significance of endomycorrhizas in tussock grassland in Otago, New Zealand. New Zeal J Bot 11:645–660. doi:10.1080/0028825X.1973.10430306

    Article  Google Scholar 

  • Currah RS, Tsuneda A (1993) Vegetative and reproductive morphology of Phialocephala fortinii (Hyphomycetes, Mycelium radicis atrovirens) in culture. T Mycol Soc Jpn 34:345–356

    Google Scholar 

  • Day M, Currah RS (2011) Role of selected dark septate endophyte species and other hyphomycetes as saprobes on moss gametophytes. Botany 89:349–359. doi:10.1139/b11-023

    Article  Google Scholar 

  • Dighton J, Mason PA (1985) Mycorrhizal dynamics during forest tree development. In: Moore D, Casselton LA, Wood DA, Frankland JC (eds) Developmental biology of higher fungi. Cambridge University Press, Cambridge, pp 117–139

    Google Scholar 

  • Emmer IM, Sevink J (1994) Temporal and vertical changes in the humus form profile during a primary succession of Pinus sylvestris. Plant Soil 167:281–295. doi:10.1007/BF00007955

    Article  CAS  Google Scholar 

  • Fernando AA, Currah RS (1996) A comparative study of the effects of the root endophytes Leptodontidium orchidicola and Phialocephala fortinii (Fungi imperfecti) on the growth of some subalpine plants in culture. Can J Bot 74:1071–1078. doi:10.1139/b96-131

    Article  Google Scholar 

  • Finlay RD, Frostegård Å, Sonnerfeldt AM (1992) Utilization of organic and inorganic nitrogen sources by ectomycorrhizal fungi in pure culture and in symbiosis with Pinus contorta Dougl. ex Loud. New Phytol 120:105–115. doi:10.1111/j.1469-8137.1992.tb01063.x

    Article  Google Scholar 

  • Garcia I, Mendoza R, Pomar MC (2012) Arbuscular mycorrhizal symbiosis and dark septate endophytes under contrasting grazing modes in the Magellanic steppe of Tierra del Fuego. Agric Ecosyst Environ 155:194–201. doi:10.1016/j.agee.2012.04.020

    Article  Google Scholar 

  • Göransson P, Olsson PA, Postma J, Falkengren-Grerup U (2008) Colonisation by arbuscular mycorrhizal and fine endophytic fungi in four woodland grasses–variation in relation to pH and aluminium. Soil Biol Biochem 40:2260–2265. doi:10.1016/j.soilbio.2008.05.002

    Article  Google Scholar 

  • Grau O, Rautio P, Heikkinen J, Saravesi K, Kozlov MV, Markkola A (2010) An ericoid shrub plays a dual role in recruiting both pines and their fungal symbionts along primary succession gradients. Oikos 119:1727–1734

    Article  Google Scholar 

  • Grelet G, Johnson D, Paterson E, Anderson IC, Alexander IJ (2009) Reciprocal carbon and nitrogen transfer between an ericaceous dwarf shrub and fungi isolated from Piceirhiza bicolorata ectomycorrhizas. New Phytol 182:359–366

    Article  CAS  PubMed  Google Scholar 

  • Hart M, Klironomos JN (2003) Diversity of arbuscular mycorrhizal fungi and ecosystem functioning. In: Van Der Heijden MGA, Sanders IR (eds) Mycorrhizal ecology. Springer, Berlin, pp 225–242. doi:10.1007/978-3-540-38364-2_9

    Chapter  Google Scholar 

  • Hartnett D, Wilson GWT (2002) The role of mycorrhizas in plant community structure and dynamics: lessons from grasslands. Plant Soil 244:319–331

    Article  CAS  Google Scholar 

  • Haselwandter K, Read DJ (1982) The significance of a root-fungus association in two Carex species of high-alpine plant communities. Oecologia 53:352–354. doi:10.1007/BF00389012

    Article  CAS  PubMed  Google Scholar 

  • Hellemaa P (2013) The development of coastal dunes and their vegetation in Finland. Fennia 176:111–221

    Google Scholar 

  • Hoffland E, Kuyper TW, Wallander H, Plassard C, Gorbushina AA, Haselwandter K, Holmström S, Landeweert R, Lundström UL, Rosling A, Sen R, Smits MM, van Hees PAW, van Breemen N (2004) The role of fungi in weathering. Front Ecol Environ 2:258–264. doi:10.1890/15409295(2004)002[0258:TROFIW]2.0.CO;2

    Article  Google Scholar 

  • Hultén E, Fries M (1986) Atlas of North European vascular plants (north of the tropic of cancer). Koeltz scientific books, Köanigstein

    Google Scholar 

  • Hyppönen M, Hallikainen V, Niemelä J, Rautio P (2013) The contradictory role of understory vegetation on the success of Scots pine regeneration. Silva Fenn 47:1–19

    Article  Google Scholar 

  • Jarvis PG (1964) Interference by Deschampsia flexuosa (L.) Trin. Oikos 15:56–78. doi:10.2307/3564748

    Article  Google Scholar 

  • John MK (1970) Colorimetric determination of phosphorus in soil and plant materials with ascorbic acid. Soil Sci 100:214–220

    Article  Google Scholar 

  • Jumpponen A, Trappe JM (1998) Dark septate endophytes: a review of facultative biotrophic root‐colonizing fungi. New Phytol 140:295–310. doi:10.1046/j.1469-8137.1998.00265.x

    Article  Google Scholar 

  • Jumpponen A, Mattson KG, Trappe JM (1998) Mycorrhizal functioning of Phialocephala fortinii with Pinus contorta on glacier forefront soil: interactions with soil nitrogen and organic matter. Mycorrhiza 7:261–265. doi:10.1007/s005720050190

    Article  CAS  PubMed  Google Scholar 

  • Kauppinen M, Raveala K, Wäli PR, Ruotsalainen AL (2014) Contrasting preferences of arbuscular mycorrhizal and dark septate fungi colonizing boreal and subarctic Avenella flexuosa. Mycorrhiza 24:171–177. doi:10.1007/s00572-013-0526-7

    Article  CAS  PubMed  Google Scholar 

  • Knapp DG, Pintye A, Kovács GM (2012) The dark side is not fastidious- dark septate endophytic fungi of native and invasive plants of semiarid sandy areas. PLoS One 7:1–11

    Article  Google Scholar 

  • Kuikka K, Härmä E, Markkola A et al (2003) Severe defoliation of Scots pine reduces reproductive investment by ectomycorrhizal symbionts. Ecology 84:2051–2206. doi:10.1890/02-0359

    Article  Google Scholar 

  • Logan VS, Clarke PJ, Allaway WG (1989) Mycorrhizas and root attributes of plants of coastal sand-dunes of New South Wales. Aust J Plant Physiol 16:141–146. doi:10.1071/PP9890141

    Article  Google Scholar 

  • Mandyam K, Jumpponen A (2005) Seeking the elusive function of the root-colonising dark septate endophytic fungi. Stud Mycol 53:173–189. doi:10.3114/sim.53.1.173

    Article  Google Scholar 

  • Mandyam KG, Jumpponen A (2014) Mutualism–parasitism paradigm synthesized from results of root-endophyte models. Front Microbiol 5:776. doi:10.3389/fmicb.2014.00776

    PubMed  Google Scholar 

  • Mandyam K, Loughin T, Jumpponen A (2010) Isolation and morphological and metabolic characterization of common endophytes in annually burned tallgrass prairies. Mycologia 103:813–821. doi:10.3852/09-212

    Article  Google Scholar 

  • McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular arbuscular mycorrhizal fungi. New Phytol 115:495–501. doi:10.1111/j.1469-8137.1990.tb00476.x

    Article  Google Scholar 

  • Menkis A, Allmer J, Vasiliauskas R, Lygis V, Stenlid J, Finlay R (2004) Ecology and molecular characterization of dark septate fungi from roots, living stems, coarse and fine woody debris. Mycol Res 108:965–973. doi:10.1017/S0953756204000668

    Article  CAS  PubMed  Google Scholar 

  • Muthukumar T, Senthilkumar M, Rajangam M, Udaiyan K (2006) Arbuscular mycorrhizal morphology and dark septate fungal associations in medicinal and aromatic plants of Western Ghats, Southern India. Mycorrhiza 17:11–24. doi:10.1007/s00572-006-0077-2

    Article  CAS  PubMed  Google Scholar 

  • Newsham KK (2011) A meta-analysis of plant responses to dark septate root endophytes. New Phytol 190:783–793. doi:10.1111/j.1469-8137.2010.03611.x

    Article  CAS  PubMed  Google Scholar 

  • Newsham KK, Fitter AH, Watkinson AR (1995) Multi-functionality and biodiversity in arbuscular mycorrhizas. Trends Ecol Evol 10:407–411. doi:10.1016/S0169-5347(00)89157-0

    Article  CAS  PubMed  Google Scholar 

  • Nilsson M-C, Wardle DA (2005) Understory vegetation as a forest ecosystem driver: evidence from the northern Swedish boreal forest. Front Ecol Environ 3:421–428

    Article  Google Scholar 

  • Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775. doi:10.1038/nrmicro1987

    Article  CAS  PubMed  Google Scholar 

  • Pella E, Colombo B (1973) Study of carbon, hydrogen and nitrogen determination by combustion-gas chromatography. Microchim Acta 61:697–719. doi:10.1007/BF01218130

    Article  Google Scholar 

  • Pennanen T, Liski J, Bååth E, Kitunen V, Uotila J, Westman CJ, Fritze H (1999) Structure of the microbial communities in coniferous forest soils in relation to site fertility and stand development stage. Microb Ecol 38:168–179

    Article  CAS  PubMed  Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–160. doi:10.1016/S0007-1536(70)80110-3

    Article  Google Scholar 

  • Pietikäinen A, Kytöviita MM, Vuoti U (2005) Mycorrhiza and seedling establishment in a subarctic meadow: effects of fertilization and defoliation. J Veg Sci 16:175–182. doi:10.1658/1100-9233(2005)016[0175:MASEIA]2.0.CO;2

    Article  Google Scholar 

  • Postma JW, Olsson PA, Falkengren-Grerup U (2007) Root colonisation by arbuscular mycorrhizal, fine endophytic and dark septate fungi across a pH gradient in acid beech forests. Soil Biol Biochem 39:400–408. doi:10.1016/j.soilbio.2006.08.007

    Article  CAS  Google Scholar 

  • Pyšek P (1992) Dominant species exchange during succession in reclaimed habitats: a case study from areas deforested by air pollution. For Ecol Manag 54:27–44. doi:10.1016/0378-1127(92)90003-R

    Article  Google Scholar 

  • R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Read DJ, Haselwandter K (1981) Observations on the mycorrhizal status of some alpine plant communities. New Phytol 88:341–352. doi:10.1111/j.1469-8137.1981.tb01729.x

    Article  Google Scholar 

  • Read DJ, Leake JR, Langdale AR (1989) The nitrogen nutrition of mycorrhizal fungi and their host plants. In: Boddy L, Marchant R, Read DJ (eds) Nitrogen. Phosphorus and Sulphur Utilization by Fungi. Cambridge University Press, Cambridge, UK, pp 181–204

    Google Scholar 

  • Ruotsalainen AL, Eskelinen A (2011) Root fungal symbionts interact with mammalian herbivory, soil nutrient availability and specific habitat conditions. Oecologia 166:807–817. doi:10.1007/s00442-011-1928-x

    Article  PubMed  Google Scholar 

  • Ruotsalainen AL, Markkola AM, Kozlov MV (2007) Root fungal colonisation in Deschampsia flexuosa: effects of pollution and neighbouring trees. Environ Pollut 147:723–728. doi:10.1016/j.envpol.2006.09.004

    Article  CAS  PubMed  Google Scholar 

  • Ruotsalainen AL, Markkola AM, Kozlov MV (2010) Birch effects on root fungal colonisation of crowberry are uniform along different environmental gradients. Basic Appl Ecol 11:459–467

    Article  Google Scholar 

  • Saravesi K, Ruotsalainen AL, Cahill JC (2014) Contrasting impacts of defoliation on root colonization by arbuscular mycorrhizal and dark septate endophytic fungi of Medicago sativa. Mycorrhiza 24:239–245. doi:10.1007/s00572-013-0536-5

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Strengbom J, Näsholm T, Ericson L (2004) Light, not nitrogen, limits growth of the grass Deschampsia flexuosa in boreal forests. Can J Bot 82:430–435. doi:10.1139/b04-017

    Article  Google Scholar 

  • Tejesvi MV, Ruotsalainen AL, Markkola AM, Pirttilä AM (2010) Root endophytes along a primary successional gradient in northern Finland. Fungal Divers 41:125–134. doi:10.1007/s13225-009-0016-6

    Article  Google Scholar 

  • Tejesvi MV, Sauvola T, Pirttilä AM, Ruotsalainen AL (2013) Neighbouring Deschampsia flexuosa and Trientalis europaea harbor contrasting root fungal endophytic communities. Mycorrhiza 23:1–10. doi:10.1007/s00572-012-0444-0

    Article  PubMed  Google Scholar 

  • Upson R, Read DJ, Newsham KK (2009) Nitrogen form influences the response of Deschampsia antarctica to dark septate root endophytes. Mycorrhiza 20:1–11. doi:10.1007/s00572-009-0260-3

    Article  PubMed  Google Scholar 

  • Usuki F, Narisawa H (2007) A mutualistic symbiosis between a dark septate endophytic fungus, Heteroconium chaetospira, and a nonmycorrhizal plant, Chinese cabbage. Mycologia 99:175–184. doi:10.3852/mycologia.99.2.175

    Article  CAS  PubMed  Google Scholar 

  • Villarreal‐Ruiz L, Anderson IC, Alexander IJ (2004) Interaction between an isolate from the Hymenoscyphus ericae aggregate and roots of Pinus and Vaccinium. New Phytol 164:183–192

    Article  Google Scholar 

  • Vohnik M, Mrnka L, Lukešová T, Bruzone MC, Kohout P, Fehrer J (2013) The cultivable endophytic community of Norway spruce ectomycorrhizas from microhabitats lacking ericaceous hosts is dominated by ericoid mycorrhizal Meliniomyces variabilis. Fungal Ecol 6:281–292

    Article  Google Scholar 

  • Vrålstad T, Fossheim T, Schumacher T (2000) Piceirhiza bicolorata-the ectomycorrhizal expression of the Hymenoscyphus ericae aggregate? New Phytol 145:549–563

    Article  Google Scholar 

  • Wagg C, Pautler M, Massicotte HB, Peterson RL (2008) The co-occurrence of ectomycorrhizal, arbuscular mycorrhizal, and dark septate fungi in seedlings of four members of the Pinaceae. Mycorrhiza 18:103–110. doi:10.1007/s00572-007-0157-y

    Article  PubMed  Google Scholar 

  • Wallander H, Wickman T (1999) Biotite and microcline as potassium sources in ectomycorrhizal and non-mycorrhizal Pinus sylvestris seedlings. Mycorrhiza 9:25–32. doi:10.1007/s005720050259

    Article  CAS  Google Scholar 

  • Zijlstra JD, Van’t Hof P, Baar J, Verkley GJ, Summerbell RC, Paradi I, Braakhekke WG, Berendse F (2005) Diversity of symbiotic root endophytes of the Helotiales in ericaceous plants and the grass, Deschampsia flexuosa. Stud Mycol 53:147–162. doi:10.3114/sim.53.1.147

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank the staff members of the Botanical Museum and Garden in the Biodiversity Unit of the University of Oulu for providing facilities and technical support during the experiment. Tarja Törmänen and Tuulikki Pakonen are warmly acknowledged for nutrient analysis of the samples and Maarit Kaukonen for field assistance and providing soil nutrient and vegetation data. The study was financed by the Academy of Finland (project number 138309 to AM Markkola) and the Centre for International Mobility (CIMO) to N.B.W. Hengodage. The land owner Metsähallitus is acknowledged for a permission to use the study site for the present study.

Author information

Authors and Affiliations

  1. Department of Ecology and Genetics, University of Oulu, P.O. Box 3000, FI-90014, Oulu, Finland

    Nirmalee Bhagya Wijayalath Hengodage, Anna Liisa Ruotsalainen, Annamari Markkola & Hely Häggman

Authors
  1. Nirmalee Bhagya Wijayalath Hengodage
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anna Liisa Ruotsalainen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Annamari Markkola
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hely Häggman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anna Liisa Ruotsalainen.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible Editor: Jesus Mercado-Blanco.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online resource 1

(JPG 1562 kb)

Online resource 2

(PDF 168 kb)

Online resource 3

(PDF 123 kb)

Online resource 4

(PDF 240 kb)

Online resource 5

(PDF 169 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hengodage, N.B.W., Ruotsalainen, A.L., Markkola, A. et al. Root fungal colonisations of the understory grass Deschampsia flexuosa after top-canopy harvesting. Plant Soil 414, 171–180 (2017). https://doi.org/10.1007/s11104-016-3108-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-016-3108-6

Keywords

Search

Navigation