Chemical Warfare in the Plant Microbiome Leads to a Balance of Antagonisms and a Healthy Plant

  • Barbara Joan SchulzEmail author
  • Laura Rabsch
  • Corina Junker


Most plants are healthy, in part due to metabolic interactions between the holobiont’s host and its microbiome, usually involving secondary metabolites. On the one hand, the host welcomes some boarders, e.g., those involved in mutualistic interactions. On the other hand, host defense prevents the microorganisms from gaining control. Consequently, the microorganisms react and have evolved mechanisms to deal with host defense, e.g., by downregulating it or by synthesizing antagonistic metabolites. The microorganisms must also deal with competition between other members of the microbiome for territory and assimilates. Examples of the secondary metabolites involved in these interactions are presented, including phytohormones, signaling molecules, phytotoxic metabolites, and antimicrobial metabolites directed toward coinhabitants of the microbiome. In the healthy plant, there are multiple equilibriums between the antagonisms of the plant residents and also between inhabitants and their host. The sum of these interactions is a healthy plant with balanced associations between all members of the holobiont. Nevertheless, multiple abiotic and biotic factors can disturb this balance, including virulence of an alien pathogen, e.g., Hymenoscyphus fraxineus, the causal agent of ash dieback in Fraxinus excelsior. Strategies are presented in which fungal endophytes could be used to combat ash dieback.


Hymenoscyphus fraxineus Secondary metabolites Microbial interactions Plant holobiont Plant microbiome Endophytes Fungi Co-culture 



We would like to thank Drs. Simone Bergmann, Sophie de Vries, and Christine Boyle for critical comments and excellent suggestions for improving the manuscript and Nicole Andrée and Patrick Bork for the permission to use photos and results from their dual culture experiments and express our gratitude to Dr. Frank Surup for drawing the structures in Figs. 9.1 and 9.2.


  1. Adame-Álvarez R-M, Mendiola-Soto J, Heil M (2014) Order of arrival shifts endophyte-pathogen interactions in bean from resistance induction to disease facilitation. FEMS Microbiol Lett 355:100–107CrossRefGoogle Scholar
  2. Andersson PF, Johansson SBK, Stenlid J et al (2010) Isolation, identification and necrotic activity of viridiol from Chalara fraxinea, the fungus responsible for dieback of ash. For Path 40:43–46CrossRefGoogle Scholar
  3. Araújo WL, Maccheroni W, Aquilar-Vildoso CI et al (2001) Variability and interactions between endophytic bacteria and fungi isolated from leaf tissues of citrus rootstocks. Can J Microbiol 47:229–236CrossRefGoogle Scholar
  4. Arnold AE, Maynard Z, Gilbert GS et al (2000) Are tropical fungal endophytes hyperdiverse? Ecol Lett 3:267–274CrossRefGoogle Scholar
  5. Babikova Z, Gilbert L, Bruce TJA et al (2013) Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack. Ecol Lett 16(7):835–843. Scholar
  6. Baral H-O, Queloz V, Hosoya T (2014) Hymenoscyphus fraxineus, the correct scientific name for the fungus causing ash dieback in Europe. IMA Fungus 5(1):79–80CrossRefGoogle Scholar
  7. Bennett JW, Hung R, Lee S et al (2012) Fungal and bacterial volatile organic compounds: an overview and their role as ecological signaling agents. In: Hock B (ed) Fungal associations, The Mycota IX, 2nd edn. Springer, Heidelberg, pp 373–393CrossRefGoogle Scholar
  8. Bloemberg GV, Camacho Carvajal MM (2006) Microbial interactions with plants: a hidden world? In: Schulz B, Boyle C, Sieber T (eds) Microbial root endopyhtes, Soil biology, vol 9. Springer, Berlin, pp 321–336CrossRefGoogle Scholar
  9. Blumenstein K, Albrectsen BR, Martín JA et al (2015) Nutritional niche overlap potentiates the use of endophytes in biocontrol of a tree disease. BioControl 60:655–667CrossRefGoogle Scholar
  10. Brian PW, McGowan JC (1945) Viridin: a highly fungistatic substance produced by Trichoderma viride. Nature 156:144–145CrossRefGoogle Scholar
  11. Brundett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154:275–304CrossRefGoogle Scholar
  12. Cao Y, Halane MK, Gassmann W et al (2017) The role of plant innate immunity in the legume-rhizobium symbiosis. Annu Rev Plant Biol 68:535–561CrossRefGoogle Scholar
  13. Carroll GC (1995) Forest endophytes: pattern and process. Can J Bot 73(S1):1316–1324CrossRefGoogle Scholar
  14. Carroll GC (1999) The foraging ascomycete. In: 16th International Botanical Congress, Abstracts, 309Google Scholar
  15. Chagas FO, Dias LG, Pupo MT (2013) A mixed culture of endophytic fungi increases production of antifungal polyketides. J Chem Ecol 39:1335–1342CrossRefGoogle Scholar
  16. Chanclud E, Morel J-B (2016) Plant hormones: a fungal point of view. Mol Plant Pathol 17(8):1289–1297CrossRefGoogle Scholar
  17. Citron C, Junker C, Schulz B et al (2014) A volatile lactone of Hymenoscyphus pseudoalbidus, pathogen of European ash dieback, inhibits host germination. Angew Chem Int Ed 53:4346–4349CrossRefGoogle Scholar
  18. Combès A, Ndoye I, Bance C et al (2012) Chemical communication between the endophytic fungus Paraconiothyrium variabile and the phytopathogen Fusarium oxysporum. PLoS One 7(10):e47313CrossRefGoogle Scholar
  19. Courty P-E, Walder F, Boller T et al (2011) Carbon and nitrogen metabolism in mycorrhizal networks and mycoheterotrophic plants of tropical forests: a stable isotope analysis. Plant Physiol 156:952–961CrossRefGoogle Scholar
  20. Demain A (2000) Microbial biotechnology. TIBTECH 18:26–31CrossRefGoogle Scholar
  21. Drenkhan R, Hanso M (2010) New host species for Chalara fraxinea. New Dis Rep 22:16CrossRefGoogle Scholar
  22. Drenkhan R, Adamson K, Hanso M (2015) Fraxinus sogdiana, a central Asian ash species, is susceptible to Hymenoscyphus fraxineus. Plant Protect Sci 51(3):150–152CrossRefGoogle Scholar
  23. Egamberdieva D, Wirth SJ, Alqarawi AA (2017) Phytohormones and beneficial microbes: essential components for plants to balance stress and fitness. Front Microbiol 8:2104. Scholar
  24. Frasz SL, Walker AK, Nsiama TK et al (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
  25. Gross A, Holdenrieder O, Pautasso M et al (2014) Hymenoscyphus pseudoalbidus, the causal agent of European ash dieback. Mol Plant Pathol 15(1):5–21CrossRefGoogle Scholar
  26. Gunatilaka AAL (2006) Natural products from plant-associated microorganisms: distribution, structural diversity, bioactivity, and implications of their occurrence. J Nat Prod 69:509–526CrossRefGoogle Scholar
  27. Halecker S, Surup F, Kuhnert E et al (2014) Hymenosetin, a 3-decalinoyltetramic acid antibiotic from cultures of the ash dieback pathogen, Hymenoscyphus pseudoalbidus. Phytochemistry 100:6–91CrossRefGoogle Scholar
  28. Hardoim PR, van Overbeek LS, Berg G et al (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol MolBiol R 79:293–320CrossRefGoogle Scholar
  29. Hassani MA, Durán P, Hacquard S (2018) Microbial interactions within the plant holobiont. Microbiome 6:58CrossRefGoogle Scholar
  30. Hiscox J, Boddy L (2017) Armed and dangerous – chemical warfare in wood decay communities. Fungal Bio Rev 31:169–184CrossRefGoogle Scholar
  31. Höller U, Wright AD, Matthée GF et al (2000) Fungi from marine sponges: diversity, biological activity and secondary metabolites. Mycol Res 104:1354–1365CrossRefGoogle Scholar
  32. Junker C, Mandey F, Pais A et al (2014) Hymenoscyphus pseudoalbidus and Hymenoscyphus albidus: viridiol concentration and virulence do not correlate. For Path 44:39–44CrossRefGoogle Scholar
  33. Klein T, Siegwolf RTW, Koerner C (2016) Belowground carbon trade among tall trees in a temperate forest. Science 352(6283):342–344CrossRefGoogle Scholar
  34. Krohn K, Schulz B (2013) Antifungal metabolites of endophytic fungi. In: Antifungal metabolites from plants. Springer, Berlin, pp 243–262CrossRefGoogle Scholar
  35. Lahrmann U, Zuccaro A (2012) Opprimo ergo sum – evasion and suppression in the root endophytic fungus Piriformospora indica. Mol Plant Microb Interact 26:727–737CrossRefGoogle Scholar
  36. Lee S, Bennett J, Behringer G et al (2018) Effects of fungal volatile organic compounds on Arabidopsis thaliana growth and gene expression. Fungal Ecol 37:1–9. Scholar
  37. Maillet F, Poinsot V, André O et al (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469:58–64CrossRefGoogle Scholar
  38. Margulis L (1991) Symbiogenesis and symbionticism. In: Margulis L, Fester R (eds) Symbiosis as a source of evolutionary innovation: speciation and morphogenesis. MIT, Cambridge MA, pp 1–14LGoogle Scholar
  39. Marmann A, Aly AH, Lin W et al (2014) Co-cultivation – a powerful emerging tool for enhancing the chemical diversity of microorganisms. Mar Drugs 12:1043–1065CrossRefGoogle Scholar
  40. Matusova R, Rani K, Verstappen FWA et al (2005) The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiol 139:920–934CrossRefGoogle Scholar
  41. McKinney LV, Nielsen LR, Collinge DB et al (2014) The ash dieback crisis: genetic variation in resistance can prove a long-term solution. Plant Pathol 63:485–449CrossRefGoogle Scholar
  42. McMullan M, Rafiqi M, Kaihakottil G et al (2018) The ash dieback invasion of Europe was founded by two genetically divergent individuals. Nat Ecol Evol 2:1000–1008CrossRefGoogle Scholar
  43. Moran-Diez E, Rubio B, Domínguez S et al (2012) Transcriptomic response of Arabidopsis thaliana after 24 h incubation with the biocontrol fungus Trichoderma harzianum. J Plant Physiol 169:614–620CrossRefGoogle Scholar
  44. Morath SU, Hung R, Bennett JW (2012) Fungal volatile organic compounds: a review with emphasis on their biotechnological potential. Fungal Biol Rev 26:73–83CrossRefGoogle Scholar
  45. Mousa WK, Raizada MN (2013) The diversity of anti-microbial secondary metabolites produced by fungal endophytes: an interdisciplinary perspective. Front Microbiol 4:65. Scholar
  46. Ola ARB, Thomy D, Lai D et al (2013) Inducing secondary metabolite production by the endophytic fungus Fusarium tricinctum through coculture with Bacillus subtilis. J Nat Prod 76:2094–2095CrossRefGoogle Scholar
  47. Oláh B, Brière C, Bécard G et al (2005) Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signalling pathway. Plant J 44:195–207CrossRefGoogle Scholar
  48. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbiosis. Nat Rev Microbiol 6:763–775CrossRefGoogle Scholar
  49. Patkar RN, Naqvi NI (2017) Fungal manipulation of hormone-regulated plant defense. PLoS Pathog 13(6):e1006334. Scholar
  50. Petrini O (1991) Fungal endophytes of tree leaves. In: Andrews JH, Hirano SS (eds) Microbial ecology of leaves. Brock/Springer series in contemporary bioscience. Springer, New York, NY, pp 179–197Google Scholar
  51. Rao RP, Hunter A, Kashpur O et al (2010) Aberrant synthesis of indole-3-acetic acid in Saccharomyces cerevisiae triggers transition, a virulence trait of pathogenic fungi. Genetics 185:211–220CrossRefGoogle Scholar
  52. Schäfer P, Pfiffi S, Voll LM et al (2009) Manipulation of plant innate immunity and gibberellin as factor of compatibility in the mutualistic association of barley roots with Piriformospora indica. Plant J 59:461-ACrossRefGoogle Scholar
  53. Schulz B (2006) Mutualistic interactions with fungal root endophytes. In: Schulz B, Boyle C, Sieber TN (eds) Microbial root endophytes. Springer, Berlin, pp 261–279CrossRefGoogle Scholar
  54. Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686CrossRefGoogle Scholar
  55. Schulz B, Sucker J, Aust H-J et al (1995) Biologically active secondary metabolites of endophytic Pezicula species. Mycol Res 99:1007–1015CrossRefGoogle Scholar
  56. Schulz B, Römmert A-K, Dammann U et al (1999) The endophyte-host interaction: a balanced antagonism. Mycol Res 103:1275–1283CrossRefGoogle Scholar
  57. Schulz B, Boyle C, Draeger S et al (2002) Review: Endophytic fungi: a source of novel biologically active secondary metabolites. Mycol Res 106:996–1004CrossRefGoogle Scholar
  58. Schulz B, Boyle C, Sieber TN (eds) (2006) Microbial root endophytes. Springer, BerlinGoogle Scholar
  59. Schulz B, Haas S, Junker C et al (2015) Fungal endophytes are involved in multiple balanced antagonisms. Curr Sci India 109:39–45Google Scholar
  60. Simard SW, Beiler KJ, Bingham MA et al (2012) Mycorrhizal networks: Mechanisms, ecology and modeling. Fungal Biol Rev 26:39–60CrossRefGoogle Scholar
  61. Singh S, Parniske M (2012) Activation of calcium- and calmodulin-dependent protein kinase (CCaMK), the central regulator of plant root endosymbiosis. Curr Opin Plant Biol 15:444–453CrossRefGoogle Scholar
  62. Stacey G, McAlvin CB, Kim S-Y et al (2006) Effects of endogenous salicylic acid on nodulation in the model legumes Lotus japonicus and Medicago truncatula. Plant Physiol 141:1473–1481CrossRefGoogle Scholar
  63. Stringlis IA, Zhang H, Corné MJ et al (2018) Microbial small molecules – weapons of plant subversion. Nat Prod Rep 35(4):410–433. Scholar
  64. Sumarah MW, Miller JD, Adams GW (2005) Measurement of a rugulosin-producing endophyte in white spruce seedlings. Mycologia 97:770–776CrossRefGoogle Scholar
  65. Sumarah MW, Puniani E, Blackwell BA et al (2008) Characterization of polyketide metabolites from foliar endophytes of Picea glauca. J Nat Prod 71(8):1393–1398CrossRefGoogle Scholar
  66. Surup F, Halecker S, Nimtz M et al (2018) Hyfraxins A and B, cytotoxic ergostane-type steroid and lanostane triterpenoid glycosides from the invasive ash dieback ascomycete Hymenoscyphus fraxineus. Steroids 135:92–97CrossRefGoogle Scholar
  67. Tan RX, Zou WX (2001) Endophytes: a rich source of functional metabolites. Nat Prod Rep 18:448–459CrossRefGoogle Scholar
  68. Terhonen E, Sipari N, Asiegbu FO (2016) Inhibition of phytopathogens by fungal root endophytes of Norway spruce. Biol Control 99:53–63. Scholar
  69. Thomas DC, Vandegrift R, Ludden A et al (2016) Spatial ecology of the fungal genus Xylaria in a tropical cloud forest. Biotropica 48:381–393CrossRefGoogle Scholar
  70. Ujor VC, Adukwu EC, Okonkwo CC (2018) Fungal wars: the underlying molecular repertoires of combating mycelia. Fungal Biol 122:191–202CrossRefGoogle Scholar
  71. Verma VC, Kharwar RN, Strobel GA (2009) Chemical and functional diversity of natural products from plant associated endophytic fungi. Nat Prod Commun 4(11):1511–1532PubMedGoogle Scholar
  72. Wang X-M, Yang B, Ren C-G et al (2014) Involvement of abscisic acid and salicylic acid in signal cascade regulating bacterial endophyte-induced volatile oil biosynthesis in plantlets of Atractylodes lancea. Physiol Plant 153(1):30–42. Scholar
  73. Zhao Y-J, Hosoya T, Baral H-O et al (2012) Hymenoscyphus pseudoalbidus, the correct name for Lambertella albida reported from Japan. Mycotaxon 122:25–41CrossRefGoogle Scholar
  74. Zhou JY, Zhao XY, Dai CC (2014) Antagonistic mechanisms of endophytic Pseudomonas fluorescens against Athelia rolfsii. J Appl Microbiol 117(4):1144–1158. Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Barbara Joan Schulz
    • 1
    Email author
  • Laura Rabsch
    • 1
  • Corina Junker
    • 2
  1. 1.Technische Universität Braunschweig, Institut für MikrobiologieBraunschweigGermany
  2. 2.Julius-Kuhn-InstitutBraunschweigGermany

Personalised recommendations