, Volume 60, Issue 5, pp 655–667 | Cite as

Nutritional niche overlap potentiates the use of endophytes in biocontrol of a tree disease

  • Kathrin Blumenstein
  • Benedicte R. Albrectsen
  • Juan A. Martín
  • Malin Hultberg
  • Thomas N. Sieber
  • Marjo Helander
  • Johanna Witzell


Asymptomatic endophytic fungi are often regarded as potent biocontrol agents in plants, but the competitive interactions between endophytes and other microbes within the same host plant are poorly understood. We tested a hypothesis that as compared to asymptomatic endophytes, an aggressive pathogen inhabiting the same host is able to utilize carbon substrates more efficiently. Using phenotype microarray, we determined the carbon utilization profiles of the highly virulent Dutch elm disease (DED) pathogen Ophiostoma novo-ulmi, and four asymptomatic elm (Ulmus spp.) endophyte isolates that were selected based on their differential association to the DED-susceptibility pattern of the host elms. The competitive interactions between isolates were evaluated using a niche overlap index. In contrast to our hypothesis, the studied endophytes exhibited extensive niche overlap with the pathogen, suggesting that some endophyte strains might protect elms against DED-pathogen through competition for substrates and provide new tools for biocontrol of DED.


Carbon utilization profile Endophytic fungi Dutch elm disease Biocontrol Niche differentiation hypothesis Niche tradeoff 



This work was supported by the Swedish Research Council FORMAS (project 2008-1090); Stiftelsen Konsul Faxes Donation, Sweden (projects KF 23 and KF 29); Ministerio de Ciencia e Innovación, Spain, project AGL2009-09289; Ministerio de Economía y Competitividad, Spain (project CTQ2011-28503-C02-02); the Spanish elm breeding program (Ministerio de Agricultura, Alimentación y Medio Ambiente; Universidad Politécnica de Madrid); and the Joint Doctoral Program “Forest and Nature for Society”, FONASO. The English language was edited by Sees editing Ltd, North Somerset, UK. The work was carried out as a part of research aiming to elucidate the role of endophytes in Dutch elm disease (DED) complex, initiated by Johanna Witzell and Juan Martín in 2008. An important goal of the research is to identify endophytes with biocontrol potential against DED.


  1. Ahlholm J, Helander M, Elamo P, Saloniemi I, Neuvonen S, Hanhimäki S, Saikkonen K (2002) Micro-fungi and invertebrate herbivores on birch trees: fungal mediated plant-herbivore interactions or responses to host quality? Ecol Lett 5:648–655CrossRefGoogle Scholar
  2. Albrectsen BR, Björkén L, Varad A, Hagner Å, Wedin M, Karlsson J, Jansson S (2010) Endophytic fungi in European aspen (Populus tremula) leaves—diversity, detection, and a suggested correlation with herbivory resistance. Fungal Divers 41:17–28CrossRefGoogle Scholar
  3. Albrectsen BR, Albrectsen BR, Witzell J, Witzell J (2012) Disentangling functions of fungal endophytes in forest trees. In: Paz Silva A, Sol M (eds) Fungi: Types, environmental impact and role in disease. Nova Science Publishers, New York, pp 235–246Google Scholar
  4. Annis SL, Goodwin PH (1997) Recent advances in the molecular genetics of plant cell wall-degrading enzymes produced by plant pathogenic fungi. Eur J Plant Pathol 103:1–14CrossRefGoogle Scholar
  5. Arnold AE (2007) Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fungal Biol Rev 21:51–66CrossRefGoogle Scholar
  6. Arnold AE, Maynard Z, Gilbert GS, Coley PD, Kursar TA (2000) Are tropical fungal endophytes hyperdiverse? Ecol Lett 3:267–274CrossRefGoogle Scholar
  7. Bernier L, Yang D, Ouellette GB, Dessureault M (1996) Assessment of Phaeotheca dimorphospora for biological control of the Dutch elm disease pathogens, Ophiostoma ulmi and O. novo-ulmi. Plant Pathol 45:609–617CrossRefGoogle Scholar
  8. Brasier CM (1991) Ophiostoma novo-ulmi sp. nov., causative agent of current Dutch elm disease pandemics. Mycopathologia 115:151–161CrossRefGoogle Scholar
  9. Brasier CM, Webber JF (1987) Positive correlations between in vitro growth rate and pathogenesis in Ophiostoma ulmi. Plant Pathol 36:462–466CrossRefGoogle Scholar
  10. Chase JM, Leibold MA (2003) Ecological niches: linking classical and contemporary approaches. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  11. Dahl AS (1934) Snowmold of turf grasses as caused by Fusarium nivale. Phytopathology 24(3):197–214Google Scholar
  12. Dvořák M, Palovčíková D, Jankovský L (2006) The occurrence of endophytic fungus Phomopsis oblonga on elms in the area of southern Bohemia. J For Sci 52:531–535Google Scholar
  13. Ernst M, Neubert K, Mendgen KW, Wirsel SGR (2011) Niche differentiation of two sympatric species of Microdochium colonizing the roots of common reed. BMC Microbiol 11:242–254PubMedCentralCrossRefPubMedGoogle Scholar
  14. Garland JL, Mills AL (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl Environ Microb 57:2351–2359Google Scholar
  15. Gaur R, Singh R, Gupta M, Gaur MK (2010) Aureobasidium pullulans, an economically important polymorphic yeast with special reference to pullulan. Afr J Biotechnol 9:7989–7997Google Scholar
  16. Glynn NC, Hare MC, Parry DW, Edwards SG (2005) Phylogenetic analysis of EF-1 alpha gene sequences from isolates of Microdochium nivale leads to elevation of varieties majus and nivale to species status. Mycol Res 109:872–880CrossRefPubMedGoogle Scholar
  17. Haack SK, Garchow H, Klug MJ, Forney LJ (1995) Analysis of factors affecting the accuracy, reproducibility, and interpretation of microbial community carbon source utilization patterns. Appl Environ Microb 61:1458–1468Google Scholar
  18. Hamilton CE, Gundel PE, Helander M, Saikkonen K (2012) Endophytic mediation of reactive oxygen species and antioxidant activity in plants: a review. Fungal Divers 54:1–10CrossRefGoogle Scholar
  19. Helander ML, Sieber T, Petrini O, Neuvonen S (1994) Ecology of pine needle endophytes: spatial variation and consequences of acid irrigation. Can J Bot 72:1108–1113CrossRefGoogle Scholar
  20. Hubbell SP (2001) Monographs in population biology, the unified neutral theory of biodiversity and biogeography. Princeton University Press, PrincetonGoogle Scholar
  21. Hubbes M, Jeng RS (1981) Aggressiveness of Ceratocystis ulmi strains and induction of resistance in Ulmus americana. Eur J For Path 11:257–264CrossRefGoogle Scholar
  22. Kaur G, Padmaja V (2009) Relationships among activities of extracellular enzyme production and virulence against Helicoverpa armigera in Beauveria bassiana. J Basic Microb 49:264–274CrossRefGoogle Scholar
  23. Klepzig KD (1998) Competition between a biological control fungus, Ophiostoma piliferum, and symbionts of the southern pine beetle. Mycologia 90:69–75CrossRefGoogle Scholar
  24. Kulkarni RK, Nickerson KW (1981) Nutritional control of dimorphism in Ceratocystis ulmi. Exp Mycol 5:148–154CrossRefGoogle Scholar
  25. Lee HB, Magan N (1999) Environmental factors and nutritional utilization patterns affect niche overlap indices between Aspergillus ochraceus and other spoilage fungi. Lett Appl Microbiol 28:300–304CrossRefPubMedGoogle Scholar
  26. Martín JA, Solla A, Domingues MR, Coimbra MA, Gil L (2008) Exogenous phenol increase resistance of Ulmus minor to Dutch elm disease through formation of suberin-like compounds on xylem tissues. Environ Exp Bot 64:97–104CrossRefGoogle Scholar
  27. Martín JA, Solla A, Esteban LG, de Palacios P, Gil L (2009) Bordered pit and ray morphology involvement in elm resistance to Ophiostoma novo-ulmi. Can J For Res 39:420–429CrossRefGoogle Scholar
  28. Martín JA, Fuentes-Utrilla P, Gil L, Witzell J (2010) Ecological factors behind the Dutch elm disease complex in Europe—a review. Ecol Bull 53:209–224Google Scholar
  29. Martín JA, Witzell J, Blumenstein K, Rozpedowska E, Helander M, Sieber TN, Gil L (2013) Resistance to Dutch elm disease reduces xylem endophytic fungi presence in elms (Ulmus spp.). PLoS ONE 8:e56987PubMedCentralCrossRefPubMedGoogle Scholar
  30. Mejía LC, Rojas EI, Maynard Z, van Bael S, Arnold AE, Hebbar P, Samuels GJ, Robbins N, Herre EA (2008) Endophytic fungi as biocontrol agents of Theobroma cacao pathogens. Biol Control 46:4–14CrossRefGoogle Scholar
  31. Meyer SE, Stewart TE, Clement S (2010) The quick and the deadly: growth vs virulence in a seed bank pathogen. New Phytol 187:209–216CrossRefPubMedGoogle Scholar
  32. Mikkelson GM (2005) Niche-based vs. neutral models of ecological communities. Biol Phil 20:557–566CrossRefGoogle Scholar
  33. Neely D, Himelick EB (1963) Root graft transmission of Dutch elm disease in municipalities. Plant Dis Rep 47:83–85Google Scholar
  34. Newcombe G (2011) Endophytes in forest management: four challenges. In: Pirttilä AM, Frank AC (eds) Endophytes in forest trees: biology and applications. Springer, Dordrecht, pp 251–262CrossRefGoogle Scholar
  35. Pagán I, Alonso-Blanco C, García-Arenal F (2007) The relationship of within-host multiplication and virulence in a plant-virus system. PLoS ONE 2:e786PubMedCentralCrossRefPubMedGoogle Scholar
  36. Rodriguez R, Redman R (2008) More than 400 million years of evolution and some plants still can’t make it on their own: plant stress tolerance via fungal symbiosis. J Exp Bot 59:1109–1114CrossRefPubMedGoogle Scholar
  37. Rudinsky JA (1962) Ecology of Scolytidae. Annu Rev of Entomol 7:327–348CrossRefGoogle Scholar
  38. Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343CrossRefGoogle Scholar
  39. Saikkonen K, Ahlholm J, Helander M, Poteri M, Tuominen J (2001) Experimental testing of rust fungus-mediated herbivory resistance in Betula pendula. Forest Pathol 31:321–329CrossRefGoogle Scholar
  40. Saikkonen K, Wäli P, Helander M, Faeth SH (2004) Evolution of endophyte-plant symbioses. Trends Plant Sci 9:275–280CrossRefPubMedGoogle Scholar
  41. Santini A, Faccoli M (2015) Dutch elm disease and elm bark beetles: a century of association. iForest 8:126–134CrossRefGoogle Scholar
  42. Scheffer RJ, Voeten JGWF, Guries RP (2008) Biological control of Dutch elm disease. Plant Dis 92:192–200CrossRefGoogle Scholar
  43. Sieber T, Riesen TK, Müller E, Fried PM (1988) Endophytic fungi in four winter wheat cultivars (Triticum aestivum L.) differing in resistance against Stagonospora nodorum (Berk.) Cast. & Germ. = Septoria nodorum (Berk.) Berk. J Phytopath 122:289–306CrossRefGoogle Scholar
  44. Singh D, Smalley EB (1969) Nitrogenous and carbohydrate compounds in the xylem sap of Ulmaceae species varying in resistance to Dutch elm disease. Can J Bot 47:335–339CrossRefGoogle Scholar
  45. Slepecky RA, Starmer WT (2009) Phenotypic plasticity in fungi: a review with observations on Aureobasidium pullulans. Mycologia 101:823–832CrossRefPubMedGoogle Scholar
  46. Solheim H, Krokene P (1998) Growth and virulence of mountain pine beetle associated blue-stain fungi, Ophiostoma clavigerum and Ophiostoma montium. Can J Bot 76:561–566Google Scholar
  47. Solla A, Dacasa MC, Nasmith C, Hubbes M, Gil L (2008) Analysis of Spanish populations of Ophiostoma ulmi and O. novo-ulmi using phenotypic characteristics and RAPD markers. Plant Pathol 57:33–44Google Scholar
  48. Tellenbach C, Sieber TN (2012) Do colonization by dark septate endophytes and elevated temperature affect pathogenicity of oomycetes? FEMS Microbiol Ecol 82:157–168CrossRefPubMedGoogle Scholar
  49. Tilman D (2004) Niche tradeoffs, neutrality, and community structure: a stochastic theory of resource competition, invasion, and community assembly. P Natl Acad Sci USA 101:10854–10861CrossRefGoogle Scholar
  50. Tonukari NJ (2003) Enzymes and fungal virulence. J Appl Sci Environ Manag 7:5–8Google Scholar
  51. Webber J (1981) A natural biological control of Dutch elm disease. Nature 292:449–451CrossRefGoogle Scholar
  52. Webber JF, Brasier CM (1984) The transmission of Dutch elm disease: A study of the process involved. In: Anderson JM, Rayner ADM, Walton D (eds) Invertebrate-microbial interactions. Cambridge University Press, Cambridge, pp 271–306Google Scholar
  53. White JF, Torres MS (2010) Is plant endophyte-mediated defensive mutualism the result of oxidative stress protection? Physiol Plant 138:440–446CrossRefPubMedGoogle Scholar
  54. Wilson M, Lindow SE (1994) Coexistence among epiphytic bacterial populations mediated through nutritional resource partitioning. Appl Environ Microb 60:4468–4477Google Scholar
  55. Witzell J, Martin JA (2008) Phenolic metabolites in the resistance of northern forest trees to pathogens—past experiences and future prospects. Can J For Res 38:2711–2727CrossRefGoogle Scholar
  56. Witzell J, Martín JA, Blumenstein K (2013) Ecological aspects of endophyte-based biocontrol of forest diseases. In: Verma VC, Gange AC (eds) Advances in endophytic research. Springer-Verlag, Heidelberg, pp 321–333Google Scholar
  57. Zalar P, Gostinčar C, de Hoog GS, Uršič V, Sudhadham M, Gunde-Cimerman N (2008) Redefinition of Aureobasidium pullulans and its varieties. Stud Mycol 61:21–38PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© International Organization for Biological Control (IOBC) 2015

Authors and Affiliations

  • Kathrin Blumenstein
    • 1
  • Benedicte R. Albrectsen
    • 2
    • 3
  • Juan A. Martín
    • 4
  • Malin Hultberg
    • 5
  • Thomas N. Sieber
    • 6
  • Marjo Helander
    • 7
    • 8
  • Johanna Witzell
    • 1
    • 9
  1. 1.Faculty of Forest Sciences, Southern Swedish Forest Research CentreSwedish University of Agricultural SciencesAlnarpSweden
  2. 2.Umeå Plant Science Centre, Department of Plant PhysiologyUmeå UniversityUmeåSweden
  3. 3.Department of Plant and Environmental SciencesUniversity of CopenhagenFredriksberg CDenmark
  4. 4.Department of Natural Systems and ResourcesTechnical University of Madrid (UPM)MadridSpain
  5. 5.Department of Biosystems and Technology, Faculty of Landscape Architecture, Horticulture and Crop Production ScienceSwedish University of Agricultural SciencesAlnarpSweden
  6. 6.Institute of Integrative BiologyETH ZurichZurichSwitzerland
  7. 7.Department of Biology, Section of EcologyUniversity of TurkuTurkuFinland
  8. 8.Plant Production ResearchMTT Agrifood Research FinlandJokioinenFinland
  9. 9.Faculty of Science and Forestry, School of Forest SciencesUniversity of Eastern FinlandJoensuuFinland

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