Plant Molecular Biology

, Volume 90, Issue 6, pp 645–655 | Cite as

Fungal endophytes: modifiers of plant disease

Article

Abstract

Many recent studies have demonstrated that non-pathogenic fungi within plant microbiomes, i.e., endophytes (“endo” = within, “phyte” = plant), can significantly modify the expression of host plant disease. The rapid pace of advancement in endophyte ecology warrants a pause to synthesize our understanding of endophyte disease modification and to discuss future research directions. We reviewed recent literature on fungal endophyte disease modification, and here report on several emergent themes: (1) Fungal endophyte effects on plant disease span the full spectrum from pathogen antagonism to pathogen facilitation, with pathogen antagonism most commonly reported. (2) Agricultural plant pathosystems are the focus of research on endophyte disease modification. (3) A taxonomically diverse group of fungal endophytes can influence plant disease severity. And (4) Fungal endophyte effects on plant disease severity are context-dependent. Our review highlights the importance of fungal endophytes for plant disease across a broad range of plant pathosystems, yet simultaneously reveals that complexity within plant microbiomes presents a significant challenge to disentangling the biotic environmental factors affecting plant disease severity. Manipulative studies integrating eco-evolutionary approaches with emerging molecular tools will be poised to elucidate the functional importance of endophytes in natural plant pathosystems that are fundamental to biodiversity and conservation.

Keywords

Microbiome Disease ecology Context-dependency Biocontrol Alternaria Cladosporium Fusarium Trichoderma Aureobasidium Penicillium 

Supplementary material

11103_2015_412_MOESM1_ESM.docx (75 kb)
Supplementary material 1 (DOCX 76 kb)

References

  1. Adame-Álvarez RM, Mendiola-Soto J, Heil M (2014) Order of arrival shifts endophyte-pathogen interactions in bean from resistance induction to disease facilitation. FEMS Microbiol Lett 355:100–107. doi:10.1111/1574-6968.12454 PubMedCrossRefGoogle Scholar
  2. Andrews JH, Berbee FM, Nordheim EV (1983) Microbial antagonism to the imperfect stage of the apple scab pathogen, Venturia inaequalis. Phytopathology 73:228–234CrossRefGoogle Scholar
  3. Arnold A, Lutzoni F (2007) Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88:541–549PubMedCrossRefGoogle Scholar
  4. Arnold A, Mejia L, Kyllo D, Rojas E, Maynard Z, Robbins N, Herre E (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci 100:15649–15654PubMedPubMedCentralCrossRefGoogle Scholar
  5. Bailey B, Bae H, Strem M, Crozier J, Thomas S, Samuels G, Vinyard B, Holmes K (2008) Antibiosis, mycoparasitism, and colonization success for endophytic Trichoderma isolates with biological control potential in Theobroma cacao. Biol Control 46:24–35. doi:10.1016/j.biocontrol.2008.01.003 CrossRefGoogle Scholar
  6. Baynes M, Newcombe G, Dixon L, Castlebury L, O’Donnell K (2012) A novel plant-fungal mutualism associated with fire. Fungal Biol 116:133–144. doi:10.1016/j.funbio.2011.10.008 PubMedCrossRefGoogle Scholar
  7. Benítez M-S, Hersh MH, Vilgalys R, Clark JS (2013) Pathogen regulation of plant diversity via effective specialization. Trends Ecol Evol 28:705–711. doi:10.1016/j.tree.2013.09.005
  8. Bills GF (1996) Isolation and analysis of endophytic fungal communities from woody plants. In: Redlin SC, Carris LM (eds) Endophytic fungi in grasses and woody plants: systematics, ecology and evolution. American Phytopathological Society, St Paul, pp 31–65Google Scholar
  9. Bonello P, Capretti P, Luchi N, Martini V, Michelozzi M (2008) Systemic effects of Heterobasidion annosum ss infection on severity of Diplodia pinea tip blight and terpenoid metabolism in Italian stone pine (Pinus pinea). Tree Physiol 28:1653–1660PubMedCrossRefGoogle Scholar
  10. Bonito G, Reynolds H, Robeson MS II, Nelson J, Hodkinson BP, Tuskan G, Schadt CW, Vilgalys R (2014) Plant host and soil origin influence fungal and bacterial assemblages in the roots of woody plants. Mol Ecol 23:3356–3370. doi:10.1111/mec.12821 PubMedCrossRefGoogle Scholar
  11. Borer E, Hosseini P, Seabloom E, Dobson A (2007) Pathogen-induced reversal of native dominance in a grassland community. Proc Natl Acad Sci 104:5473–5478PubMedPubMedCentralCrossRefGoogle Scholar
  12. Borges ÁV, Saraiva RM, Maffia LA (2015) Biocontrol of gray mold in tomato plants by Clonostachys rosea. Trop Plant Path 40:71–76CrossRefGoogle Scholar
  13. Brame C, Flood J (1983) Antagonism of Aureobasidium pullulans towards Alternaria solani. Trans Brit Mycol Soc 81:621–624CrossRefGoogle Scholar
  14. Breen JP (1994) Acremonium endophyte interactions with enhanced plant resistance to insects. Annu Rev Entomol 39:401–423CrossRefGoogle Scholar
  15. Busby PE, Zimmerman N, Weston DJ, Jawdy SS, Houbraken J, Newcombe G (2013) Leaf endophytes and Populus genotype affect severity of damage from the necrotrophic leaf pathogen, Drepanopeziza populi. Ecosphere. doi:10.1890/ES13-00127.1 Google Scholar
  16. Busby PE, Peay K, Newcombe G (2015) Common foliar fungi of Populus trichocarpa modify Melampsora rust disease severity. New Phytol. doi:10.1111/nph.13742 PubMedGoogle Scholar
  17. Caesar AJ (2003) Synergistic interaction of soilborne plant pathogens and root-attacking insects in classical biological control of an exotic rangeland weed. Biol Control 28(1):144–153CrossRefGoogle Scholar
  18. Carisse O, Philion V, Rolland D, Bernier J (2000) Effect of fall application of fungal antagonists on spring ascospore production of the apple scab pathogen, Venturia inaequalis. Phytopathology 90:31–37PubMedCrossRefGoogle Scholar
  19. Carroll GC (1992) Fungal mutualism. In: Carroll GC, Wicklow DT (eds) The fungal community. Its organization and role in the ecosystem. Dekker, New York, pp 327–354Google Scholar
  20. Christian N, Whitaker BK, Clay K (2015) Microbiomes: unifying animal and plant systems through the lens of community ecology theory. Front Microbiol 6:869. doi:10.3389/fmicb.2015.00869 PubMedPubMedCentralCrossRefGoogle Scholar
  21. Clay K (1988) Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 69:10–16CrossRefGoogle Scholar
  22. Clay K (1990) Fungal endophytes of grasses. Annu Rev Ecol Syst 21:275–279CrossRefGoogle Scholar
  23. Clay K (2014) Defensive symbiosis: a microbial perspective. Funct Ecol 28:293–298. doi:10.1111/1365-2435.12258 CrossRefGoogle Scholar
  24. Compant S, Duffy B, Nowak J, Clément C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959PubMedPubMedCentralCrossRefGoogle Scholar
  25. Cook RJ, Baker KF (1983) The nature and practice of biological control of plant pathogens. American Phytopathological Society (APS Press), University of Michigan, Ann Arbor, p 539Google Scholar
  26. Cota LV, Maffia LA, Mizubuti ES, Macedo PE, Antunes RF (2008) Biological control of strawberry gray mold by Clonostachys rosea under field conditions. Biol Control 46:515–522CrossRefGoogle Scholar
  27. Dangl JL, Horvath DM, Staskawicz BJ (2013) Pivoting the plant immune system from dissection to deployment. Science 341:746–751. doi:10.1126/science.1236011 PubMedCrossRefGoogle Scholar
  28. Danielsen S, Jensen DF (1999) Fungal endophytes from stalks of tropical maize and grasses: isolation, identification, and screening for antagonism against Fusarium verticillioides in maize stalks. Biocontrol Sci Technol 9:545–553CrossRefGoogle Scholar
  29. de Capdeville G, Wilson CL, Beer SV, Aist JR (2002) Alternative disease control agents induce resistance to blue mold in harvested ‘Red Delicious’ apple fruit. Phytopathology 92:900–908PubMedCrossRefGoogle Scholar
  30. de Melo EA, Rosa de Lima RM, Laranjeira D, dos Santos LA, de Omena Gusmão L, de Souza EB (2015) Efficacy of yeast in the biocontrol of bacterial fruit blotch in melon plants. Trop Plant Pathol 40:56–64CrossRefGoogle Scholar
  31. Dingle J, Mcgee PA (2003) Some endophytic fungi reduce the density of pustules of Puccinia recondite f. sp. tritici in wheat. Mycol Res 107:310–316PubMedCrossRefGoogle Scholar
  32. Elad Y, Chet I, Katan J (1980) Trichoderma harzianum: a biocontrol agent effective against Sclerotium rolfsii and Rhizoctonia solani. Phytopathology 70:119–121CrossRefGoogle Scholar
  33. Ellis B (1972) Dematiaceous hyphomycetes. Commonwealth Mycological Institute, State CollegeGoogle Scholar
  34. Fox JE, Gulledge J, Engelhaupt E, Burrow ME, McLachlan JA (2007) Pesticides reduce symbiotic efficiency of nitrogen-fixing rhizobia and host plants. PNAS 104:10282–10287PubMedPubMedCentralCrossRefGoogle Scholar
  35. Freeman S, Rodriguez RJ (1993) Genetic conversion of a fungal plant pathogen to a nonpathogenic, endophytic mutualist. Science 260:75–78PubMedCrossRefGoogle Scholar
  36. Funk A, Centre PFR (1985) Foliar fungi of western trees. Pacific Forest Research Centre, VictoriaGoogle Scholar
  37. Gallai N et al (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ 68:810–821CrossRefGoogle Scholar
  38. Ganley R, Brunsfeld S, Newcombe G (2004) A community of unknown, endophytic fungi in western white pine. Proc Natl Acad Sci USA 101:10107–10112Google Scholar
  39. Grosch R, Scherwinski K, Lottmann J, Berg G (2006) Fungal antagonists of the plant pathogen Rhizoctonia solani: selection, control efficacy and influence on the indigenous microbial community. Mycol Res 110:1464–1474PubMedCrossRefGoogle Scholar
  40. Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species—opportunistic, avirulent plant symbionts. Nat Rev Micro 2:43–56. doi:10.1038/nrmicro797
  41. Hanada RE, de Jorge Souza T, Pomella AW, Hebbar KP, Pereira JO, Ismaiel A, Samuels GJ (2008) Trichoderma martiale sp. nov., a new endophyte from sapwood of Theobroma cacao with a potential for biological control. Mycol Res 112:1335–1343PubMedCrossRefGoogle Scholar
  42. Hanada RE, Pomella AWV, 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 Biol 114:901–910PubMedCrossRefGoogle Scholar
  43. Heather WA, Sharma IK (1987) Physiologic specialisation in the hyperparasitism of races of Melampsora larici-populina by isolates of Cladosporium tenuissimum. For Pathol 17:185–188Google Scholar
  44. Hoch HC, Staples RC, Whitehead B, Comeau J, Wolf ED (1987) Signaling for growth orientation and cell differentiation by surface topography in Uromyces. Science 235:1659–1662PubMedCrossRefGoogle Scholar
  45. Houterman PM, Cornelissen BJC, Rep M (2008) Suppression of plant resistance gene-based immunity by a fungal effector. PLoS Pathog 4:e1000061PubMedPubMedCentralCrossRefGoogle Scholar
  46. Hue AG, Voldeng HD, Savard ME, Fedak G, Tian X, Hsiang T (2009) Biological control of Fusarium head blight of wheat with Clonostachys rosea strain ACM941. Can J Plant Pathol 31:169–179CrossRefGoogle Scholar
  47. Istifadah N, McGee PA (2006) Endophytic Chaetomium globosum reduces development of tan spot in wheat caused by Pyrenophora tritici-repentis. Austral Plant Pathol 35:411–418CrossRefGoogle Scholar
  48. Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism–parasitism continuum. New Phytol 135:575–585. doi:10.1046/j.1469-8137.1997.00729.x CrossRefGoogle Scholar
  49. Jones EE, Bienkowski DA (2015) The importance of water potential range tolerance as a limiting factor on Trichoderma spp. biocontrol of Sclerotinia sclerotiorum. Ann Appl Biol. doi:10.1111/aab.12240 Google Scholar
  50. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329. doi:10.1038/nature05286 PubMedCrossRefGoogle Scholar
  51. Jones EE, Rabeendran N, Stewart A (2014) Biocontrol of Sclerotinia sclerotiorum infection of cabbage by Coniothyrium minitans and Trichoderma spp. Biocontrol Sci Technol 24:1363–1382CrossRefGoogle Scholar
  52. Kandula DRW, Jones EE, Stewart A, McLean KL, Hampton JG (2015) Trichoderma species for biocontrol of soil-borne plant pathogens of pasture species. Biocontrol Sci Technol. doi:10.1080/09583157.2015.1028892 Google Scholar
  53. Kefialew Y, Ayalew A (2008) Postharvest biological control of anthracnose (Colletotrichum gloeosporioides) on mango (Mangifera indica). Postharvest Biol Technol 50:8–11CrossRefGoogle Scholar
  54. Khastini RO, Ohta H, Narisawa K (2012) The role of a dark septate endophytic fungus, Veronaeopsis simplex Y34, in Fusarium disease suppression in Chinese cabbage. J Microbiol 50:618–624PubMedCrossRefGoogle Scholar
  55. Kiers ET, van der Heijden MGA (2006) Mutualistic stability in the arbuscular mycorrhizal symbiosis: exploring hypotheses of evolutionary cooperation. Ecology 87:1627–1636PubMedCrossRefGoogle Scholar
  56. Kiers ET et al (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882PubMedCrossRefGoogle Scholar
  57. Kiss L (2003) A review of fungal antagonists of powdery mildews and their potential as biocontrol agents. Pest Manag Sci 59:475–483PubMedCrossRefGoogle Scholar
  58. Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70. doi:10.1038/417067a
  59. Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM et al (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277PubMedCrossRefGoogle Scholar
  60. Kosaka H, Aikawa T, Ogura N, Tabata K, Kiyohara T (2001) Pine wilt disease caused by the pine wood nematode: the induced resistance of pine trees by the avirulent isolates of nematode. Eur J Plant Pathol 107(7):667–675Google Scholar
  61. Kruske CR, Hesse CN, Challacombe JF, Cullen D, Herr JR, Mueller C, Tsang A, Vilgalys R (2015) Prospects and challenges for fungal metatranscriptomics of complex communities. Fungal Ecol 14:133–137CrossRefGoogle Scholar
  62. Kurose D, Furuya N, Tsuchiya K, Tsushima S, Evans HC (2012) Endophytic fungi associated with Fallopia japonica (Polygonaceae) in Japan and their interactions with Puccinia polygoni-amphibii var. tovariae, a candidate for classical biological control. Fungal Biol 116:785–791Google Scholar
  63. Larkin RP, Fravel DR (1998) Efficacy of various fungal and bacterial biocontrol organisms for control of Fusarium wilt of tomato. Plant Dis 82:1022–1028CrossRefGoogle Scholar
  64. Larran S, Simón MR, Moreno MV, Siurana MS, Perelló A (2016) Endophytes from wheat as biocontrol agents against tan spot disease. Biol Control 92:17–23CrossRefGoogle Scholar
  65. Lebeis SL, Paredes SH, Lundberg DS, Breakfield N, Gehring J, McDonald M, Malfatti S, Glavina del Rio T, Jones CD, Tringe SG, Dangl JL (2015) Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 349:860–864. doi:10.1126/science.aaa8764 PubMedCrossRefGoogle Scholar
  66. Ledford H (2015) Plant dwellers take the limelight. Nature 523:137–138PubMedCrossRefGoogle Scholar
  67. Lee K, Pan JJ, May G (2009) Endophytic Fusarium verticillioides reduces disease severity caused by Ustilago maydis on maize. FEMS Microbiol Lett 299:31–37. doi:10.1111/j.1574-6968.2009.01719.x PubMedCrossRefGoogle Scholar
  68. Maleszka R, Mason PH, Barron AB (2014) Epigenomics and the concept of degeneracy in biological systems. Brief Funct Genomics 13:191–202PubMedPubMedCentralCrossRefGoogle Scholar
  69. Martín JA, Macaya-Sanz D, Witzell J (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 Plant Pathol 142:185–196. doi:10.1007/s10658-015-0602-2 CrossRefGoogle Scholar
  70. Martinez-Medina A, Del Mar Alguacil M, Pascual JA, Van Wees SCM (2014) Phytohormone profiles induced by Trichoderma isolates correspond with their biocontrol and plant growth-promoting activity on melon plants. J Chem Ecol 40:804–815. doi:10.1007/s10886-014-0478-1 PubMedCrossRefGoogle Scholar
  71. Masih EI, Paul B (2002) Secretion of β-1, 3-glucanases by the yeast Pichia membranifaciens and its possible role in the biocontrol of Botrytis cinerea causing grey mold disease of the grapevine. Curr Microb 44:391–395CrossRefGoogle Scholar
  72. Mejía LC, Herre EA, Sparks JP, Winter K, García 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 5:479. doi:10.3389/fmicb.2014.00479 PubMedPubMedCentralGoogle Scholar
  73. Mekbib SB, Regnier TJ, Korsten L (2011) Efficacy and mode of action of yeast antagonists for control of Penicillium digitatum in oranges. Trop Plant Pathol 36:233–240Google Scholar
  74. Michereff SJ, da Silveira NSS, Reis A, de Mariano RLR (1995) Greenhouse screening of Trichoderma isolates for control of Curvularia leaf spot of yam. Mycopathologia 130:103–108CrossRefGoogle Scholar
  75. Moraga-Suazo P, Opazo A, Zaldúa S, González G, Sanfuentes E (2011) Evaluation of Trichoderma spp. and Clonostachys spp. strains to control Fusarium circinatum in Pinus radiata seedlings. Chil J Agric Res 71:412–417CrossRefGoogle Scholar
  76. Mousseaux MR, Dumroese RK, James RL, Wenny DL, Knudsen GR (1998) Efficacy of Trichoderma harzianum as a biological control of Fusarium oxysporum in container-grown Douglas-fir seedlings. New For 15:11–21CrossRefGoogle Scholar
  77. Narisawa K, Kawamata H, Currah RS, Hashiba T (2002) Suppression of Verticillium wilt in eggplant by some fungal root endophytes. Eur J Plant Pathol 108:103–109CrossRefGoogle Scholar
  78. Nischwitz C, Newcombe G, Anderson CL (2005) Host specialization of the mycoparasite Eudarluca caricis and its evolutionary relationship to Ampelomyces. Mycol Res 109:421–428. doi:10.1017/S0953756205002431
  79. Newcombe G, Lee B, Robb J (1990) Early vascular sporulation: a possible role in the virulence of Verticillium albo-atrum in wilt of alfalfa. Physiol Mol Plant Pathol 36:441–449. doi:10.1016/0885-5765(90)90017-R CrossRefGoogle Scholar
  80. Newsham KK, Fitter AH, Watkinson AR (1995) Arbuscular mycorrhiza protect an annual grass from root pathogenic fungi in the field. J Ecol 83:991–1000Google Scholar
  81. Nguyen NH, Smith D, Peay K, Kennedy P (2014) Parsing ecological signal from noise in next generation amplicon sequencing. New Phytol 205:1389–1393. doi:10.1111/nph.12923 PubMedCrossRefGoogle Scholar
  82. Pandey RR, Arora DK, Dubey RC (1993) Antagonistic interactions between fungal pathogens and phylloplane fungi of guava. Mycopathologia 124:31–39CrossRefGoogle Scholar
  83. Perazzolli M, Dagostin S, Ferrari A, Elad Y, Pertot I (2008) Induction of systemic resistance against Plasmopara viticola in grapevine by Trichoderma harzianum T39 and benzothiadiazole. Biol Control 47:228–234CrossRefGoogle Scholar
  84. Perello A, Simon MR, Arambarri AM (2002) Interactions between foliar pathogens and the saprophytic microflora of the wheat (Triticum aestivum L.) phylloplane. J Phytopathol 150:232–243CrossRefGoogle Scholar
  85. Petrini O (1991) Fungal endophytes of tree leaves. In: Andrews JH, Hirano SS (eds) Microbial ecology of leaves. Springer, New York, pp 179–197CrossRefGoogle Scholar
  86. Photita W, Lumyong S, Lumyong P, McKenzie E, Hyde KD (2004) Are some endophytes of Musa acuminata latent pathogens? Fungal Divers 16:131–140Google Scholar
  87. Pimm SL, Joppa LN (2015) How many plant species are there, where are they, and at what rate are they going extinct? Ann Mo Bot Gard 100:170–176CrossRefGoogle Scholar
  88. Pozo MJ, Cordier C, Dumas-Gaudot E, Gianinazzi S, Barea JM, Azcon-Aguilar C (2002) Localized versus systemic effect of arbuscular mycorrhizal fungi on defense responses to Phytophthora infection in tomato plants. J Exp Bot 53:525–534PubMedCrossRefGoogle Scholar
  89. Pruss Gail et al (1997) Plant viral synergism: the potyviral genome encodes a broad-range pathogenicity enhancer that transactivates replication of heterologous viruses. Plant Cell 9(6):859–868PubMedPubMedCentralCrossRefGoogle Scholar
  90. Raaijmakers JM, Vlami M, De Souza JT (2002) Antibiotic production by bacterial biocontrol agents. Antonie Van Leeuwenhoek 81:537–547PubMedCrossRefGoogle Scholar
  91. Raghavendra AKH, Newcombe G (2013) The contribution of foliar endophytes to quantitative resistance to Melampsora rust. New Phytol 197:909–918. doi:10.1111/nph.12066 PubMedCrossRefGoogle Scholar
  92. Redman R, Freeman S, Clifton D, Morrel J, Brown G, Rodriguez R (1999) Biochemical analysis of plant protection afforded by a nonpathogenic endophytic mutant of Colletotrichum magna. Plant Physiol 119:795–804PubMedPubMedCentralCrossRefGoogle Scholar
  93. Richter DL (2008) Revival of saprotrophic and mycorrhizal basidiomycete cultures after 20 years in cold storage in sterile water. Can J Microbiol 54:595–599. doi:10.1139/w08-049
  94. Ridout M, Newcombe G (2015) The frequency of modification of Dothistroma pine needle blight severity by fungi within the native range. For Ecol Manag 337:153–160. doi:10.1016/j.foreco.2014.11.010 CrossRefGoogle Scholar
  95. Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim Y-O, Redman RS (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2:404–416PubMedCrossRefGoogle Scholar
  96. Rodriguez RJ, White JF Jr, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330. doi:10.1111/j.1469-8137.2009.02773.x PubMedCrossRefGoogle Scholar
  97. Rodríguez MA, Rothen C, Lo TE, Cabrera GM, Godeas AM (2015) Suppressive soil against Sclerotinia sclerotiorumas a source of potential biocontrol agents: selection and evaluation of Clonostachys rosea BAFC1646. Biocontrol Sci Technol. doi:10.1080/09583157.2015.1052372 Google Scholar
  98. Rodriguez-Estrada AE, Jonkers W, Kistler HC, May G (2012) Interactions between Fusarium verticillioides, Ustilago maydis, and Zea mays: an endophyte, a pathogen, and their shared plant host. Fungal Gen Biol 49:578–587CrossRefGoogle Scholar
  99. Romeralo CARMEN, Santamaría O, Pando V, Diez JJ (2015) Fungal endophytes reduce necrosis length produced by Gremmeniella abietina in Pinus halepensis seedlings. Biol Control 80:30–39CrossRefGoogle Scholar
  100. Ross AF (1961) Systemic acquired resistance induced by localized virus infections in plants. Virology 14:340–358PubMedCrossRefGoogle Scholar
  101. 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
  102. Sasan RK, Bidochka MJ (2013) Antagonism of the endophytic insect pathogenic fungus Metarhizium robertsii against the bean plant pathogen Fusarium solani f. sp. phaseoli. Can J Plant Pathol 35:288–293CrossRefGoogle Scholar
  103. Schulz B, Rommert A-K, Dammann U, Aust H-J, Strack D (1999) The endophyte-host interaction: a balanced antagonism? Mycol Res 103:1275–1283CrossRefGoogle Scholar
  104. Segarra G, Casanova E, Bellido D, Odena MA, Oliveira E, Trillas I (2007) Proteome, salicylic acid, and jasmonic acid changes in cucumber plants inoculated with Trichoderma asperellum strain T34. Proteomics 7:3943–3952PubMedCrossRefGoogle Scholar
  105. Selosse M et al (2006) Mycorrhizal networks: des liaisons dangereuses? Trends Ecol Evol 21(11):621–628PubMedCrossRefGoogle Scholar
  106. Sequeira L, Gaard G, De Zoeten GA (1977) Interaction of bacteria and host cell walls: its relation to mechanisms of induced resistance. Physiol Plant Pathol 10:43–50CrossRefGoogle Scholar
  107. Spadaro D, Gullino ML (2004) State of the art and future prospects of the biological control of postharvest fruit diseases. Int J Food Microbiol 91:185–194PubMedCrossRefGoogle Scholar
  108. Stadler M, von Tiedemann A (2014) Biocontrol potential of Microsphaeropsis ochracea on microsclerotia of Verticillium longisporum in environments differing in microbial complexity. Biocontrol 59:449–460CrossRefGoogle Scholar
  109. Stevens RB (1960) Plant pathology: an advanced treatise. Academic Press, New YorkGoogle Scholar
  110. Stone J, Bacon C, White J (2000) An overview of endopytic microbes: endophytism defined. In: Bacon C, White J (eds) Microbial endophytes. Marcel Dekker, New York, pp 3–29Google Scholar
  111. Tack AJM, Laine A, Burdon JJ, Bissett A, Thrall P (2015) Belowground abiotic and biotic heterogeneity shapes above-ground infection outcomes and spatial divergence in a host-parasite interaction. New Phytol 207:1159–1169PubMedCrossRefGoogle Scholar
  112. Usall J, Teixidó N, Fons E, Vinas I (2000) Biological control of blue mould on apple by a strain of Candida sake under several controlled atmosphere conditions. Int J Food Microbiol 58:83–92PubMedCrossRefGoogle Scholar
  113. Van Wees SCM, de Swart EAM, van Pelt JA, van Loon LC, Pieterse CMJ (2000) Enhancement of induced disease resistance by simultaneous activation of salicylate-and jasmonate-dependent defense pathways in Arabidopsis thaliana. Proc Natl Acad Sci 97:8711–8716PubMedPubMedCentralCrossRefGoogle Scholar
  114. Vázquez de Aldana BR, Bills G, Zabalgogeazcoa I (2013) Are endophytes an important link between airborne spores and allergen exposure? Fungal Divers 60:33–42. doi:10.1007/s13225-013-0223-z CrossRefGoogle Scholar
  115. Vorholt JA (2012) Microbial life in the phyllosphere. Nat Rev Microbiol 10:828–840PubMedCrossRefGoogle Scholar
  116. Wachowska U, Głowacka K (2014) Antagonistic interactions between Aureobasidium pullulans and Fusarium culmorum, a fungal pathogen of winter wheat. Biocontrol 59:635–645CrossRefGoogle Scholar
  117. Waqas M, Khan AL, Muhammad H, Shahzad R, Kang SM, Kim JG, Lee IJ (2015) Endophytic fungi promote plant growth and mitigate the adverse effects of stem rot: an example of Penicillium citrinum and Aspergillus terreus. J Plant Interact 10:280–287. doi:10.1080/17429145.2015.1079743 CrossRefGoogle Scholar
  118. Weller DM (1988) Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Ann Rev Phytopathol 26:379–407CrossRefGoogle Scholar
  119. Wennstrom A (1994) Endophyte: the misuse of an old term. Oikos 71:535–536CrossRefGoogle Scholar
  120. Wilson D (1993) Fungal endophytes: out of sight but should not be out of mind. Oikos 68:379–384CrossRefGoogle Scholar
  121. Wilson D (1995) Endophyte: the evolution of a term, and clarification of its use and definition. Oikos 73:274–276CrossRefGoogle Scholar
  122. Yohalem DS (2004) Evaluation of fungal antagonists for grey mould management in early growth of pot roses. Ann Appl Biol 144:9–15CrossRefGoogle Scholar
  123. Zeilinger S, Omann M (2007) Trichoderma biocontrol: signal transduction pathways involved in host sensing and mycoparasitism. Gene Regul Syst Bio 1:227–234PubMedPubMedCentralGoogle Scholar
  124. Zimmerman NB, Vitousek PM (2012) Fungal endophyte communities reflect environmental structuring across a Hawaiian landscape. Proc Natl Acad Sci 109:13022–13027PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Department of BiologyDuke UniversityDurhamUSA
  2. 2.Department of Forest, Rangelands and Fire SciencesUniversity of IdahoMoscowUSA

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