Skip to main content

Defense and Nutrient Mutualisms in Populus

  • Chapter
  • First Online:

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

Abstract

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.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Arnold AE, Maynard Z, Gilbert GS, Coley PD, Kursar TA (2000) Are tropical fungal endophytes hyperdiverse? Ecol Lett 3:267–274.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Beckers GJ, Conrath. U (2007) Priming for stress resistance: from the lab to the field. Curr Opin Plant Biol 10:425–431.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Bittel P, Robatzek. S (2007) Microbe-associated molecular patterns (MAMPs) probe plant immunity. Curr Opin Plant Biol 10:335–341.

    Article  CAS  PubMed  Google Scholar 

  • Boddy L (2000) Interspecific combative interactions between wood-decaying basidiomycetes. FEMS Microbiol Ecol 31:185–194.

    Article  CAS  PubMed  Google Scholar 

  • Borowicz VA (2001) Do arbuscular mycorrhizal fungi alter plant-pathogen relations? Ecology 82:3057–3068.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • Brundrett M (2004) Diversity and classification of mycorrhizal associations. Biol Rev 79:473–495.

    Article  PubMed  Google Scholar 

  • Brundrett M, Bougher N, Dell B, Grove T, Malajczuk. N (1996) Working with Mycorrhizas in Forestry and Agriculture. ACIAR, Canberra, Australia.

    Google Scholar 

  • Brunner AM, Busov VB, Strauss. SH (2004) Poplar genome sequence: functional genomics in an ecologically dominant plant species. Trends Plant Sci 9:49–56.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Calhoun LA, Findlay JA, Miller JD, Whitney. NJ (1992) Metabolites toxic to spruce budworm from balsam fir needle endophytes. Mycol Res 96:281–286.

    Article  Google Scholar 

  • Chapela IH (1989) Fungi in healthy stems and branches of American beech and aspen: a comparative study. New Phytol 113:65–75.

    Article  Google Scholar 

  • Chase JM (2003) Community assembly: when should history matter? Oecologia 136:489–498.

    Article  PubMed  Google Scholar 

  • Clark CL, Miller JD, Whitney. NJ (1989) Toxicity of conifer needle endophytes to spruce budworm. Mycol Res 93:508–512.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Clay K (1988) Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 69:10–16.

    Article  Google Scholar 

  • Clay K, Holah. J (1999) Fungal endophyte symbiosis and plant diversity in successional fields. Science 285:1742–1744.

    Article  CAS  PubMed  Google Scholar 

  • Clay K, Schardl. C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160:S99–S127.

    Article  PubMed  Google Scholar 

  • Cox CB, Moore. PD (2005) Biogeography – An Ecological and Evolutionary Approach. Blackwell, Oxford, U.K.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Doty SL (2008) Enhancing phytoremediation through the use of transgenics and endophytes. New Phyt 179:318–333.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Druege U, Baltruschat H, Franken. P (2007) Piriformospora indica promotes adventitious root formation in cuttings. Scientia Horticulturae 112:422–426.

    Article  Google Scholar 

  • 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 

  • Erb M, Ton J, Degenhardt J, Turlings. TCJ (2008) Interactions between arthropod-induced aboveground and belowground defenses in plants. Plant Physiol 146:867–874.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Farr DF, Rossman AY, Palm ME, McCray. EB (n.d.) Fungal Databases. Systematic Mycology and Microbiology, USDA, ARS http://nt.ars-grin.gov/fungaldatabases/.

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Freeman S, Rodriguez. RJ (1993) Genetic conversion of a fungal plant pathogen to a nonpathogenic, endophytic mutualist. Science 260:75–78.

    Article  CAS  PubMed  Google Scholar 

  • Fukami T, Morin. PJ (2003) Productivity-biodiversity relationships depend on the history of community assembly. Nature 424:423–426.

    Article  CAS  PubMed  Google Scholar 

  • Ganley RJ, Brunsfeld SJ, Newcombe. G (2004) A community of unknown, endophytic fungi in western white pine. Proc Nat Acad Sci 101:10107–10112.

    Article  CAS  PubMed  Google Scholar 

  • Ganley RJ, Sniezko RA, Newcombe. G (2008) Endophyte-mediated resistance against white pine blister rust in Pinus monticola. For Ecol Manag 255:2751–2760.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Glazebrook J, Ton. J (2007) Biotic interactions: Recurring themes and expanding scales. Curr Opin Plant Biol 10:331–334.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Haine ER (2008) Symbiont-mediated protection. Proc Roy Soc B: Biol Sci 275:353–361.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Harman GE, Howell CR, Viterbo A, Chet I, Lorito. M (2004) Trichoderma species – opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56.

    Article  CAS  PubMed  Google Scholar 

  • Hawksworth DL (2001) The magnitude of fungal diversity: the 1.5 million species estimate revisited. Mycol Res 105:1422–1432.

    Article  Google Scholar 

  • Helm DJ, Allen EB, Trappe. JM (1996) Mycorrhizal chronosequence near Exit Glacier, Alaska. Can J Botany 74:1496–1506.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Hooker JE, Black KE, Perry RL, Atkinson. D (1995) Arbuscular mycorrhizal fungi induced alteration to root longevity of poplar. Plant Soil 172:327–329.

    Article  CAS  Google Scholar 

  • Hutchinson LJ (1999) Wood-inhabiting microfungi isolated from Populus tremuloides from Alberta and northeastern British Columbia. Can J Botany 77:898–905.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Jones JDG, Dangl. JL (2006) The plant immune system. Nature 444:323–329.

    Article  CAS  PubMed  Google Scholar 

  • Jones MD, Smith. SE (2004) Exploring functional definitions of mycorrhizas: are mycorrhizas always mutualisms? Can J Botany 82:1089–1109.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70.

    Article  CAS  PubMed  Google Scholar 

  • Kogel KH, Franken P, Hückelhoven R (2006) Endophyte or parasite–what decides? Curr Opin Plant Biol 9:358–363.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • Laflamme G, Lortie. M (1973) Micro-organismes dans les tissus colorés et cariés du peuplier faux-tremble. Can J For Res 3:155–160.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Liu CH, Zou WX, Hong L, Tan. RX (2001) Antifungal activity of Artemisia annua endophyte cultures against phytopathogenic fungi. J Biotechnol 88:277–282.

    Article  CAS  PubMed  Google Scholar 

  • Lodge DJ (2000) Ecto-or arbuscular mycorrhizas-which are best? New Phytol 146:353–354.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Martin F, Kohler A, Duplessis. S (2007) Living in harmony in the wood underground: ectomycorrhizal genomics. Curr Opin Plant Biol 10:204–210.

    Article  CAS  PubMed  Google Scholar 

  • Martin F, Tuskan GA, DiFazio SP, Lammers P, Newcombe G, Podila. GK (2004) Symbiotic sequencing for the Populus mesocosm. New Phytol 161:330–335.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Mitchell CE, Power. AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627.

    Article  CAS  PubMed  Google Scholar 

  • Mlot C (2004) Microbial diversity unbound. BioSci 54:1064–1068.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • Nehls U, Grunze N, Willmann M, Reich M, Kuester. H (2007) Sugar for my honey: carbohydrate partitioning in ectomycorrhizal symbiosis. Phytochemistry 68:82–91.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Newcombe G (2003) Native Venturia inopina sp. nov., specific to Populus trichocarpa and its hybrids. Mycol Res 107:108–116.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Omacini M, Chaneton EJ, Ghersa CM, Muller. CB (2001) Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature 409:78–81.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Opler PA (1978) Insects of American Chestnut: Possible Importance and Conservation Concerns. The American Chestnut Symposium, Morgantown, West Virginia.

    Google Scholar 

  • Paillet FL (2002) Chestnut: history and ecology of a transformed species. J Biogeogr 29:1517–1530.

    Article  Google Scholar 

  • Pei MH, McCracken. AR (2005) Rust Diseases of Willow and Poplar. CABI Publishing, Wallingford.

    Book  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Phipps CJ (2007) Entopeltacites remberi sp. nov. from the Miocene of Clarkia, Idaho, USA. Rev Palaeobot Palynol 145:193–200.

    Article  Google Scholar 

  • Pieterse CMJ, Dicke. M (2007) Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends Plant Sci 12:564–569.

    Article  CAS  PubMed  Google Scholar 

  • Pimentel D (2008) Preface special issue: conservation biological control. Biol Control 45:171.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Pirozynski KA (1976) Fossil fungi. Ann Rev Phytopathol 14:237–246.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Pozo MJ, Azcon-Aguilar. C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Redman RS, Seehan KB, Stout RG, Rodriquez RJ, Henson. JM (2002) Thermotolerance generated by plant/fungal symbiosis. Science 298:1581.

    Article  CAS  PubMed  Google Scholar 

  • Rember WC (1991) Stratigraphy and Paleobotany of Miocene Lake Sediments Near Clarkia. Idaho, University of Idaho, Moscow, Idaho.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Rossman AY (2009) The impact of invasive fungi on agricultural ecosystems in the United States. Biol Invasions 11:97–107.

    Article  Google Scholar 

  • Rossman AY, Farr DF, Platas G, Newcombe. G 2008. Hydropisphaera fungicola Rossman, Farr & Newcombe, sp. nov., Fungal Planet.

    Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Schulz B, Boyle. C (2005) The endophytic continuum. Mycol Res 109:661–686.

    Article  PubMed  Google Scholar 

  • SchÜßLer A, Schwarzott D, Walker. C (2002) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Shigo A (1963) Fungi associated with the discolorations around rot columns caused by Fomes igniarius. Plant Dis Rep 47:820–823.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Sieber TN (2007) Endophytic fungi in forest trees: are they mutualists? Fungal Biol Rev 21:75–89.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Strauss SH, Brunner AM, Busov VB, Ma C, Meilan. R (2004) Ten lessons from 15 years of transgenic Populus research. Forestry 77:455–465.

    Article  Google Scholar 

  • Strobel G (2006) Muscodor albus and its biological promise. J Ind Microbiol Biotechnol 33:514–522.

    Article  CAS  PubMed  Google Scholar 

  • Strobel GA, Dirkse E, Sears J, Markworth. C (2001) Volatile antimicrobials from Muscodor albus, a novel endophytic fungus. Microbiology 147:2943–2950.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Thormann MN, Currah RS, Bayley. SE (2003) Succession of microfungal assemblages in decomposing peatland plants. Plant Soil 250:323–333.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Tsuneda A, Hambleton S, Currah. RS (2004) Morphology and phylogenetic placement of Endoconidioma, a new endoconidial genus from trembling aspen. Mycologia 96:1128–1135.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Ulrich K, Ulrich A, Ewald. D (2008) Diversity of endophytic bacterial communities in poplar grown under field conditions. FEMS Microbiol Ecol 63:169–180.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Van Wees SCM, Van der Ent S, Pieterse. CMJ (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11:443–448.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Vega FE, Posada F, Catherine Aime M, Pava-Ripoll M, Infante F, Rehner. SA (2008) Entomopathogenic fungal endophytes. Biol Control 46:72–82.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Wang B, Qiu. YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Wilson D, Carrol. GC (1997) Avoidance of high-endophyte space by gall-forming insects. Ecology 78:2153–2163.

    Article  Google Scholar 

  • Xin Y, Shang. J (2005) Bio-control trials of Chaetomium spirale ND35 against apple canker. J For Res 16:121–124.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to George Newcombe .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Newcombe, G., Martin, F., Kohler, A. (2010). Defense and Nutrient Mutualisms in Populus . In: Jansson, S., Bhalerao, R., Groover, A. (eds) Genetics and Genomics of Populus. Plant Genetics and Genomics: Crops and Models, vol 8. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-1541-2_12

Download citation

Publish with us

Policies and ethics