Dark Septate Endophytes (DSE) in Boreal and Subarctic Forests

  • Anna Liisa RuotsalainenEmail author
Part of the Forestry Sciences book series (FOSC, volume 86)


Dark septate endophytes (DSE) are root-associated fungi that inhabit plant roots and soil in a wide variety of ecosystems and host plants worldwide. They are recognized by their distinctive growth habit inside healthy roots, although the taxonomic and functional variety of the fungi forming the associations is high. DSE fungi have the potential to act as beneficial symbionts of the trees and other plants, but the evidence is unequivocal. They grow in the roots together with mycorrhizal- and other root-associated fungi, but the relationships between these fungal groups are unknown. Boreal and subarctic forests constitute a continuous belt in the cool and cold areas of the Northern Hemisphere. Roughly, boreal forests are characterized by coniferous trees. The subarctic is most distinctive in the Northernmost Europe where mountain birch (Betula pubescens ssp. czerepanovii) forests form a continuous forest cover near the Arctic treeline. In this chapter, information from studies on DSE fungi in the boreal and subarctic forests is compiled and discussed.



Internal transcribed spacer


Amplified fragment length polymorphism


Restriction fragment length polymorphism


Phialocephala fortinii s.l. – Acephala applanata group


  1. Addy HD, Hambleton S, Currah RS (2000) Distribution and molecular characterization of the root endophyte Phialocephala fortinii along an environmental gradient in the boreal forest of Alberta. Mycol Res 104:1213–1221CrossRefGoogle Scholar
  2. Addy HD, Piercey MM, Currah RS (2005) Microfungal endophytes in roots. Can J Bot 83:1–13CrossRefGoogle Scholar
  3. Ahlich K, Sieber TN (1996) The profusion of dark septate endophytic fungi in non-ectomycorrhizal fine roots of forest trees and shrubs. New Phytol 132:259–270CrossRefGoogle Scholar
  4. Barrow JR, Aaltonen RE (2001) Evaluation of the internal colonization of Atriplex canescens (Pursh.) Nutt. roots by dark septate fungi and the influence of host physiological activity. Mycorrhiza 11:199–205CrossRefGoogle Scholar
  5. Bent E, Kiekel P, Brenton R, Taylor DL (2011) Root-associated ectomycorrhizal fungi shared by various boreal forest seedlings naturally regenerating after a fire in interior Alaska and correlation of different fungi with host growth responses. Appl Env Microbiol 77:3351–3359CrossRefGoogle Scholar
  6. Björbäkmo MFM, Carlsen T, Brysting A, Vrålstad T, Hoiland K, Ugland KI, Geml J, Schumacher T, Kauserud H (2010) High diversity of root associated fungi in both alpine and arctic Dryas octopetala. BMC Plant Biol 10:244CrossRefGoogle Scholar
  7. Blaalid R, Davey ML, Kauserud H, Carlsen T, Halvorsen R, Høiland K, Eidesen PB (2014) Arctic root-associated fungal community composition reflects environmental filtering. Mol Ecol 23:649–659CrossRefPubMedGoogle Scholar
  8. Bodeker ITM, Lindahl BD, Olson Å, Clemmensen KE (2016) Mycorrhizal and saprotrophic fungal guilds compete for the same organic substrates but affect decomposition differently. Funct Ecol 30:1967–1978CrossRefGoogle Scholar
  9. Caldwell BA, Jumpponen A, Trappe JM (2000) Utilization of major detrital substrates by dark-septate, root endophytes. Mycologia 92:230–232CrossRefGoogle Scholar
  10. Currah RS, Van Dyk M (1986) A survey of some perennial vascular plant species native to Alberta for occurrence of mycorrhizal fungi. Can Field Nat 100:330–342Google Scholar
  11. DeBellis T, Kernaghan G, Bradley R, Widden P (2006) Relationship between stand composition and ectomycorrhizal community structure in boreal mixed-wood forest. Microb Ecol 52:114–126CrossRefPubMedGoogle Scholar
  12. Grünig CR, Sieber TN (2005) Molecular and phenotypic description of the widespread root symbiont Acephala applanata gen. et sp. nov. formerly know as dark-septate endophyte Type 1. Mycologia 97:628–640CrossRefPubMedGoogle Scholar
  13. Grünig CR, Duò A, Sieber TN, Holdenrieder O (2008) Assignment of species rank to six reproductively isolated cryptic species of the Phialocephala fortinii s.l.—Acephala applanata species complex. Mycologia 100:47–67CrossRefPubMedGoogle Scholar
  14. Hambleton S, Currah RS (1997) Fungal endophytes from the roots of alpine and boreal Ericaceae. Can J Bot 75:1570–1581CrossRefGoogle Scholar
  15. Harney SK, Rogers SO, Wang CJK (1997) Molecular characterization of dematiaceous root endophytes. Mycol Res 101:1397–1404CrossRefGoogle Scholar
  16. Haselwandter K (1979) Mycorrhizal status of ericaceous plants in alpine and subalpine areas. New Phytol 83:427–431CrossRefGoogle Scholar
  17. Haselwandter K (1987) Mycorrhizal infection and possible ecological significance in climatically and nutritionally stressed alpine plant communities. Angew Botanik 61:107–114Google Scholar
  18. Haselwandter K, Read DJ (1980) Fungal associations of dominant and sub-dominant plants in high-alpine vegetation systems with special reference to mycorrhiza. Oecologia 45:57–62CrossRefPubMedGoogle Scholar
  19. Haselwandter K, Read DJ (1982) The significance of root-fungus association in two Carex species in high-alpine plant communities. Oecologia 53:352–354CrossRefPubMedGoogle Scholar
  20. Hashiba T, Narisawa K (2005) The development and endophytic nature of the fungus Heteroconium chaetospira. FEMS Microbiol Ecol 252:191–196CrossRefGoogle Scholar
  21. Hengodage NBW, Ruotsalainen AL, Markkola A, Häggman H (2017) Root fungal colonisations of the understory grass Deschampsia flexuosa after top-canopy harvesting. Plant Soil 414:171–180CrossRefGoogle Scholar
  22. Huusko K, Tarvainen O, Saravesi K, Pennanen T, Fritze H, Kubin E, Markkola A (2015) Short.term impacts of energy wood harvesting on ectomycorrhizal fungal communities of Norway spruce saplings. ISME J 9:581–591CrossRefPubMedGoogle Scholar
  23. Huusko K, Ruotsalainen AL, Markkola AM (2017) A shift from arbuscular mycorrhizal to dark septate endophytic colonization in Deschampsia flexuosa roots occurs along primary successional gradient. Mycorrhiza 27:129–138CrossRefPubMedGoogle Scholar
  24. Jepsen JU, Hagen SB, Ims RA, Yoccoz NG (2008) Climate change and outbreaks of the geometrids Operophtera brumata and Epirrita autumnata in subarctic birch forest: evidence of a recent outbreak range expansion. J Anim Ecol 77:257–264CrossRefPubMedGoogle Scholar
  25. Jumpponen A (2001) Dark septate endophytes—are they mycorrhizal? Mycorrhiza 11:207–211CrossRefGoogle Scholar
  26. Jumpponen A, Trappe JM (1998) Dark-septate root endophytes: a review with special reference to facultative biotrophic symbiosis. New Phytol 140:295–310CrossRefGoogle Scholar
  27. Jumpponen A, Mattson KG, Trappe JM (1998) Mycorrhizal functioning of Phialocephala fortinii: interactions with soil nitrogen and organic matter. Mycorrhiza 7:261–265CrossRefPubMedGoogle Scholar
  28. Jumpponen A, Herrera J, Porras-Alfaro A, Rudgers J (2017) Biogeography of root-associated fungal endophytes. In: Tedersoo L (ed) Biogeography of mycorrhizal symbiosis. Springer International Publishing, pp 195–222CrossRefGoogle Scholar
  29. Karst J, Erbilgin N, Pec GJ, Cigan PW, Najar A, Simard SW, Cahill JF Jr (2015) Ectomycorrhizal fungi mediate indirect effects of a bark beetle outbreak on secondary chemistry and establishment of pine seedlings. New Phytol. Scholar
  30. 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 24:171–177CrossRefPubMedGoogle Scholar
  31. Kernaghan G, Patriquin G (2011) Host associations between fungal root endophytes and boreal trees. Microb Ecol 62:460–473CrossRefPubMedGoogle Scholar
  32. Kernaghan G, Patriquin (2015) Diversity and host preference of fungi co-inhabiting Cenococcum mycorrhizae. Fungal Ecol 17: 84–95CrossRefGoogle Scholar
  33. Knapp DG, Kovács GM, Zajta E, Groenewald JZ, Crous PW (2015) Dark septate endophyte pleosporalean genera from semiarid areas. Persoonia 35:87–100CrossRefPubMedPubMedCentralGoogle Scholar
  34. Lahlali R, McGregor L, Song T, Gossen BD, Narisawa K, Peng G (2014) Heteroconium chaetospira induces resistance to clubroot via upregulation of host genes involved in jasmonic acid, ethylene, and auxin Biosynthesis. PLoS ONE 9:e94144CrossRefPubMedPubMedCentralGoogle Scholar
  35. Lazaruk LW, Macdonald SE, Kernaghan G (2008) The effect of mechanical site preparation on ectomycorrhizae of planted white spruce seedlings in conifer-dominated boreal mixedwood forest. Can J For Res 38:2072–2079CrossRefGoogle Scholar
  36. Lehtonen J, Heikkinen K (1995) On the recovery of mountain birch after Epirrita damage in Finnish Lapland, with a particular emphasis on reindeer grazing. Ecoscience 2:349–356CrossRefGoogle Scholar
  37. MacDonald GM, Gajewski K (1992) The northern treeline of Canada. In: Janelle D G (ed) Geographical snapshots of North America. Guilford Press, pp 34–37Google Scholar
  38. Mahmoud RS, Narisawa K (2013) A new fungal endophyte, Scolecobasidium humicola, promotes tomato growth under organic nitrogen conditions. PLoS ONE 8:e78746CrossRefPubMedPubMedCentralGoogle Scholar
  39. Mandyam K, Jumpponen A (2005) Seeking the elusive function of the root-colonizing dark septate endophytes. Stud Mycol 53:173–189CrossRefGoogle Scholar
  40. Mayerhofer MS, Kernaghan G, Harper KA (2013) The effects of fungal root endophytes on plant growth: a meta-analysis. Mycorrhiza 23:119–128CrossRefPubMedGoogle Scholar
  41. 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 108:965–973CrossRefPubMedGoogle Scholar
  42. Narisawa K, Hambleton S, Currah RS (2007) Heteroconium chaetospira, a dark septate root endophyte allied to the Herpotrichiellaceae (Chaetothyriales) obtained from come forest soil samples in Canada using bait plants. Mycoscience 48:274–281CrossRefGoogle Scholar
  43. Newsham KK (2011) A meta-analysis of plant responses to dark septate root endophytes. New Phytol 190:783–793CrossRefPubMedGoogle Scholar
  44. Newsham KK, Upson R, Read DJ (2009) Mycorrhiza and dark septate endophytes in Polar Regions. Fungal Ecol 2:10–20CrossRefGoogle Scholar
  45. Olsrud M, Carlsson BÅ, Svensson BM, Michelsen A, Melillo JM (2010) Responses of root fungal colonization, plant cover and leaf nutrients to long-term exposure to elevated atmospheric CO2 and warming in a subarctic birch forest understory. Global Change Biol 16:1820–1829CrossRefGoogle Scholar
  46. Piercey MM, Graham SW, Currah RS (2004) Patterns of genetic variation in Phialocephala fortinii across a broad latitudinal transect in Canada. Mycol Res 108:955–964CrossRefPubMedGoogle Scholar
  47. Poosakkannu A, Nissinen R, Kytöviita M-M (2015) Culturable endophytic microbial communities in the circumpolar grass, Deschampsia flexuosa in a sub-Arctic inland primary succession are habitat and growth stage specific. Environ Microbiol Rep 7:111–122CrossRefPubMedGoogle Scholar
  48. Porras-Alfaro A, Bayman P (2011) Hidden fungi, emergent properties: endophytes and microbiomes. Annu Rev Phytopathol 49:291–315CrossRefPubMedGoogle Scholar
  49. Postma JWM, 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 39:400–408CrossRefGoogle Scholar
  50. Queloz V, Sieber TN, Holdenrieder O, McDonald BA, Grünig CR (2011) No biogeographical pattern for a root-associated species complex. Glob Ecol Biogeogr 20:160–169CrossRefGoogle Scholar
  51. Read DJ, Haselwandter K (1981) Observations of the mycorrhizal status of some alpine plant communities. New Phytol 88:341–352CrossRefGoogle Scholar
  52. Reininger V, Grünig CR, Sieber TN (2012) Host species and strain combination determine growth reduction of spruce and birch seedlings colonized by root-associated dark septate endophytes. Env Microbiol 14:1064–1076CrossRefGoogle Scholar
  53. Rodriquez RJ, White JF Jr, Arnold AE, Redman RS (2009) Fungal endophytes, diversity and functional roles. New Phytol 182:314–330CrossRefGoogle Scholar
  54. Ruotsalainen AL, Markkola AM, Kozlov MV (2007) Root fungal colonisation in Deschampsia flexuosa: effects of pollution and neighbouring trees. Environ Poll 147:723–728CrossRefGoogle Scholar
  55. Ruotsalainen AL, Markkola AM, Kozlov MV (2010) Birch effects on root fungal colonisation of crowberry are uniform along different environmental gradients. Basic Appl Ecol 11:459–467CrossRefGoogle Scholar
  56. 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 69:788–797CrossRefPubMedGoogle Scholar
  57. Sieber TN (2007) Endophytic fungi in forest trees: are they mutualists? Fungal Biol Rev 21:75–89CrossRefGoogle Scholar
  58. Sieber TN, Grünig CR (2013) Fungal root endophytes. In: Eshel A, Beeckman T (eds) Plant roots—the hidden half. Boca Raton, FL, USA. CRC Press, Taylo & Francis Group, 38.1–38.49Google Scholar
  59. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, LondonCrossRefGoogle Scholar
  60. Stoyke G, Currah RS (1991) Endophytic fungi from the mycorrhiza of alpine ericoid plants. Can J Bot 69:347–352CrossRefGoogle Scholar
  61. Stoyke G, Egger K, Currah RS (1992) Characterization of sterile endophytic fungi from the mycorrhizae of subalpine plants. Can J Bot 70:2009–2016CrossRefGoogle Scholar
  62. Summerbell R (2005) Root endophyte and mycorrhizosphere fungi of black spruce, Picea mariana, in a boreal forest habitat: influence of site factors on fungal distributions. Stud Mycol 53:121–145CrossRefGoogle Scholar
  63. Taylor DL, Herriott IC, Stone KE, McFarland JW, Booth MG, Leigh MB (2010) Structure and resilience of fungal communities in Alaskan boreal forest soils. Can J For Res 40:1288–1301CrossRefGoogle Scholar
  64. Tejesvi MV, Ruotsalainen AL, Markkola AM, Pirttilä AM (2010) Root endophytes along a primary successional gradient in northern Finland. Fungal Divers 41:125–134CrossRefGoogle Scholar
  65. Tejesvi MV, Sauvola T, Pirttilä AM, Ruotsalainen AL (2013) Neighboring Deschampsia flexuosa and Trientalis europaea harbor contrasting root fungal endophytic communities. Mycorrhiza 23:1–10CrossRefPubMedGoogle Scholar
  66. Terhonen E, Keriö S, Sun H, Asiegbu FO (2014) Endophytic fungi of Norway spruce roots in boreal pristine mire, drained peatland and mineral soil and their inhibitory effect on Heterobasidion parviporum in vitro. Fungal Ecol 9:17–26CrossRefGoogle Scholar
  67. Upson R, Read DJ, Newsham KK (2009) Nitrogen form influences the response of Deschampsia antarctica to dark septate root endophytes. Mycorrhiza 20:1–11CrossRefPubMedGoogle Scholar
  68. Usuki F, Narisawa K (2007) A mutualistic symbiosis between a dark septate endophytic fungus, Heteroconium chaetospira, and a nonmycorrhizal plant, Chinese cabbage. Mycologia 99:175–184CrossRefPubMedGoogle Scholar
  69. Väre H, Vestberg M, Eurola S (1992) Mycorrhiza and root-associated fungi in Spitsbergen. Mycorrhiza 1:93–104CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Ecology and GeneticsUniversity of OuluOuluFinland

Personalised recommendations