Tree Endophytes: Cryptic Drivers of Tropical Forest Diversity

  • Eric A. Griffin
  • Walter P. Carson
Part of the Forestry Sciences book series (FOSC, volume 86)


Roots and leaves comprise two of the largest microbial habitats on Earth, particularly in tropical forests where root and leaf surface areas are extremely high and microbes are abundant and diverse. Fungal and bacterial endophytes are primarily acquired via contagious spread from the surrounding environment. The soil is an important reservoir for both fungal and bacterial endophytes; we term this a soil microbial bank and suggest that it functions similarly to a soil seed bank. Because most (~75%) studies have found a strong positive relationship between plant diversity and soil microbial diversity, we predict that as plant diversity increases so will endophyte taxonomic and functional diversity. Once inside plant host tissues, endophytes can act as mutualists and increase plant performance directly by producing plant hormones, or indirectly by decreasing fungal or insect damage by up to 80%. Recent studies, however, have demonstrated that there are costs associated with hosting “beneficial” endophytes for tropical trees. This is important because it challenges more traditional dichotomies (e.g., beneficial or deleterious) about endophytes and suggests that there are highly complex and context-dependent trade-offs and costs involved in plant-endophyte interactions. Though they comprise a cryptic component of tropical forests, plant-microbe interactions may typically regulate tree diversity, composition, and forest function at neighborhood and even regional scales. For example, pathogens may maintain tree diversity by reducing the fitness of common species in areas where plant host density is high or where hosts are close to reproductive conspecific adults. Moreover, plant-endophyte interactions, whether pathogenic or mutualistic, may comprise an entirely novel dimension of niche differentiation for coexisting tree species. Overall, tree endophytes in tropical forests are complex, yet critical drivers of forest dynamics and function.



We thank Melissa McCormick, Dennis Whigham, and Natalie Christian for helpful discussions over the course of this work and comments on earlier drafts of this manuscript. We like to thank Allen Herre and Betsy Arnold in particular for extensive help and comments during the course of this work. Moreover, we thank Betsy Arnold and Francois Lutzoni for permission to use Fig. 1. We acknowledge financial support from the National Science Foundation, the University of Pittsburgh, the Smithsonian Tropical Research Institute, the Smithsonian Environmental Research Center, Sigma Xi, and the American Philosophical Society.


  1. Adam M, Heuer H, Hallman J (2014) Bacterial antagonists of fungal pathogens also control root-knot nematodes by induced systemic resistance of tomato plants. PLoS ONE 9:e90402PubMedPubMedCentralCrossRefGoogle Scholar
  2. Agrios GN (2005) Plant diseases caused by prokaryotes: bacteria and mollicutes. Plant Pathology, 5th edn. Elsevier Academic Press, New York, pp 616–704Google Scholar
  3. Aly AH, Debbab A, Kjer J, Proksch P (2010) Fungal endophytes from higher plants: a prolific source of phytochemicals and other bioactive natural products. Fungal Divers 41:1–16CrossRefGoogle Scholar
  4. Amman RI, Ludwig W, Sckleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169Google Scholar
  5. Antoninka A, Wolf JE, Bowker M et al (2009) Linking above- and belowground responses to global change at community and ecosystem scales. Glob Change Biol 15:914–929CrossRefGoogle Scholar
  6. Antoninka A, Reich PB, Johnson NC (2011) Seven years of carbon dioxide enrichment, nitrogen fertilization and plant diversity influence arbuscular mycorrhizal fungi in a grassland ecosystem. New Phytol 192:200–214PubMedCrossRefPubMedCentralGoogle Scholar
  7. Arnold AE (2005) Diversity and ecology of fungal endophytes in tropical forests. In: Current trends in mycological research. IBH Publishing Co. Pvt. Ltd., New Delhi, pp 49–68Google Scholar
  8. Arnold AE (2007) Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fungal Biol Rev 21:51–66CrossRefGoogle Scholar
  9. Arnold AE (2008) Endophytic fungi: hidden components of tropical community ecology. In: Carson WP, Schnitzer SA (eds) Tropical forest community ecology. Wiley, Oxford, pp 254–271Google Scholar
  10. Arnold AE, Herre EA (2003) Canopy cover and leaf age affect colonization by tropical fungal endophytes: ecological patterns and process in Theobroma cacao (Malvaceae). Mycologia 95:388–398PubMedPubMedCentralCrossRefGoogle Scholar
  11. Arnold AE, Lutzoni F (2007) Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88:541–549PubMedPubMedCentralCrossRefGoogle Scholar
  12. Arnold AE, Maynard Z, Gilbert GS et al (2000) Are tropical fungal endophytes hyperdiverse? Ecol Lett 3:267–274CrossRefGoogle Scholar
  13. Arnold AE, Mejia LC, Kyllo D et al (2003) Fungal endophytes limit pathogen damage in a tropical tree. P Natl Acad Sci USA 100:15649–15654CrossRefGoogle Scholar
  14. Augspurger CK (1983) Seed dispersal of the tropical tree, Platypodium elegans, and the escape of its seedlings from fungal pathogens. J Ecol 71:759–771CrossRefGoogle Scholar
  15. Augspurger CK (1984) Pathogen mortality of tropical tree seedlings: a comparative study of growth and survival. J Ecol 72:777–795CrossRefGoogle Scholar
  16. Augspurger CK, Kelly CK (1984) Pathogen mortality of tropical tree seedlings: experimental studies of the effects of dispersal distance, seedling density, and light conditions. Oecologia 61:211–217PubMedCrossRefPubMedCentralGoogle Scholar
  17. Azevedo JL, Araujo WL, Lacava PT (2016) The diversity of citrus endophytic bacteria and their interactions with Xylella fastidiosa and host plants. Genet Mol Biol 39:476–491PubMedPubMedCentralCrossRefGoogle Scholar
  18. Bagchi R, Gallery RE, Gripenberg S et al (2014) Pathogens and insect herbivores drive rainforest plant diversity and composition. Nature 506:85–88PubMedCrossRefPubMedCentralGoogle Scholar
  19. Bahram M, Polme S, Koljalg U et al (2012) Regional and local patterns of ectomycorrhizal fungal diversity and community structure along an altitudinal gradient in the Hyrcanian forests of northern Iran. New Phytol 193:465–473PubMedCrossRefPubMedCentralGoogle Scholar
  20. Bajo J, Santamaria O, Diez JJ (2008) Cultural characteristics and pathogenicity of Pestalotiopsis funera on Cupressus arizonica. Forest Pathol 38:263–274CrossRefGoogle Scholar
  21. Bakker PA, Doornbos RF, Zamioudis C et al (2013) Induced systemic resistance and the rhizosphere microbiome. Plant Pathology J 29:136–143CrossRefGoogle Scholar
  22. Baldani J, Caruso L, Baldani VLD et al (1997) Recent advances in BNF with non-legume plants. Soil Biol Biochem 29:911–922CrossRefGoogle Scholar
  23. Barbieri E, Potenza L, Rossi I et al (2000) Phylogenetic characterization and in situ detection of Cytophaga-Flexibacter-Bacteroides phylogroup bacterium in Tuber borchii Vittad. Ectomycorrhizal mycelium. Appl Environ Microb 66:5035–5042CrossRefGoogle Scholar
  24. Bargabus RL, Zidack NK, Sherwood JE, Jacobsen BJ (2002) Characterization of systemic resistance in sugar beet elicited by a non-pathogenic, phyllosphere-colonizing Bacillus mycoides, biological control agent. Physiol Mol Plant P 61:289–298CrossRefGoogle Scholar
  25. Bargabus RL, Zidack NK, Sherwood JE, Jacobsen BJ (2004) Screening for the identification of potential biological control agents that induce systemic resistance in sugar beet. Biol Control 30:342–350CrossRefGoogle Scholar
  26. Barone JA (1998) Host-specificity of folivorous insects in a moist tropical forest. J Anim Ecol 67:400–409CrossRefGoogle Scholar
  27. Bashan Y, Okon Y (1981) Inhibition of seed germination and development of tomato plants in soil infested with Pseudomonas tomato. Ann Appl Biol 98:413–417CrossRefGoogle Scholar
  28. Beattie GA, Lindow SE (1995) The secret life of foliar bacterial pathogens on leaves. Annu Rev Phytopathol 33:145–172PubMedCrossRefPubMedCentralGoogle Scholar
  29. Beattie GA, Lindow SE (1999) Bacterial colonization of leaves: a spectrum of strategies. Phytopathology 89:353–359PubMedCrossRefPubMedCentralGoogle Scholar
  30. Benitez-Malvido J, Garcia-Guzman G, Kossmann-Ferraz ID (1999) Leaf-fungal incidence and herbivory on tree seedlings in tropical rainforest fragments: an experimental study. Biol Conserv 91:143–150CrossRefGoogle Scholar
  31. Berdy J (2005) Bioactive microbial metabolites. J Antibiot 58:1–26PubMedCrossRefPubMedCentralGoogle Scholar
  32. Berdy J (2012) Thoughts and facts about antibiotics: where we are now and where we are heading. J Antibiot 65:385–395PubMedCrossRefPubMedCentralGoogle Scholar
  33. Berg G (2009) Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Tech 84:11–18CrossRefGoogle Scholar
  34. Bertaux J, Schmid M, Hutzler P et al (2005) Occurrence and distribution of endobacteria in the plant-associated mycelium of the ectomycorrhizal fungus Laccaria bicolor S238N. Environ Microbiol 7:1786–1795PubMedCrossRefPubMedCentralGoogle Scholar
  35. Bever JD, Dickie IA, Facelli E et al (2010) Rooting theories of plant community ecology in microbial interactions. Trends Ecol Evol 25:468–478PubMedPubMedCentralCrossRefGoogle Scholar
  36. Bhore SJ, Ravichanter N, Loh CY (2010) Screening of endophytic bacteria isolated from leaves of Sambung Nyawa [Gynura procumbens (Lour.) Merr.] for cytokinin-like compounds. Bioinformation 5:191–196PubMedPubMedCentralCrossRefGoogle Scholar
  37. Bianciotto V, Bandi C, Minerdi D et al (1996) An obligately endosymbiotic mycorrhizal fungus itself harbors obligately intracellular bacteria. Appl Environ Microb 62:3005–3010Google Scholar
  38. Bianciotto V, Lumini E, Bonfante P, Vandamme P (2003) ‘Candidatus Glomeribacter gigasporarum’ gen nov., sp. nov., an endosymbiont of arbuscular mycorrhizal fungi. Int J Syst Evol Microbiol 53:121–124PubMedCrossRefPubMedCentralGoogle Scholar
  39. Bianciotto V, Genre A, Jargeat P et al (2004) Vertical transmission of endobacteria in the arbuscular mycorrhizal fungus Gigaspora margarita through generation of vegetative spores. Appl Environ Microb 70:3600–3608CrossRefGoogle Scholar
  40. Biruma M, Pillay M, Tripathi L et al (2007) Banana Xanthomonas wilt: a review of the disease, management strategies and future research directions. Afr J Biotechnol 6:953–962Google Scholar
  41. Bittleston LS, Brockmann F, Wcislo W, Van Bael SA (2011) Endophytic fungi reduce leaf-cutting ant damage to seedlings. Biol Letters 7:30–32CrossRefGoogle Scholar
  42. Blanton CM, Ewel JJ (1985) Leaf-cutting ant herbivory in successional and agricultural tropical ecosystems. Ecology 66:861–869CrossRefGoogle Scholar
  43. Bonfante P, Anca IA (2009) Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annu Rev Microbiol 63:363–383PubMedCrossRefPubMedCentralGoogle Scholar
  44. Borstler B, Renker C, Kahmen A, Buscot F (2006) Species composition of arbuscular mycorrhizal fungi in two mountain meadows with differing management types and levels of plant biodiversity. Biol Fert Soils 42:286–298CrossRefGoogle Scholar
  45. Bove JM, Ayres AJ (2007) Etiology of three recent diseases of citrus in Sao Paulo State: sudden death, variegated chlorosis and huanglongbing. IUBMB Life 59:346–354PubMedCrossRefPubMedCentralGoogle Scholar
  46. Brader G, Compant G, Mitter B et al (2014) Metabolic potential of endophytic bacteria. Curr Opin Biotech 27:30–37PubMedPubMedCentralCrossRefGoogle Scholar
  47. Brader G, Compant S, Vescio K et al (2017) Ecology and genomic insights into plant-pathogenic and plant-nonpathogenic endophytes. Annu Rev Phytopathol 55:61–83PubMedCrossRefPubMedCentralGoogle Scholar
  48. Brotman Y, Lisec J, Meret M (2012) Transcript and metabolite analysis of the Trichoderma-induced systemic resistance response to Pseudomonas syringae in Arabidopsis thaliana. Microbiology 158:139–146PubMedCrossRefPubMedCentralGoogle Scholar
  49. Brown JKM, Hovmoller MS (2002) Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297:537–541PubMedCrossRefPubMedCentralGoogle Scholar
  50. Buee M, Reich M, Murat C, Morin E, Nilsson RH, Uroz S, Martin F (2009) 454 pyrosequencing analysis of forest soils reveal an unexpectedly high fungal diversity. New Phytol 184:449–456PubMedCrossRefPubMedCentralGoogle Scholar
  51. Burrows RL, Pflegar FL (2002a) Host responses to AMP from plots differing in plant diversity. Plant Soil 240:169–180CrossRefGoogle Scholar
  52. Burrows RL, Pflegar FL (2002b) Arbuscular mycorrhizal fungi respond to increasing plant diversity. Can J Bot 80:120–130CrossRefGoogle Scholar
  53. Cannon PF, Simmons CM (2002) Diversity and host preference of leaf endophytic fungi in the Iwokrama Forest Reserve. Guyana, Mycologia 94:210–220CrossRefGoogle Scholar
  54. Cannon PF, Damm U, Johnston PR, Weir BS (2012) Colletotrichum- current status and future directions. Stud Mycol 73:181–213PubMedPubMedCentralCrossRefGoogle Scholar
  55. Cao X, Xu X, Che H, West JS, Luo D (2017) Distribution and fungicide sensitivity of species complexes from rubber tree in Hainan, China. Plant Dis PDIS-03-17-0352Google Scholar
  56. Carney KM, Matson PA, Bohannan JM (2004) Diversity and composition of tropical soil nitrifiers across a plant diversity gradient and among land-use types. Ecol Lett 7:684–694CrossRefGoogle Scholar
  57. Carrell AA, Frank AC (2014) Pinus flexilis and Picea engelmannii share a sample and consistent needle endophyte microbiota and a potential role in nitrogen fixation. Fron Microbiol 5:333Google Scholar
  58. Carrell AA, Frank AC (2015) Bacterial endophyte communities in the foliage of coast redwood and giant sequoia. Front Microbiol 6:1008PubMedPubMedCentralCrossRefGoogle Scholar
  59. Carson WP, Anderson J, Leigh EG Jr, Schnitzer SA (2008) Challenges associated with testing and falsifying the Janzen-Connell Hypothesis: a review and critique. In: Carson WP, Schnitzer SA (eds) Tropical forest community ecology. Wiley, Oxford, pp 210–241Google Scholar
  60. Castro RA, Quecine MC, Lacava PT et al (2014) Isolation and enzyme bioprospection of endophytic bacteria associated with plants of Brazilian mangrove ecosystem. Springer Plus 3:382PubMedPubMedCentralCrossRefGoogle Scholar
  61. Chapman JW, Reynolds DR, Wilson K (2015) Long-range seasonal migration in insects: mechanisms, evolutionary drivers and ecological consequences. Ecol Lett 18:287–302PubMedCrossRefPubMedCentralGoogle Scholar
  62. Chave J (2004) Neutral theory and community ecology. Ecol Lett 7:241–253CrossRefGoogle Scholar
  63. Chen X, Tang J, Fang Z, Shimizu K (2004) Effects of weed communities with various species numbers on soil features in a subtropical orchard ecosystem. Agr Ecosyst Environ 102:377–388CrossRefGoogle Scholar
  64. Cherrett JM (1968) Foraging behaviour of Atta cephalotes L. (Hymenoptera, Formicadae). J Anim Ecol 37:387–403CrossRefGoogle Scholar
  65. Chesson P (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Evol S 31:343–366CrossRefGoogle Scholar
  66. Christian N, Whitaker BK, Clay K (2015) Microbiomes: unifying animal and plant systems through the lens of community ecology theory. Front Microbiol 6:1–15CrossRefGoogle Scholar
  67. Christian N, Whitaker BK, Clay K (2017a) A novel framework for decoding fungal endophyte diversity. In: Dighton J, White JF (eds) The fungal community: its organization and role in the ecosystem, 4th edn. CRC Press, Boca Raton, pp 65–78Google Scholar
  68. Christian N, Herre EA, Mejia LC, Clay K (2017b) Exposure to the leaf litter microbiome of healthy adults protects seedlings from pathogen damage. Proc R Soc B 284:20170641PubMedCrossRefPubMedCentralGoogle Scholar
  69. Chung H, Zak DR, Reich PB, Ellsworth DS (2007) Plant species richness, elevated CO2, and atmospheric nitrogen deposition alter soil microbial community composition and function. Glob Change Biol 13:980–989CrossRefGoogle Scholar
  70. Clark DB, Clark DA (1985) Seedling dynamics of a tropical tree: impacts of herbivory and meristem damage. Ecology 66:1884–1892CrossRefGoogle Scholar
  71. Clark DB, Clark DA, Read JM (1998) Edaphic variation and the mesoscale distribution of tree species in a neotropical rain forest. J Ecol 86:101–112CrossRefGoogle Scholar
  72. Clay K (1989) Clavicipitaceous endophytes of grasses: their potential as biocontrol agents. Mycol Res 92:1–12CrossRefGoogle Scholar
  73. Clay K, Holah J (1999) Fungal endophyte symbiosis and plant diversity in successional fields. Science 285:1742–1744PubMedCrossRefPubMedCentralGoogle Scholar
  74. Clay K, Schardl C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160:S99–S127PubMedPubMedCentralCrossRefGoogle Scholar
  75. Coblentz KE, Van Bael SA (2013) Field colonies of leaf-cutting ants select plant materials containing low abundances of endophytic fungi. Ecosphere 4:1–10CrossRefGoogle Scholar
  76. Coley PD, Barone JA (1996) Herbivory and plant defenses in tropical forests. Annu Rev Ecol Syst 27:305–335CrossRefGoogle Scholar
  77. Combes A, Ndoye I, Bance C et al (2012) Chemical communication between the endophyte fungus Paraconiothyrium variabile and the phytopathogen Fusarium oxysporum. PLoS ONE 7:e47313PubMedPubMedCentralCrossRefGoogle Scholar
  78. Comita LS, Muller-Landau HC, Aguilar S, Hubbell SP (2010) Asymmetric density dependence shapes species abundances in a tropical tree community. Science 329:330–332PubMedCrossRefPubMedCentralGoogle Scholar
  79. Comita LS, Queenborough SA, Murphy SJ et al (2014) Testing predictions of the Janzen-Connell hypothesis: a meta-analysis of experimental evidence for distance- and density-dependent seed and seedling survival. J Ecol 102:845–856PubMedPubMedCentralCrossRefGoogle Scholar
  80. Compant S, Clement C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678CrossRefGoogle Scholar
  81. Condit R, Ashton PS, Baker P et al (2000) Spatial patterns in the distribution of tropical tree species. Science 288:1414–1418PubMedCrossRefPubMedCentralGoogle Scholar
  82. Connell JH (1971) On the role of natural enemies in preventing competitive exclusion in some marine nimals and in rain forest trees. In: J. den Boer P, Gradwell GR (eds) Dynamics of populations. Center for Agricultural Publishing and Documentation, Wageningen, Netherlands, pp 298–312Google Scholar
  83. Curl EA, Truelove B (2012) The rhizosphere, 12th edn. Springer, BerlinGoogle Scholar
  84. Dalla Santa OR, Hernandez RF, Alvarez GLM (2004) Azospirillium sp. Inoculation in wheat, barley and oats seeds greenhouse experiments. Braz Arch Biol Tech 47:843–850CrossRefGoogle Scholar
  85. Dashiff A, Junka RA, Libera M, Kadouri DE (2011) Predation of human pathogens by the predatory bacteria Micavibrio aeruginosavorus and Bdellovibrio bacteriovorus. Journal of Appl Microbiol 110(2):431–444PubMedCrossRefPubMedCentralGoogle Scholar
  86. Davies PJ (2010) Plant hormones; their nature, occurrence, and function. Springer, DordrechtCrossRefGoogle Scholar
  87. De Bary A (1866) Morphologie und Physiologie der Pilze, Flechten, und Myxomyceten. Hofmeister’s Handbook of Physiological Botany. Vol II, Engelmannm, Leipzig, GermanyGoogle Scholar
  88. Dean R, Van Kan JA, Pretorius ZA et al (2012) The top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430PubMedCrossRefPubMedCentralGoogle Scholar
  89. Denance N, Sanchez-Vallet A, Goffner D, Molina A (2013) Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs. Front Plant Sci 4:155PubMedPubMedCentralCrossRefGoogle Scholar
  90. Desiro A, Faccio A, Kaech A et al (2015) Endogone, one of the oldest plant-associated fungi, host unique Mollicutes-related endobacteria. New Phytol 205:1464–1472PubMedCrossRefPubMedCentralGoogle Scholar
  91. Desoignies N, Schramme F, Ongena M, Legreve A (2013) Systemic resistance induced by Bacillus lipopeptides in Beta vulgaris reduces infection by the Rhizomania disease vector Polymyxa betae. Mol Plant Pathol 14:416–421PubMedCrossRefPubMedCentralGoogle Scholar
  92. Dixon RA (2001) Natural products and plant disease resistance. Nature 411:843–847PubMedCrossRefPubMedCentralGoogle Scholar
  93. Duffy JE, Godwin CM, Cardinale BJ (2017) Biodiversity effects in the wild are common and as strong as key drivers of productivity. Nature 549:261–264PubMedCrossRefPubMedCentralGoogle Scholar
  94. Edwards J, Johnson C, Santos-Medllin C et al (2015) Structure, variation, and assembly of the root- associated microbiomes of rice. P Natl Acad Sci USA 112:E911–E920CrossRefGoogle Scholar
  95. Eisenhauer N, Milcu A, Sabais AC et al (2011) Plant diversity surpasses plant functional groups and plant productivity as driver of soil biota in the long term. PLoS ONE 6:e16055PubMedPubMedCentralCrossRefGoogle Scholar
  96. Eisenhauer N, Dobies T, Cesarz S et al (2013) Plant diversity effects on soil food webs are stronger than those of elevated CO2 and N deposition in a long-term grassland experiment. P Natl Acad Sci USA 110:6889–6894CrossRefGoogle Scholar
  97. Ellis JG, Rafiqi M, Gan P et al (2009) Recent progress in discovery and functional analysis of effector proteins of fungal and oomycete plant pathogens. Curr Opin Plant Biol 12:399–405PubMedCrossRefPubMedCentralGoogle Scholar
  98. Estrada C, Wcislo WT, Van Bael SA (2013) Symbiotic fungi alter plant chemistry that discourages leaf-cutting ants. New Phytol 198:241–251PubMedCrossRefPubMedCentralGoogle Scholar
  99. Estrada C, Degner EC, Rojas EI et al (2015) The role of endophyte diversity in protecting plants from defoliation by leaf-cutting ants. Curr Sci 109:55–61Google Scholar
  100. Faeth SH, Saari S (2012) Fungal grass endophytes and arthropod communities: lessons from plant defence theory and multitrophic interactions. Fung Ecol 5:364–371CrossRefGoogle Scholar
  101. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. P Natl Acad Sci USA 103:626–631CrossRefGoogle Scholar
  102. Fierer N, Breitbart M, Nulton J et al (2007a) Metagenomic and small-subunit rRNA analyses reveal the genetic diversity of bacteria, Archaea, fungi, and viruses in soil. Appl Environ Microb 73:7059–7066CrossRefGoogle Scholar
  103. Fierer N, Bradford MA, Jackson RB (2007b) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364PubMedCrossRefPubMedCentralGoogle Scholar
  104. Flores-Sanchez IJ, Verpoorte R (2009) Plant polyketide synthases: a fascinating group of enzymes. Plant Physiol Bioch 47:167–174CrossRefGoogle Scholar
  105. Frampton RA, Pitman AR, Fineran PC (2012) Advances in bacteriophage-mediated control of plant pathogens. Int J Microbiol 2012:326452PubMedPubMedCentralCrossRefGoogle Scholar
  106. Frank AC, Saldierna Guzman JP, Shay JE (2017) Transmission of bacterial endophytes. Microorganisms 5:70Google Scholar
  107. Frohlich J, Hyde KD (1999) Biodiversity of palm fungi in the tropics: are global fungal diversity estimates realistic? Biodivers Conserv 8:977–1004CrossRefGoogle Scholar
  108. Gaiero JR, McCall CA, Thompson KA et al (2013) Inside the root microbiome: bacterial root endophytes and plant growth promotion. Am J Bot 100:1738–1750PubMedCrossRefPubMedCentralGoogle Scholar
  109. Gamboa MA, Bayman P (2001) Communities of endophytic fungi in leaves of a tropical timber tree Guarea Guidonia: Meliaceae) 1. Biotropica 33:352–360CrossRefGoogle Scholar
  110. Gamboa MA, Laureano S, Bayman P (2003) Measuring diversity of endophytic fungi in leaf fragments: does size matter? Mycopathologia 156:41–45CrossRefGoogle Scholar
  111. Ganley RJ, Newcombe G (2006) Fungal endophytes in seeds and needles of Pinus monticola. Mycol Res 110:318–327PubMedCrossRefPubMedCentralGoogle Scholar
  112. Gans J, Wolinsky M, Dunbar J (2005) Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309:1387–1390PubMedCrossRefPubMedCentralGoogle Scholar
  113. Gao C, Shi NN, Liu YX et al (2013) Host plant genus-level diversity is the best predictor of ectomycorrhizal fungal diversity in a Chinese subtropical forest. Mol Ecol 22:3403–3414PubMedCrossRefPubMedCentralGoogle Scholar
  114. Gao C, Shi NN, Chen L et al (2017) Relationships between soil fungi and woody plant assemblages differ between ridge and valley habitats in a subtropical mountain forest. New Phytol 213:1874–1885PubMedCrossRefPubMedCentralGoogle Scholar
  115. Garbeva P, Potsma J, Van Veen JA, Van Elas JD (2006) Effect of above-ground plant species on soil microbial community structure and its impact on suppression of Rhizoctonia solani AG3. Environm Microbiol 8:233–246CrossRefGoogle Scholar
  116. Garcia-Guzman G, Dirzo R (2001) Patterns of leaf-pathogen infection in the understory of a Mexican rain forest: incidence, spatiotemporal variation, and mechanisms of infection. Am J Bot 88:634–645PubMedCrossRefPubMedCentralGoogle Scholar
  117. Gaume L, McKey D, Terrin S (1998) Ant-plant-homopteran mutualism: how the third partner affects the interaction between a plant-specialist ant and its myrmecophyte host. P Roy Soc B-Biol Sci 265:569–575CrossRefGoogle Scholar
  118. Gayathri S, Saravanan D, Radhakrishnan M, Balagurunathan R, Kathiresan K (2010) Bioprospecting potential of fast growing endophytic bacteria from leaves of mangrove and salt-marsh plant species. Indian J Biotechnol 9:397–402Google Scholar
  119. Gentry AH (1988) Changes in plant community diversity and floristic composition on environmental and geographical gradients. Ann Mo Bot Gard 75:1–34CrossRefGoogle Scholar
  120. Gilbert GS (1995) Rain forest plant diseases: the canopy-understory connection. Selbyana 15:75–77Google Scholar
  121. Gilbert GS (2005) Dimensions of plant disease in tropical forests. In: Burslem DFRP, Pinard MA, Hartley SE (eds) Biotic interactions in the tropics. Cambridge University Press, Cambridge, pp 141–164CrossRefGoogle Scholar
  122. Gilbert GS, De Steven D (1996) A canker disease of seedlings and saplings of Tetragastris panamensis (Burseraceae) caused by Botryosphaeria dothidea in a lowland tropical forest. Plant Dis 80:684–687CrossRefGoogle Scholar
  123. Gilbert GS, Reynolds DR (2005) Nocturnal fungi: airborne spores in the canopy and understory of a tropical rain forest. Biotropica 37:462–464CrossRefGoogle Scholar
  124. Gilbert GS, Webb CO (2007) Phylogenetic signal in plant-pathogenic host range. P Natl Acad Sci USA 104:4979–4983CrossRefGoogle Scholar
  125. Gilbert GS, Foster RB, Hubbell SP (1994) Density and distance-to-adult effects of a canker disease of trees in a moist tropical forest. Oecologia 98:100–108PubMedCrossRefPubMedCentralGoogle Scholar
  126. Gilbert GS, Harms KE, Hamill DN, Hubbell SP (2001) Effects of seedling size, El Nino drought, seedling density, and distance to nearest conspecific adult on 6-year survival of Ocotea whitei seedlings in Panama. Oecologia 127:1502–1507CrossRefGoogle Scholar
  127. Gillet JB (1962) Pest pressure, an underestimated factor in evolution. In: Systematics Association Publication no. 4, Taxonomy and Geography, pp 37–46Google Scholar
  128. Giraldo MC, Valent B (2013) Filamentous plant pathogen effectors in action. Nat Rev Microbiol 11:800–814PubMedCrossRefPubMedCentralGoogle Scholar
  129. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytoapthol 43:205–227CrossRefGoogle Scholar
  130. Gottwald TR, Irey M (2007) Post-hurricane analysis of citrus canker II: predictive model estimation of disease spread and area potentially impacted by various eradication protocols following catastrophic weather events. Plant Health Progress. Scholar
  131. Gottwald TR, Graham JH, Schubert TS (2002) Citrus canker: the pathogen and its impact. Plant Health Progress. Scholar
  132. Gourion B, Berrabah F, Ratet P, Stacey G (2015) Rhizobium-legume symbioses: the crucial role of plant immunity. Trends Plant Sci 20:186–194PubMedCrossRefPubMedCentralGoogle Scholar
  133. Graham JH, Gottwald TR, Cubero J, Achor DS (2004) Xanthomonas axonopodis pv.citri: factors affecting successful eradication of citrus canker. Mol Plant Pathol 5:1–15PubMedCrossRefPubMedCentralGoogle Scholar
  134. Griffin EA (2016) The greater unseen: on the identities, distributions, and impacts of foliar bacteria on tropical arboreal species. PhD thesis, University of Pittsburgh, PittsburghGoogle Scholar
  135. Griffin EA, Carson WP (2015) The ecology and natural history of foliar bacteria with a focus on tropical forests and agroecosystems. Bot Rev 81:105–149CrossRefGoogle Scholar
  136. Griffin EA, Traw MB, Morin PJ et al (2016) Foliar bacteria and soil fertility mediate seedling performance: a new and cryptic dimension of niche differentiation. Ecology 97:2998–3008PubMedCrossRefPubMedCentralGoogle Scholar
  137. Griffin EA, Wright SJ, Morin PJ, Carson WP (2017) Pervasive interactions between foliar microbes and soil nutrients mediate leaf production and herbivore damage in a tropical forest. New Phytol 216:99–112PubMedCrossRefPubMedCentralGoogle Scholar
  138. Gunatilaka AL (2006) Natural products from plant-associated microorganisms: distribution, structural diversity, bioactivity, and implications of their occurrence. J Nat Prod 69:509–526PubMedPubMedCentralCrossRefGoogle Scholar
  139. Gutierrez-Manero FJ, Ramos-Solano B, Probanza A et al (2001) The plant-growth-promoting rhizobacteria Bacillus pumilus and Bacillus licheniformis produce high amounts of physiologically active gibberellins. Physiol Plant 111:206–211CrossRefGoogle Scholar
  140. Hallmann J, Quadt-Hallmann A, Mahaffee WF, Kloepper JW (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43:895–914CrossRefGoogle Scholar
  141. Hamilton AJ, Basset Y, Benke KK et al (2010) Quantifying uncertainty in estimation of tropical arthropod species richness. Am Nat 176:90–95PubMedCrossRefPubMedCentralGoogle Scholar
  142. Hammer TJ, Van Bael SA (2015) An endophyte-rich diet increases ant predation on a specialist herbivorous insect. Ecol Entomol 40:316–321CrossRefGoogle Scholar
  143. Hardoim PR, van Overbeek LS, van Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471PubMedPubMedCentralCrossRefGoogle Scholar
  144. 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 Mol Biol R 79:293–320CrossRefGoogle Scholar
  145. Harms KE, Condit R, Hubbell SP, Foster RB (2001) Habitat associations of trees and shrubs in a 50- ha Neotropical forest plot. J Ecol 89:947–959CrossRefGoogle Scholar
  146. Hausmann NT, Hawkes CV (2009) Plant neighborhood control of arbuscular mycorrhizal community composition. New Phytol 183:1188–1200PubMedCrossRefPubMedCentralGoogle Scholar
  147. He J, Tedersoo L, Hu A et al (2017) Greater diversity of soil fungal communities and distinguishable seasonal variation in temperate deciduous forests compared with subtropical evergreen forests of eastern China. FEMS Microbiol Ecol 93:fix069Google Scholar
  148. Hedin LO, Brookshire EJ, Menge DN, Barron AR (2009) The nitrogen paradox in tropical forest ecosystems. Annu Rev of Ecol Evol S 40:613–635CrossRefGoogle Scholar
  149. Heil M, McKey D (2003) Protective ant-plant interactions as model systems in ecological and evolutionary research. Annu Rev Ecol Evol S 34:425–553CrossRefGoogle Scholar
  150. Henis Y, Bashan Y (1986) Epiphytic survival of bacterial leaf pathogens. In: Fokkema NJ, van den Heuvel J (eds) Microbiology of the phyllosphere. Cambridge University Press, New York, pp 252–268Google Scholar
  151. Higgins KL, Arnold AE, Miadlikowska J et al (2007) Phylogenetic relationships, host affinity, and geographic structure of boreal and arctic endophytes from three major plant lineages. Mol Phylogenet Evol 42:543–555PubMedPubMedCentralCrossRefGoogle Scholar
  152. Hiiesalu I, Partel M, Davidson J et al (2014) Species richness of arbuscular mycorrhizal fungi: associations with grasslands plant richness and biomass. New Phytol 203:233–244PubMedCrossRefPubMedCentralGoogle Scholar
  153. Hiiesalu I, Bahram M, Tedersoo L (2017) Plant species richness and productivity determine the diversity of soil fungal guilds in temperate coniferous forest and bog habitats. Mol Ecol 26:4846–4858CrossRefPubMedPubMedCentralGoogle Scholar
  154. Hill DS, Waller JM (1982) Pests and disease of tropical crops. Longman, LondonGoogle Scholar
  155. Hodgson S, Cates C, Hodgson J et al (2014) Vertical transmission of fungal endophytes is widespread in forbs. Ecol Evol 4:1199–1208PubMedPubMedCentralCrossRefGoogle Scholar
  156. Hoffman MT, Gunatilaka MK, Wijeratne K et al (2013) Endohyphal bacterium enhances production of indole-3-acetic acid by a foliar fungal endophyte. PLoS ONE 8:e73132PubMedPubMedCentralCrossRefGoogle Scholar
  157. Holldobler B, Wilson EO (2010) The leafcutter ants: civilization by instinct. WW Norton and Company Inc, New YorkGoogle Scholar
  158. Hooper DU, Bignell DE, Brown VK et al (2000) Interactions between aboveground and belowground biodiversity in terrestrial ecosystems: patterns, mechanisms, and feedbacks: we assess the evidence for correlation between aboveground and belowground diversity and conclude that a variety of mechanisms could lead to positive, negative, or no relationship-developing on the strength and type of interactions among species. AIBS Bulletin 50:1049–1061Google Scholar
  159. Horn S, Hempel S, Verbruggen E et al (2017) Linking the community structure of arbuscular mycorrhizal fungi and plants: a story of interdependence? ISME J 11:1400–1411PubMedPubMedCentralCrossRefGoogle Scholar
  160. Horst RK (1990) Westcott’s plant disease handbook, 5th edn. Chapman and Hall, New YorkCrossRefGoogle Scholar
  161. Hubbell SP (2001) The unified theory of biogeography and biodiversity. University Press, PrincetonGoogle Scholar
  162. Hubbell SP, Foster RB, O’Brien ST et al (1999) Light-gap disturbances, recruitment limitation, and tree diversity in a neotropical forest. Science 283:554–557PubMedCrossRefPubMedCentralGoogle Scholar
  163. Hyde KD, Soytong K (2008) The fungal endophyte dilemma. Fungal Divers 163:e73Google Scholar
  164. Hyde KD, Cai L, McKenzie EHC et al (2009) Colletotrichum: a catalogue of confusion. Fungal Divers 39:1–17Google Scholar
  165. Innerebner G, Knief C, Vorholt JA (2011) Protection of Arabidopsis thaliana against leaf-pathogenic Pseudomonas syringae by Sphingomonas strains in a controlled model system. Appl Environ Microb 77:3202–3210CrossRefGoogle Scholar
  166. Irey M, Gottwald TR, Graham JH et al (2006) Post-hurricane analysis of citrus canker spread and progress towards the development of a predictive model to estimate disease spread due to catastrophic weather events. Plant Health Progress. Scholar
  167. Jaber LR, Vidal S (2010) Fungal endophyte negative effects on herbivory are enhanced on intact plants and maintained in a subsequent generation. Ecol Entomol 35:25–36CrossRefGoogle Scholar
  168. Jackson RW (2009) Plant pathogenic bacteria: genomic and molecular biology. Horizon Scientific PressGoogle Scholar
  169. Jackson RB, Mooney HA, Schulze ED (1997) A global budget for fine root biomass, surface area, and nutrient contents. P Natl Acad Sci USA 94:7362–7366CrossRefGoogle Scholar
  170. Janzen DH (1966) Coevolution of mutualism between ants and acacias in Central America. Evolution 20:249–275PubMedCrossRefPubMedCentralGoogle Scholar
  171. Janzen DH (1970) Herbivores and the number of tree species in tropical forests. Am Nat 104:501–528CrossRefGoogle Scholar
  172. Ji P, Wilson M (2002) Assessment of the importance of similarity in carbon source utilization profiles between the biological control agent and the pathogen in biological control of bacterial speck of tomato. Appl Environ Microb 68:4383–4389CrossRefGoogle Scholar
  173. Jiang RHY, Tyler BM (2012) Mechanisms and evolution of virulence in oomycetes. Annu Rev Phytopathol 50:295–318PubMedCrossRefPubMedCentralGoogle Scholar
  174. Johnson NC, Graham JH (2013) The continuum concept remains a useful framework for studying mycorrhizal functioning. Plant Soil 363:411–419CrossRefGoogle Scholar
  175. Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualist-parasitism continuum. New Phytol 135:575–585CrossRefGoogle Scholar
  176. Johnson D, Vandenkoornhuyse PJ, Leake JR et al (2003) Plant communities affect arbuscular mycorrhizal fungal diversity and community composition in grassland microcosms. New Phytol 161:503–515CrossRefGoogle Scholar
  177. Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329PubMedCrossRefPubMedCentralGoogle Scholar
  178. Kembel SW, O’Conner TK, Arnold HK et al (2014) Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest. P Natl Acad Sci USA 111:13715–13720CrossRefGoogle Scholar
  179. Kernaghan G, Widden P, Bergeron Y et al (2003) Biotic and biotic factors affecting ectomycorrhizal diversity in boreal mixed-woods. Oikos 102:497–504CrossRefGoogle Scholar
  180. Kitajima K, Augspurger CK (1989) Seed and seedling ecology of a monocarpic tropical tree, Tachigalia versicolor. Ecology 70:1102–1114CrossRefGoogle Scholar
  181. Kitajima K, Poorter L (2008) Functional basis for resource niche partitioning by tropical trees. In: Carson WP, Schnitzer SA (eds) Tropical Forest Community Ecology, pp 160–181Google Scholar
  182. Kivlin SN, Hawkes CV (2011) Differentiating between effects of invasion and diversity: impacts of aboveground plant communities on belowground fungal communities. New Phytol 189:526–535PubMedCrossRefPubMedCentralGoogle Scholar
  183. Kivlin SN, Hawkes CV (2016a) Tree species, spatial heterogeneity, and seasonality drive soil fungal abundance, richness, and composition in Neotropical rainforests. Environ Microbiol 18:4662–4673PubMedCrossRefPubMedCentralGoogle Scholar
  184. Kivlin SN, Hawkes CV (2016b) Tree species, spatial heterogeneity, and seasonality drive soil fungal abundance, richness, and composition in Neotropical rainforests. Environm Microbiol 18:4662–4673CrossRefGoogle Scholar
  185. Kogel KH, Franken P, Huckelhoven R (2006) Endophyte or parasite—what decides? Curr Opin Plant Biol 9:358–363PubMedCrossRefPubMedCentralGoogle Scholar
  186. Konig S, Wubet T, Dormann CF et al (2010) TaqMan real-time PCR assays to assess arbuscular mycorrhizal responses to field manipulation of grassland biodiversity: effects of soil characteristics, plant species richness, and functional traits. Appl Environ Microbiol 76:3765–3775PubMedPubMedCentralCrossRefGoogle Scholar
  187. Kowalchuk GA, Buma DS, de Boer W et al (2002) Effects of above-ground plant species composition and diversity on the diversity of soil-borne microorganisms. Antonie Van Leeuwenhoek 815:509–520CrossRefGoogle Scholar
  188. Krugner R, Lopes MDC, Santos JD et al (2000) Transmission efficiency of Xylella fastidiosa to citrus by sharpshooters and identification of two new vector species. In: Conference of international organization of citrus virologists, vol 14, p 423Google Scholar
  189. Kuldau G, Bacon C (2008) Clavivipitaceous endophytes: their ability to enhance resistance of grasses to multiple stresses. Biol Control 46:57–71CrossRefGoogle Scholar
  190. Kuzyakov Y, Domanski G (2000) Carbon input by plants into the soil. J Plant Nutr Soil Sci 163:421–431CrossRefGoogle Scholar
  191. Laforest-Lapointe I, Paquette A, Messier C, Kembel SW (2017) Leaf bacterial diversity mediates plant diversity and ecosystem function relationships. Nature 546:145–147PubMedCrossRefPubMedCentralGoogle Scholar
  192. LaManna JA, Mangan SA, Alonso A et al (2017) Plant diversity increases with the strength of negative density dependence at the global scale. Science 356:1389–1392PubMedCrossRefPubMedCentralGoogle Scholar
  193. Lambais MR, Crowley DE, Cury JC et al (2006) Bacterial diversity in tree canopies of the Atlantic forest. Science 312:1917--1917CrossRefGoogle Scholar
  194. Lambais MR, Lucheta AR, Crowley DE (2014) Bacterial community assemblages associated with the phyllosphere, dermosphere, and rhizosphere of tree species of the Atlantic forest are host taxon dependent. Microb Ecol 68:567–574PubMedCrossRefPubMedCentralGoogle Scholar
  195. Lambais MR, Barrera SE, Santos EC et al (2017) Phyllosphere metaproteomes of trees from the Brazilian Atlantic forest show high levels of functional redundancy. Microb Ecol 73:123–134PubMedCrossRefPubMedCentralGoogle Scholar
  196. Landis FC, Gargas A, Givnish TJ (2004) Relationships among arbuscular mycorrhizal fungi, vascular plants and environmental conditions in oak savannas. New Phytol 164:493–504CrossRefGoogle Scholar
  197. Lange M, Eisenhauer N, Sierra CA et al (2015) Plant diversity increases soil microbial activity and soil carbon storage. Nature Comm 6:6707CrossRefGoogle Scholar
  198. Lefcheck JS, Byrnes JE, Isbell F et al (2015) Biodiversity enhances ecosystem multifunctionality across trophic levels and habitats. Nat Comm 6:6936CrossRefGoogle Scholar
  199. Lennon JT, Jones SE (2011) Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev Microbiol 9:119–130PubMedCrossRefPubMedCentralGoogle Scholar
  200. Lindow SE, Brandl MT (2003) Microbiology of the phyllosphere. Appl Environ Microb 69:1875–1883CrossRefGoogle Scholar
  201. Lindow SE, Desurmont C, Elkins R et al (1998) Occurrence of indole-3-acetic acid-producing bacteria on pear trees and their association with fruit russet. Phytopathology 88:1149–1157PubMedCrossRefPubMedCentralGoogle Scholar
  202. Llado S, Lopez-Mondejar R, Baldrian P (2017) Forest soil bacteria: diversity, involvement in ecosystem processes, and response to global change. Microbiol Mol Biol R 81:e00063--16CrossRefGoogle Scholar
  203. Lodge D, Hawksworth DL, Ritchie BJ (1996) Microbial diversity and tropical forest functioning. Biodiversity and ecosystem processes in tropical forests. Springer, Berlin Heidelberg, pp 69–100CrossRefGoogle Scholar
  204. Lopes JRS, Krugner R, Brown J (2016) Transmission ecology and epidemiology of the citrus variegated chlorosis strain of Xylella fastidiosa. In: Brown JK (ed) Vector-mediated transmission of plant pathogens. APS Press, pp 195–208Google Scholar
  205. Loranger-Merciris G, Barthes L, Gastine A, Leadley P (2006) Rapid effects of plant species diversity and identity on soil microbial communities in experimental grassland ecosystems. Soil Biol Biochem 38:2336–2343CrossRefGoogle Scholar
  206. Ludwig-Muller J (2015) Plants and endophytes: equal partners in secondary metabolite production? Biotechnol Lett 37:1325–1334PubMedCrossRefPubMedCentralGoogle Scholar
  207. Ma B, Hibbing ME, Kim H-S et al (2007) Host range and molecular phylogenies of the soft rot Enterobacterial genera Pectobacterium and Dickeya. Phytopathology 97:1150–1163PubMedCrossRefPubMedCentralGoogle Scholar
  208. Malcolm GM, Kuldau GA, Gugino BK, Jimenez-Gasco MDM (2013) Hidden host plant associations of soilbourne fungal pathogens: an ecological perspective. Phytopathology 103:538–544PubMedCrossRefPubMedCentralGoogle Scholar
  209. Mandyam KG, Roe J, Jumpponen A (2014) Mutualism-parasitism paradigm synthesized from results of root-endophyte models. Front Microbiol 5:776PubMedPubMedCentralGoogle Scholar
  210. Mangan SA, Schnitzer SA, Herre EA et al (2010) Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466:752–755PubMedCrossRefPubMedCentralGoogle Scholar
  211. Mansfield J, Genin S, Magori S et al (2012) Top 10 plant pathogenic bacteria in molecular plant pathology. Mol Plant Pathol 13:614–629PubMedCrossRefPubMedCentralGoogle Scholar
  212. Maor R, Haskin S, Levi-Kedmi H, Sharon A (2004) In planta production of indole-3-acetic acid by Colletotrichum gloeosporioides f. sp. aeschynomene. Appl Environ Microbiol 70:1852–1854PubMedPubMedCentralCrossRefGoogle Scholar
  213. Marcelino J, Giordano R, Gouli S et al (2008) Colletrtrichum acutatum var. fioriniae (telemorph: Glomerella acutata var. fioriniae var. nov.) infection of a scale insect. Mycologia 100:353–374PubMedCrossRefPubMedCentralGoogle Scholar
  214. Marquez SS, Bills GF, Herrero N, Zabalgogeazcoa I (2012) Non-systemic fungal endophytes of grasses. Fungal Endophyes 5:289–297CrossRefGoogle Scholar
  215. Mathimaran N, Ruh R, Jama B et al (2007) Impact of agricultural management on arbuscular mycorrhizal fungal communities in Kenyan ferralsol. Agr Ecosyst Environ 119:22–32CrossRefGoogle Scholar
  216. May RM (1988) How many species are there on earth? Science 241:1441–1449PubMedCrossRefPubMedCentralGoogle Scholar
  217. May RM (1990) How many species? Philos Trans Biol Sci 330:293–304CrossRefGoogle Scholar
  218. Mejia LC, Rojas EI, Maynard Z et al (2008) Endophytic fungi as biocontrol agents of Theobroma cacao pathogens. Biol Control 46:4–14CrossRefGoogle Scholar
  219. Mejia LC, Herre EA, Sparks JP et al (2014) Pervasive effects of a dominant foliar endophytic fungus on host genetic and phenotypic expression in a tropical tree. Front Microbiol 5:479PubMedPubMedCentralGoogle Scholar
  220. Mellotto M, Underwood W, Koczan J et al (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–980CrossRefGoogle Scholar
  221. Mellotto M, Underwood W, He SY (2008) Role of stomata in plant innate immunity and foliar bacterial diseases. Annu Rev Phytoapthol 46:101–122CrossRefGoogle Scholar
  222. Mercado-Blanco J, Prieto P (2012) Bacterial endophytes and root hairs. Plant Soil 361:301–306CrossRefGoogle Scholar
  223. Meyer KM, Leveau JHJ (2012) Microbiology of the phyllosphere: a playground for testing ecological concepts. Oecologia 168:621–629PubMedCrossRefPubMedCentralGoogle Scholar
  224. Milcu A, Allan E, Roscher C et al (2013) Functionally and phylogenetically diverse plant communities key to soil biota. Ecology 94:1878–1885PubMedCrossRefPubMedCentralGoogle Scholar
  225. Mirzaei J, Moradi M (2017) Relationships between flora biodiversity, soil physiochemical properties, and arbuscular mycorrhizal fungi (AMF) diversity in a semi-arid forest. Plant Ecol Evol 150(2):151–159CrossRefGoogle Scholar
  226. Mordecai EA (2011) Pathogen impacts on plant communities: unifying theory, concepts, and empirical work. Ecol Monogr 81:429–441CrossRefGoogle Scholar
  227. Morris CE, Monteil CL, Berge O (2013) The life history of Pseudomonas syringae: linking agriculture to earth system processes. Annu Rev Phytopathol 51:85–104PubMedCrossRefPubMedCentralGoogle Scholar
  228. Moyes AB, Kueppers LM, Pett-Ridge J et al (2016) Evidence of foliar endophytic nitrogen fixation in a widely distributed subalpine conifer. New Phytol 210:657–668PubMedCrossRefPubMedCentralGoogle Scholar
  229. Murali TS, Suryanarayanan TS, Geeta R (2006) Endophytic Phomopsis species: host range and implications for diversity estimates. Can J Microbiol 52:673–680PubMedPubMedCentralCrossRefGoogle Scholar
  230. Negus D, Moore C, Baker M, Raghunathan D, Tyson J, Sockett RE (2017) Killing Gram-negative pathogens in a host setting? Annu Rev Microbiol 71:441–457PubMedCrossRefPubMedCentralGoogle Scholar
  231. Newsham KK, Fitter AH, Watkinson AR (1994) Root pathogenic and arbuscular mycorrhizal fungi determine fecundity of asymptomatic plants in the field. J Ecol 82:805–814CrossRefGoogle Scholar
  232. Nisa H, Kamili AN, Nawchoo IA et al (2015) Fungal endophytes as prolific source of phytochemicals and other bioactive natural products: a review. Microb Pathogenesis 82:50–59CrossRefGoogle Scholar
  233. Nunan N, Daniell TJ, Singh BK et al (2005) Links between rhizoplane bacterial communities in grassland soils, characterized using molecular technologies. Appl Environm Microbiol 71:6784–6792CrossRefGoogle Scholar
  234. Ohm RA, Feau N, Henrissat B, Schoch CL, Horwitz BA, Barry KW, Condon BJ, Copeland AC, Dhillon B, Glaser F, Hesse SN (2012) Diverse lifestyles and strategies of plant pathogenesis encoded in the genomes of eighteen Dothideomycetes fungi. PLoS Pathog 8:e1003037PubMedPubMedCentralCrossRefGoogle Scholar
  235. Oliver TH, Heard MS, Isaac NJ et al (2015) Biodiversity and resilience of ecosystem functions. Trends Ecol Evol 11:673–684CrossRefGoogle Scholar
  236. Opik M, Moora M, Liira J, Zobel M (2006) Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. J Ecol 94:778–790CrossRefGoogle Scholar
  237. Pajares S, Bohannan BJ (2016) Ecology of nitrogen fixing, nitrifying, and denitrifying microorganisms in tropical forest soils. Front Microbiol 7:1045PubMedPubMedCentralGoogle Scholar
  238. Partida-Martinez LP, Hertweck C (2005) Pathogenic fungus harbours endosymbiotic bacteria for toxin production. Nature 437:884–888PubMedCrossRefPubMedCentralGoogle Scholar
  239. Partida-Martinez LP, Groth I, Schmitt I et al (2007a) Burkholderia rhizoxinica sp. nov. and Burkholderia endofungorum sp. nov., bacterial endosymbionts of the plant-pathogenic fungus Rhizopus microspores. Int J Syst Evol Micr 57:2583–2590CrossRefGoogle Scholar
  240. Partida-Martinez LP, Monajembashi S, Greulich K-O, Hertweck C (2007b) Endosymbiont-dependent host reproduction maintains bacterial-fungal mutualism. Curr Biol 17:773–777PubMedCrossRefPubMedCentralGoogle Scholar
  241. Pawlowski J, Audic S, Adl S et al (2012) CBOL protest working group: barcoding eukaryotic richness beyond the animal, plant, and fungal kingdoms. PLoS Biol 10:e1001419PubMedPubMedCentralCrossRefGoogle Scholar
  242. Peay KG, Kennedy PG, Davies SJ et al (2010) Potential link between plant and fungal distributions in a dipterocarp rainforest: community and phylogenetic structure of tropical ectomycorrhizal fungi across a plant and soil ecotone. New Phytol 185:529–542PubMedCrossRefPubMedCentralGoogle Scholar
  243. Peay KG, Baraloto C, Fine PV (2013) Strong coupling of plant and fungal community structure across western Amazonian rainforests. ISME J 7 (9):1852–1861PubMedPubMedCentralCrossRefGoogle Scholar
  244. Petrini O (1991) Fungal endophytes of tree leaves. Microbial ecology of leaves. Springer, New York, pp 179–197CrossRefGoogle Scholar
  245. Phillips RP, Finzi AC, Bernhardt ES (2011) Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol Lett 14:187–194PubMedCrossRefPubMedCentralGoogle Scholar
  246. Pieterse CM, Zamioudis C, Berendsen RL et al (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375PubMedCrossRefPubMedCentralGoogle Scholar
  247. Pineda A, Zheng SJ, van Loon JJ et al (2010) Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci 15:507–514PubMedCrossRefPubMedCentralGoogle Scholar
  248. Pires DP, Cleto S, Sillankorva S, Azaredo J, Lu TK (2016) Genetically engineered phages: a review of advances over the last decade. Microbiol Mol Biol Rev 80:523–543PubMedPubMedCentralCrossRefGoogle Scholar
  249. Porazinska DL, Bardgett RD, Blaauw MB et al (2003) Relationships at the above-ground-belowground interface: plants, soil biota, and soil processes. Ecol Monog 73:377–395CrossRefGoogle Scholar
  250. Porras-Alfaro A, Bayman P (2011) Hidden fungi, emergent properties: endophytes and microbiomes. Annu Rev Phytopathol 49:291–315PubMedPubMedCentralCrossRefGoogle Scholar
  251. Prober SM, Leff JW, Bates ST et al (2015) Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide. Ecol Lett 18:85–95PubMedCrossRefPubMedCentralGoogle Scholar
  252. Prusky D (1996) Pathogen quiescence in postharvest harvest. Annu Rev Phytol 34:413–434CrossRefGoogle Scholar
  253. Purcell AH, Finlay AH, McLean DL (1979) Pierce’s disease bacterium: mechanism of transmission by leafhopper vectors. Science 206:839–841PubMedCrossRefPubMedCentralGoogle Scholar
  254. Ramos Solano B, Barriuso Maicas J, Pereyra De La Iglesia MT et al (2008) Systemic disease protection elicited by plant growth promoting rhizobacteria strains: relationship between metabolic responses, systemic disease protection, and biotic elicitors. Phytopathology 98:451–457PubMedCrossRefPubMedCentralGoogle Scholar
  255. Redak RA, Purcell AH, Lopes JRS et al (2004) The biology of xylem fluid-feeding insect vectors of Xylella fastidiosa and their relation to disease epidemiology. Annu Rev Entomol 49:243–270PubMedCrossRefPubMedCentralGoogle Scholar
  256. Reinhold-Hurek B, Hurek T (1998) Life in grasses: diazotrophic endophytes. Trends Microbiol 6:139–144PubMedCrossRefPubMedCentralGoogle Scholar
  257. Robinson M, Riov J, Sharon A (1998) Indole-3-acetic acid biosynthesis in Colletotrichum gloeosporioides f. sp. aeschynomene. Appl Environ Microbiol 64:5030–5032PubMedPubMedCentralGoogle Scholar
  258. Rockwood LL (1976) Plant selection and foraging patterns in two species of leaf-cutting ants (Atta). Ecology 57:48–61CrossRefGoogle Scholar
  259. Rodriguez RJ, White JF Jr, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330PubMedPubMedCentralCrossRefGoogle Scholar
  260. Rojas EI, Rehner SA, Samuels GJ et al (2010) Colletotrichum gloeosporioides sl associated with Theobroma cacao and other plants in Panama: multilocus phylogenies distinguish host-associated pathogens from asymptomatic endophytes. Mycologia 102:1318–1338PubMedCrossRefPubMedCentralGoogle Scholar
  261. Rousk J, Baath E, Brookes PC et al (2010) Soil bacteria and fungal communities across a pH gradient in an arable soil. The ISME J 4:1340–1351PubMedCrossRefPubMedCentralGoogle Scholar
  262. Rudgers JA, Clay K (2007) Endophyte symbiosis with tall fescue: how strong are the impacts on communities and ecosystems? Fungal Biol Rev 21:107–124CrossRefGoogle Scholar
  263. Ryan RP, Vorholter FJ, Potnis N (2011) Pathogenomics of Xanthomonas: understanding bacterium-plant interactions. Nat Rev Microbiol 9:344–355PubMedCrossRefPubMedCentralGoogle Scholar
  264. Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev of Ecol S 29:319–343CrossRefGoogle Scholar
  265. Saikkonen K, Wali P, Helander M, Faeth SH (2004) Evolution of endophyte-plant symbioses. Trends Plant Sci 9:275–280PubMedCrossRefPubMedCentralGoogle Scholar
  266. Saikkonen K, Saari S, Helander M (2010) Defensive mutualism between plants and endophytic fungi? Fungal Divers 41:101–113CrossRefGoogle Scholar
  267. Salvioli A, Chiapello M, Fontaine J et al (2010) Endobacteria affect the metabolic profile of their host Gigaspora margarita, and arbuscular myccorhizal fungus. Environ Microbiol 12:2083–2095PubMedPubMedCentralGoogle Scholar
  268. Salvioli A, Ghignone S, Novero M et al (2016) Symbiosis with an endobacterium increases the fitness of a mycorhhizal fungus, raising its bioenergentic potential. ISME J 10:130–144PubMedCrossRefPubMedCentralGoogle Scholar
  269. Santoyo G, Moredno-Hagelsieb G, del Carmen Orozco-Mosqueda M, Glick BR (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99PubMedPubMedCentralCrossRefGoogle Scholar
  270. Sarkar S, Guttman DS (2004) Evolution of the core genome of Pseudomonas syringae, a highly clonal, endemic plant pathogen. Appl Environ Microb 70:1999–2012CrossRefGoogle Scholar
  271. Sarmiento C, Zalamea P-C, Dalling JW et al (2017) Soilborne fungi have host affinity and host-specific effects on seed germination and survival in a lowland tropical forest. P Natl Acad Sci 14:11458–11463CrossRefGoogle Scholar
  272. Sato Y, Narisawa K, Tsuruta K et al (2010) Detection of Betaproteobacteria inside the mycelium of the fungus Mortierella elongate. Microbes Environ 25:321–324PubMedCrossRefPubMedCentralGoogle Scholar
  273. Scardaci SC, Webster RK, Greer CA et al (1997) Rice blast: a new disease in California, Agronomy Fact, Department of Agronomy and Range Science, University of California, Davis, Sheet Series, 1997–2Google Scholar
  274. Schappe T, Albornoz FE, Turner BL et al (2017) The role of soil chemistry and plant neighbourhoods in structuring fungal communities in three Panamanian rainforests. J Ecol 105:569–579CrossRefGoogle Scholar
  275. Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 55:315–340PubMedCrossRefPubMedCentralGoogle Scholar
  276. Schellenber B, Ramel C, Dudler R (2010) Pseudomonas syringae virulence factor syringolin A counteracts stomatal immunity by proteasome inhibition. Mol Plant-Microbe In 23:1287–1293CrossRefGoogle Scholar
  277. Schlatter DC, Bakker MG, Bradeen JM, Kinkel LL (2015) Plant community richness and microbial interactions structure bacterial communities in soil. Ecology 96:134–142PubMedCrossRefPubMedCentralGoogle Scholar
  278. Schleuning M, Frund J, Garcia D (2015) Predicting ecosystem functions from biodiversity and mutualistic networks: an extension of trait-based concepts to plant-animal interactions. Ecography 38:380–392CrossRefGoogle Scholar
  279. Schloss PD, Handelsman J (2006) Toward a census of bacteria in soil. PLoS Comput Biol 2:e92PubMedPubMedCentralCrossRefGoogle Scholar
  280. Schmelz EA, Engelbert J, Alborn HT et al (2003) Simultaneous analysis of phytohormones, phytotoxins, and volatile organic compounds in plants. P Natl Acad Sci USA 100:10552–10557CrossRefGoogle Scholar
  281. Schultz B, Boyle C, Draeger S et al (2002) Endophytic fungi: a source of novel biologically active secondary metabolites. Mycolog Res 106:996–1004CrossRefGoogle Scholar
  282. Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686PubMedCrossRefPubMedCentralGoogle Scholar
  283. Schulz B, Coyne DP (2006) What are endophytes? In: Schulz BJE, Boyle CJC, Sieber TN (eds) Microbial root endophytes. Springer, Berlin, pp 1–13CrossRefGoogle Scholar
  284. Shaffer JP, Sarmiento C, Zalamea PC et al (2016) Diversity, specificity, and phylogenetic relationships of endophyphal bacteria in fungi that inhabit tropical seeds and leaves. Front Ecol Evol 4:116CrossRefGoogle Scholar
  285. Sharma M, Schmid M, Rothballer M et al (2008) Detection and identification of bacteria intimately associated with fungi in the order Sebacinales. Cell Microbiol 10:2235–2246PubMedCrossRefPubMedCentralGoogle Scholar
  286. Shivas RG, Hyde KD (1997) Biodiversity of plant pathogenic fungi in the tropics. Biodiversity of tropical microfungi. Hong Kong University Press, Hong Kong, pp 47–56Google Scholar
  287. Silby MW, Winstanley C, Godfrey SAC et al (2011) Pseudomonas genomes: diverse and adaptable. FEMS Microbiol Rev 35:652–680PubMedCrossRefPubMedCentralGoogle Scholar
  288. Silvertown J (2004) Plant coexistence and the niche. Trends Ecol Evol 19:605–611CrossRefGoogle Scholar
  289. Sockett RE (2009) Predatory lifestyle of Bdellovibrio bacteriovorus. Annu Rev Microb 63:523–539CrossRefGoogle Scholar
  290. Sorensen J, Sessitsch A (2007) Plant-associated bacteria-lifestyle and molecular interactions. Modern Soil Microbiology CRC Press LLCGoogle Scholar
  291. Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetoc acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448PubMedCrossRefPubMedCentralGoogle Scholar
  292. Stephan A, Meyer AH, Schmid B (2000) Plant diversity affects culturable soil bacteria in experimental grassland communities. J Ecol 88:988–998CrossRefGoogle Scholar
  293. Stergiopoulos I, de Wit PJ (2009) Fungal effector proteins. Annu Rev Phytopathol 47:233–263PubMedCrossRefPubMedCentralGoogle Scholar
  294. Stone JK, Bacon CW, White JF (2000) An overview of endophytic microbes: endophytism defined. Microb endophy 3:29–33Google Scholar
  295. Stork NE, McBroom J, Gely C, Hamilton AJ (2015) New approaches narrow global species estimates for beetles, insects, and terrestrial arthropods. P Natl Acad Sci USA 112:7519–7523CrossRefGoogle Scholar
  296. Strack D, Fester T, Hause B et al (2003) Arbuscular mycorrhiza: biological, chemical, and molecular aspects. J Chem Ecol 29:1955–1979PubMedCrossRefPubMedCentralGoogle Scholar
  297. Strobel G (2012) Genetic diversity of microbial endophytes and their biotechnical applications. Genomics applications for the developing world. Springer, New York, pp 249–262CrossRefGoogle Scholar
  298. Strobel G, Daisy B, Castillo U, Harper J (2004) Natural products from endophytic microorganisms. J Nat Prod 67:257–268PubMedPubMedCentralCrossRefGoogle Scholar
  299. Suryanarayanan TS, Murali TS, Venkatesan G (2002) Occurrence and distribution of fungal endophytes in tropical forests across a rainfall gradient. Can J Bot 80:818–826CrossRefGoogle Scholar
  300. Suryanarayanan TS, Venkatesan G, Murali TS (2003) Endophytic fungal communities in leaves of tropical forest trees: diversity and distribution patterns. Current Sci 85:489–493Google Scholar
  301. Suryanarayanan TS, Murali TS, Thirunavukkarasu N et al (2011) Endophytic fungal communities in woody perennials of three tropical forest types of the Western Ghats, southern India. Biodivers Conserv 20:913–928CrossRefGoogle Scholar
  302. Tanaka A, Takemoto D, Chuji T, Scott B (2012) Fungal endophytes of grasses. Curr Opin Plant Biol 15:462–468PubMedCrossRefPubMedCentralGoogle Scholar
  303. Tedersoo L, Bahram M, Cajthaml T et al (2016) Tree diversity and species identity effects on soil fungi, protists and animals are context dependent. ISME J 10:346–362PubMedCrossRefPubMedCentralGoogle Scholar
  304. Thines M (2014) Phylogeny and evolution of plant pathogenic oomycetes—a global overview. Eur J Plant Pathol 138:431–447CrossRefGoogle Scholar
  305. Thompson GL, Kao-Kniffin J (2016) Diversity enhances NPP, N retention, and soil microbial diversity in experimental urban grassland assemblages. PLoS ONE 11:e0155986PubMedPubMedCentralCrossRefGoogle Scholar
  306. Thurston HD (1998) Tropical plant diseases, 2nd edn. American Phytopathological Society, St. Paul, MNGoogle Scholar
  307. Tiemann LK, Grandy AS, Atkinson EE et al (2015) Ecol Lett 18:761–771PubMedCrossRefPubMedCentralGoogle Scholar
  308. Tilman D (2016) Biodiversity: from evolutionary origins to ecosystem functioning. Contr Sci 11:11–20Google Scholar
  309. Tilman D, Isbell F, Cowles JM (2014) Biodiversity and ecosystem function. Annu Rev Ecol Evol S 45:471–493CrossRefGoogle Scholar
  310. Torsvik V, Ovrea L, Thingstad TF (2002) Prokaryotic diversity—magnitude, dynamics, and controlling factors. Science 296:1064–1066PubMedCrossRefPubMedCentralGoogle Scholar
  311. Tortora GJ, Funke BR, Case CL, Johnson TR (2016) Microbiology: an introduction, 12th ed. Pearson Education, IncGoogle Scholar
  312. Tran H, Ficke A, Asiimwe T et al (2007) Role of the cyclic lipopeptide massetolide A in biological control of Phyphthora infestans and in colonization of tomato plants by Pseudomonas fluorescens. New Phytol 175:731–742PubMedCrossRefPubMedCentralGoogle Scholar
  313. Tripathi L, Mwangi M, Abele S et al (2009) Xanthomonas wilt: a threat to banana production in East and Central Africa. Plant Dis 93:440–451CrossRefGoogle Scholar
  314. Truyens S, Weyens N, Cuypers A, Vangronsveld J (2015) Bacterial seed endophytes: genera, vertical transmission and interaction with plants. Env Microbiol Rep 7:40–50CrossRefGoogle Scholar
  315. Urcelay C, Diaz S, Gurvich DE et al (2009) Mycorrhizal community resilience to experimental plant functional type removals in a woody ecosystem. J Ecol 97:1291–1301CrossRefGoogle Scholar
  316. Van Bael SA, Valencia MC, Rojas EI et al (2009) Effects of foliar endophytic fungi on the preference and performance of the leaf beetle Chelymorpha alternans in Panama. Biotropica 41:221–225CrossRefGoogle Scholar
  317. Van Bael SA, Seid MA, Wcislo WT (2012) Endophytic fungi increase the processing rate of leaves by leaf-cutting ants (Atta). Ecol Entomol 37:318–321CrossRefGoogle Scholar
  318. Van Bael S, Estrada C, Arnold AE (2017) Foliar endophyte communities and leaf traits in tropical trees. In: Dighton J, White JF (eds) The fungal community: its organization and role in the ecosystem, 4th edn. CRC Press, Boca Raton, pp 79–92Google Scholar
  319. Van Peer R, Niemann GJ, Schippers B (1991) Induced resistance and phytoalexin accumulation in biological control of Fusarium wilt of carnation by Pseudomonas sp. strain WCS 417 r. Phytopathology 81:728–734CrossRefGoogle Scholar
  320. Velicer GJ, Vos M (2009) Sociobiology of the myxobacteria. Annu Rev Microbiol 63:599–623PubMedCrossRefPubMedCentralGoogle Scholar
  321. Verhagen BW, Trotel-Aziz P, Couderchet M et al (2010) Pseudomonas spp.-induced systemic resistance to Botrytis cinerea is associated with induction and priming of defence responses in grapevine. J Exp Bot 61:249–260PubMedCrossRefPubMedCentralGoogle Scholar
  322. Vitousek PM, Menge DNL, Reed SC, Cleveland CC (2013) Biological nitrogen fixation: rates, patterns, and ecological controls in terrestrial ecoystems. Phil Trans R Soc B 368:20130119PubMedPubMedCentralCrossRefGoogle Scholar
  323. Vorholt JA (2012) Microbial life in the phyllosphere. Nat Rev Microbiol 10:828–840PubMedCrossRefPubMedCentralGoogle Scholar
  324. Waksman SA, Schatz A, Reynolds DM (2010) Production of antibiotic substances by actinomycetes. Ann New York Acad Sci 1213:112–124CrossRefGoogle Scholar
  325. Waldrop MP, Zak DR, Blackwood CB et al (2006) Resource availability controls fungal diversity across a plant diversity gradient. Ecol Lett 9:1127–1135PubMedCrossRefPubMedCentralGoogle Scholar
  326. Wang J, Chapman SJ, Yao H (2016) Incorporation of 13 C-labelled rice rhizodeposiition into soil microbial communities under different fertilizer applications. Appl Soil Ecol 101:11–19CrossRefGoogle Scholar
  327. Wardle DA, Bonner KI, Barker GM et al (1999) Plant removals in perennial grassland: vegetation dynamics, decomposers, soil biodiversity, and ecosystem properties. Ecol Monog 69:535–568CrossRefGoogle Scholar
  328. Wardle DA, Yeates GW, Williamson W, Bonner KI (2003) The response of a three trophic level soil food web to the identity and diversity of plant species and functional groups. Oikos 102:45–56CrossRefGoogle Scholar
  329. Wellman FL (1968) More disease on crops in the tropics than in the temperate zone. Ceiba 14:17–28Google Scholar
  330. Wellman FL (1972) Tropical American plant disease. The Scarecrow Press Inc., Metuchen, NJGoogle Scholar
  331. Werth M, Kuzyakov Y (2010) 13C fractionation at the root-microorganisms-soil interface: a review and outlook for partitioning studies. Soil Biol Biochem 42:1372–1384CrossRefGoogle Scholar
  332. Whitman WB, Coleman DC, Wiebe WJ (1998) Prokaryotes: the unseen majority. P Natl Acad Sci USA 95:6578–6583CrossRefGoogle Scholar
  333. Willey J, Sherwood L, Woolverton CJ (2016) Prescott’s microbiology, 10th edn. McGraw-Hill Education, New YorkGoogle Scholar
  334. Wilson D (1995) Endophyte: the evolution of the term, and clarification of its use and definition. Oikos 73:274–276CrossRefGoogle Scholar
  335. Wilson M, Lindow SE (1994) Coexistence among epiphytic bacterial populations mediated through nutritional resource partitioning. Appl Environ Microb 60:4468–4477Google Scholar
  336. Wooldridge K (2009) Bacterial secreted proteins: secretory mechanisms and role in pathogenesis. Horizon Scientific PressGoogle Scholar
  337. Wright SJ (2002) Plant diversity in tropical forests: a review of mechanisms of species coexistence. Oecologia 130:1–14PubMedCrossRefPubMedCentralGoogle Scholar
  338. Yang S, Zhang Q, Guo J et al (2006) Global effect of indole-3-acetic acid biosynthesis on multiple virulence factors of Erwinia chrysanthemi 3937. Appl Environ Microb 73:1079–1088CrossRefGoogle Scholar
  339. Yang T, Adams JM, Shi Y et al (2017) Soil fungal diversity in natural grasslands of the Tibetan Plateau: associations with plant diversity and productivity. New Phytol 215:756–765CrossRefPubMedPubMedCentralGoogle Scholar
  340. Zak DR, Holmes WE, White DC et al (2003) Plant diversity, soil microbial communities, and ecosystem function: are there any links? Ecology 84:2042–2050CrossRefGoogle Scholar
  341. Zalamea PC, Sarmiento C, Arnold AE et al (2015) Do soil microbes and abrasion by soil particles influence persistence and loss of physical dormancy in seeds of tropical pioneers? Front Plant Sci 5:799PubMedPubMedCentralCrossRefGoogle Scholar
  342. Zamioudis C, Pieterse CM (2012) Modulation of host immunity by beneficial microbes. Mol Plant- Microbe In 25:139–150CrossRefGoogle Scholar
  343. Zhao Y, Thilmony R, Bender CL et al (2003) Virulence systems of Pseudomonas syringae pv. tomato promote bacterial speck disease in tomato by targeting the jasmonate signaling pathway. Plant J 36:485–499PubMedCrossRefPubMedCentralGoogle Scholar
  344. Zimmerman NB, Vitousek PM (2012) Fungal endophyte communities reflect environmental structuring across a Hawaiian landscape. P Natl Acad Sci USA 109:13022–13027CrossRefGoogle Scholar

Copyright information

© This chapter is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply 2018

Authors and Affiliations

  1. 1.Smithsonian Environmental Research CenterEdgewaterUSA
  2. 2.University of PittsburghPittsburghUSA

Personalised recommendations