Advertisement

Biocontrol Potential of Forest Tree Endophytes

  • Eeva Terhonen
  • Andriy Kovalchuk
  • Artin Zarsav
  • Fred O. Asiegbu
Chapter
Part of the Forestry Sciences book series (FOSC, volume 86)

Abstract

In the natural forest environment, the spread of pathogens may have dramatic effects on ecosystem functioning. To successfully control devastating forest pathogens, application of endophytes as biocontrol agents is an emerging area of research. There are several ways by which endophytic microorganisms can protect their tree hosts against pathogens. Endophytes promote plant growth by producing beneficial secondary metabolites (e.g. phytohormones) or providing nutrients (e.g. phosphorus). Endophytes can compete with pathogens and herbivores by successfully utilizing available substrates (colonization of shared niche can restrict pathogen invasion), or endophytes can produce antagonistic metabolites. Endophytes can enhance plant resistance by triggering and priming host defensive reactions. Endophytes could provide several opportunities for application in integrated pest management (IPM) to gain sustainable forestry practices. To utilize endophytes as biocontrol agents, the mechanisms behind the possible mode of action should be determined. Novel advances in cultivation-independent techniques including next generation sequencing technology (NGS), association analyses and network inference modelling will greatly facilitate identification of endophytes and unravel potential beneficial functions of endophytic communities. A further understanding of these mechanisms could help to minimize the use of environmental harming chemicals in plant and forest tree protection. We propose simple guidelines that could facilitate the use of fungal endophytes as biocontrol agents and simultaneously study their ecological functions.

Abbreviations

ACC

1-aminocyclopropane-1-carboxylic acid

AHL

N-acyl-L-homoserine lactone

BCAs

Biocontrol agents

BHI

Brain Heart infusion medium

C-endophytes

Clavicipitaceous endophytes

DED

Dutch elm tree disease

DSEs

Dark septate endophytes

dsRNA

Double-stranded RNA

EtOAc

Ethyl acetate

HPLC

High performance liquid chromatography

IAA

Indole-3-acetic acid

IPM

Integrated pest management

ISR

Induced systemic resistance

ITS

Internal transcribed spacer

JA

Jasmonic acid

K

Potassium

KBA

King’s B agar

LA

Luria agar

LC-MS

Liquid chromatography–mass spectrometry

MEA

Malt extract agar

MS

Mass spectrometry

MWAS

Metagenome-wide association studies

N

Nitrogen

NC-endophytes

Non-clavicipitaceous endophytes

NGS

Next generation sequencing

NMR

Nuclear magnetic resonance spectroscopy

P

Phosphorus

PAC

Phialocephala fortinii s.l.- Acephala applanata Species complex

PDA

Potato dextrose agar

PGPR

Plant growth-promoting rhizobacteria

PPP

Plant protection product

PR proteins

Pathogenesis-related proteins

RFLP

Restriction fragment length polymorphism

SA

Salicylic acid

SAR

Systemic acquired resistance

TSA

Tryptic soy agar

VWO

Verticillium wilt of olive trees

YPDA

Yeast Peptone Dextrose Agar

References

  1. Abarenkov K, Nilsson RH, Larsson KH, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T, Sen R, Taylor AF, Tedersoo L, Ursing BM, Vrålstad T, Liimatainen K, Peintner U, Kõljalg U (2010) The UNITE database for molecular identification of fungi—recent updates and future perspectives. New Phytol 186:281–285PubMedCrossRefPubMedCentralGoogle Scholar
  2. Adomas A, Eklund M, Johansson M, Asiegbu FO (2006) Identification and analysis of differentially expressed cDNA’s during non-self competitive interaction between Phlebiopsis gigantea and Heterobasidion parviporum. FEMS Microbiol Ecol 57:26–39PubMedCrossRefPubMedCentralGoogle Scholar
  3. Ahlholm JU, Helander M, Henriksson J, Metzler M, Saikkonen K (2002) Environmental conditions and host genotype direct genetic diversity of Venturia ditricha, a fungal endophyte of birch trees. Evolution 56(8):1566–1573PubMedPubMedCentralCrossRefGoogle Scholar
  4. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedPubMedCentralCrossRefGoogle Scholar
  5. Ardanov P, Sessitsch A, Haggman H, Kozyrovska N, Pirttilä AM (2012) Methylobacterium-Induced Endophyte Community Changes Correspond with Protection of Plants against Pathogen Attack. Plos One 7(10)PubMedPubMedCentralCrossRefGoogle Scholar
  6. Arnold AE, Henk DA, Eells RL, Lutzoni F, Vilgalys R (2007) Diversity and phylogenetic affinities of foliar fungal endophytes in loblolly pine inferred by culturing and environmental PCR. Mycologia 99:185–206PubMedCrossRefPubMedCentralGoogle Scholar
  7. Arnold AE, Maynard Z, Gilbert GS (2001) Fungal endophytes in dicotyledonous neotropical trees: patterns of abundance and diversity. Mycol Res 105:1502–1507CrossRefGoogle Scholar
  8. Arnold AE, Mejía LC, Kyllo D, Rojas EI, Maynard Z, Robbins N, Herre EA (2003) Fungal endophytes limit pathogen damage in a tropical tree. P Natl Acad Sci USA 100:15649–15654CrossRefGoogle Scholar
  9. Arnold AE (2002) Neotropical fungal endophytes: diversity and ecology [Doctoral dissertation]. University of Arizona, Tucson, p 337Google Scholar
  10. Asiegbu FO, Adomas A, Stenlid J (2005) Conifer root and butt rot caused by Heterobasidion annosum (Fr.) Bref. s.l. Mol Plant Pat 6:395–409CrossRefGoogle Scholar
  11. Avis TJ, Belanger RR (2001) Specificity and mode of action of the antifungal fatty acid cis-9-heptadecenoic acid produced by Pseudozyma flocculosa. Appl Environ Microb 67(2):956–960CrossRefGoogle Scholar
  12. Backman PA, Sikora RA (2008) Endophytes: An emerging tool for biological control. Biol Control 46(1):1–3CrossRefGoogle Scholar
  13. Backman PA, Wilson M, Murphy JF (1997) Bacteria for biological control of plant diseases. In: Rechcigl NA, Rechcigl JE (eds) Environmentally safe approaches to plant disease control. CRC/Lewis Press, Boca Raton, FL, pp 95–109Google Scholar
  14. Bacon CW, Porter JK, Robbins JD, Luttrell ES (1977) Epichloë typhina from toxic tall fescue grasses. Appl Environ Microb 34:576–581Google Scholar
  15. Balint M, Tiffin P, Hallstrom B, O’Hara RB, Olson MS, Fankhauser JD, Piepenbring M Schmitt I (2013) Host genotype shapes the foliar fungal microbiome of balsam poplar (Populus balsamifera). Plos One 8(1)PubMedPubMedCentralCrossRefGoogle Scholar
  16. Barka EA, Nowak J, Clément C (2006) Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth-promoting rhizobacterium, Burkholderia phytofirmans strain PsJN. Appl Environ Microb 72(11):7246–7252CrossRefGoogle Scholar
  17. Benhamou N, Rey P, Cherif M, Hockenhull J, Tirilly Y (1997) Treatment with the mycoparasite Pythium oligandrum triggers induction of defense-related reactions in tomato roots when challenged with Fusarium oxysporum f. sp. radicis-lycopersici. Phytopathology 87(1):108–122PubMedCrossRefPubMedCentralGoogle Scholar
  18. Bennett C, Aime MC, Newcombe G (2011) Molecular and pathogenic variation within Melampsora on Salix in western North America reveals numerous cryptic species. Mycologia 103:1004–1018PubMedCrossRefPubMedCentralGoogle Scholar
  19. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL (2006) GenBank. Nucleic Acids Res 34:D16–D20PubMedCrossRefPubMedCentralGoogle Scholar
  20. Bills GF, Polyshook JD (1992) Recovery of endophytic fungi from Chmiuecypuris lhyuiiies. Sydowia 44:1–12Google Scholar
  21. Blumenstein K, Albrectsen BR, Martin JA, Hultberg M, Sieber TN, Helander M, Witzell J (2015) Nutritional niche overlap potentiates the use of endophytes in biocontrol of a tree disease. Biocontrol 60(5):655–667CrossRefGoogle Scholar
  22. Brooks DS, Gonzale CF, Appel DN, Filer TH (1994) Evaluation of endophytic bacteria as potential biological-control agents for oak wilt. Biol Control 4(4):373–381CrossRefGoogle Scholar
  23. Budge SP, Whipps JM (2001) Potential for integrated control of Sclerotinia sclerotiorum in glasshouse lettuce using Coniothyrium minitans and reduced fungicide application. Phytopathology 91(2):221–227PubMedCrossRefPubMedCentralGoogle Scholar
  24. Calhoun LA, Findlay JA, Miller JD, Whitney NJ (1992) Metabolites toxic to spruce budworm from balsam fir needle endophytes. Mycol Res 96:281–286CrossRefGoogle Scholar
  25. Campbell R (1989) Biological control of microbial plant pathogens, Cambridge University Press, 218 pp Google Scholar
  26. Canadell JG, Raupach MR (2008) Managing forests for climate change mitigation. Science 320:1456–1457PubMedCrossRefPubMedCentralGoogle Scholar
  27. Cankar K, Kraigher H, Ravnikar M, Rupnik M (2005) Bacterial endophytes from seeds of Norway spruce (Picea abies L. Karst). FEMS Microbiol Lett 244(2):341–345PubMedPubMedCentralCrossRefGoogle Scholar
  28. Cazorla FM, Mercado-Blanco J (2016) Biological control of tree and woody plant diseases: an impossible task? Biocontrol 61(3):233–242CrossRefGoogle Scholar
  29. Chakraborty S, Newton AC (2011) Climate change, plant diseases and food security: an overview. Plant Pathol 60(1):2–14CrossRefGoogle Scholar
  30. Cheng YL, McNally DJ, Labbe C, Voyer N, Belzile F, Belanger RR (2003) Insertional mutagenesis of a fungal biocontrol agent led to discovery of a rare cellobiose lipid with antifungal activity. Appl Environ Microbiol 69(5):2595–2602PubMedPubMedCentralCrossRefGoogle Scholar
  31. Chernin L, Chet I (2002) Microbial enzymes in the biocontrol of plant pathogens and pests. In: Burns RG, Dick RP (eds) Enzymes in the environment: activity, ecology, and applications. Markel Dekker Inc, New York, pp 171–225Google Scholar
  32. Chimwamurombe PM, Grönemeyer JL, Reinhold-Hurek B (2016) Isolation and characterization of culturable seed-associated bacterial endophytes from gnotobiotically grown Marama bean seedlings. FEMS Microbiol Ecol 92(6):p.fiw083PubMedCrossRefPubMedCentralGoogle Scholar
  33. Christian N, Herre EA, Mejía LC, Clay K (2017) Exposure to the leaf litter microbiome of healthy adults protects seedlings from pathogen damage. Proc Roy Soc B Biol Sci 12:284Google Scholar
  34. Clay K, Schardl C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160:S99–S127PubMedPubMedCentralCrossRefGoogle Scholar
  35. Crous PW, Gams W, Stalpers JA, Robert V, Stegehuis G (2004) MycoBank: an online initiative to launch mycology into the 21st century. Stud Mycol 50:19–22Google Scholar
  36. De Beer EJ, Sherwood MB (1945) The Paper-Disc Agar-Plate method for the assay of antibiotic substances. J Bacteriol 50:459–467PubMedPubMedCentralGoogle Scholar
  37. Desprez-Loustau ML, Aguayo J, Dutech C, Hayden KJ, Husson C, Jakushkin B, Marcais B, Piou D, Robin C, Vacher C (2016) An evolutionary ecology perspective to address forest pathology challenges of today and tomorrow Ann For Sci 73(1):45–67Google Scholar
  38. Downing KJ, Leslie G, Thomson JA (2000) Biocontrol of the sugarcane borer Eldana saccharina by expression of the Bacillus thuringiensis cry1Ac7 and Serratia marcescens chiA genes in sugarcane-associated bacteria. Appl Environ Microbiol 66(7):2804–2810PubMedPubMedCentralCrossRefGoogle Scholar
  39. Dowkiw A, Bastien C (2004) Characterization of two major genetic factors controlling quantitative resistance to Melampsora larici-populina leaf rust in hybrid poplars: strain specificity, field expression, combined effects, and relationship with a defeated qualitative resistance gene. Phytopathology 94:1358–1367PubMedCrossRefPubMedCentralGoogle Scholar
  40. Duong LM, Jeewon R, Lumyong S, Hyde KD (2006) DGGE coupled with ribosomal DNA gene phylogenies reveal uncharacterized fungal phylotypes. Fungal Divers 23:121–138Google Scholar
  41. Duplessis S, Major I, Martin F, Séguin A (2009) Poplar and pathogen interactions: insights from populus genome-wide analyses of resistance and defense gene families and gene expression profiling. Crit Rev Plant Sci 28:309–334CrossRefGoogle Scholar
  42. Eaton CJ, Cox MP, Ambrose B, Becker M, Hesse U, Schardl CL, Scott B (2010) Disruption of signaling in a fungal-grass symbiosis leads to pathogenesis. Plant Physiol 153:1780–1794PubMedPubMedCentralCrossRefGoogle Scholar
  43. Eilenberg J, Hajek A, Lomer C (2001) Suggestions for unifying the terminology in biological control. Biocontrol 46(4):387–400CrossRefGoogle Scholar
  44. Elad Y, Kapat A (1999) The role of Trichoderma harzianum protease in the biocontrol of Botrytis cinerea. Eur J Plant Pathol 105(2):177–189CrossRefGoogle Scholar
  45. Eljounaidi K, Lee SK, Bae H (2016) Bacterial endophytes as potential biocontrol agents of vascular wilt diseases—Review and future prospects. Biol Control 103:62–68CrossRefGoogle Scholar
  46. Evans H, Holmes K, Thomas S (2003) Endophytes and mycoparasites associated with an indigenous forest tree, Theobroma gileri, in Ecuador and a preliminary assessment of their potential as biocontrol agents of cocoa diseases. Mycol Prog 2:149–160CrossRefGoogle Scholar
  47. Ezra D, Castillo UF, Strobel GA, Hess WM, Porter H, Jensen JB, Condron MA, Teplow DB, Sears J, Maranta M, Hunter M (2004) Coronamycins, peptide antibiotics produced by a verticillate Streptomyces sp. (MSU-2110) endophytic on Monstera sp. Microbiology 150(4):785–793PubMedCrossRefPubMedCentralGoogle Scholar
  48. Feau N, Vialle A, Allaire M, Tanguay P, Joly DL, Frey P, Callan BE, Hamelin RC (2009) Fungal pathogen (mis-) identifications: a case study with DNA barcodes on Melampsora rusts of aspen and white poplar. Mycol Res 113:713–724PubMedCrossRefPubMedCentralGoogle Scholar
  49. Filonow AB (1998) Role of competition for sugars by yeasts in the biocontrol of gray mold of apple. Biocontrol Sci Techn 8(2):243–256CrossRefGoogle Scholar
  50. Findlay JA, Li G, Miller JD, Womiloju TO (2003) Insect toxins from spruce endophytes. Can J Chem 81:284–292CrossRefGoogle Scholar
  51. Food Agric. Organ. U. N. (FAO) (2009) State of the world’s forests 2009—main report. Rome: FAOGoogle Scholar
  52. Frankowski J, Lorito M, Scala F, Schmid R, Berg G, Bahl H (2001) Purification and properties of two chitinolytic enzymes of Serratia plymuthica HRO-C48. Arch Microbiol 176(6):421–426PubMedCrossRefPubMedCentralGoogle Scholar
  53. Frasz SL, Walker AK, Nsiama TK, Adams GW, Miller JD (2014) Distribution of the foliar fungal endophyte Phialocephala scopiformis and its toxin in the crown of a mature white spruce tree as revealed by chemical and qPCR analyses. Can J For Res 44:1138–1143CrossRefGoogle Scholar
  54. Fravel DR (2005) Commercialization and implementation of biocontrol. Annu Rev Phytopathol 43:337–359PubMedCrossRefPubMedCentralGoogle Scholar
  55. Fröhlich J, Hyde KD, Petrini O (2000) Endophytic fungi associated with palms. Mycol Res 104:1202–1212CrossRefGoogle Scholar
  56. Ganley RJ, Sniezko RA, Newcombe G (2008) Endophyte-mediated resistance against white pine blister rust in Pinus monticola. Forest Ecol Manag 255:2751–2760CrossRefGoogle Scholar
  57. Gazis R, Chaverri P (2010) Diversity of fungal endophytes in leaves and stems of wild rubber trees (Hevea brasiliensis) in Peru. Fungal Ecol 3:240–254CrossRefGoogle Scholar
  58. Gazis R, Chaverri P (2015) Wild trees in the Amazon basin harbor a great diversity of beneficial endosymbiotic fungi: is this evidence of protective mutualism? Fungal Ecol 17:18–29CrossRefGoogle Scholar
  59. Giczey G, Kerenyi Z, Fulop L, Hornok L (2001) Expression of cmg1, an exo-beta-1,3-glucanase gene from Coniothyrium minitans, increases during sclerotial parasitism. Appl Environ Microbiol 67(2):865–871PubMedPubMedCentralCrossRefGoogle Scholar
  60. Glick BR (2015) Beneficial plant-bacterial interactions. Springer. 243 ppCrossRefGoogle Scholar
  61. González-Teuber M (2016) The defensive role of foliar endophytic fungi for a South American tree. AoB Plants 8:plw050PubMedPubMedCentralCrossRefGoogle Scholar
  62. Gromovykh TI, Tyulpanova VA, Sadykova VS, Malinovsky AL (2007) Control of root diseases with Trichoderma spp. in forest nurseries of Central Siberia. In: Vincent C, Goettel MS, Lazarovits G (eds) Biological control: a global perspective: case studies from around the world. CAB International, Trowbridge, pp 197–202CrossRefGoogle Scholar
  63. Grünig CR, Duò A, Sieber TN (2006) Population genetic analysis of Phialocephala fortinii s.l. and Acephala applanata in two undisturbed forests in Switzerland and evidence for new cryptic species. Fungal Genet Biol 43:410–421PubMedCrossRefPubMedCentralGoogle Scholar
  64. 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 100:47–67PubMedPubMedCentralCrossRefGoogle Scholar
  65. Grünwald NJ, Garbelotto M, Goss EM, Heungens K, Prospero S (2012) Emergence of the sudden oak death pathogen Phytophthora ramorum. Trends Microbiol 20(3):131–138PubMedCrossRefPubMedCentralGoogle Scholar
  66. Guo LD, Hyde KD, Liew EC (2001) Detection and taxonomic placement of endophytic fungi within frond tissues of Livistona chinensis based on rDNA sequences. Mol Phylogenet Evol 20:1–13PubMedCrossRefPubMedCentralGoogle Scholar
  67. Guttman DS, McHardy AC, Schulze-Lefert P (2014) Microbial genome-enabled insights into plant–microorganism interactions. Nat Rev Genet 15(12):797–813PubMedPubMedCentralCrossRefGoogle Scholar
  68. Hamilton C, 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
  69. Hanada RE, Pomella AW, Costa HS, Bezerra JL, Loguercio LL, Pereira JO (2010) Endophytic fungal diversity in Theobroma cacao (cacao) and T. grandiflorum (cupuaçu) trees and their potential for growth promotion and biocontrol of black-pod disease. Fungal Biolo 114:901–910CrossRefGoogle Scholar
  70. Hardoim PR, van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Doring M, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79(3):293–320PubMedPubMedCentralCrossRefGoogle Scholar
  71. Hardwood TD, Tomlinson I, Potter CA, Knight JD (2011) Dutch elm disease revisited: past, present and future management in Great Britain. Plant Pathol 60(3):545–555CrossRefGoogle Scholar
  72. Hartley MJ (2002) Rationale and methods for conserving biodiversity in plantation forests. Forest Ecol Manag 155(1–3):81–95CrossRefGoogle Scholar
  73. Hibbett DS, Taylor JW (2013) Fungal systematics: is a new age of enlightenment at hand? Nat Rev Microbiol 11:129–133PubMedCrossRefPubMedCentralGoogle Scholar
  74. Holmes KA, Schroers H-J, Thomas SE, Evans HC, Samuels GJ (2004) Taxonomy and biocontrol potential of a new species of Trichoderma from the Amazon basin of South America. Mycol Prog 3(199):e210Google Scholar
  75. Howell CR (2003) Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Dis 87(1):4–10CrossRefGoogle Scholar
  76. Hyde K, Soytong K (2007) Understanding microfungal diversity—a critique. Cryptogamie Mycol 28:281–289Google Scholar
  77. Hyde K, Soytong K (2008) The fungal endophyte dilemma. Fungal Divers 33:163–173Google Scholar
  78. Izumi H (2011) Diversity of endophytic bacteria in forest trees. In: Pirttilä A, Frank A (eds) Endophytes of forest trees. Forestry sciences, vol 80, Springer, Dordrecht, pp 95–105CrossRefGoogle Scholar
  79. Jumpponen A (2001) Dark septate endophytes—are they mycorrhizal? Mycorrhiza 11:207–211CrossRefGoogle Scholar
  80. Jungqvist G, Oni SK, Teutschbein C, Futter MN (2014) Effect of climate change on soil temperature in Swedish boreal forests. PLoS ONE 9(4):e93957PubMedPubMedCentralCrossRefGoogle Scholar
  81. Kapat A, Zimand G, Elad Y (1998) Effect of two isolates of Trichoderma harzianum on the activity of hydrolytic enzymes produced by Botrytis cinerea. Physiol Mol Plant Pathol 52(2):127–137CrossRefGoogle Scholar
  82. Kloepper JW, Leong J, Teintze M, Schroth MN (1980) Pseudomonas Siderophores—a mechanism explaining disease-suppressive soils. Curr Microbiol 4(5):317–320CrossRefGoogle Scholar
  83. Kobayashi DY, Palumbo JD (2000) Bacterial endophytes and their effects on plants and uses in agriculture. In: Bacon CW, White JF Jr (eds) Microbial endophytes. Marcel Dekker Inc, New York, pp 199–233Google Scholar
  84. Kovalchuk A, Keriö S, Oghenekaro AO, Jaber E, Raffaello T, Asiegbu FO (2013) Antimicrobial defenses and resistance in forest trees: challenges and perspectives in a genomic era. Annu Rev Phytopathol 51:221–244PubMedCrossRefPubMedCentralGoogle Scholar
  85. La Porta N, Capretti P, Thomsen IM, Kasanen R, Hietala AM, Von Weissenberg K (2008) Forest pathogens with higher damage potential due to climate change in Europe. Can J Plant Pathol 30:177–195CrossRefGoogle Scholar
  86. Lee S, Flores-Encarnacion M, Contreras-Zentella M, Garcia-Flores L, Escamilla JE, Kennedy C (2004) Indole-3-acetic acid biosynthesis is deficient in Gluconacetobacter diazotrophicus strains with mutations in cytochrome c biogenesis genes. J Bacteriol 186(16):5384–5391PubMedPubMedCentralCrossRefGoogle Scholar
  87. Lilja A, Poteri M, Petäistö R-L, Rikala R, Kurkela T, Kasanen R (2010) Fungal diseases in forest nurseries in Finland. Silva Fenn 44:525–545CrossRefGoogle Scholar
  88. Lodewyckx C, Vangronsveld J, Porteous F, Moore ER, Taghavi S, Mezgeay M, van der Lelie DV (2002) Endophytic bacteria and their potential applications. CRC Crit Rev Plant Sci 21:583–606CrossRefGoogle Scholar
  89. López-Escudero FJ, Mercado-Blanco J (2011) Verticillium wilt of olive: a case study to implement an integrated strategy to control a soil-borne pathogen. Plant Soil 344(1–2):1–50CrossRefGoogle Scholar
  90. Long HH, Sonntag DG, Schmidt DD, Baldwin IT (2010) The structure of the culturable root bacterial endophyte community of Nicotiana attenuata is organized by soil composition and host plant ethylene production and perception. New Phytol 185:554–567PubMedCrossRefPubMedCentralGoogle Scholar
  91. Lorito M, Woo SL, DAmbrosio M, Harman GE, Hayes CK, Kubicek CP, Scala F (1996) Synergistic interaction between cell wall degrading enzymes and membrane affecting compounds. Mol Plant Microbe Interact 9(3):206–213CrossRefGoogle Scholar
  92. Luginbuhl M, Muller E (1980) Endophytische Pilze in den oberirdischen Organen von 4 gemeinsam an gleichen Standorten wachsenden Pflanzen (Buxus, Hedera, Ilex, Ruscus). Sydowia 33:185–209Google Scholar
  93. Madsen AM, de Neergaard E (1999) Interactions between the mycoparasite Pythium oligandrum and sclerotia of the plant pathogen Sclerotinia sclerotiorum. Eur J For Pathol 105(8):761–768CrossRefGoogle Scholar
  94. Mandyam K, Jumpponen A (2005) Abundance and possible functions of the root-colonising dark septate endophytic fungi. Stud Mycol 53:173–190CrossRefGoogle Scholar
  95. Martín JA, Macaya-Sanz D, Witzell J, Blumenstein K, Gil L (2015) Strong in vitro antagonism by elm xylem endophytes is not accompanied by temporally stable in planta protection against a vascular pathogen under field conditions. Eur J For Pathol 142(1):185–196CrossRefGoogle Scholar
  96. Martin F, Nehls U (2009) Harnessing ectomycorrhizal genomics for ecological insights. Curr Opin Plant Biol 12(4):508–515PubMedCrossRefPubMedCentralGoogle Scholar
  97. Martín JA, Witzell J, Blumenstein K, Rozpedowska E, Helander M, Sieber TN, Gil L (2013) Resistance to Dutch Elm Disease Reduces Presence of Xylem Endophytic Fungi in Elms (Ulmus spp.). PLoS ONE 8(2):e56987PubMedPubMedCentralCrossRefGoogle Scholar
  98. McMullin DR, Green BD, Miller JD (2015) Antifungal sesquiterpenoids and macrolides from an endophytic Lophodermium species of Pinus strobus. Phytochem Lett 14:148–152CrossRefGoogle Scholar
  99. Mejía LC, Herre EA, Sparks JP, Winter K, Garcia MN, Van Bael SA, Stitt J, Shi Z, Zhang Y, Guiltinan MJ, Maximova SN (2014) Pervasive effects of a dominant foliar endophytic fungus on host genetic and phenotypic expression in a tropical tree. Front Microbiol 5:479PubMedPubMedCentralGoogle Scholar
  100. 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
  101. Melnick RL, Zidack NK, Bailey BA, Maximova SN, Guiltinan M, Backman PA (2008) Bacterial endophytes: Bacillus spp. from annual crops as potential biological control agents of black pod rot of cacao. Biol Control 46(1):46–56CrossRefGoogle Scholar
  102. Melnick RL, Suárez C, Bailey BA, Backman PA (2011) Isolation of endophytic endospore-forming bacteria from Theobroma cacao as potential biological control agents of cacao diseases. Biol Control 57(3):236–245CrossRefGoogle Scholar
  103. 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 108:965–973PubMedPubMedCentralCrossRefGoogle Scholar
  104. Mercado-Blanco J, Lugtenberg BJJ (2014) Biotechnological applications of bacterial endophytes. Curr Biotechnol 3(1):60–75CrossRefGoogle Scholar
  105. Milgroom MG, Cortesi P (2004) Biological control of chestnut blight with hypovirulence: a critical analysis. Annu Rev Phytopathol 42:311–338PubMedCrossRefPubMedCentralGoogle Scholar
  106. Miller JD, Mackenzie S, Foto M, Adams GW, Findlay JA (2002) Needles of white spruce inoculated with rugulosin-producing endophytes contain rugulosin reducing spruce budworm growth rate. Mycol Res 106:471–479CrossRefGoogle Scholar
  107. Miller JD, Sumarah MW, Adams GW (2008) Effect of a rugulosin-producing endophyte in Picea glauca on Choristoneura fumiferana. J Chem Ecol 34:362–368PubMedPubMedCentralCrossRefGoogle Scholar
  108. Misaghi IJ, Donndelinger CR (1990) Endophytic bacteria in symptom-free cotton plants. Phytopathology 80(9):808–811CrossRefGoogle Scholar
  109. Moore FP, Barac T, Borremans B, Oeyen L, Vanqronsveld J, van der Lelie D, Campbell CD, Moore ER (2006) Endophytic bacterial diversity in poplar trees growing on a BTEX-contaminated site: the characterisation of isolates with potential to enhance phytoremediation. Syst Appl Microbiol 29:539–556PubMedPubMedCentralCrossRefGoogle Scholar
  110. Narayanasamy P (2013) Biological management of diseases of crops. Springer, Dordrecht, p 673CrossRefGoogle Scholar
  111. Navarro-Meléndez AL, Heil M (2014) Symptomless endophytic fungi suppress endogenous levels of salicylic acid and interact with the jasmonate-dependent indirect defense traits of their host, lima bean (Phaseolus lunatus). J Chem Ecol 40:816–825PubMedCrossRefPubMedCentralGoogle Scholar
  112. Newman LA, Reynolds CM (2005) Bacteria and phytoremediation: new uses for endophytic bacteria in plants. Trends Biotechnol 23(1):6–8PubMedCrossRefPubMedCentralGoogle Scholar
  113. Newsham KK (2011) A meta-analysis of plant responses to dark septate root endophytes. New Phytol 190:783–793PubMedPubMedCentralCrossRefGoogle Scholar
  114. Newton AC, Gravouil C, Fountaine JM (2010) Managing the ecology of foliar pathogens: ecological tolerance in crops. Ann Appl Biol 157(3):343–359CrossRefGoogle Scholar
  115. Nilsson RH, Ryberg M, Abarenkov K, Sjökvist E, Kristiansson E (2009) The ITS region as a target for characterization of fungal communities using emerging sequencing technologies. FEMS Microbiol Lett 296(1):97–101PubMedCrossRefPubMedCentralGoogle Scholar
  116. Nilsson RH, Ryberg M, Kristiansson E, Abarenkov K, Larsson K-H, Kõljalg U (2006) Taxonomic reliability of DNA sequences in public sequence databases: a fungal perspective. PLoS ONE 1(1):e59PubMedPubMedCentralCrossRefGoogle Scholar
  117. Ovaskainen O, Nokso-Koivista J, Hottola J, Rajala T, Pennanen T, Ali-Kovero H, Miettinen O, Oinonen P, Auvinen P, Paulin L, Larsson K-H, Mäkipää R (2010) Identifying wood-inhabiting fungi with 454 sequencing—what is the probability that BLAST gives the correct species? Fungal Ecol 3:274–283CrossRefGoogle Scholar
  118. Panaccione DG, Beaulieu WT, Cook D (2013) Bioactive alkaloids in vertically transmitted fungal endophytes. Funct Ecol 28(2):299–314CrossRefGoogle Scholar
  119. Parent JL, James TY, Vasaitis R, Taylor AF (2009) Friend or foe? Evolutionary history of glycoside hydrolase family 32 genes encoding for sucrolytic activity in fungi and its implications for plant-fungal symbioses. BMC Evol Biol 9:148CrossRefGoogle Scholar
  120. Patosaari P (2007) Forests and climate change: mitigation and adaptation through sustainable forest management. DPI/NGO conference: climate change 5–7 September 2007, United Nations, New York, USAGoogle Scholar
  121. Paulitz TC, Belanger RR (2001) Biological control in greenhouse systems. Annu Rev Phytopathol 39:103–133PubMedCrossRefPubMedCentralGoogle Scholar
  122. Pautasso M, Schlegel M, Holdenrieder O (2015) Forest health in a changing world. Microb Ecol 69(4):826–842PubMedPubMedCentralCrossRefGoogle Scholar
  123. Petrini O, Dreyfuss M (1981) Endophytische Pilze in epiphytischen Araceae, Bromeliaceae und Orchidaceae. Sydowia 34:135–145Google Scholar
  124. Petrini O, Sieber TN, Toti L, Viret O (1992) Ecology, metabolite production, and substrate utilization in endophytic fungi. Nat Toxins 1:185–196PubMedCrossRefPubMedCentralGoogle Scholar
  125. Pillay VK, Nowak J (1997) Inoculum density, temperature, and genotype effects on in vitro growth promotion and epiphytic and endophytic colonization of tomato (Lycopersicon esculentum L.) seedlings inoculated with a pseudomonad bacterium. Can J Microbiol 43(4):354–361CrossRefGoogle Scholar
  126. Ponkä A, Andersson Y, Siitonen A, de Jong B, Jahkola M, Haikala O, Kuhmonen A, Pakkala P (1995) Salmonella in alfalfa sprouts. The Lancet 345(8947):462–463CrossRefGoogle Scholar
  127. Porras-Alfaro A, Bayman P (2011) Hidden fungi, emergent properties: endophytes and microbiomes. Annu Rev Phytopathol 49:291–315PubMedPubMedCentralCrossRefGoogle Scholar
  128. Postma J, Goossen-van de Geijn H (2016) Twenty-four years of Dutch Trig (R) application to control Dutch elm disease. Biocontrol 61(3):305–312CrossRefGoogle Scholar
  129. Poudel R, Jumpponen A, Schlatter DC, Paulitz TC, Gardener BB, Kinkel LL, Garrett KA (2016) Microbiome networks: a systems framework for identifying candidate microbial assemblages for disease management. Phytopathology 106(10):1083–1096PubMedPubMedCentralCrossRefGoogle Scholar
  130. Pratt JE, Niemi M, Sierota ZH (2000) Comparison of three products based on Phlebiopsis gigantea for the control of Heterobasidion annosum in Europe. Biocontrol Sci Technol 10(4):467–477CrossRefGoogle Scholar
  131. Preszler RW, Gaylord ES, Boecklen WJ (1996) Reduced parasitism of a leaf-mining moth on trees with high infection frequencies of an endophytic fungus. Oecologia 108:159–166PubMedCrossRefPubMedCentralGoogle Scholar
  132. Prieto P, Schilirò E, Maldonado-González MM, Valderrama R, Barroso-Albarracín JB, Mercado-Blanco J (2011) Root hairs play a key role in the endophytic colonization of olive roots by Pseudomonas spp. with biocontrol activity. Microb Ecol 62:435–445PubMedPubMedCentralCrossRefGoogle Scholar
  133. Puente ME, Li CY, Bashan Y (2009) Endophytic bacteria in cacti seeds can improve the development of cactus seedlings. Environ Exp Bot 66(3):402–408CrossRefGoogle Scholar
  134. Punja ZK, Utkhede RS (2003) Using fungi and yeasts to manage vegetable crop diseases. Trends Biotechnol 21(9):400–407PubMedCrossRefPubMedCentralGoogle Scholar
  135. Queloz V, Duo A, Grûnig CR (2008) Isolation and characterization of microsatellite markers for the tree-root endophytes Phialocephala subalpina and Phialocephala fortinii s.s. Mol Ecol Resour 8:1322–1325PubMedCrossRefPubMedCentralGoogle Scholar
  136. Queloz V, Duo A, Sieber TN, Grûnig CR (2010) Microsatellite size homoplasies and null alleles do not affect species diagnosis and population genetic analysis in a fungal species complex. Mol Ecol Resour 10:348–367PubMedCrossRefPubMedCentralGoogle Scholar
  137. Raghavendra AKH, Newcombe G (2013) The contribution of foliar endophytes to quantitative resistance to Melampsora rust. New Phytol 197:909–918PubMedCrossRefPubMedCentralGoogle Scholar
  138. Rashid S, Charles TC, Glick BR (2012) Isolation and characterization of new plant growth-promoting bacterial endophytes. Appl Soil Ecol 61:217–224CrossRefGoogle Scholar
  139. Ravensberg WJ (2015) Commercialisation of microbes: present situation and future prospects. In: Lugtenberg B (ed) Principles of Plant-Microbe Interactions. Springer, Cham, pp 309–317Google Scholar
  140. Ren JH, Li H, Wang YF, Ye JR, Yan AQ, Wu XQ (2013) Biocontrol potential of an endophytic Bacillus pumilus JK-SX001 against poplar canker. Biol Control 67(3):421–430CrossRefGoogle Scholar
  141. Richardson SN, Walker AK, Nsiama TK, McFarlane J, Sumarah MW, Ibrahim A, Miller JD (2014) Griseofulvin-producing Xylaria endophytes of Pinus strobus and Vaccinium angustifolium: evidence for a conifer-understory species endophyte ecology. Fungal Ecol 11:107–113CrossRefGoogle Scholar
  142. Richardson SN, Nsiama TK, Walker AK, McMullin DR, Miller JD (2015) Antimicrobial dihydrobenzofurans and xanthenes from a foliar endophyte of Pinus strobus. Phytochemistry 117:436–443PubMedCrossRefPubMedCentralGoogle Scholar
  143. Ridout M, Newcombe G (2015) The frequency of modification of Dothistroma pine needle blight severity by fungi withion the native range. Fort Ecol Manage 337:153–160CrossRefGoogle Scholar
  144. Robert-Seilaniantz A, Grant M, Jones JD (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 49:317–343PubMedCrossRefPubMedCentralGoogle Scholar
  145. Roderick GK, Navajas M (2003) Genes in new environments: Genetics and evolution in biological control. Nat Rev Genet 4(11):889–899PubMedCrossRefPubMedCentralGoogle Scholar
  146. Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim Y, Redman RS (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2:404–416PubMedCrossRefPubMedCentralGoogle Scholar
  147. Rodriguez RJ, White JF Jr, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330PubMedPubMedCentralCrossRefGoogle Scholar
  148. Rosenblueth M, Martínez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant Microbe Interact 19(8):827–837PubMedCrossRefPubMedCentralGoogle Scholar
  149. Rotem Y, Yarden O, Sztejnberg A (1999) The mycoparasite Ampelomyces quisqualis expresses exgA encoding an exo-beta-1,3-glucanase in culture and during mycoparasitism. Phytopathology 89(8):631–638PubMedCrossRefPubMedCentralGoogle Scholar
  150. Rubini MR, Silva-Ribeiro RT, Pomella AWV, Maki CS, Arau’ jo WL, Santos DR, Azevedo JL (2005) Diversity of endophytic fungal community of cacao (Theobroma cacao L.) and biological control of Crinipellis perniciosa, causal agent of witches’ broom disease. Int J Biol Sci 1:24e33Google Scholar
  151. Ruocco M, Woo S, Vinale F, Lanzuise S, Lorito M (2011) Identified difficulties and conditions for field success of biocontrol. 2. Technical aspects: factors of efficacy. In: Nicot PC (eds) International classical and augmentative biological control against diseases and pests: critical status analysis and review of factors influencing their success. Organization for biological and integrated control of noxious animals and plants, West palaearctic regional section (IOBC/WPRS), pp 45–57Google Scholar
  152. Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278(1):1–9PubMedCrossRefPubMedCentralGoogle Scholar
  153. Ryberg M, Kristansson E, Sjökvist E, Nilsson RH (2009) An outlook on the fungal internal transcribed spacer sequences in GenBank and the introduction of a web-based tool for the exploration of fungal diversity. New Phytol 181:471–477PubMedCrossRefPubMedCentralGoogle Scholar
  154. 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
  155. Saikkonen K, Gundel PE, Helander M (2013) Chemical ecology mediated by fungal endophytes in grasses. J Chem Ecol 39:962–968PubMedCrossRefPubMedCentralGoogle Scholar
  156. Saikkonen K, Wäli P, Helander M, Faeth SH (2004) Evolution of endophyte-plant symbioses. Trends Plant Sci 9:275–280PubMedPubMedCentralCrossRefGoogle Scholar
  157. Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 55:315–340PubMedPubMedCentralCrossRefGoogle Scholar
  158. Schirmbock M, Lorito M, Wang YL, Hayes CK, Arisanatac I, Scala F, Harman GE, Kubicek CP (1994) Parallel formation and synergism of hydrolytic enzymes and peptaibol antibiotics, molecular mechanisms involved in the antagonistic action of Trichoderma-Harzianum against phytopathogenic fungi. App Environ Microbiol 60(12):4364–4370Google Scholar
  159. Schlaeppi K, Bulgarelli D (2015) The plant microbiome at work. Mol Plant-Microbe Interact 28(3):212–217PubMedCrossRefPubMedCentralGoogle Scholar
  160. Schmid J, Day R, Zhang N, Dupont P-Y, Cox MP, Schardl CL, Minards N, Truglio M, Moore N, Harris DR, Zhou Y (2017) Host tissue environment directs activities of an Epichloë endophyte, while it induces systemic hormone and defense responses in its native perennial ryegrass host. Mol Plant-Microbe Interact 30(2):138–149PubMedCrossRefPubMedCentralGoogle Scholar
  161. Schulz BJE, Boyle CJC (2005) The endophytic continuum. Mycol Res 109:661–686PubMedPubMedCentralCrossRefGoogle Scholar
  162. Schulz BJE, Boyle CJC, Draeger S, Römmrt AK, Krohn K (2002) Endophytic fungi: a source of novel biologically active secondary metabolites. Mycol Res 106:996–1004CrossRefGoogle Scholar
  163. Schulz BJE, Guske S, Dammann U, Boyle C (1998) Endophyte-host interactions II. Defining symbiosis of the endophyte-host interaction. Symbiosis 25:213–227Google Scholar
  164. Schulz BJE, Haas S, Junker C, Andree N, Schobert M (2015) Fungal endophytes are involved in multiple balanced antagonisms. Curr Sci 109:39–45Google Scholar
  165. Schulz BJE, Römmert A-K, Dammann U, Aust H-J, Strack D (1999) The endophyte-host interaction: a balanced antagonism. Mycol Res 103:1275–1283CrossRefGoogle Scholar
  166. Schulz BJE, Sucker J, Aust HJ, Krohn K, Ludewig K, Jones PG, Döring D (1995) Biologically active secondary metabolites of endophytic Pezicula species. Mycol Res 99:1007–1015CrossRefGoogle Scholar
  167. Schulz BJE, Wanke U, Draeger S, Aust H-J (1993) Endophytes from herbaceous plants and shrubs: effectiveness of surface sterilization methods. Mycol Res 97(12):1447–1450CrossRefGoogle Scholar
  168. Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43PubMedCrossRefPubMedCentralGoogle Scholar
  169. Sieber TN (2007) Endophytic fungi of forest trees: are they mutualists? Fungal Biol Rev 21:75–89CrossRefGoogle Scholar
  170. Sieber TN, Grünig CR (2013) Fungal root endophytes. In: Eshel A, Beeckman T (eds) Plant roots—the hidden half, 4th edn. FL, USA, CRC Press, Taylor and Francis Group, Boca Raton, pp 38–49Google Scholar
  171. Sieber TN, Rys J, Holdenrieder O (1999) Mycobiota in symptomless needles of Pinus mugo ssp. Uncinata Mycol Res 103:306–310CrossRefGoogle Scholar
  172. Siegel MR, Bush LP (1996) Defensive chemicals in grass–fungal endophyte associations. Rec Adv Phytochem 30:81–118Google Scholar
  173. Siegel MR, Latch GCM, Bush LP, Fannin FF, Rowan DD, Tapper BA, Bacon CW, Johnson MC (1990) Fungal endophyte infected grasses: alkaloid accumulation and aphid response. J Chem Ecol 16:3301–3314PubMedCrossRefPubMedCentralGoogle Scholar
  174. Solis MJL, dela Cruz TE TE, Schnittler M, Unterseher M (2016) The diverse community of leafinhabiting fungal endophytes from Philippine natural forests reflects phylogenetic patterns of their host plant species Ficus benjamina. F elastica and F religiosa. Mycoscience 57(2):96–106CrossRefGoogle Scholar
  175. Stadler M (2011) Importance of secondary metabolites in the Xylariaceae as parameters for assessment of their taxonomy, phylogeny, and functional biodiversity. Curr Res Environ Appl Mycol 1:75–133CrossRefGoogle Scholar
  176. Stadler M, Hellwig V (2005) Chemotaxonomy of the Xylariaceae and remarkable bioactive compounds from Xylariales and their associated asexual stages. Recent Res Dev Phytochem 9:41–93Google Scholar
  177. Steenackers J, Steenackers M, Steenackers V, Stevens M (1996) Poplar diseases, consequences on growth and wood quality. Biomass Bioenergy 10:267–274CrossRefGoogle Scholar
  178. Stone JK, Polishook JD, White JRJ (2004) Endophytic fungi. In: Mueller G, Bills GF, Foster MS (eds) Biodiversity of fungi: inventory and monitoring methods. Elsevier, Burlington, pp 241–270CrossRefGoogle Scholar
  179. Strobel GA (2003) Endophytes as sources of bioactive products. Microbes Infect 5:535–544PubMedCrossRefPubMedCentralGoogle Scholar
  180. Sturz AV, Christie BR, Matheson BG (1998) Associations of bacterial endophyte populations from red clover and potato crops with potential for beneficial allelopathy. Can J Microbiol 44:162–167CrossRefGoogle Scholar
  181. Sturz AV, Christie BR, Matheson BG, Nowak J (1997) Biodiversity of endophytic bacteria which colonize red clover nodules, roots, stems and foliage and their influence on host growth. Biol Fertil Soils 25(1):13–19CrossRefGoogle Scholar
  182. Sumarah MW, Walker AK, Seifert KA, Todorov A, Miller JD (2015) Screening of fungal endophytes isolated from eastern white pine needles. Recent Adv Phytochem 45:195–206Google Scholar
  183. Sumarah MW, Puniani E, Blackwell BA, Miller JD (2008a) Characterization of polyketide metabolites from foliar endophytes of Picea glauca. J Nat Prod 71:1393–1398PubMedCrossRefPubMedCentralGoogle Scholar
  184. Sumarah MW, Adams GW, Bergout J, Slack GJ, Wilson AM, Miller JD (2008b) Spread and persistence of a rugulosin-producing endophyte in white spruce seedlings. Mycol Res 112:731–736PubMedCrossRefPubMedCentralGoogle Scholar
  185. Sumarah MW, Puniani E, Sørensen D, Blackwell BA, Miller JD (2010) Secondary metabolites from anti-insect extracts of endophytic fungi isolated from Picea rubens. Phytochemistry 71:760–765PubMedCrossRefPubMedCentralGoogle Scholar
  186. Sumarah MW, Kesting JR, Sørensen D, Miller JD (2011) Antifungal metabolites from fungal endophytes of Pinus strobus. Phytochemistry 72:14–15CrossRefGoogle Scholar
  187. Sun H, Korhonen K, Hantula J, Asiegbu FO, Kasanen R (2009) Use of a breeding approach for improving biocontrol efficacy of Phlebiopsis gigantea strains against Heterobasidion infection of Norway spruce stumps. FEMS Microbiol Ecol 69(2):266–273PubMedCrossRefPubMedCentralGoogle Scholar
  188. Sun H, Terhonen E, Koskinen K, Paulin L, Kasanen R, Asiegbu FO (2013) The impacts of treatment with biocontrol fungus (Phlebiopsis gigantea) on bacterial diversity in Norway spruce stumps. Biol Control 64(3):238–246CrossRefGoogle Scholar
  189. Surette MA, Sturz AV, Lada RR, Nowak J (2003) Bacterial endophytes in processing carrots (Daucus carota L. var. sativus): their localization, population density, biodiversity and their effects on plant growth. Plant Soil 253:381–390CrossRefGoogle Scholar
  190. Swinton J, Gilligan CA (1999) Selecting hyperparasites for biocontrol of Dutch elm disease. Proc R Soc Lond B Biol Sci 266(1418):437–445CrossRefGoogle Scholar
  191. Taghavi S, Barac T, Greenberg B, Borremans B, Vangronsveld J, van der Lelie D (2005) Horizontal gene transfer to endogenous endophytic bacteria from poplar improves phytoremediation of toluene. App Environ Microbiol 71(12):8500–8505CrossRefGoogle Scholar
  192. Tan RX, Zou WX (2001) Endophytes: a rich source of functional metabolites. Nat Prod Rep 18:448–459PubMedCrossRefPubMedCentralGoogle Scholar
  193. Tanney JB, McMullin DR, Green BD, Miller JD, Seifert KA (2016) Production of antifungal and antiinsectan metabolites by the Picea endophyte Diaporthe maritima sp. nov. Fungal Biol. 120:1448–1457PubMedCrossRefPubMedCentralGoogle Scholar
  194. Tao G, Liu ZY, Hyde KD, Lui XZ, Yu ZN (2008) Whole rDNA analysis reveals novel and endophytic fungi in Bletilla ochracea (Orchidaceae). Fungal Divers 33(1):101–112Google Scholar
  195. Tellenbach C, Sieber TN (2012) Do colonization by dark septate endophytes and elevated temperature affect pathogenicity of oomycetes? FEMS Microbiol Ecol 82:157–168PubMedCrossRefPubMedCentralGoogle Scholar
  196. Tellenbach C, Sumarah MW, Grünig CR, Miller DJ (2012) Inhibition of Phytophthora species by secondary metabolites produced by the dark septate endophyte Phialocephala europaea. Fungal Ecol 6:12–18CrossRefGoogle Scholar
  197. Terhonen E (2008) Juurten endofyyttisienten vaikutus hybridihaavan versojen juurtumiseen in vitro. (DS-endophytes in roots of hybrid aspen and their effects on hybrid aspen shoots in vitro.) M.Sc. thesis, University of Helsinki, Department of Applied Biology (In Finnish)Google Scholar
  198. 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
  199. Terhonen E, Sipari S, Asiegbu FO (2016) Inhibition of phytopathogens by fungal root endophytes of Norway spruce. Biol Control 99:53–63CrossRefGoogle Scholar
  200. Terhonen E, Sun S, Buee M, Kasanen R, Paulin L, Asiegbu FO (2013) Effects of the use of biocontrol agent (Phlebiopsis gigantea) on fungal communities on the surface of Picea abies stumps. Forest Ecol Manage 310:428–433CrossRefGoogle Scholar
  201. Tjamos EC, Tjamos SE, Antoniou PP (2010) Biological management of plant diseases: highlights on research and application. J Plant Pathol 92(4):S17–S21Google Scholar
  202. Tondje PR, Roberts DP, Bon MC, Widmer T, Samuels GJ, Ismaiel A, Begoude AD, Tchana T, Nyemb-Tshomb E, Ndoumbe-Nkeng M, Bateman R, Fontem D, Hebbar KP (2007) Isolation and identification of mycoparasitic isolates of Trichoderma asperellum with potential for suppression of black pod disease of cacao in Cameroon. Biol Control 43:202–212CrossRefGoogle Scholar
  203. Ulrich K, Ulrich A, Ewald D (2008) Diversity of endophytic bacterial communities in poplar grown under field conditions. FEMS Microbiol Ecol 63(2):169–180PubMedPubMedCentralCrossRefGoogle Scholar
  204. Unterseher M, Schnittler M (2009) Dilution-to-extinction cultivation of leaf-inhabiting endophytic fungi in beech (Fagus sylvatica L.)—Different cultivation techniques influence fungal biodiversity assessment. Mycol Res 113:645–654PubMedCrossRefPubMedCentralGoogle Scholar
  205. van der Heijden MG, Hartmann M (2016) Networking in the plant microbiome. PLoS Biol 14(2):e1002378PubMedPubMedCentralCrossRefGoogle Scholar
  206. van Lenteren JC, Bolckmans K, Köhl J, Ravensberg WJ, Urbaneja A (2017) Biological control using invertebrates and microorganims: plenty of new opportunities. BioControl:1–21Google Scholar
  207. Van Driesche RG, Bellows TS (1996) Biological control. Kluwer Academic Publishers, Dordrecht, p 539CrossRefGoogle Scholar
  208. Verma SC, Singh A, Chowdhury SP, Tripathi AK (2004) Endophytic colonization ability of two deep-water rice endophytes, Pantoea sp. and Ochrobactrum sp. using green fluorescent protein reporter. Biotechnol Lett 26(5):425–429PubMedCrossRefPubMedCentralGoogle Scholar
  209. Vincent JG, Vincent HW (1944) Filter paper disc modification of the oxford cup penicillin determination. Proc Soc Exp Biol Med 55:162–164CrossRefGoogle Scholar
  210. Wagner RG, Flynn J, Gregory R, Mertz CK, Slovic P (1998) Acceptable practices in Ontario’s forests: Differences between the public and forestry professionals. New For 16(2):139–154CrossRefGoogle Scholar
  211. Wang J, Jia H (2016) Metagenome-wide association studies: fine-mining the microbiome. Nat Rev Microbiol 14(8):508–522PubMedCrossRefPubMedCentralGoogle Scholar
  212. Zhao JH, Zhang YL, Wang LW, Wang JY, Zhang CL (2012) Bioactive secondary metabolites from Nigrospora sp. LLGLM003, an endophytic fungus of the medicinal plant Moringa oleifera Lam. World J Microbiol Biotechnol 28:2107–2112PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Eeva Terhonen
    • 1
    • 2
  • Andriy Kovalchuk
    • 1
  • Artin Zarsav
    • 1
  • Fred O. Asiegbu
    • 1
  1. 1.Department of Forest SciencesUniversity of HelsinkiHelsinkiFinland
  2. 2.Georg-August-Universität GöttingenGöttingenGermany

Personalised recommendations