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Mycorrhizal Networks Facilitate Tree Communication, Learning, and Memory

  • Suzanne W. Simard
Chapter
Part of the Signaling and Communication in Plants book series (SIGCOMM)

Abstract

Mycorrhizal fungal networks linking the roots of trees in forests are increasingly recognized to facilitate inter-tree communication via resource, defense, and kin recognition signaling and thereby influence the sophisticated behavior of neighbors. These tree behaviors have cognitive qualities, including capabilities in perception, learning, and memory, and they influence plant traits indicative of fitness. Here, I present evidence that the topology of mycorrhizal networks is similar to neural networks, with scale-free patterns and small-world properties that are correlated with local and global efficiencies important in intelligence. Moreover, the multiple exploration strategies of interconnecting fungal species have parallels with crystallized and fluid intelligence that are important in memory-based learning. The biochemical signals that transmit between trees through the fungal linkages are thought to provide resource subsidies to receivers, particularly among regenerating seedlings, and some of these signals appear to have similarities with neurotransmitters. I provide examples of neighboring tree behavioral, learning, and memory responses facilitated by communication through mycorrhizal networks, including, respectively, (1) enhanced understory seedling survival, growth, nutrition, and mycorrhization, (2) increased defense chemistry and kin selection, and (3) collective memory-based interactions among trees, fungi, salmon, bears, and people that enhance the health of the whole forest ecosystem. Viewing this evidence through the lens of tree cognition, microbiome collaborations, and forest intelligence may contribute to a more holistic approach to studying ecosystems and a greater human empathy and caring for the health of our forests.

Notes

Acknowledgments

I thank my graduate students, postdoctoral fellows, and collaborators who contributed to this research on mycorrhizal networks over the years, including Amanda Asay, Jason Barker, Marcus Bingham, Camille Defrenne, Julie Deslippe, Dan Durall, Monika Gorzelak, Melanie Jones, Justine Karst, Allen Larocque, Deon Louw, Katie McMahen, Gabriel Orrego, Huamani Orrego, Julia Amerongen Maddison, Greg Pec, Leanne Philip, Brian Pickles, Teresa Ryan, Laura Super, Francois Teste, Brendan Tweig, and Matt Zustovic. This research was supported by a Natural Sciences and Engineering Research Council (NSERC) Discovery Grant to SWS.

References

  1. Agerer R (2001) Exploration types of ectomycorrhizal mycelial systems: a proposal to classify mycorrhizal mycelial systems with respect to their ecologically important contact area with the substrate. Mycorrhiza 11:107–114CrossRefGoogle Scholar
  2. Agerer R (2006) Fungal relationships and structural identity of their ectomycorrhizae. Mycol Prog 5:67–107CrossRefGoogle Scholar
  3. Archibald JM (2011) Origin of eukaryotic cells: 40 years on. Symbiosis 54:69–86CrossRefGoogle Scholar
  4. Arnebrant K, Ek H, Finlay RD, Söderström B (1993) Nitrogen translocation between Alnus glutinosa (L.) Gaertn. seedlings inoculated with Frankia sp. and Pinus contorta Dougl. ex Loud seedlings connected by a common ectomycorrhizal mycelium. New Phytol 24:231–242CrossRefGoogle Scholar
  5. Asay AK (2013) Mycorrhizal facilitation of kin recognition in interior Douglas-fir (Pseudotsuga menziesii var. glauca). Master of Science thesis. University of British Columbia, Vancouver, CanadaGoogle Scholar
  6. Babikova Z, Gilbert L, Bruce TJA, Birkett M, Caulfield JC, Woodcock C, Pickett JA, Johnson D (2013) Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack. Ecol Lett 16:835–843PubMedCrossRefGoogle Scholar
  7. Bago B, Zipfel W, Williams RM, Jun J, Arreola R, Lammers PJ, Pfeffer PE, Shachar-Hill Y (2002) Translocation and utilization of fungal storage lipid in the arbuscular mycorrhizal symbiosis. Plant Physiol 128:109–124CrossRefGoogle Scholar
  8. Baluška F, Mancuso S (2013) Microorganism and filamentous fungi drive evolution of plant synapses. Front Cell Infect Microbiol 3:1–9CrossRefGoogle Scholar
  9. Baluška F, Volkmann D, Menzel D (2005) Plant synapses: actin-based domains for cell-to-cell communication. Trends Plant Sci 10:106–111PubMedCrossRefGoogle Scholar
  10. Baluška F, Mancuso S, Volkmann D, Darwin F (2009) The ‘root-brain’ hypothesis of Charles and Francis Darwin. Plant Signal Behav 4:1121–1127PubMedPubMedCentralCrossRefGoogle Scholar
  11. Baluška F, Mancuso S, Volkmann D, Barlow PW (2010) Root apex transition zone: a signalling-response nexus in the root. Trends Plant Sci 15:402–408PubMedCrossRefGoogle Scholar
  12. Barabási A-L, Albert R (1999) Emergence of scaling in random networks. Science 286:509–512PubMedCrossRefGoogle Scholar
  13. Barbey AK (2017) Network neuroscience theory of human intelligence. Trends Cogn Sci 22:8–20PubMedCrossRefGoogle Scholar
  14. Barto EK, Hilker M, Muller F, Mohney BK, Weidenhamer JD, Rillig MC (2011) The fungal fast lane: common mycorrhizal networks extend bioactive zones of allelochemicals in soils. PLoS One 6:e27195PubMedPubMedCentralCrossRefGoogle Scholar
  15. Bascompte J (2009) Mutualistic networks. Front Ecol Environ 7:429e436CrossRefGoogle Scholar
  16. Beiler KJ, Durall DM, Simard SW, Maxwell SA, Kretzer AM (2010) Architecture of the wood-wide web: Rhizopogon spp. genets link multiple Douglas-fir cohorts. New Phytol 185:543–553PubMedCrossRefGoogle Scholar
  17. Beiler KJ, Simard SW, LeMay V, Durall DM (2012) Vertical partitioning between sister species of Rhizopogon fungi on mesic and xeric sites in an interior Douglas-fir forest. Mol Ecol 21:6163–6174PubMedCrossRefGoogle Scholar
  18. Beiler KJ, Simard SW, Durall DM (2015) Topology of tree-mycorrhizal fungus interaction networks in xeric and mesic Douglas-fir forests. J Ecol (3):616–628CrossRefGoogle Scholar
  19. Bierdrzycki ML, Jilany TA, Dudley SA, Bais HP (2010) Root exudates mediate kin recognition in plants. Commun Integr Biol 3:28–35CrossRefGoogle Scholar
  20. Bingham MA, Simard SW (2012) Ectomycorrhizal networks of old Pseudotsuga menziesii var. glauca trees facilitate establishment of conspecific seedlings under drought. Ecosystems 15:188–199CrossRefGoogle Scholar
  21. Boddy L, Jones TH (2007) Mycelial responses in heterogeneous environments: parallels with macroorganisms. In: Gadd G, Watkinson SC, Dyer P (eds) Fungi in the environment. Cambridge University Press, Cambridge, pp 112–158CrossRefGoogle Scholar
  22. Bowery NG, Smart TG (2006) GABA and glycine as neurotransmitters: a brief history. Br J Pharmacol 147:S109–S119PubMedPubMedCentralCrossRefGoogle Scholar
  23. Bray D (2003) Molecular networks: the top-down view. Science 301:1864–1865PubMedCrossRefGoogle Scholar
  24. Brenner ED, Stahlberg R, Mancuso S, Vivanco J, Baluška F, Van Volkenburgh E (2006) Plant neurobiology: an integrated view of plant signaling. Trends Plant Sci 11:413–419PubMedPubMedCentralCrossRefGoogle Scholar
  25. Brownlee C, Duddridge J, Malibari A, Read D (1983) The structure and function of mycelial systems of ectomycorrhizal roots with special reference to their role in forming inter-plant connections and providing pathways for assimilate and water transport. Plant Soil 71:433–443CrossRefGoogle Scholar
  26. Craik F, Bialystok E (2006) Cognition through the lifespan: mechanisms of change. Trends Cogn Sci 10:131–148PubMedCrossRefGoogle Scholar
  27. Darwin CR (1880) The power of movement in plants. John Murray, LondonCrossRefGoogle Scholar
  28. Dehaene S, Sergent C, Changeux J-P (2003) A neuronal network model linking subjective reports and objective physiological data during conscious perception. Proc Natl Acad Sci USA 100:8520–8525PubMedPubMedCentralCrossRefGoogle Scholar
  29. Deslippe JR, Simard SW (2011) Below-ground carbon transfer among Betula nana may increase with warming in Arctic tundra. New Phytol 192:689–698PubMedCrossRefGoogle Scholar
  30. Deslippe JR, Hartmann M, Grayston SJ, Simard SW, Mohn WW (2016) Stable isotope probing implicates Cortinarius collinitus in carbon transfer through ectomycorrhizal mycelial networks in the field. New Phytol 210:383–390PubMedCrossRefGoogle Scholar
  31. Dudley SA, File AL (2008) Kin recognition in an annual plant. Biol Lett 3:435–438CrossRefGoogle Scholar
  32. Dudley SA, Murphy GP, File AL (2013) Kin recognition and competition in plants. Funct Ecol 27:898–906CrossRefGoogle Scholar
  33. Eason WR, Newman EI, Chuba PN (1991) Specificity of interplant cycling of phosphorus: the role of mycorrhizas. Plant Soil 137:267–274CrossRefGoogle Scholar
  34. Egerton-Warburton LM, Querejeta JI, Allen MF (2007) Common mycorrhizal networks provide a potential pathway for the transfer of hydraulically lifted water between plants. J Exp Bot 58:1473–1483PubMedCrossRefGoogle Scholar
  35. Ek H, Andersson S, Söderström B (1996) Carbon and nitrogen flow in silver birch and Norway spruce connected by a common mycorrhizal mycelium. Mycorrhiza 6:465–467CrossRefGoogle Scholar
  36. Ekblad A, Huss-Danell K (1995) Nitrogen fixation by Alnus incana and nitrogen transfer from A. incana to Pinus sylvestris influenced by macronutrient and ectomycorrhiza. New Phytol 131:453–459CrossRefGoogle Scholar
  37. Faust K, Raes J (2012) Microbial interactions: from networks to models. Nat Rev Microbiol 10:538–550PubMedCrossRefGoogle Scholar
  38. File AL, Klironomos J, Maherali H, Dudley SA (2012a) Plant kin recognition enhances abundance of symbiotic microbial partner. PLoS One 7:e45648PubMedPubMedCentralCrossRefGoogle Scholar
  39. File AL, Murphy GP, Dudley SA (2012b) Fitness consequences of plants growing with siblings: reconciling kin selection, niche partitioning and competitive ability. Proc R Soc B 279:209–218PubMedCrossRefGoogle Scholar
  40. Finlay RD (1989) Functional aspects of phosphorus uptake and carbon translocation in incompatible ectomycorrhizal associations between Pinus sylvestris and Suillus grevillei and Boletinus cavipes. New Phytol 112:185–192CrossRefGoogle Scholar
  41. Finlay RD, Read DJ (1986) The structure and function of the vegetative mycelium of ectomycorrhizal plants. II. The uptake and distribution of phosphorus by mycelial strands interconnecting host plants. New Phytol 103:157–165CrossRefGoogle Scholar
  42. Gagliano M (2012) Green symphonies: a call for studies on acoustic communication in plants. Behav Ecol 24:289–796Google Scholar
  43. Gagliano M (2014) In a green frame of mind: perspectives on the behavioural ecology and cognitive nature of plants. AoB Plants 7:plu075PubMedPubMedCentralGoogle Scholar
  44. Gagliano M, Grimonprez M (2015) Breaking the silence – language and the making of meaning in plants. Ecophys 7:145–152Google Scholar
  45. Garcia-Garrido JM, Ocampo JA (2002) Regulation of the plant defence response in arbuscular mycorrhizal symbiosis. J Exp Bot 53:1377–1386PubMedCrossRefGoogle Scholar
  46. Giovannetti M, Sbrana C, Avio L, Stranil P (2004) Patterns of belowground plant interconnections established by means of arbuscular mycorrhizal networks. New Phytol 164:175–181CrossRefGoogle Scholar
  47. Giovannetti M, Avio L, Fortuna P, Pellegrino E, Sbrana C, Strani P (2005) At the root of the Wood Wide Web: self recognition and non-self incompatibility in mycorrhizal networks. Plant Signal Behav 1:1–5CrossRefGoogle Scholar
  48. Gorzelak M (2017) Kin selected signal transfer through mycorrhizal networks in Douglas-fir. PhD Dissertation. University of British Columbia, Vancouver, CanadaGoogle Scholar
  49. Gorzelak M, Asay AK, Pickles BJ, Simard SW (2015) Inter-plant communication through mycorrhizal networks mediates complex adaptive behaviour in plant communities. AoB Plants 7:plv050PubMedPubMedCentralCrossRefGoogle Scholar
  50. Gyuricza V, Thiry Y, Wannijn J, Declerck S, de Boulois HD (2010) Radiocesium transfer between Medicago truncatula plants via a common mycorrhizal network. Environ Microbiol 12:2180–2189PubMedGoogle Scholar
  51. He X-H, Critchley C, Bledsoe C (2003) Nitrogen transfer within and between plants through common mycorrhizal networks (CMNs). Crit Rev Plant Sci 22:531–567CrossRefGoogle Scholar
  52. He XH, Critchley C, Ng H, Bledsoe C (2004) Reciprocal N (15NH4+ or 15NO3-) transfer between non-N2-fixing Eucalyptus maculata and N2-fixing Casuarina cunninghamiana linked by the ectomycorrhizal fungus Pisolithus sp. New Phytol 163:629–640CrossRefGoogle Scholar
  53. He XH, Critchley C, Ng H, Bledsoe C (2005) Nodulated N2-fixing Casuarina cunninghamiana is the sink for net N transfer from non-N2-fixing Eucalyptus maculata via an ectomycorrhizal fungus Pisolithus sp. supplied as ammonium nitrate. New Phytol 167:897–912PubMedCrossRefGoogle Scholar
  54. He XH, Bledsoe CS, Zasoski RJ, Southworth D, Horwath WR (2006) Rapid nitrogen transfer from ectomycorrhizal pines to adjacent ectomycorrhizal and arbuscular mycorrhizal plants in a California oak woodland. New Phytol 170:143–151PubMedCrossRefGoogle Scholar
  55. He XH, Xu M, Qiu GY, Zhou J (2009) Use of 15Nstable isotope to quantify nitrogen transfer between mycorrhizal plants. J Plant Ecol 2:107–118CrossRefGoogle Scholar
  56. Heaton L, Obara B, Grau V, Jones N, Nakagaki T, Boddy L, Fricker MD (2012) Analysis of fungal networks. Fungal Biol Rev 26:12e29CrossRefGoogle Scholar
  57. Heil M, Karban R (2009) Explaining evolution of plant communication by airborne signals. Trends Ecol Evol 25:137–144CrossRefGoogle Scholar
  58. Hobbie E, Agerer R (2010) Nitrogen isotopes in ectomycorrhizal sporocarps correspond to belowground exploration types. Plant Soil 327:71–83CrossRefGoogle Scholar
  59. Hocking MD, Reynolds JD (2011) Impacts of Salmon on riparian plant diversity. Science 331:1609–1612PubMedCrossRefGoogle Scholar
  60. Horton TR (ed) (2015) Mycorrhizal networks. Ecological studies. Netherlands: Springer, 224Google Scholar
  61. Humphreys CP, Franks PJ, Rees M, Bidartondo MI, Leake JR, Beerling DJ (2010) Mutualistic mycorrhiza-like symbiosis in the most ancient group of land plants. Nat Commun 1:103PubMedCrossRefGoogle Scholar
  62. Ingham RE, Trofymow JA, Ingham ER, Coleman DC (1985) Interactions of bacteria, fungi, and their nematode grazers: effects on nutrient cycling and plant growth. Ecol Monogr 55:119–140CrossRefGoogle Scholar
  63. Karban R, Shiojiri K (2009) Self-recognition affects plant communication and defense. Ecol Lett 12:502–506PubMedCrossRefGoogle Scholar
  64. Karban R, Yang LH, Edwards KF (2014) Volatile communication between plants that affects herbivory: a meta-analysis. Ecol Lett 17:44–52PubMedCrossRefGoogle Scholar
  65. Karst J, Erbilgin N, Pec GJ, Cigan PW, Najar A, Simard SW, Cahill JF Jr (2015) Ectomycorrhizal fungi mediate indirect effects of a bark beetle outbreak on secondary chemistry and establishment of pine seedlings. New Phytol 208:904–914PubMedCrossRefGoogle Scholar
  66. Kretzer AM, Luoma DL, Molina R, Spatafora JW (2003) Taxonomy of the Rhizopogon vinicolor species complex based on analysis of ITS sequences and microsatellite loci. Mycologia 95:480–487PubMedCrossRefGoogle Scholar
  67. Kurz WA, Dymond CC, Stinson G, Rampley GJ, Neilson ET, Carroll AL, Ebata T, Safranyik L (2008) Mountain pine beetle and forest carbon feedback to climate change. Nature 452:987–990PubMedCrossRefGoogle Scholar
  68. 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 Bot 82:1016–1045CrossRefGoogle Scholar
  69. Lehto T, Zwiazek JJ (2011) Ectomycorrhizas and water relations of trees: a review. Mycorrhiza 21:71–90PubMedCrossRefGoogle Scholar
  70. Levin SA (2005) Self-organization and the emergence of complexity in ecological systems. Bioscience 55:1075CrossRefGoogle Scholar
  71. Lian C, Narimatsu M, Nara K, Hogetsu T (2006) Tricholoma matsutake in a natural Pinus densiflora forest: correspondence between above- and below- ground genets, association with multiple host trees and alteration of existing ectomycorrhizal communities. New Phytol 171:825–836PubMedCrossRefGoogle Scholar
  72. Lilleskov EA, Hobbie EA, Horton TR (2011) Conservation of ectomycorrhizal fungi: exploring the linkages between functional and taxonomic responses to anthropogenic N deposition. Fungal Ecol 4:174–183CrossRefGoogle Scholar
  73. Margulis L (1981) Symbiosis in cell evolution. WH Freeman Company, San FranciscoGoogle Scholar
  74. Martin F, Stewart GR, Genetet I, Le Tacon F (1986) Assimilation of 15NH4 by beech (Fagus sylvatica L.) ectomycorrhizas. New Phytol 102:85–94CrossRefGoogle Scholar
  75. McNickle GG, St. Clair CC, Cahill JF Jr (2009) Focusing the metaphor: plant root foraging behavior. Trends Ecol Evol 24:419–426PubMedCrossRefGoogle Scholar
  76. Meding SM, Zasoski RJ (2008) Hyphal-mediated transfer of nitrate, arsenic, cesium, rubidium, and strontium between arbuscular mycorrhizal forbs and grasses from a California oak woodland. Soil Biol Biochem 40:126–134CrossRefGoogle Scholar
  77. Molina R (2013) Rhizopogon. In: Cairney JWG, Chamber SM (eds) Ectomycorrhizal fungi: key Genera in profile. Springer Verlag, Berlin, pp 129–152Google Scholar
  78. Molina R, Horton TR (2015) Mycorrhiza specificity: its role in the development and function of common mycelial networks. In: Horton TR (ed) Mycorrhizal networks, Ecological studies, vol 224. Springer, Netherlands, pp 1–39CrossRefGoogle Scholar
  79. Molina R, Massicotte H, Trappe J (1992) Specificity phenomena in mycorrhizal symbioses: community-ecological consequences and practical implications. In: Allen MF (ed) Mycorrhizal functioning: an integrative plant–fungal process. Chapman and Hall, New York, pp 357–423Google Scholar
  80. Nehls U, Grunze B, Willmann M, Reich M, Küster H (2007) Sugar for my honey: carbohydrate partitioning in ectomycorrhizal symbiosis. Phytochemistry 68:82–91PubMedCrossRefGoogle Scholar
  81. Novoplansky A (2009) Picking battles wisely: plant behaviour under competition. Plant Cell Environ 32:726–741PubMedCrossRefGoogle Scholar
  82. Pelagio-Flores R, Ortíz-Castro R, Méndez-Bravo A, Macías-Rodríguez L, López-Bucio J (2011) Serotonin, a tryptophan-derived signal conserved in plants and animals, regulates root system architecture probably acting as a natural auxin inhibitor in Arabidopsis thaliana. Plant Cell Physiol 52:490–508PubMedCrossRefGoogle Scholar
  83. Perry DA, Margolis H, Choquette C, Molina R, Trappe JM (1989) Ectomycorrhizal mediation of competition between coniferous tree species. New Phytol 112:501–511PubMedCrossRefGoogle Scholar
  84. Pickles BJ, Wilhelm R, Asay AK, Hahn A, Simard SW, Mohn WW (2016) Transfer of 13C between paired Douglas-fir seedlings reveals plant kinship effects and uptake of exudates by ectomycorrhizas. New Phytol 214:400–411PubMedCrossRefGoogle Scholar
  85. Poorter H, Niklas KJ, Reich PB, Oleksy J, Poot P, Mommer L (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol 193:30–50PubMedCrossRefGoogle Scholar
  86. Pozo MJ, López-Ráez JA, Azcón-Aguilar C, García-Garrido JM (2015) Phytohormones as integrators of environmental signals in the regulation of mycorrhizal symbioses. New Phytol 205:1431–1436PubMedCrossRefGoogle Scholar
  87. Querejeta JI, Egerton-Warburton LM, Prieto I, Vargas R, Allen MF (2012) Changes in soil hyphal abundance and viability can alter the patterns of hydraulic redistribution by plant roots. Plant Soil 355:63–73CrossRefGoogle Scholar
  88. Rai V (2002) Role of amino acids in plant responses to stresses. Biol Plant 45:481–487CrossRefGoogle Scholar
  89. Rygiewicz PT, Anderson CP (1994) Mycorrhizae alter quality and quantity of carbon allocated below ground. Nature 369:58–60CrossRefGoogle Scholar
  90. Scheffer M, Carpenter S, Foley JA, Folke C, Walker B (2001) Catastrophic shifts in ecosystems. Nat Rev 413:591–596Google Scholar
  91. Selosse M-A, Richard F, He X, Simard SW (2006) Mycorrhizal network: des liaisons dangereuses? Trends Ecol Evol 21:621–628PubMedCrossRefGoogle Scholar
  92. Semchenko M, John EA, Hutchings MJ (2007) Effects of physical connection and genetic identity of neighbouring ramets on root-placement patterns in two clonal species. New Phytol 176:644–654PubMedCrossRefGoogle Scholar
  93. Simard SW (2012) Mycorrhizal networks and seedling establishment in Douglas-fir forests (Chapter 4). In: Southworth D (ed) Biocomplexity of plant–fungal interactions, 1st edn. Wiley, Chichester, pp 85–107. isbn-10:0813815940 | isbn-13:978-0813815947CrossRefGoogle Scholar
  94. Simard SW, Durall DM (2004) Mycorrhizal networks: a review of their extent, function, and importance. Can J Bot 82:1140–1165CrossRefGoogle Scholar
  95. Simard SW, Beiler KJ, Bingham MA, Deslippe JR, Philip LJ, Teste FP (2012) Mycorrhizal networks: mechanisms, ecology and modelling. Fungal Biol Rev 26:39–60CrossRefGoogle Scholar
  96. Simard SW, Martin K, Vyse A, Larson B (2013) Meta-networks of fungi, fauna and flora as agents of complex adaptive systems. In: Puettmann K, Messier C, Coates KD (eds) Managing world forests as complex adaptive systems: building resilience to the challenge of global change, vol 7. Routledge, New York, pp 133–164Google Scholar
  97. Simard SW, Asay AK, Beiler KJ, Bingham MA, Deslippe JR, He X, Philip LJ, Song Y, Teste FP (2015) Resource transfer between plants through ectomycorrhizal networks. In: Horton TR (ed) Mycorrhizal networks, Ecological studies, vol 224. Springer, Netherlands, pp 133–176CrossRefGoogle Scholar
  98. Smith S, Read D (2008) Mycorrhizal symbiosis. Academic, LondonGoogle Scholar
  99. Smith SE, Smith FA (1990) Structure and function of the interfaces in biotrophic symbioses as they relate to nutrient transport. New Phytol 114:1–38CrossRefGoogle Scholar
  100. Song YY, Zeng RS, Xu JF, Li J, Shen X, Yihdego WG (2010) Interplant communication of tomato plants through underground common mycorrhizal networks. PLoS One 5:e13324PubMedPubMedCentralCrossRefGoogle Scholar
  101. Song YY, Ye M, Li C, He X, Zhu-Salzman K, Wang RL, Su YJ, Luo SM, Zheng RS (2014) Hijacking common mycorrhizal networks for herbivore-induced defence signal transfer between tomato plants. Sci Rep 4:3915PubMedPubMedCentralCrossRefGoogle Scholar
  102. Song YY, Simard SW, Carroll A, Mohn WW, Zheng RS (2015) Defoliation of interior Douglas-fir elicits carbon transfer and defense signalling to ponderosa pine neighbors through ectomycorrhizal networks. Sci Rep 5:8495PubMedPubMedCentralCrossRefGoogle Scholar
  103. Southworth D, He X-H, Swenson W, Bledsoe CS (2005) Application of network theory to potential mycorrhizal networks. Mycorrhiza 15:589–595PubMedCrossRefGoogle Scholar
  104. Taylor AFS, Gebauer G, Read DJ (2004) Uptake of nitrogen and carbon from double-labelled (15N and 13C) glycine by mycorrhizal pine seedlings. New Phytol 164:383–388CrossRefGoogle Scholar
  105. Teste FP, Simard SW, Durall DM, Guy RD, Jones MD (2009) Access to mycorrhizal networks and roots of trees: importance for seedling survival and resource transfer. Ecology 90:2808–2822PubMedCrossRefGoogle Scholar
  106. Teste FP, Simard SW, Durall DM, Guy RD, Berch SM (2010) Net carbon transfer between Pseudotsuga menziesii var. glauca seedlings in the field is influenced by soil disturbance. J Ecol 98:429–439CrossRefGoogle Scholar
  107. Toju H, Sato H, Tanabe AS (2014) Diversity and spatial structure of belowground plant– fungal symbiosis in a mixed subtropical forest of ectomycorrhizal and arbuscular mycorrhizal plants. PLoS One:e86566Google Scholar
  108. Trappe JM (1987) Phylogenetic and ecologic aspects of mycotrophy in the angiosperms from an evolutionary standpoint. In: Safir GR (ed) Ecophysiology of VA mycorrhizal plants. CRC Press, FloridaGoogle Scholar
  109. Treu R, Karst J, Randall M, Pec GJ, Cigan P, Simard SW, Cooke J, Erbilgin N, Cahill JF Jr (2014) Decline of ectomycorrhizal fungi following mountain pine beetle infestation. Ecology 95:1096–1103PubMedCrossRefGoogle Scholar
  110. Twieg B, Durall DM, Simard SW (2007) Ectomycorrhizal fungal succession in mixed temperate forests. New Phytol 176:437–447PubMedCrossRefGoogle Scholar
  111. Van der Heijden MGA, Hartmann M (2016) Networking in the plant microbiome. PLoS Biol 14:e1002378PubMedPubMedCentralCrossRefGoogle Scholar
  112. Van der Heijden MGA, Horton TR (2009) Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems. J Ecol 97:1139–1150CrossRefGoogle Scholar
  113. Van Dorp C (2016) Rhizopogon mycorrhizal networks with interior douglas-fir in selectively harvested and non-harvested forests. Master of Science Thesis, University of British ColumbiaGoogle Scholar
  114. Wipf D, Ludewig U, Tegeder M, Rentsch D, Koch W, Frommer WB (2002) Conservation of amino acid transporters in fungi, plants and animals. Trends Biochem Sci 27:139–147PubMedCrossRefGoogle Scholar
  115. Yang H, Bognor M, Steinhoff Y-D, Ludewig U (2010) H+-independent glutamine transport in plant root tips. PLoS One 5:e8917PubMedPubMedCentralCrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Forest and Conservation Sciences, Faculty of ForestryUniversity of British ColumbiaVancouverCanada

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