Defense and Nutrient Mutualisms in Populus

Part of the Plant Genetics and Genomics: Crops and Models book series (PGG, volume 8)


The effects of symbionts on plant defense and nutrition are increasingly seen as significant but neglected factors in plant ecology. The roles of some endophytic and mycorrhizal fungi associated with Populus are beginning to be addressed with advanced tools of genetics and genomics. At the same time previously unknown Populus symbionts are still being discovered and described. In this chapter, defense and nutrient mutualists of Populus are reviewed in the context of the wider literature, and with an eye towards potential applications to poplar culture.


Arbuscular Mycorrhizal Fungus Arbuscular Mycorrhizae Mycorrhizal Fungus Coffee Berry Arbuscular Mycorrhizae 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Antunes PM, Miller J, Carvalho LM, Klironomos JN, Newman. JA (2008) Even after death the endophytic fungus of Schedonorus phoenix reduces the arbuscular mycorrhizas of other plants. Funct Ecol 22:912–918.CrossRefGoogle Scholar
  2. Arnold AE, Henk DA, Eells RL, Lutzoni F, Vilgalys. R (2007) Diversity and phylogenetic affinities of foliar fungal endophytes in loblolly pine inferred by culturing and environmental PCR. Mycologia 99:185–206.PubMedCrossRefGoogle Scholar
  3. Arnold AE, Herre. EA (2003) Canopy cover and leaf age affect colonisation by tropical fungal endophytes: ecological pattern and process in Theobroma cacao (Malvaceae). Mycologia 95:388–398.CrossRefPubMedGoogle Scholar
  4. Arnold AE, Maynard Z, Gilbert GS, Coley PD, Kursar TA (2000) Are tropical fungal endophytes hyperdiverse? Ecol Lett 3:267–274.CrossRefGoogle Scholar
  5. Arnold AE, Mejia LC, Kyllo D, Rojas EI, Maynard Z, Robins N, Herre. EA (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Nat Acad Sci 100:15649–15654.PubMedCrossRefGoogle Scholar
  6. Babst BA, Ferrieri RA, Gray DW, Lerdau M, Schlyer DJ, Schueller M, Thorpe MR, Orians. CM (2005) Jasmonic acid induces rapid changes in carbon transport and partitioning in Populus. New Phytol 167:63–72.PubMedCrossRefGoogle Scholar
  7. Bailey BA, Bae H, Strem MD, Crozier J, Thomas SE, Samuels GJ, Vinyard BT, Holmes. KA (2008) Antibiosis, mycoparasitism, and colonization success for endophytic Trichoderma isolates with biological control potential in Theobroma cacao. Biol Control 46:24–35.CrossRefGoogle Scholar
  8. Bailey BA, Bae H, Strem MD, Roberts DP, Thomas SE, Crozier J, Samuels GJ, Choi I-Y, Holmes. KA (2006) Fungal and plant gene expression during the colonization of cacao seedlings by endophytic isolates of four Trichoderma species. Planta 224:1449–1464.PubMedCrossRefGoogle Scholar
  9. Bailey JK, Deckert R, Schweitzer JA, Rehill BJ, Lindroth RL, Gehring C, Whitham. TG (2005) Host plant genetics affect hidden ecological players: links among Populus, condensed tannins, and fungal endophyte infection. Can J Botany 83:356–361.CrossRefGoogle Scholar
  10. Baum C, Stetter U, Makeschin. F (2002) Growth response of Populus trichocarpa to inoculation by the ectomycorrhizal fungus Laccaria laccata in a pot and a field experiment. For Ecol Manag 163:1–8.CrossRefGoogle Scholar
  11. Beauchamp VB, Stromberg JC, Stutz. JC (2006) Arbuscular mycorrhizal fungi associated with Populus-Salix stands in a semiarid riparian ecosystem. New Phytol 170:369–380.PubMedCrossRefGoogle Scholar
  12. Beckers GJ, Conrath. U (2007) Priming for stress resistance: from the lab to the field. Curr Opin Plant Biol 10:425–431.PubMedCrossRefGoogle Scholar
  13. Bendz-Hellgren M, Stenlid. J (1997) Decreased volume growth of Picea abies in response to Heterobasidion annosum infection. Can J For Res 27:1519–1524.CrossRefGoogle Scholar
  14. Bier JE, Rowat. MH (1962) The relation of bark moisture to the development of canker diseases caused by native, facultative parasites: VII. Some effects of the saprophytes on the bark of poplar and willow on the incidence of Hypoxylon canker. Can J Botany 40:61–69.CrossRefGoogle Scholar
  15. Bittel P, Robatzek. S (2007) Microbe-associated molecular patterns (MAMPs) probe plant immunity. Curr Opin Plant Biol 10:335–341.PubMedCrossRefGoogle Scholar
  16. Boddy L (2000) Interspecific combative interactions between wood-decaying basidiomycetes. FEMS Microbiol Ecol 31:185–194.PubMedCrossRefGoogle Scholar
  17. Borowicz VA (2001) Do arbuscular mycorrhizal fungi alter plant-pathogen relations? Ecology 82:3057–3068.Google Scholar
  18. Bradshaw HD, Ceulemans R, Davis J, Stettler. R (2000) Emerging model systems in plant biology: Poplar (POPULUS) as a model forest tree. J Plant Growth Regul 19:306–313.CrossRefGoogle Scholar
  19. Bradshaw HD Jr., Strauss SH (2001) Breeding strategies for the 21st century: domestication of poplar. In: Dickmann JGIDI, Eckenwalder JE, Richardson J (eds) Poplar Culture in North America. Part B,  Chapter 14, 383–394. NRC Research Press, National Research Council of Canada, Ottawa, ON K1A 0R6, Canada.Google Scholar
  20. Brundrett M (2004) Diversity and classification of mycorrhizal associations. Biol Rev 79:473–495.PubMedCrossRefGoogle Scholar
  21. Brundrett M, Bougher N, Dell B, Grove T, Malajczuk. N (1996) Working with Mycorrhizas in Forestry and Agriculture. ACIAR, Canberra, Australia.Google Scholar
  22. Brunner AM, Busov VB, Strauss. SH (2004) Poplar genome sequence: functional genomics in an ecologically dominant plant species. Trends Plant Sci 9:49–56.PubMedCrossRefGoogle Scholar
  23. Bucking H, Heyser. W (2001) Microautoradiographic localization of phosphate and carbohydrates in mycorrhizal roots of Populus tremula x Populus alba and the implications for transfer processes in ectomycorrhizal associations. Tree Physiol 21:101–107.PubMedGoogle Scholar
  24. Bultman TL, Bell G, Martin. WD (2004) A fungal endophyte mediates reversal of wound-induced resistance and constrains tolerance in a grass. Ecology 85:679–685.CrossRefGoogle Scholar
  25. Calhoun LA, Findlay JA, Miller JD, Whitney. NJ (1992) Metabolites toxic to spruce budworm from balsam fir needle endophytes. Mycol Res 96:281–286.CrossRefGoogle Scholar
  26. Chapela IH (1989) Fungi in healthy stems and branches of American beech and aspen: a comparative study. New Phytol 113:65–75.CrossRefGoogle Scholar
  27. Chase JM (2003) Community assembly: when should history matter? Oecologia 136:489–498.PubMedCrossRefGoogle Scholar
  28. Clark CL, Miller JD, Whitney. NJ (1989) Toxicity of conifer needle endophytes to spruce budworm. Mycol Res 93:508–512.CrossRefGoogle Scholar
  29. Clarke BB, White JF Jr, Hurley RH, Torres MS, Sun S, Huff. DR (2006) Endophyte-mediated suppression of dollar spot disease in fine fescues. Plant Dis 90:994–998.CrossRefGoogle Scholar
  30. Clay K (1988) Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 69:10–16.CrossRefGoogle Scholar
  31. Clay K, Holah. J (1999) Fungal endophyte symbiosis and plant diversity in successional fields. Science 285:1742–1744.PubMedCrossRefGoogle Scholar
  32. Clay K, Schardl. C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160:S99–S127.PubMedCrossRefGoogle Scholar
  33. Cox CB, Moore. PD (2005) Biogeography – An Ecological and Evolutionary Approach. Blackwell, Oxford, U.K.Google Scholar
  34. Cuomo CA, Guldener U, Xu JR, Trail F, Turgeon BG, Di Pietro A, Walton JD, Ma LJ, Baker SE, Rep. M (2007) The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317:1400–1402.PubMedCrossRefGoogle Scholar
  35. Deshmukh S, Huckelhoven R, SchÄFer P, Imani J, Sharma M, Weiss M, Waller F, Kogel. KH (2006) The root endophytic fungus Piriformospora indica requires host cell death for proliferation during mutualistic symbiosis with barley. Proc Nat Acad Sci USA 103:18450–18457.PubMedCrossRefGoogle Scholar
  36. Djonovic S, Pozo MJ, Dangott LJ, Howell CR, Kenerley. CM (2006) Sm1, a proteinaceous elicitor secreted by the biocontrol fungus Trichoderma virens induces plant defense responses and systemic resistance. Mol Plant-Microbe Interact 19:838–853.PubMedCrossRefGoogle Scholar
  37. Doty SL (2008) Enhancing phytoremediation through the use of transgenics and endophytes. New Phyt 179:318–333.CrossRefGoogle Scholar
  38. Doty SL, Dosher MR, Singleton GL, Moore AL, Aken B, Stettler RF, Strand SE, Gordon. MP (2005) Identification of an endophytic Rhizobium in stems of Populus. Symbiosis 39:27–35.Google Scholar
  39. Druege U, Baltruschat H, Franken. P (2007) Piriformospora indica promotes adventitious root formation in cuttings. Scientia Horticulturae 112:422–426.CrossRefGoogle Scholar
  40. Eckenwalder JE (1996) Systematics and evolution of Populus. Part I,  Chapter 1. In: Stettler HDBRF Jr, Heilman PE, Hinckley TM (eds) Biology of Populus and its Implications for Management and Conservation. NRC Research Press, National Research Council of Canada, Ottawa, ON, pp. 7–32.Google Scholar
  41. Erb M, Ton J, Degenhardt J, Turlings. TCJ (2008) Interactions between arthropod-induced aboveground and belowground defenses in plants. Plant Physiol 146:867–874.PubMedCrossRefGoogle Scholar
  42. Evans HC, Holmes KA, Thomas. SE (2003) Endophytes and mycoparasites associated with an indigenous forest tree, Theobroma gileri, in Ecuador and a preliminary assessment of their potential as biocontrol agents of cocoa diseases. Mycol Prog 2:149–160.CrossRefGoogle Scholar
  43. Farr DF, Rossman AY, Palm ME, McCray. EB (n.d.) Fungal Databases. Systematic Mycology and Microbiology, USDA, ARS
  44. Felten J, Kohler A, Morin E, Palme K, Martin F, Ditengou F, Legué. V (2009) The ectomycorrhizal fungus Laccaria bicolor stimulates lateral root formation in poplar and Arabidopsis through auxin transport and signaling. Plant Physiol DOI:10.1104/pp.109.147231.Google Scholar
  45. Felton GW, Korth KL, Bi JL, Wesley SV, Huhman DV, Mathews MC, Murphy JB, Lamb C, Dixon. RA (1999) Inverse relationship between systemic resistance of plants to microorganisms and to insect herbivory. Curr Biol 9:317–320.PubMedCrossRefGoogle Scholar
  46. Freeman S, Rodriguez. RJ (1993) Genetic conversion of a fungal plant pathogen to a nonpathogenic, endophytic mutualist. Science 260:75–78.PubMedCrossRefGoogle Scholar
  47. Fukami T, Morin. PJ (2003) Productivity-biodiversity relationships depend on the history of community assembly. Nature 424:423–426.PubMedCrossRefGoogle Scholar
  48. Ganley RJ, Brunsfeld SJ, Newcombe. G (2004) A community of unknown, endophytic fungi in western white pine. Proc Nat Acad Sci 101:10107–10112.PubMedCrossRefGoogle Scholar
  49. Ganley RJ, Sniezko RA, Newcombe. G (2008) Endophyte-mediated resistance against white pine blister rust in Pinus monticola. For Ecol Manag 255:2751–2760.CrossRefGoogle Scholar
  50. Gehring CA, Mueller RC, Whitham. TG (2006) Environmental and genetic effects on the formation of ectomycorrhizal and arbuscular mycorrhizal associations in cottonwoods. Oecologia 149:158–164.Google Scholar
  51. Germaine K, Keogh E, Garcia-Cabellos G, Borremans B, Lelie D, Barac T, Oeyen L, Vangronsveld J, Moore FP, Moore. ERB (2004) Colonisation of poplar trees by gfp-expressing bacterial endophytes. FEMS Microbiol Ecol 48:109–118.PubMedCrossRefGoogle Scholar
  52. Glazebrook J, Ton. J (2007) Biotic interactions: Recurring themes and expanding scales. Curr Opin Plant Biol 10:331–334.CrossRefGoogle Scholar
  53. Godbold DL, Hoosbeek MR, Lukac M, Cotrufo MF, Janssens IA, Ceulemans R, Polle A, Velthorst EJ, Scarascia-Mugnozza G, De Angelis P, Miglietta F, Peressotti. A (2006) Mycorrhizal hyphal turnover as a dominant process for carbon input into soil organic matter. Plant Soil 281:15–24.CrossRefGoogle Scholar
  54. Green H, Larsen J, Olsson PA, Jensen DF, Jakobsen. I (1999) Suppression of the biocontrol agent Trichoderma harzianum by mycelium of the arbuscular mycorrhizal fungus Glomus intraradices in root-free soil. Appl Environ Microbiol 65:1428–1434.PubMedGoogle Scholar
  55. Grünig CR, Queloz V, Sieber TN, Holdenrieder. O (2008) Dark septate endophytes (DSE) of the Phialocephala fortinii s.l. – Acephala applanata species complex in tree roots: classification, population biology, and ecology. Botany 86:1355–1369.CrossRefGoogle Scholar
  56. Gyenis L, Anderson NA, Ostry. ME (2003) Biological control of septoria leaf spot disease of hybrid poplar in the field. Plant Dis 87:809–813.CrossRefGoogle Scholar
  57. Haine ER (2008) Symbiont-mediated protection. Proc Roy Soc B: Biol Sci 275:353–361.CrossRefGoogle Scholar
  58. Hampp R, Ecke M, Schaeffer C, Wallenda T, Wingler A, Kottke I, Sundberg. B (1996) Axenic mycorrhization of wild type and transgenic hybrid aspen expressing T-DNA indoleacetic acid-biosynthetic genes. Trees-Struct Funct 11:59–64.Google Scholar
  59. Hanada RE, Jorge Souza T, Pomella AWV, 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 112:1335–1343.PubMedCrossRefGoogle Scholar
  60. Harman GE, Howell CR, Viterbo A, Chet I, Lorito. M (2004) Trichoderma species – opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56.PubMedCrossRefGoogle Scholar
  61. Hawksworth DL (2001) The magnitude of fungal diversity: the 1.5 million species estimate revisited. Mycol Res 105:1422–1432.CrossRefGoogle Scholar
  62. Helm DJ, Allen EB, Trappe. JM (1996) Mycorrhizal chronosequence near Exit Glacier, Alaska. Can J Botany 74:1496–1506.CrossRefGoogle Scholar
  63. Hiremath ST, Balasubramanian S, Zheng J, Podila. GK (2006) Symbiosis-regulated expression of an acetyl-CoA acetyltransferase gene in the ectomycorrhizal fungus Laccaria bicolor. Can J Botany 84:1405–1416.CrossRefGoogle Scholar
  64. Hooker JE, Black KE, Perry RL, Atkinson. D (1995) Arbuscular mycorrhizal fungi induced alteration to root longevity of poplar. Plant Soil 172:327–329.CrossRefGoogle Scholar
  65. Hutchinson LJ (1999) Wood-inhabiting microfungi isolated from Populus tremuloides from Alberta and northeastern British Columbia. Can J Botany 77:898–905.CrossRefGoogle Scholar
  66. Iavicoli A, Boutet E, Buchala A, Metraux. JP (2003) Induced systemic resistance in Arabidopsis thaliana in response to root Inoculation with Pseudomonas fluorescens CHA0. Mol Plant-Microbe Interact 16:851–858.PubMedCrossRefGoogle Scholar
  67. Jokipii S, Haggman H, Brader G, Kallio PT, Niemi. K (2008) Endogenous PttHb1 and PttTrHb, and heterologous Vitreoscilla vhb haemoglobin gene expression in hybrid aspen roots with ectomycorrhizal interaction. J Exp Botany 59:2449–2459.CrossRefGoogle Scholar
  68. Jones JDG, Dangl. JL (2006) The plant immune system. Nature 444:323–329.PubMedCrossRefGoogle Scholar
  69. Jones MD, Smith. SE (2004) Exploring functional definitions of mycorrhizas: are mycorrhizas always mutualisms? Can J Botany 82:1089–1109.CrossRefGoogle Scholar
  70. Kaldorf M, Koch B, Rexer KH, Kost G, Varma. A (2005) Patterns of interaction between Populus Esch5 and Piriformospora indica: a transition from mutualism to antagonism. Plant Biology 7:210–218.PubMedCrossRefGoogle Scholar
  71. Khasa PD, Chakravarty P, Robertson A, Thomas BR, Dancik. BP (2002) The mycorrhizal status of selected poplar clones introduced in Alberta. Bioenergy Res 22:99–104.Google Scholar
  72. Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70.PubMedCrossRefGoogle Scholar
  73. Kogel KH, Franken P, Hückelhoven R (2006) Endophyte or parasite–what decides? Curr Opin Plant Biol 9:358–363.PubMedCrossRefGoogle Scholar
  74. Kohler A, Rinaldi C, Duplessis S, Baucher M, Geelen D, Duchaussoy F, Meyers BC, Boerjan W, Martin. F (2008) Genome-wide identification of NBS resistance genes in Populus trichocarpa. Plant Mol Biol 66:619–636.PubMedCrossRefGoogle Scholar
  75. Koike N, Hyakumachi M, Kageyama K, Tsuyumu S, Doke. N (2001) Induction of systemic resistance in cucumber against several diseases by plant growth-promoting fungi: lignification and superoxide generation. Eu J Plant Pathol 107:523–533.CrossRefGoogle Scholar
  76. Kuffner M, Puschenreiter M, Wieshammer G, Gorfer M, Sessitsch. A (2008) Rhizosphere bacteria affect growth and metal uptake of heavy metal accumulating willows. Plant Soil 304:35–44.CrossRefGoogle Scholar
  77. Kuldau GA, Yates. IE (2000) Evidence for Fusarium endophytes in cultivated and wild plants. In: Bacon CW, White JF Jr. (eds) Microbial Endophytes. Marcel Dekker, New York, pp. 85–117.Google Scholar
  78. Laflamme G, Lortie. M (1973) Micro-organismes dans les tissus colorés et cariés du peuplier faux-tremble. Can J For Res 3:155–160.CrossRefGoogle Scholar
  79. Leake J, Johnson D, Donnelly D, Muckle G, Boddy L, Read. D (2004) Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can J Botany 82:1016–1045.CrossRefGoogle Scholar
  80. Lesaulnier C, Papamichail D, McCorkle S, Ollivier B, Skiena S, Taghavi S, Zak D, van der Lelie. D (2008) Elevated atmospheric CO2 affects soil microbial diversity associated with trembling aspen. Environ Microbiol 10:926–941.PubMedCrossRefGoogle Scholar
  81. Lingua G, Franchin C, Todeschini V, Castiglione S, Biondi S, Burlando B, Parravicini V, Torrigiani P, Berta. G (2008) Arbuscular mycorrhizal fungi differentially affect the response to high zinc concentrations of two registered poplar clones. Environ Pollut 153:137–147.PubMedCrossRefGoogle Scholar
  82. Liu CH, Zou WX, Hong L, Tan. RX (2001) Antifungal activity of Artemisia annua endophyte cultures against phytopathogenic fungi. J Biotechnol 88:277–282.PubMedCrossRefGoogle Scholar
  83. Lodge DJ (2000) Ecto-or arbuscular mycorrhizas-which are best? New Phytol 146:353–354.CrossRefGoogle Scholar
  84. Lopez MF, Manner P, Willmann A, Hampp R, Nehls. U (2007) Increased trehalose biosynthesis in Hartig net hyphae of ectomycorrhizas. New Phytol 174:389–398.PubMedCrossRefGoogle Scholar
  85. Luster J, Finlay R (eds) (2006) Handbook of Methods Used in Rhizophere Research. Swiss Federal Research Institute WSL, Birmensdorf, Switzerland, pp. 399–400.Google Scholar
  86. Major IT, Constabel. CP (2007) Shoot-root defense signaling and activation of root defense by leaf damage in poplar. Can J Botany 85:1171–1181.CrossRefGoogle Scholar
  87. Marjanovic Z, Uehlein N, Kaldenhoff R, Zwiazek JJ, Weiss M, Hampp R, Nehls. U (2005) Aquaporins in poplar: What a difference a symbiont makes! Planta 222:258–268.Google Scholar
  88. Martin F, Aerts A, Ahren D, Brun A, Danchin EG, Duchaussoy F, Gibon J, Kohler A, Lindquist E, Pereda. V (2008) The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452:88–93.PubMedCrossRefGoogle Scholar
  89. Martin F, Duplessis S, Ditengou F, Lagrange H, Voiblet C, Lapeyrie. F (2001) Developmental cross talking in the ectomycorrhizal symbiosis: signals and communication genes. New Phytol 151:145–154.CrossRefGoogle Scholar
  90. Martin F, Kohler A, Duplessis. S (2007) Living in harmony in the wood underground: ectomycorrhizal genomics. Curr Opin Plant Biol 10:204–210.PubMedCrossRefGoogle Scholar
  91. Martin F, Tuskan GA, DiFazio SP, Lammers P, Newcombe G, Podila. GK (2004) Symbiotic sequencing for the Populus mesocosm. New Phytol 161:330–335.CrossRefGoogle Scholar
  92. Mattson WJ, Hart ER, Volney. WJA (2001) Insect pests of Populus: coping with the inevitable. In: Dickmann DI, Isebrands JG, Eckenwalder JE, Richardson J (eds) Poplar Culture in North America, Part A,  Chapter 7, pp. 219–248. NRC Research Press, Ottawa, ON K1A 0R6, Canada.Google Scholar
  93. McGormick JF, Platt RB (1980) Recovery of an Appalachian forest following the chestnut blight or Catherine Keever – you were right!. Am Midl Nat 104:264–273.CrossRefGoogle Scholar
  94. Miller JD, Mackenzie S, Foto M, Adams GW, Findlay. JA (2002) Needles of white spruce inoculated with rugulosin-producing endophytes contain rugulosin reducing spruce budworm growth rate. Mycol Res 106:471–479.CrossRefGoogle Scholar
  95. Miranda M, Ralph SG, Mellway R, White R, Heath MC, Bohlmann J, Constabel. CP (2007) The transcriptional response of hybrid poplar (Populus trichocarpa x P. deltoides) to infection by Melampsora medusae leaf rust involves induction of flavonoid pathway genes leading to the accumulation of proanthocyanidins. Mol Plant-Microbe Interact 20:816–831.PubMedCrossRefGoogle Scholar
  96. Mitchell CE, Power. AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627.PubMedCrossRefGoogle Scholar
  97. Mlot C (2004) Microbial diversity unbound. BioSci 54:1064–1068.CrossRefGoogle Scholar
  98. Mohamed R, Meilan R, Ostry ME, Michler CH, Strauss. SH (2001) Bacterio-opsin gene overexpression fails to elevate fungal disease resistance in transgenic poplar (Populus). Can J For Res 31:268–275.CrossRefGoogle Scholar
  99. Molina R, Massicotte H, Trappe. JM (1992) Specificity phenomena in mycorrhizal symbioses: community-ecological consequences and practical implications. In: Allen MF (ed) Mycorrhizal Functioning: an Integrative Plant-Fungal Process. Routledge, Chapman & Hall, New York, pp. 357–423.Google Scholar
  100. Nehls U, Grunze N, Willmann M, Reich M, Kuester. H (2007) Sugar for my honey: carbohydrate partitioning in ectomycorrhizal symbiosis. Phytochemistry 68:82–91.PubMedCrossRefGoogle Scholar
  101. Newcombe G (1996) The specificity of fungal pathogens of Populus. In: Stettler RF, Bradshaw HD jr, Heilman PE, Hinckley TM (eds) Biology of Populus and Its Implications for Management and Conservation. NRC Research Press, National Research Council of Canada, Ottawa, pp. 223–246.Google Scholar
  102. Newcombe G (2003) Native Venturia inopina sp. nov., specific to Populus trichocarpa and its hybrids. Mycol Res 107:108–116.PubMedCrossRefGoogle Scholar
  103. Newcombe G, Chastagner. GA (1993) First report of the Eurasian poplar leaf rust fungus, Melampsora laricici-populina, in North America. Plant Dis 77:532–535.CrossRefGoogle Scholar
  104. Newcombe G, Chastagner GA, Schuette W, Stanton. BJ (1994) Mortality among hybrid poplar clones in a stool bed following leaf rust caused by Melampsora medusae f.sp. deltoidae. Can J For Res 24:1984–1987.CrossRefGoogle Scholar
  105. Newcombe G, Ostry M, Hubbes M, Perinet P, Mottet. M-J (2001) Poplar Diseases. In: Dickmann JGIDI, Eckenwalder JE, Richardson J (eds) Poplar Culture in North America. Part A,  Chapter 8. NRC Research Press, National Research Council of Canada, Ottawa, ON K1A 0R6, Canada, pp. 249–276.Google Scholar
  106. Newcombe G, Shipunov A, Eigenbrode SD, Raghavendra A, Ding H, Anderson CL, Menjivar R, Crawford M, Schwarzländer. M (2009) Endophytes influence protection and growth of an invasive plant. Commun Integr Biol 2:1–3.CrossRefGoogle Scholar
  107. Nischwitz C, Newcombe G, Anderson. CL (2004) Host specialization of the mycoparasite Eudarluca caricis and its evolutionary relationship to Ampelomyces. Mycol Res 109:421–428.CrossRefGoogle Scholar
  108. Obase K, Tamai Y, Yajima T, Miyamoto. T (2007) Mycorrhizal associations in woody plant species at the Mt. Usu volcano, Japan. Mycorrhiza 17:209–215.PubMedCrossRefGoogle Scholar
  109. Omacini M, Chaneton EJ, Ghersa CM, Muller. CB (2001) Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature 409:78–81.PubMedCrossRefGoogle Scholar
  110. Omacini M, Eggers T, Bonkowski M, Gange. AC (2006) Leaf endophytes affect mycorrhizal status and growth of co-infected and neighbouring plants. Funct Ecol 20:226–232.CrossRefGoogle Scholar
  111. Opler PA (1978) Insects of American Chestnut: Possible Importance and Conservation Concerns. The American Chestnut Symposium, Morgantown, West Virginia.Google Scholar
  112. Paillet FL (2002) Chestnut: history and ecology of a transformed species. J Biogeogr 29:1517–1530.CrossRefGoogle Scholar
  113. Pei MH, McCracken. AR (2005) Rust Diseases of Willow and Poplar. CABI Publishing, Wallingford.CrossRefGoogle Scholar
  114. Peskan-Berghofer T, Shahollari B, Giong PH, Hehl S, Markert C, Blanke V, Kost G, Varma A, Oelmuller. R (2004) Association of Piriformospora indica with Arabidopsis thaliana roots represents a novel system to study beneficial plant-microbe interactions and involves early plant protein modifications in the endoplasmic reticulum and at the plasma membrane. Physiol Plant 122:465–477.CrossRefGoogle Scholar
  115. Phipps CJ (2007) Entopeltacites remberi sp. nov. from the Miocene of Clarkia, Idaho, USA. Rev Palaeobot Palynol 145:193–200.CrossRefGoogle Scholar
  116. Pieterse CMJ, Dicke. M (2007) Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends Plant Sci 12:564–569.PubMedCrossRefGoogle Scholar
  117. Pimentel D (2008) Preface special issue: conservation biological control. Biol Control 45:171.CrossRefGoogle Scholar
  118. Piotrowski JS, Lekberg Y, Harner MJ, Ramsey PW, Rillig. MC (2008) Dynamics of mycorrhizae during development of riparian forests along an unregulated river. Ecography 31:245–253.CrossRefGoogle Scholar
  119. Pirozynski KA (1976) Fossil fungi. Ann Rev Phytopathol 14:237–246.CrossRefGoogle Scholar
  120. Pirttila AM, Pospiech H, Laukkanen H, Myllyla R, Hohtola. A (2003) Two Endophytic Fungi in Different Tissues of Scots Pine Buds. Microb Ecol 45:53–62.PubMedCrossRefGoogle Scholar
  121. Pozo MJ, Azcon-Aguilar. C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398.PubMedCrossRefGoogle Scholar
  122. Quoreshi AM, Khasa. DP (2008) Effectiveness of mycorrhizal inoculation in the nursery on root colonization, growth, and nutrient uptake of aspen and balsam poplar. Biomass and Bioenergy 32:381–391.CrossRefGoogle Scholar
  123. Raacke IC, von Rad U, Mueller MJ, Berger. S (2006) Yeast increases resistance in Arabidopsis against Pseudomonas syringae and Botrytis cinerea by salicylic acid-dependent as well as – independent mechanisms. Mol Plant-Microbe Interact 19:1138–1146.PubMedCrossRefGoogle Scholar
  124. Rai M, Acharya D, Singh A, Varma. A (2001) Positive growth responses of the medicinal plants Spilanthes calva and Withania somnifera to inoculation by Piriformospora indica in a field trial. Mycorrhiza 11:123–128.CrossRefGoogle Scholar
  125. Rasmussen S, Parsons AJ, Bassett S, Christensen MJ, Hume DE, Johnson LJ, Johnson RD, Simpson WR, Stacke C, Voisey. CR (2007) High nitrogen supply and carbohydrate content reduce fungal endophyte and alkaloid concentration in Lolium perenne. New Phytol 173:787–797.PubMedCrossRefGoogle Scholar
  126. Rasmussen S, Parsons AJ, Fraser K, Xue H, Newman. JA (2008) Metabolic profiles of Lolium perenne are differentially affected by nitrogen supply, carbohydrate content, and fungal endophyte infection. Plant Physiol 146:1440–1453.PubMedCrossRefGoogle Scholar
  127. Redman RS, Ranson JC, Rodriguez. RJ (1999) Conversion of the pathogenic fungus Colletotrichum magna to a nonpathogenic, endophytic mutualist by gene disruption. Mol Plant-Microbe Interact 12:969–975.CrossRefGoogle Scholar
  128. Redman RS, Seehan KB, Stout RG, Rodriquez RJ, Henson. JM (2002) Thermotolerance generated by plant/fungal symbiosis. Science 298:1581.PubMedCrossRefGoogle Scholar
  129. Rember WC (1991) Stratigraphy and Paleobotany of Miocene Lake Sediments Near Clarkia. Idaho, University of Idaho, Moscow, Idaho.Google Scholar
  130. Remy W, Taylor TN, Hass H, Kerp. H (1994) 400 million year old vesicular arbuscular mycorrhizae (VAM). Proc Nat Acad Sci USA 91:11841–11843.PubMedCrossRefGoogle Scholar
  131. Richter J, Kohler A, Morin E, Palme K, Martin F, Ditengou F, Legué. V (2009) The ectomycorrhizal fungus L. bicolor stimulates lateral root formation in A. thaliana and P. tremula x P. alba through auxin signaling pathways. Plant Physiol. submitted.Google Scholar
  132. Riemenschneider DE, Stanton BJ, Vallée G, Périnet. P (2001) Poplar breeding strategies. Part A,  Chapter 2. In: Luster DIDickmann, Isebrands JG, Eckenwalder JE,Richardson J(eds) Poplar Culture in North America. NRC Research Press, National Research Council of Canada, Ottawa, Ontario, Canada, pp. 43–76.Google Scholar
  133. Rinaldi C, Kohler A, Frey P, Duchaussoy F, Ningre N, Couloux A, Wincker P, Le Thiec D, Fluch S, Martin F, Duplessis. S (2007) Transcript profiling of poplar leaves upon infection with compatible and incompatible strains of the foliar rust Melampsora larici-populina. Plant Physiol 144:347–366.PubMedCrossRefGoogle Scholar
  134. Rodriguez R, Redman. R (2008) More than 400 million years of evolution and some plants still can’t make it on their own: plant stress tolerance via fungal symbiosis. J Exp Botany 59:1109–1114.CrossRefGoogle Scholar
  135. Rossman AY (2009) The impact of invasive fungi on agricultural ecosystems in the United States. Biol Invasions 11:97–107.CrossRefGoogle Scholar
  136. Rossman AY, Farr DF, Platas G, Newcombe. G 2008. Hydropisphaera fungicola Rossman, Farr & Newcombe, sp. nov., Fungal Planet.Google Scholar
  137. Rubini MR, Silva-Ribeiro RT, Pomella AWV, Maki CS, Araújo WL, dos Santos DR, Azevedo JL (2005) Diversity of endophytic fungal community of cacao (Theobroma cacao L.) and biological control of Crinipellis perniciosa, causal agent of Witches’ Broom Disease. Int J Biol Sci 1:24–33.PubMedGoogle Scholar
  138. Ruiz-Lozano JM, Gianinazzi S, Gianinazzi-Pearson. V (1999) Genes involved in resistance to powdery mildew in barley differentially modulate root colonization by the mycorrhizal fungus Glomus mosseae. Mycorrhiza 9:237–240.CrossRefGoogle Scholar
  139. Santamaria O, Diez. JJ (2005) Fungi in leaves, twigs and stem bark of Populus tremula from northern Spain. For Pathol 35:95–104.Google Scholar
  140. Sauter M, Hager. A (1989) The mycorrhizal fungus Amanita muscaria induces chitinase activity in roots and in suspension-cultured cells of its host Picea abies. Planta 179:61–66.CrossRefGoogle Scholar
  141. Scervino JM, Ponce MA, Erra-Bassells R, Vierheilig H, Ocampo JA, Godeas. A (2005) Arbuscular mycorrhizal colonization of tomato by Gigaspora and Glomus species in the presence of root flavonoids. J Plant Physiol 162:625–633.PubMedCrossRefGoogle Scholar
  142. Schafer P, Khatabi B, Kogel. K-H (2007) Root cell death and systemic effects of Piriformospora indica: a study on mutualism. FEMS Microbiol Lett 275:1–7.PubMedCrossRefGoogle Scholar
  143. Schulz B, Boyle. C (2005) The endophytic continuum. Mycol Res 109:661–686.PubMedCrossRefGoogle Scholar
  144. SchÜßLer A, Schwarzott D, Walker. C (2002) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421.Google Scholar
  145. Selle A, Willmann M, Grunze N, Geßler A, Weiß M, Nehls. U (2005) The high-affinity poplar ammonium importer PttAMT1. 2 and its role in ectomycorrhizal symbiosis. New Phytol 168:697–706.PubMedCrossRefGoogle Scholar
  146. Shahollari B, Vadassery J, Varma A, Oelmuller. R (2007) A leucine-rich repeat protein is required for growth promotion and enhanced seed production mediated by the endophytic fungus Piriformospora indica in Arabidopsis thaliana. Plant J 50:1–13.PubMedCrossRefGoogle Scholar
  147. Shigo A (1963) Fungi associated with the discolorations around rot columns caused by Fomes igniarius. Plant Dis Rep 47:820–823.Google Scholar
  148. Shipunov, A., Newcombe, G, Raghavendra, and A, Anderson. C (2008) Hidden diversity of endophytic fungi in an invasive plant. Am J Botany 95:1096–1108.CrossRefGoogle Scholar
  149. Sieber TN (2007) Endophytic fungi in forest trees: are they mutualists? Fungal Biol Rev 21:75–89.CrossRefGoogle Scholar
  150. Siemens JA, Zwiazek. JJ (2008) Root hydraulic properties and growth of balsam poplar (Poplus balsamifera) mycorrhizal with Hebeloma crustuliniforme and Wilcoxina mikolae var. mikolae mycorrhiza 18:393–401.Google Scholar
  151. Sirrenberg A, Gobel C, Grond S, Cempinski N, Feussner I, Pawlowski. K (2007) Piriformospora indica induces increased root branching in Arabidopsis through IAA production. Physiol Plant 131:581–589.PubMedCrossRefGoogle Scholar
  152. Stein E, Molitor A, Kogel KH, Waller. F (2008) Systemic resistance in Arabidopsis conferred by the mycorrhizal fungus Piriformospora indica requires jasmonic acid signaling and the cytoplasmic function of NPR1. Plant Cell Physiol 49:1747–1751.PubMedCrossRefGoogle Scholar
  153. Stone JK, Bacon CW, White JF Jr. (2000) An overview of endophytic microbes: endophytism defined. In: Bacon CW, White, JF Jr (eds) Microbial Endophytes. Marcel Dekker, Inc., New York, 3–29.Google Scholar
  154. Strauss SH, Brunner AM, Busov VB, Ma C, Meilan. R (2004) Ten lessons from 15 years of transgenic Populus research. Forestry 77:455–465.CrossRefGoogle Scholar
  155. Strobel G (2006) Muscodor albus and its biological promise. J Ind Microbiol Biotechnol 33:514–522.PubMedCrossRefGoogle Scholar
  156. Strobel GA, Dirkse E, Sears J, Markworth. C (2001) Volatile antimicrobials from Muscodor albus, a novel endophytic fungus. Microbiology 147:2943–2950.PubMedGoogle Scholar
  157. Tagu D, Bastien C, Faivre-Rampant P, Garbaye J, Vion P, Villar M, Martin. F (2005) Genetic analysis of phenotypic variation for ectomycorrhiza formation in an interspecific F1 poplar full-sib family. Mycorrhiza 15:87–91.PubMedCrossRefGoogle Scholar
  158. Tagu D, Faivre Rampant P, Lapeyrie F, Frey-Klett P, Vion P, Villar. M (2001) Variation in the ability to form ectomycorrhizas in the F1 progeny of an interspecific poplar (Populus spp.) cross. Mycorrhiza 10:237–240.CrossRefGoogle Scholar
  159. Tanaka A, Christensen MJ, Takemoto D, Park P, Scotta. B (2006) Reactive oxygen species play a role in regulating a fungus-perennial ryegrass mutualistic interaction. Plant Cell 18:1052–1066.PubMedCrossRefGoogle Scholar
  160. Thormann MN, Currah RS, Bayley. SE (2003) Succession of microfungal assemblages in decomposing peatland plants. Plant Soil 250:323–333.CrossRefGoogle Scholar
  161. Tikhonovich IA, Provorov. NA (2007) Cooperation of plants and microorganisms: getting closer to the genetic construction of sustainable agro-systems. Biotechnol J 2:833–848.PubMedCrossRefGoogle Scholar
  162. Tsuneda A, Currah. RS (2005) Knufia endospora, a new dematiaceous hyphomycete from trembling aspen [Populus]. Reports of the Tottori Mycological Institute (Japan) 42:1–9.Google Scholar
  163. Tsuneda A, Hambleton S, Currah. RS (2004) Morphology and phylogenetic placement of Endoconidioma, a new endoconidial genus from trembling aspen. Mycologia 96:1128–1135.CrossRefPubMedGoogle Scholar
  164. Tuskan, GA., DiFazio, S, Jansson, S, Bohlmann, J, Grigoriev, I, Hellsten, U, Putnam, and N, Ralph, S, Rombauts, S., Salamov, A., Schein, J., Sterck, L., Aerts, A., Bhalerao, RR., Bhalerao, RP., Blaudez, D., Boerjan, W., Brun, A., Brunner, A., Busov, V., Campbell, M., Carlson, J., Chalot, M., Chapman, J., Chen, GL., Cooper, D., Coutinho, PM., Cou-turier, J., Covert, S., Cronk, Q., Cunningham, R., Davis, J., Degroeve, S., Dejardin, A., Depamphilis, C., Detter, J., Dirks, B., Dubchak, I., Duplessis, S., Ehlting, J., Ellis, B., Gendler, K., Goodstein, D., Gribskov, M., Grimwood, J., Groover, A., Gunter, L., Ham-berger, B., Heinze, B., Helariutta, Y., Henrissat, B., Holligan, D., Holt, R., Huang, W., Islam-Faridi, N., Jones, S., Jones-Rhoades, M., Jorgensen, R., Joshi, C., Kangasjarvi, J., Karlsson, J., Kelleher, C., Kirkpatrick, R., Kirst, M., Kohler, A., Kalluri, U., Larimer, F., Leebens-Mack, J., Leple, JC., Locascio, P., Lou, Y., Lucas, S., Martin, F., Montan-ini, B., Napoli, C., Nelson, DR., Nelson, C., Nieminen, K., Nilsson, O., Pereda, V., Peter, G., Philippe, R., Pilate, G., Poliakov, A., Razumovskaya, J., Richardson, P., Rinaldi, C., Ritland, K., Rouze, P., Ryaboy, D., Schmutz, J., Schrader, J., Segerman, B., Shin, H., Siddiqui, A., Sterky, F., Terry, A., Tsai, CJ., Uberbacher, E., Unneberg, P., Vahala, J., Wall, K., Wessler, S., Yang, G., Yin, T., Douglas, C., Marra, M., Sandberg, G., Van de Peer, Y,and, Rokhsar, D (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604.PubMedCrossRefGoogle Scholar
  165. Ulrich K, Ulrich A, Ewald. D (2008) Diversity of endophytic bacterial communities in poplar grown under field conditions. FEMS Microbiol Ecol 63:169–180.PubMedCrossRefGoogle Scholar
  166. Valdez Barillas JR, Paschke MW, Ralphs MH, Child. RD (2007) White locoweed toxicity is facilitated by a fungal endophyte and nitrogen-fixing bacteria. Ecology 88:1850–1856.PubMedCrossRefGoogle Scholar
  167. Van Aken B, Peres CM, Doty SL, Yoon JM, Schnoor. JL (2004) Methylobacterium populi sp. nov., a novel aerobic, pink-pigmented, facultatively methylotrophic, methane-utilizing bacterium isolated from poplar trees (Populus deltoides× nigra DN34). Int J Syst Evol Microbiol 54:1191–1196.PubMedCrossRefGoogle Scholar
  168. van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders. IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72.CrossRefGoogle Scholar
  169. Van Wees SCM, Van der Ent S, Pieterse. CMJ (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11:443–448.PubMedCrossRefGoogle Scholar
  170. Varma A, Verma S, Sahay N, Butehorn B, Franken. P (1999) Piriformospora indica, a cultivable plant-growth-promoting root endophyte. Appl Environ Microbiol 65:2741–2744.PubMedGoogle Scholar
  171. Vega FE, Posada F, Catherine Aime M, Pava-Ripoll M, Infante F, Rehner. SA (2008) Entomopathogenic fungal endophytes. Biol Control 46:72–82.CrossRefGoogle Scholar
  172. Verma S, Varma A, Rexer KH, Hassel A, Kost G, Sarbhoy A, Bisen P, Bütehorn B, Franken. P (1998) Piriformospora indica, gen. et sp. nov., a new root-colonizing fungus. Mycologia 90:896–903.CrossRefGoogle Scholar
  173. Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Huckelhoven R, Neumann C, Wettstein D, Franken P, Kogel. KH (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Nat Acad Sci 102:13386–13391.PubMedCrossRefGoogle Scholar
  174. Wang Y, Ohara Y, Nakayashiki H, Tosa Y, Mayama. S (2005) Microarray analysis of the gene expression profile induced by the endophytic plant growth-promoting rhizobacteria, Pseudomonas fluorescens FPT9601-T5 in Arabidopsis. Mol Plant-Microbe Interact 18:385–396.PubMedCrossRefGoogle Scholar
  175. Wang B, Qiu. YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363.PubMedCrossRefGoogle Scholar
  176. Weingartner DH, Basham. JT (1985) Variations in the Growth and Defect of Aspen (Populus tremuloides Michx.) Clones in Northern Ontario. Ontario Ministry of Natural Resources, Toronto, Ontario.Google Scholar
  177. Weiss M, Selosse MA, Rexer KH, Urban A, Oberwinkler. F (2004) Sebacinales: a hitherto overlooked cosm of heterobasidiomycetes with a broad mycorrhizal potential. Mycol Res 108:1003–1010.PubMedCrossRefGoogle Scholar
  178. Whitham TG, Floate KD, Martinsen GD, Driebe EM, Keim. P (1996) Ecological and evolutionary implications of hybridization: Populus-herbivore interactions. Part I,  Chapter 11. In: Stettler RF, Bradshaw HD, Heilman PE, Hinckley TM(eds) Biology of Populus and Its Implications for Management And Conservation. NRC Research Press, Ottawa, Ontario, Canada, pp. 247–275.Google Scholar
  179. Wicklow DT, Roth S, Deyrup ST, Gloer. JB (2005) A protective endophyte of maize: Acremonium zeae antibiotics inhibitory to Aspergillus flavus and Fusarium verticillioides. Mycol Res 109:610–618.PubMedCrossRefGoogle Scholar
  180. Wilkinson HH, Siegel MR, Blankenship JD, Mallory AC, Bush LP, Schardl. CL (2000) Contribution of fungal loline alkaloids to protection from aphids in a grass-endophyte mutualism. Mol Plant-Microbe Interact 13:1027–1033.PubMedCrossRefGoogle Scholar
  181. Wilson D, Carrol. GC (1997) Avoidance of high-endophyte space by gall-forming insects. Ecology 78:2153–2163.CrossRefGoogle Scholar
  182. Xin Y, Shang. J (2005) Bio-control trials of Chaetomium spirale ND35 against apple canker. J For Res 16:121–124.CrossRefGoogle Scholar
  183. Yi H, Calvo Polanco M, MacKinnon MD, Zwiazek. JJ (2008) Responses of ectomycorrhizal Populus tremuloides and Betula papyrifera seedlings to salinity. Environ Exp Botany 62:357–363.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • George Newcombe
    • 1
  • Francis Martin
    • 2
  • Annegret Kohler
    • 2
  1. 1.Department of Forest ResourcesCenter for Research on Invasive Species and Small Populations, University of IdahoMoscowUSA
  2. 2.UMR INRA-UHP “Interactions Arbres/Micro-Organismes”, INRA-NancyChampenouxFrance

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