Beneficial Soil Microbiota as Mediators of the Plant Defensive Phenotype and Aboveground Plant-Herbivore Interactions

  • Martin SchädlerEmail author
  • Daniel J. Ballhorn
Part of the Progress in Botany book series (BOTANY, volume 78)


The symbiosis with beneficial soil microbiota importantly affects plant physiology, growth and community structure. These effects are known to translate into changes of aboveground plant-herbivore interactions, and there is increasing evidence that microbial symbioses alter the defensive plant phenotype far beyond the primary plant metabolism. Microbe-mediated changes in plant defensive traits have been reported for various plant-microbe systems including both bacterial and fungal mutualists. Microbial mutualists not only affect the expression of direct plant defences, but also alter indirect defences like volatile production and extrafloral nectaries and thus have cascading effects on higher trophic levels. By simultaneously affecting a suite of plant defensive traits, they may modulate the benefits and costs of alternative defence strategies. Our understanding of the impact of plant-associated microbial mutualists in food webs is critical to elucidate their functional role in ecosystems. However, it is still limited by a lack of integration of natural complexity and evolutionary context into concepts and studies of microbe-plant-herbivore interactions.


Mycorrhizal Fungus Jasmonic Acid Iridoid Glycoside Extrafloral Nectar Indirect Defence 
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.



We thank Mehmet A. Balkan (Portland State University) for commenting on a former version of the manuscript. Funding by the National Science Foundation (NSF) to DJB (IOS grant #1457369) is gratefully acknowledged.


  1. Abu-Zeyad R, Khan AG, Khoo C (1999) Occurrence of arbuscular mycorrhiza in Castanospermum australe A. Cunn & C Fraser and effects on growth and production of castanospermine. Mycorrhiza 9:111–117. doi: 10.1007/s005720050008 Google Scholar
  2. Afkhami ME, Rudgers JA, Stachowicz JJ (2014) Multiple mutualist effects: conflict and synergy in multispecies mutualisms. Ecology 95:833–844. doi: 10.1890/13-1010.1 PubMedCrossRefGoogle Scholar
  3. Alguacil MD, Torrecillas E, Lozano Z, Roldan A (2011) Evidence of differences between the communities of arbuscular mycorrhizal fungi colonizing galls and roots of Prunus persica Infected by the root-knot nematode Meloidogyne incognita. Appl Environ Microbiol 77:8656–8661. doi: 10.1128/aem.05577-11 PubMedCentralCrossRefGoogle Scholar
  4. Andrade SAL, Malik S, Sawaya A, Bottcher A, Mazzafera P (2013) Association with arbuscular mycorrhizal fungi influences alkaloid synthesis and accumulation in Catharanthus roseus and Nicotiana tabacum plants. Acta Physiol Plant 35:867–880. doi: 10.1007/s11738-012-1130-8 CrossRefGoogle Scholar
  5. Antunes PM, de Varennes A, Rajcan I, Goss MJ (2006) Accumulation of specific flavonoids in soybean (Glycine max (L.) Merr.) as a function of the early tripartite symbiosis with arbuscular mycorrhizal fungi and Bradyrhizobium japonicum (Kirchner) Jordan. Soil Biol Biochem 38:1234–1242. doi: 10.1016/j.soilbio.2005.09.016 CrossRefGoogle Scholar
  6. Araim G, Saleem A, Arnason JT, Charest C (2009) Root colonization by an arbuscular mycorrhizal (AM) fungus Increases growth and secondary metabolism of purple Coneflower, Echinacea purpurea (L) Moench. J Agric Food Chem 57:2255–2258PubMedCrossRefGoogle Scholar
  7. Awasthi A, Bharti N, Nair P, Singh R, Shukla AK, Gupta MM, Darokar MP, Kalra A (2011) Synergistic effect of Glomus mosseae and nitrogen fixing Bacillus subtilis strain Daz26 on artemisinin content in Artemisia annua L. Appl Soil Ecol 49:125–130. doi:
  8. Babikova Z, Gilbert LBruce 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 16:835–843. doi: 10.1111/ele.12115 PubMedCrossRefGoogle Scholar
  9. Babikova Z, Gilbert L, Bruce T, Dewhirst SY, Pickett JA, Johnson D (2014a) Arbuscular mycorrhizal fungi and aphids interact by changing host plant quality and volatile emission. Funct Ecol 28:375–385CrossRefGoogle Scholar
  10. Babikova Z, Johnson D, Bruce T, Pickett J, Gilbert L (2014b) Underground allies: how and why do mycelial networks help plants defend themselves? Bioessays 36:21–26. doi: 10.1002/bies.201300092 PubMedCrossRefGoogle Scholar
  11. Babst BA et al (2005) Jasmonic acid induces rapid changes in carbon transport and partitioning in Populus. New Phytol 167:63–72. doi: 10.1111/j.1469-8137.2005.01388.x PubMedCrossRefGoogle Scholar
  12. Babst BA, Ferrieri RA, Thorpe MR, Orians CM (2008) Lymantria dispar herbivory induces rapid changes in carbon transport and partitioning in Populus nigra. Entomol Exp Appl 128:117–125CrossRefGoogle Scholar
  13. Bacht M (2015) Multitrophic interactions in oak. PhD doctoral thesis, University of Marburg, MarburgGoogle Scholar
  14. Baldwin IT, Halitschke R, Kessler A, Schittko U (2001) Merging molecular and ecological approaches in plant-insect interactions. Curr Opin Plant Biol 4:351–358PubMedCrossRefGoogle Scholar
  15. Ballare CL (2011) Jasmonate-induced defenses: a tale of intelligence, collaborators and rascals. Trends Plant Sci 16:249–257. doi: 10.1016/j.tplants.2010.12.001 PubMedCrossRefGoogle Scholar
  16. Ballhorn DJ, Heil M, Pietrowski A, Lieberei R (2007) Quantitative effects of cyanogenesis on an adapted herbivore. J Chem Ecol 33:2195–2208. doi: 10.1007/s10886-007-9380-4 PubMedCrossRefGoogle Scholar
  17. Ballhorn DJ, Kautz S, Lion U, Heil M (2008) Trade-offs between direct and indirect defences of lima bean (Phaseolus lunatus). J Ecol 96:971–980CrossRefGoogle Scholar
  18. Ballhorn DJ, Kautz S, Rakotoarivelo FP (2009) Quantitative variability of cyanogenesis in Cathariostachys madagascariensis – the main food plant of Bamboo Lemurs in Southeastern Madagascar. Am J Primatol 71:305–315PubMedCrossRefGoogle Scholar
  19. Ballhorn DJ, Kautz S, Schädler M (2013) Induced plant defense via volatile production is dependent on rhizobial symbiosis. Oecologia 172:833–846. doi: 10.1007/s00442-012-2539-x PubMedCrossRefGoogle Scholar
  20. Ballhorn DJ, Godschalx AL, Smart SM, Kautz S, Schadler M (2014a) Chemical defense lowers plant competitiveness. Oecologia 176:811–824. doi: 10.1007/s00442-014-3036-1 PubMedCrossRefGoogle Scholar
  21. Ballhorn DJ, Kay J, Kautz S (2014b) Quantitative effects of leaf area removal on indirect defense of lima Bean (Phaseolus lunatus) in nature. J Chem Ecol 40:294–296. doi: 10.1007/s10886-014-0392-6 PubMedCrossRefGoogle Scholar
  22. Ballhorn DJ, Schädler M, Elias JD, Millar JA, Kautz S (2016) Friend or foe-light availability determines the relationship between mycorrhizal fungi, rhizobia and lima bean (Phaseolus lunatus). Plos One 11(5), e0154116. doi: 10.1371/journal.pone.0154116 PubMedPubMedCentralCrossRefGoogle Scholar
  23. Barber NA (2013) Arbuscular mycorrhizal fungi are necessary for the induced response to herbivores by Cucumis sativus. J Plant Ecol 6:171–176. doi: 10.1093/jpe/rts026 CrossRefGoogle Scholar
  24. Barrett LG, Broadhurst LM, Thrall PH (2012) Geographic adaptation in plant-soil mutualisms: tests using Acacia spp. and rhizobial bacteria. Funct Ecol 26:457–468. doi: 10.1111/j.1365-2435.2011.01940.x CrossRefGoogle Scholar
  25. Barto EK, Rillig MC (2010) Does herbivory really suppress mycorrhiza? A meta-analysis. J Ecol 98:745–753. doi: 10.1111/j.1365-2745.2010.01658.x CrossRefGoogle Scholar
  26. Battaglia D et al (2013) Tomato below ground-above ground interactions: Trichoderma longibrachiatum affects the performance of Macrosiphum euphorbiae and its natural antagonists. Mol Plant Microbe Interact 26:1249–1256. doi: 10.1094/mpmi-02-13-0059-r PubMedCrossRefGoogle Scholar
  27. Baum C, Toljander YK, Eckhardt KU, Weih M (2009) The significance of host-fungus combinations in ectomycorrhizal symbioses for the chemical quality of willow foliage. Plant and Soil 323:213–224. doi: 10.1007/s11104-009-9928-x CrossRefGoogle Scholar
  28. Beckers GJM, Spoel SH (2006) Fine-tuning plant defence signalling: salicylate versus jasmonate. Plant Biol 8:1–10. doi: 10.1055/s-2005-872705 PubMedCrossRefGoogle Scholar
  29. Bennett AE, Bever JD (2007) Mycorrhizal species differentially alter plant growth and response to herbivory. Ecology 88:210–218PubMedCrossRefGoogle Scholar
  30. Bennett AE, Alers-Garcia J, Bever JD (2006) Three-way interactions among mutualistic mycorrhizal fungi, plants, and plant enemies: hypotheses and synthesis. Am Nat 167:141–152PubMedCrossRefGoogle Scholar
  31. Bennett AE, Bever JD, Bowers MD (2009) Arbuscular mycorrhizal fungal species suppress inducible plant responses and alter defensive strategies following herbivory. Oecologia 160:771–779. doi: 10.1007/s00442-009-1338-5 PubMedCrossRefGoogle Scholar
  32. Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486. doi:
  33. Bezemer TM, Fountain MT, Barea JM, Christensen S, Dekker SC, Duyts H, van Hal R, Harvey JA, Hedlund K, Maraun M, Mikola J, Mladenov MG, Robin C, de Ruiter PC, Scheu S, Setälä H, Smilauer P, van der Putten WH (2010) Divergent composition but similar function of soil food webs of individual plants: plant species and community effects. Ecology 91:3027–3036PubMedCrossRefGoogle Scholar
  34. Bi HH, Song YY, Zeng RS (2007) Biochemical and molecular responses of host plants to mycorrhizal infection and their roles in plant defence. Allelopathy J 20:15–27Google Scholar
  35. Biere A, Tack AJM (2013) Evolutionary adaptation in three-way interactions between plants, microbes and arthropods. Funct Ecol 27:646–660. doi: 10.1111/1365-2435.12096 CrossRefGoogle Scholar
  36. Bonfante P, Anca IA (2009) Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annu Rev Microbiol 63:363–383. doi: 10.1146/annurev.micro.091208.073504 PubMedCrossRefGoogle Scholar
  37. Borowicz VA (1997) A fungal root symbiont modifies plant resistance to an insect herbivore. Oecologia 112:534–542CrossRefGoogle Scholar
  38. Borowicz VA (2013) The impact of arbuscular mycorrhizal fungi on plant growth following herbivory: a search for pattern. Acta Oecol 52:1–9. doi: 10.1016/j.actao.2013.06.004 CrossRefGoogle Scholar
  39. Bronstein JL (2001) The exploitation of mutualisms. Ecol Lett 4:277–287. doi: 10.1046/j.1461-0248.2001.00218.x CrossRefGoogle Scholar
  40. Brunner SM, Goos RJ, Swenson SJ, Foster SP, Schatz BG, Lawley YE, Prischmann-Voldseth DA (2015) Impact of nitrogen fixing and plant growth-promoting bacteria on a phloem-feeding soybean herbivore. Appl Soil Ecol 86:71–81. doi: 10.1016/j.apsoil.2014.10.007 CrossRefGoogle Scholar
  41. Cameron DD, Neal AL, van Wees SCM, Ton J (2013) Mycorrhiza-induced resistance: more than the sum of its parts? Trends Plant Sci 18:539–545. doi: 10.1016/j.tplants.2013.06.004 PubMedPubMedCentralCrossRefGoogle Scholar
  42. Carreon-Abud Y, Torres-Martinez R, Farfan-Soto B, Hernandez-Garcia A, Rios-Chavez P, Bello-Gonzalez MA, Martinez-Trujillo M, Salgado-Garciglia R (2015) Arbuscular mycorrhizal symbiosis increases the content of volatile terpenes and plant performance in Satureja macrostema (Benth.) Briq. Boletin Latinoamericano Y Del Caribe De Plantas Medicinales Y Aromaticas 14:273–279Google Scholar
  43. Cartieaux F, Contesto C, Gallou A, Desbrosses G, Kopka J, Taconnat L, Renou JP, Touraine B (2008) Simultaneous interaction of Arabidopsis thaliana with Bradyrhizobium sp strain ORS278 and Pseudomonas syringae pv. tomato DC3000 leads to complex transcriptome changes. Mol Plant Microbe Interact 21:244–259. doi: 10.1094/mpmi-21-2-0244 PubMedCrossRefGoogle Scholar
  44. Castell W, Fleischmann F, Heger T, Matyssek R (2015) Shaping theoretic foundations of holobiont-like systems. In: Canovas F, Luettge U, Matyssek R (eds) Progress in botany, vol 77. Springer, Heidelberg, pp 219–244. doi: 10.1007/978-3-319-25689.7_7
  45. Castillo G, Cruz LL, Tapia-Lopez R, Olmedo-Vicente E, Carmona D, Anaya-Lang AL, Fornoni J, Andraca-Gomez G, Valverde PL, Nunez-Faran J (2014) Selection mosaic exerted by specialist and generalist herbivores on chemical and physical defense of Datura stramonium. PLoS One 9. doi: 10.1371/journal.pone.0102478
  46. Ceccarelli N, Curadi M, Martelloni L, Sbrana C, Picciarelli P, Giovannetti M (2010) Mycorrhizal colonization impacts on phenolic content and antioxidant properties of artichoke leaves and flower heads two years after field transplant. Plant and Soil 335:311–323. doi: 10.1007/s11104-010-0417-z CrossRefGoogle Scholar
  47. Chandanie WA, Kubota M, Hyakumachi M (2009) Interactions between the arbuscular mycorrhizal fungus Glomus mosseae and plant growth-promoting fungi and their significance for enhancing plant growth and suppressing damping-off of cucumber (Cucumis sativus L.). Appl Soil Ecol 41:336–341CrossRefGoogle Scholar
  48. Choudhary DK, Kasotia A, Jain S, Vaishnav A, Kumari S, Sharma KP, Varma A (2016) Bacterial-mediated tolerance and resistance to plants under abiotic and biotic stress. J Plant Growth Regul 35:276–300. doi: 10.1007/s00344-015-9521-x CrossRefGoogle Scholar
  49. Colebatch G, Trevaskis B, Udvardi M (2002a) Functional genomics: tools of the trade. New Phytol 153:27–36CrossRefGoogle Scholar
  50. Colebatch G, Trevaskis B, Udvardi M (2002b) Symbiotic nitrogen fixation research in the postgenomics era. New Phytol 153:37–42CrossRefGoogle Scholar
  51. Conrath U (2009) Priming of induced plant defense responses. Plant Innate Immun 51:361–395Google Scholar
  52. Corby HDL (1981) The systematic value of leguminous root nodules. In: Polhill RM, Raven PH (eds) Advances in legume systematics, Parts 1 and 2. Vol. 2 of the Proceedings of the International Legume Conference, Kew, Surrey, England, 24–29 July 1978. Xvi+425p. (Part 1); V+622p. (Part 2). Royal Botanic Gardens: Surrey, England. Illus. Paper:P657-670Google Scholar
  53. Cosme M, Stout MJ, Wurst S (2011) Effect of arbuscular mycorrhizal fungi (Glomus intraradices) on the oviposition of rice water weevil (Lissorhoptrus oryzophilus). Mycorrhiza 21:651–658. doi: 10.1007/s00572-011-0399-6 PubMedCrossRefGoogle Scholar
  54. Crawley MJ (1997) Plant-herbivore dynamics. In: Crawley MJ (ed) Plant ecology. Blackwell Science, Oxford, pp 401–474Google Scholar
  55. Crooks JA (2002) Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97:153–166CrossRefGoogle Scholar
  56. Crotti E, Balloi A, Hamdi C, Sansonno L, Marzorati M, Gonella E, Favia G, Cherif A, Alma A, Daffonchio D (2012) Microbial symbionts: a resource for the management of insect-related problems. J Microbial Biotechnol 5:307–317. doi: 10.1111/j.1751-7915.2011.00312.x CrossRefGoogle Scholar
  57. De Lange ES, Balmer D, Mauch-Mani B, Turlings TCJ (2014) Insect and pathogen attack and resistance in maize and its wild ancestors, the teosintes. New Phytol 204:329–341. doi: 10.1111/nph.13005 CrossRefGoogle Scholar
  58. Dean JM, Mescher MC, De Moraes CM (2009) Plant-rhizobia mutualism influences aphid abundance on soybean. Plant and Soil 323:187–196. doi: 10.1007/s11104-009-9924-1 CrossRefGoogle Scholar
  59. Dean JM, Mescher MC, De Moraes CM (2014) Plant dependence on rhizobia for nitrogen influences induced plant defenses and herbivore performance. Int J Mol Sci 15:1466–1480. doi: 10.3390/ijms15011466 PubMedPubMedCentralCrossRefGoogle Scholar
  60. Demirözer O, Tyler-Julian K, Funderburk J (2014) Association of pepper with arbuscular mycorrhizal fungi influences populations of the herbivore Frankliniella occidentalis (Thysanoptera: Thripidae). J Entomol Sci 49:156–165CrossRefGoogle Scholar
  61. Demirözer O, Özkaya HÖ, Aldemir T, Karapire M (2015) Does the association of arbuscular mycorrhizal fungi and two-spotted spider mite increase gossypol synthesis in two cotton cultivars? Fresenius Environ Bull 24:4199–4204Google Scholar
  62. Douglas AE (2008) Conflict, cheats and the persistence of symbioses. New Phytol 177:849–858. doi: 10.1111/j.1469-8137.2007.02326.x PubMedCrossRefGoogle Scholar
  63. Dresler-Nurmi A, Fewer DP, Räsänen LA, Lindström K (2007) The diversity and evolution of rhizobia. In: Pawlowski K (ed) Prokaryotic symbionts in plants. Springer, Heidelberg, pp 4–41. doi: 10.1007/7171_2007_099
  64. Eisenhauer N, Konig S, Sabais ACW, Renker C, Buscot F, Scheu S (2009) Impacts of earthworms and arbuscular mycorrhizal fungi (Glomus intraradices) on plant performance are not interrelated. Soil Biol Biochem 41:561–567CrossRefGoogle Scholar
  65. Eom AH, Wilson GWT, Hartnett DC (2001) Effects of ungulate grazers on arbuscular mycorrhizal symbiosis and fungal community structure in tallgrass prairie. Mycologia 93:233–242CrossRefGoogle Scholar
  66. Erb M, Veyrat N, Robert CAM, Xu H, Frey M, Ton J, Turlings TCJ (2015) Indole is an essential herbivore-induced volatile priming signal in maize. Nat Commun 6. doi: 10.1038/ncomms7273
  67. Fontana A, Reichelt M, Hempel S, Gershenzon J, Unsicker SB (2009) The effects of arbuscular mycorrhizal fungi on direct and indirect defense metabolites of Plantago lanceolata L. J Chem Ecol 35:833–843. doi: 10.1007/s10886-009-9654-0 PubMedPubMedCentralCrossRefGoogle Scholar
  68. Frey-Klett P, Garbaye J, Tarkka M (2007) The mycorrhiza helper bacteria revisited. New Phytol 176:22–36PubMedCrossRefGoogle Scholar
  69. Fritz M, Jakobsen I, Lyngkjaer MF, Thordal-Christensen H, Pons-Kuhnemann J (2006) Arbuscular mycorrhiza reduces susceptibility of tomato to Alternaria solani. Mycorrhiza 16:413–419. doi: 10.1007/s00572-006-0051-z PubMedCrossRefGoogle Scholar
  70. Frost CJ, Hunter MD (2008) Herbivore-induced shifts in carbon and nitrogen allocation in red oak seedlings. New Phytol 178:835–845PubMedCrossRefGoogle Scholar
  71. Gange AC, Ayres RL (1999) On the relation between arbuscular mycorrhizal colonization and plant ‘benefit’. Oikos 87:615–621. doi: 10.2307/3546829 CrossRefGoogle Scholar
  72. Gange AC, West HM (1994) Interactions between arbuscular mycorrhizal fungi and foliar-feeding insects in Plantago lanceolata L. New Phytol 128:79–87CrossRefGoogle Scholar
  73. Gange AC, Bower E, Brown VK (2002a) Differential effects of insect herbivory on arbuscular mycorrhizal colonization. Oecologia 131:103–112CrossRefGoogle Scholar
  74. Gange AC, Stagg PG, Ward LK (2002b) Arbuscular mycorrhizal fungi affect phytophagous insect specialism. Ecol Lett 5:11–15CrossRefGoogle Scholar
  75. Gange AC, Brown VK, Aplin DM (2003) Multitrophic links between arbuscular mycorrhizal fungi and insect parasitoids. Ecol Lett 6:1051–1055CrossRefGoogle Scholar
  76. Gange AC, Gane DRJ, Chen Y, Gong M (2005) Dual colonization of Eucalyptus urophylla S.T. Blake by arbuscular and ectomycorrhizal fungi affects levels of insect herbivore attack. Agric For Entomol 7:253–263. doi: 10.1111/j.1461-9555.2005.00268.x CrossRefGoogle Scholar
  77. Garcia I, Mendoza R (2012) Impact of defoliation intensities on plant biomass, nutrient uptake and arbuscular mycorrhizal symbiosis in Lotus tenuis growing in a saline-sodic soil. Plant Biol 14:964–971. doi: 10.1111/j.1438-8677.2012.00581.x PubMedCrossRefGoogle Scholar
  78. Garrido E, Bennett AE, Fornoni J, Strauss SY (2010) Variation in arbuscular mycorrhizal fungi colonization modifies the expression of tolerance to above-ground defoliation. J Ecol 98:43–49. doi: 10.1111/j.1365-2745.2009.01586.x CrossRefGoogle Scholar
  79. Gehring CA, Whitham TG (1994) Interactions between aboveground herbivores and the mycorrhizal mutualists of plants. Trends Ecol Evol 9:251–255PubMedCrossRefGoogle Scholar
  80. Gehring CA, Whitham TG (2002) Mycorrhizae-herbivore interactions: population and community consequences. In: van der Heijden MGA, Sanders IR (eds) Mycorrhizal ecology. Springer, Berlin, pp 295–320CrossRefGoogle Scholar
  81. Genre A, Russo G (2016) Does a common pathway transduce symbiotic signals in plant-microbe interactions? Front Plant Sci 7:96. doi: 10.3389/fpls.2016.00096 PubMedPubMedCentralCrossRefGoogle Scholar
  82. Gerlach N, Schmitz J, Polatajko A, Schlüter U, Fahnenstich H, Witt S, Fernie AR, Uroic K, Scholz U, Sonnewald U, Bucher M (2015) An integrated functional approach to dissect systemic responses in maize to arbuscular mycorrhizal symbiosis. Plant Cell Environ 38:1591–1612. doi: 10.1111/pce.12508 PubMedCrossRefGoogle Scholar
  83. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227. doi: 10.1146/annurev.phyto.43.040204.135923 PubMedCrossRefGoogle Scholar
  84. Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109–117. doi: 10.1139/m95-015 CrossRefGoogle Scholar
  85. Godschalx AL, Schadler M, Trisel JA, Balkan MA, Ballhorn DJ (2015) Ants are less attracted to the extrafloral nectar of plants with symbiotic, nitrogen-fixing rhizobia. Ecology 96:348–354. doi: 10.1890/14-1178.1 PubMedCrossRefGoogle Scholar
  86. Gopalakrishnan S, Sathya A, Vijayabharathi R, Varshney RK, Gowda CLL, Krishnamurthy L (2015) Plant growth promoting rhizobia: challenges and opportunities. 3 Biotech 5:355–377. doi: 10.1007/s13205-014-0241-x CrossRefGoogle Scholar
  87. Groten K, Nawaz A, Nguyen NHT, Santhanam R, Baldwin IT (2015) Silencing a key gene of the common symbiosis pathway in Nicotiana attenuata specifically impairs arbuscular mycorrhizal infection without influencing the root-associated microbiome or plant growth. Plant Cell Environ 38:2398–2416. doi: 10.1111/pce.12561 PubMedCrossRefGoogle Scholar
  88. Guerrieri E, Lingua G, Digilio MC, Massa N, Berta G (2004) Do interactions between plant roots and the rhizosphere affect parasitoid behaviour? Ecol Entomol 29:753–756CrossRefGoogle Scholar
  89. Halldorsson G, Sverrisson H, Eyjolfsdottir GG, Oddsdottir ES (2000) Ectomycorrhizae reduce damage to Russian larch by Otiorhynchus larvae. Scand J For Res 15:354–358CrossRefGoogle Scholar
  90. Hart M et al (2015) Inoculation with arbuscular mycorrhizal fungi improves the nutritional value of tomatoes. Mycorrhiza 25:359–376. doi: 10.1007/s00572-014-0617-0 PubMedCrossRefGoogle Scholar
  91. Hartley SE, Gange AC (2009) Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Annu Rev Entomol 54:323–342. doi: 10.1146/annurev.ento.54.110807.090614 PubMedCrossRefGoogle Scholar
  92. Hause B, Schaarschmidt S (2009) The role of jasmonates in mutualistic symbioses between plants and soil-born microorganisms. Phytochemistry 70:1589–1599. doi: 10.1016/j.phytochem.2009.07.003 PubMedCrossRefGoogle Scholar
  93. Heath KD, Lau JA (2011) Herbivores alter the fitness benefits of a plant-rhizobium mutualism. Acta Oecol 37:87–92. doi: 10.1016/j.actao.2010.12.002 CrossRefGoogle Scholar
  94. Heath KD, McGhee KE (2012) Coevolutionary constraints? The environment alters tripartite interaction traits in a legume. PLoS One 7. doi: 10.1371/journal.pone.0041567
  95. Heath KD, Stock AJ, Stinchcombe JR (2010) Mutualism variation in the nodulation response to nitrate. J Evol Biol 23:2494–2500. doi: 10.1111/j.1420-9101.2010.02092.x PubMedCrossRefGoogle Scholar
  96. Hector A et al (1999) Plant diversity and productivity experiments in European grasslands. Science 286:1123–1127PubMedCrossRefGoogle Scholar
  97. Heil M (2004) Direct defense or ecological costs: responses of herbivorous beetles to volatiles released by Wild Lima Bean (Phaseolus lunatus). J Chem Ecol 30:1289–1295. doi: 10.1023/B:JOEC.0000030299.59863.69 PubMedCrossRefGoogle Scholar
  98. Heil M (2011) Nectar: generation, regulation and ecological functions. Trends Plant Sci 16:191–200. doi:
  99. Heil M, Bueno JCS (2007) Herbivore-induced volatiles as rapid signals in systemic plant responses: how to quickly move the information? Plant Signal Behav 2:191–193PubMedPubMedCentralCrossRefGoogle Scholar
  100. Hempel S et al (2009) Specific bottom-up effects of arbuscular mycorrhizal fungi across a plant-herbivore-parasitoid system. Oecologia 160:267–277. doi: 10.1007/s00442-009-1294-0 PubMedPubMedCentralCrossRefGoogle Scholar
  101. Hendrickson OQ, Burgess D, Perinet P, Tremblay F, Chatatpaul L (1993) Effects of Frankia on field performance of Alnus clones and seedlings. Plant and Soil 150:295–302. doi: 10.1007/BF00013027 CrossRefGoogle Scholar
  102. Henke C et al (2015) Analysis of volatiles from Picea abies triggered by below-ground interactions. Environ Exp Bot 110:56–61. doi: 10.1016/j.envexpbot.2014.09.009 CrossRefGoogle Scholar
  103. Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335. doi: 10.1086/417659 CrossRefGoogle Scholar
  104. Hermsmeier D, Schittko U, Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. I. Large-scale changes in the accumulation of growth- and defense-related plant mRNAs. Plant Physiol 125:683–700PubMedPubMedCentralCrossRefGoogle Scholar
  105. Herridge DF, Peoples MB, Boddey RM (2008) Global inputs of biological nitrogen fixation in agricultural systems. Plant and Soil 311:1–18CrossRefGoogle Scholar
  106. Herrmann S, Buscot F (2007) Cross talks at the morphogenetic, physiological and gene regulation levels between the mycobiont Piloderma croceum and oak microcuttings (Quercus robur) during formation of ectomycorrhizas. Phytochemistry 68:52–67. doi: 10.1016/j.phytochem.2006.09.028 PubMedCrossRefGoogle Scholar
  107. Hobbie JE, Hobbie EA (2006) N-15 in symbiotic fungi and plants estimates nitrogen and carbon flux rates in Arctic tundra. Ecology 87:816–822PubMedCrossRefGoogle Scholar
  108. Hoeksema JD, Piculell BJ, Thompson JN (2009) Within-population genetic variability in mycorrhizal interactions. Commun Integr Biol 2:110–112PubMedPubMedCentralCrossRefGoogle Scholar
  109. Hoffmann D, Vierheilig H, Riegler P, Schausberger P (2009) Arbuscular mycorrhizal symbiosis increases host plant acceptance and population growth rates of the two-spotted spider mite Tetranychus urticae. Oecologia 158:663–671PubMedCrossRefGoogle Scholar
  110. Hoffmann D, Vierheilig H, Peneder S, Schausberger P (2011a) Mycorrhiza modulates aboveground tri-trophic interactions to the fitness benefit of its host plant. Ecol Entomol 36:574–581. doi: 10.1111/j.1365-2311.2011.01298.x CrossRefGoogle Scholar
  111. Hoffmann D, Vierheilig H, Riegler P, Schausberger P (2011b) Arbuscular mycorrhizal symbiosis increases host plant acceptance and population growth rates of the two-spotted spider mite Tetranychus urticae (vol 158, pg 663, 2009). Oecologia 165:545. doi: 10.1007/s00442-010-1852-5 CrossRefGoogle Scholar
  112. Hoffmann D, Vierheilig H, Schausberger P (2011c) Arbuscular mycorrhiza enhances preference of ovipositing predatory mites for direct prey-related cues. Physiol Entomol 36:90–95. doi: 10.1111/j.1365-3032.2010.00751.x CrossRefGoogle Scholar
  113. Hoffmann D, Vierheilig H, Schausberger P (2011d) Mycorrhiza-induced trophic cascade enhances fitness and population growth of an acarine predator. Oecologia 166:141–149. doi: 10.1007/s00442-010-1821-z PubMedCrossRefGoogle Scholar
  114. Hol WHG et al (2010) Reduction of rare soil microbes modifies plant-herbivore interactions. Ecol Lett 13:292–301. doi: 10.1111/j.1461-0248.2009.01424.x PubMedCrossRefGoogle Scholar
  115. Hui D, Iqbal J, Lehmann K, Gase K, Saluz HP, Baldwin IT (2003) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata: V. Microarray analysis and further characterization of large-scale changes in herbivore-induced mRNAs. Plant Physiol 131:1877–1893. doi: 10.1104/pp.102.018176 PubMedPubMedCentralCrossRefGoogle Scholar
  116. Irmer S et al (2015) New aspect of plant-rhizobia interaction: alkaloid biosynthesis in Crotalaria depends on nodulation. Proc Natl Acad Sci U S A 112:4164–4169. doi: 10.1073/pnas.1423457112 PubMedPubMedCentralCrossRefGoogle Scholar
  117. Jogaiah S, Abdelrahman M, Tran L-SP, Shin-ichi I (2013) Characterization of rhizosphere fungi that mediate resistance in tomato against bacterial wilt disease. J Exp Bot 64:3829–3842. doi: 10.1093/jxb/ert212 PubMedCrossRefGoogle Scholar
  118. Johnson SN, Rasmann S (2015) Root-feeding insects and their interactions with organisms in the rhizosphere. In: Berenbaum MR (ed) Annual review of entomology, vol 60. Annual Reviews, Palo Alto, pp 517–535Google Scholar
  119. Johnson ND, Liu B, Bentley BL (1987) The effects of nitrogen-fixation, soil nitrate, and defoliation on the growth, alkaloids, and nitrogen levels of Lupinus succulentus (Fabaceae). Oecologia 74:425–431CrossRefGoogle Scholar
  120. Johnson ND, Bentley, BL, Barbosa A, Krischik VA, Jones CG (1991) Symbiotic N 2 -fixation and the elements of plant resistance to herbivores: lupine alkaloids and tolerance to defoliation. In: Barbosa P, Krischik VA, Jones CG (eds) Microbial mediation of plant-herbivore interactions. Wiley Interscience, pp 45–63Google Scholar
  121. Johnson SN, Birch ANE, Gregory PJ, Murray PJ (2006) The ‘mother knows best’ principle: should soil insects be included in the preference–performance debate? Ecol Entomol 31:395–401. doi: 10.1111/j.1365-2311.2006.00776.x CrossRefGoogle Scholar
  122. Jones CG, Last FT, Barbosa A, Krischik VA (1991) Ectomycorrhizae and tress: implications for aboveground herbivory. Microbial mediation of plant-herbivore interactions. Wiley Interscience, pp 65–103Google Scholar
  123. Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38:651–664. doi: 10.1007/s10886-012-0134-6 PubMedCrossRefGoogle Scholar
  124. Kapoor R, Chaudhary V, Bhatnagar AK (2007) Effects of arbuscular mycorrhiza and phosphorus application on artemisinin concentration in Artemisia annua L. Mycorrhiza 17:581–587. doi: 10.1007/s00572-007-0135-4 PubMedCrossRefGoogle Scholar
  125. Karst J et al (2015) Ectomycorrhizal fungi mediate indirect effects of a bark beetle outbreak on secondary chemistry and establishment of pine seedlings. New Phytol 208:904–914. doi: 10.1111/nph.13492 PubMedCrossRefGoogle Scholar
  126. Kaschuk G, Kuyper TW, Leffelaar PA, Hungria M, Giller KE (2009) Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biol Biochem 41:1233–1244. doi: 10.1016/j.soilbio.2009.03.005 CrossRefGoogle Scholar
  127. Katayama N, Nishida T, Zhang ZQ, Ohgushi T (2010) Belowground microbial symbiont enhances plant susceptibility to a spider mite through change in soybean leaf quality. Popul Ecol 52:499–506. doi: 10.1007/s10144-010-0207-8 CrossRefGoogle Scholar
  128. Katayama N, Zhang ZQ, Ohgushi T (2011a) Belowground rhizobia positively affect abundances of aboveground sap feeding and leaf chewing herbivores. J Plant Interact 6:173–174. doi: 10.1080/17429145.2010.536264 CrossRefGoogle Scholar
  129. Katayama N, Zhang ZQ, Ohgushi T (2011b) Community-wide effects of below-ground rhizobia on above-ground arthropods. Ecol Entomol 36:43–51. doi: 10.1111/j.1365-2311.2010.01242.x CrossRefGoogle Scholar
  130. Katayama N, Silva AO, Kishida O, Ushio M, Kita S, Ohgushi T (2014) Herbivorous insect decreases plant nutrient uptake: the role of soil nutrient availability and association of below-ground symbionts. Ecol Entomol 39:511–518. doi: 10.1111/een.12125 CrossRefGoogle Scholar
  131. Kempel A, Brandl R, Schädler M (2009) Symbiotic soil microorganisms as players in aboveground plant-herbivore interactions – the role of rhizobia. Oikos 118:634–640CrossRefGoogle Scholar
  132. Kempel A, Schmidt AK, Brandl R, Schädler M (2010) Support from the underground: induced plant resistance depends on arbuscular mycorrhizal fungi. Funct Ecol 24:293–300. doi: 10.1111/j.1365-2435.2009.01647.x CrossRefGoogle Scholar
  133. Kempel A, Schädler M, Chrobock T, Fischer M, van Kleunen M (2011) Tradeoffs associated with constitutive and induced plant resistance against herbivory. Proc Natl Acad Sci U S A 108:5685–5689. doi: 10.1073/pnas.1016508108 PubMedPubMedCentralCrossRefGoogle Scholar
  134. Kempel A, Nater P, Fischer M, van Kleunen M (2013) Plant-microbe-herbivore interactions in invasive and non-invasive alien plant species. Funct Ecol 27:498–508. doi: 10.1111/1365-2435.12056 CrossRefGoogle Scholar
  135. Khaitov B, Patiño-Ruiz JD, Pina T, Schausberger P (2015) Interrelated effects of mycorrhiza and free-living nitrogen fixers cascade up to aboveground herbivores. Ecol Evol 5:3756–3768. doi: 10.1002/ece3.1654 PubMedPubMedCentralCrossRefGoogle Scholar
  136. Kiers ET, Denison RF (2008) Sanctions, cooperation, and the stability of plant-rhizosphere mutualisms. Annu Rev Ecol Evol Syst 39:215–236CrossRefGoogle Scholar
  137. Kiers ET, Adler LS, Grman EL, van der Heijden MGA (2010) Manipulating the jasmonate response: how do methyl jasmonate additions mediate characteristics of aboveground and belowground mutualisms? Funct Ecol 24:434–443. doi: 10.1111/j.1365-2435.2009.01625.x CrossRefGoogle Scholar
  138. Koller R, Rodriguez A, Robin C, Scheu S, Bonkowski M (2013a) Protozoa enhance foraging efficiency of arbuscular mycorrhizal fungi for mineral nitrogen from organic matter in soil to the benefit of host plants. New Phytol 199:203–211. doi: 10.1111/nph.12249 PubMedCrossRefGoogle Scholar
  139. Koller R, Scheu S, Bonkowski M, Robin C (2013b) Protozoa stimulate N uptake and growth of arbuscular mycorrhizal plants. Soil Biol Biochem 65:204–210. doi: 10.1016/j.soilbio.2013.05.020 CrossRefGoogle Scholar
  140. Koorneef A, Pieterse CMJ (2008) Cross-talk in defense signalling. Plant Physiol 146:839–844CrossRefGoogle Scholar
  141. Koricheva J, Gange AC, Jones T (2009) Effects of mycorrhizal fungi on insect herbivores: a meta-analysis. Ecology 90:2088–2097PubMedCrossRefGoogle Scholar
  142. Koschier EH, Khaosaad T, Vierheilig H (2007) Root colonization by the arbuscular mycorrhizal fungus Glomus mosseae and enhanced phosphorous levels in cucumber do not affect host acceptance and development of Frankliniella occidentalis. J Plant Interact 2:11–15. doi: 10.1080/17429140701231459 CrossRefGoogle Scholar
  143. Kost C, Heil M (2008) The defensive role of volatile emission and extrafloral nectar secretion for Lima Bean in nature. J Chem Ecol 34:2–13. doi: 10.1007/s10886-007-9404-0 CrossRefGoogle Scholar
  144. Krupa S, Fries N (1971) Studies on ectomycorrhizae of pine. I Production of volatile organic compounds. Can J Bot 49:1425–1431. doi: 10.1139/b71-200 CrossRefGoogle Scholar
  145. Krupa S, Andersson J, Marx DH (1973) Studies on ectomycorrhizae of pine III. Volatile organic compounds in mycorrhizal and nonmycorrhizal root systems of Pinus echinata Mill. Eur J For Pathol 3:194–200. doi: 10.1111/j.1439-0329.1973.tb00394.x CrossRefGoogle Scholar
  146. Kula AAR, Hartnett DC (2015) Effects of mycorrhizal symbiosis on aboveground arthropod herbivory in tallgrass prairie: an in situ experiment. Plant Ecol 216:589–597. doi: 10.1007/s11258-015-0461-0 CrossRefGoogle Scholar
  147. Kula AAR, Hartnett DC, Wilson GWT (2005) Effects of mycorrhizal symbiosis on tallgrass prairie plant-herbivore interactions. Ecol Lett 8:61–69CrossRefGoogle Scholar
  148. Laird R, Addicott J (2007) Arbuscular mycorrhizal fungi reduce the construction of extrafloral nectaries in Vicia faba. Oecologia 152:541–551. doi: 10.1007/s00442-007-0676-4 PubMedCrossRefGoogle Scholar
  149. Landgraf R, Schaarschmidt S, Hause B (2012) Repeated leaf wounding alters the colonization of Medicago truncatula roots by beneficial and pathogenic microorganisms. Plant Cell Environ 35:1344–1357. doi: 10.1111/j.1365-3040.2012.02495.x PubMedCrossRefGoogle Scholar
  150. Larimer AL, Bever JC, Clay K (2010) The interactive effects of plant microbial symbionts: a review and meta-analysis. Symbiosis 51:139–148. doi: 10.1007/s13199-010-0083-1 CrossRefGoogle Scholar
  151. Lehr NA, Schrey SD, Bauer R, Hampp R, Tarkka MT (2007) Suppression of plant defence response by a mycorrhiza helper bacterium. New Phytol 174:892–903. doi: 10.1111/j.1469-8137.2007.02021.x PubMedCrossRefGoogle Scholar
  152. Leimu R, Koricheva J (2006) A meta-analysis of tradeoffs between plant tolerance and resistance to herbivores: combining the evidence from ecological and agricultural studies. Oikos 112:1–9. doi: 10.1111/j.0030-1299.2006.41023.x CrossRefGoogle Scholar
  153. Leitner M, Kaiser R, Hause B, Boland W, Mithofer A (2010) Does mycorrhization influence herbivore-induced volatile emission in Medicago truncatula? Mycorrhiza 20:89–101. doi: 10.1007/s00572-009-0264-z PubMedCrossRefGoogle Scholar
  154. Li H et al (2013) Impact of the earthworm Aporrectodea trapezoides and the arbuscular mycorrhizal fungus Glomus intraradices on N-15 uptake by maize from wheat straw. Biol Fertil Soils 49:263–271. doi: 10.1007/s00374-012-0716-z CrossRefGoogle Scholar
  155. Liu JY et al (2003) Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. Plant Cell 15:2106–2123. doi: 10.1105/tpc.014183 PubMedPubMedCentralCrossRefGoogle Scholar
  156. Liu J, Maldonado-Mendoza I, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ (2007) Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J 50:529–544. doi: 10.1111/j.1365-313X.2007.03069.x PubMedCrossRefGoogle Scholar
  157. Manninen AM (1999) Susceptibility of Scots pine seedlings to specialist and generalist insect herbivores – importance of plant defense and mycorrhizal status. Natural and Environmental Sciences 100. PhD, University Kuopio, Kuopio University Publications CGoogle Scholar
  158. Manninen AM, Holopainen T, Holopainen JK (1998) Susceptibility of ectomycorrhizal and nonmycorrhizal Scots pine (Pinus sylvestris) seedlings to a generalist insect herbivore, Lygus rugulipennis, at two nitrogen availability levels. New Phytol 140:55–63CrossRefGoogle Scholar
  159. Manninen AM, Holopainen T, Holopainen JK (1999) Performance of grey pine aphid, Schizolachnus pineti, on ectomycorrhizal and non-mycorrhizal Scots pine seedlings at different levels of nitrogen availability. Entomol Exp Appl 93:117–120CrossRefGoogle Scholar
  160. Manninen AM, Holopainen T, Lyytikaeinen-Saarenmaa P, Holopainen JK (2000) The role of low-level ozone exposure and mycorrhizas in chemical quality and insect herbivore performance on Scots pine seedlings. Glob Chem Biol 5:1–11CrossRefGoogle Scholar
  161. Markkola A, Kuikka K, Rautio P, Harma E, Roitto M, Tuomi J (2004) Defoliation increases carbon limitations in ectomycorrhizal symbiosis of Betula pubescens. Oecologia 140:234–240. doi: 10.1007/s00442-004-1587-2 PubMedCrossRefGoogle Scholar
  162. Martinuz A, Schouten A, Menjivar RD, Sikora RA (2012) Effectiveness of systemic resistance toward Aphis gossypii (Hom., Aphididae) as induced by combined applications of the endophytes Fusarium oxysporum Fo162 and Rhizobium etli G12. Biol Control 62. doi: 10.1016/j.biocontrol.2012.05.006
  163. Marx J (2004) The roots of plant-microbe collaborations. Science 304:234–236PubMedCrossRefGoogle Scholar
  164. Matyssek R, Koricheva J, Schnyder H, Ernst D, Munch JC, Oßwald W, Pretzsch H (2012) The balance between resource sequestration and retention: a challenge in plant science. In: Matyssek R, Schnyder R, Oßwald W, Ernst D, Munch JC, Pretzsch H (eds) Growth and defence in plants. Springer, Heidelberg, pp 3–23. doi: 10.1007/978-3-642-30645-7_1
  165. Mechri B, Tekaya M, Cheheb H, Attia F, Hammami M (2015) Accumulation of flavonoids and phenolic compounds in olive tree roots in response to mycorrhizal colonization: a possible mechanism for regulation of defense molecules. J Plant Physiol 185:40–43. doi: 10.1016/j.jplph.2015.06.015 PubMedCrossRefGoogle Scholar
  166. Medina A, Probanza A, Gutierrez Mañero FJ, Azcón R (2003) Interactions of arbuscular-mycorrhizal fungi and Bacillus strains and their effects on plant growth, microbial rhizosphere activity (thymidine and leucine incorporation) and fungal biomass (ergosterol and chitin). Appl Soil Ecol 22:15–28. doi:
  167. Michel K, Abderhalden O, Bruggmann R, Dudler R (2006) Transcriptional changes in powdery mildew infected wheat and Arabidopsis leaves undergoing syringolin-triggered hypersensitive cell death at infection sites. Plant Mol Biol 62:561–578. doi: 10.1007/s11103-006-9045-7 PubMedCrossRefGoogle Scholar
  168. Middleton EL, Richardson S, Koziol L, Palmer CE, Yermakov Z, Henning JA, Schultz PA, Bever JD (2015) Locally adapted arbuscular mycorrhizal fungi improve vigor and resistance to herbivory of native prairie plant species. Ecosphere 6:276. doi: 10.1890/ES15-00152.1 CrossRefGoogle Scholar
  169. Mikola J, Nieminen M, Ilmarinen K, Vestberg M (2005) Belowground responses by AM fungi and animal trophic groups to repeated defoliation in an experimental grassland community. Soil Biol Biochem 37:1630–1639CrossRefGoogle Scholar
  170. Milcu A, Bonkowski M, Collins CM, Crawley MJ (2015) Aphid honeydew-induced changes in soil biota can cascade up to tree crown architecture. Pedobiologia 58:119–127. doi: 10.1016/j.pedobi.2015.07.002 CrossRefGoogle Scholar
  171. Miller RE, Gleadow RM, Cavagnaro TR (2014) Age versus stage: does ontogeny modify the effect of phosphorus and arbuscular mycorrhizas on above- and below-ground defence in forage sorghum? Plant Cell Environ 37:929–942. doi: 10.1111/pce.12209 PubMedCrossRefGoogle Scholar
  172. Moon DC, Barnouti J, Younginger B (2013) Context-dependent effects of mycorrhizae on herbivore density and parasitism in a tritrophic coastal study system. Ecol Entomol 38:31–39. doi: 10.1111/j.1365-2311.2012.01399.x CrossRefGoogle Scholar
  173. Morandi D (1996) Occurrence of phytoalexins and phenolic compounds in endomycorrhizal interactions, and their potential role in biological control. Plant and Soil 185:241–251. doi: 10.1007/BF02257529 CrossRefGoogle Scholar
  174. Mueller RC, Sthultz CM, Martinez T, Gehring CA, Whitham TG (2005) The relationship between stem-galling wasps and mycorrhizal colonization of Quercus turbinella. Can J Bot 83:1349–1353CrossRefGoogle Scholar
  175. Murrell EG, Hanson CR, Cullen EM (2015) European corn borer oviposition response to soil fertilization practices and arbuscular mycorrhizal colonization of corn. Ecosphere 6. doi: 10.1890/es14-00501.1
  176. Ness JH (2006) A mutualism's indirect costs: the most aggressive plant bodyguards also deter pollinators. Oikos 113:506–514. doi: 10.1111/j.2006.0030-1299.14143.x CrossRefGoogle Scholar
  177. Neuhauser C, Fargione JE (2004) A mutualism-parasitism continuum model and its application to plant-mycorrhizae interactions. Ecol Model 177:337–352. doi: 10.1016/j.ecolmodel.2004.02.010 CrossRefGoogle Scholar
  178. Nishida T, Izumi N, Katayama N, Ohgushi T (2009) Short-term response of arbuscular mycorrhizal association to spider mite herbivory. Popul Ecol 51:329–334CrossRefGoogle Scholar
  179. Okada K, Abe H, Arimura G (2015) Jasmonates induce both defense responses and communication in monocotyledonous and dicotyledonous plants. Plant Cell Physiol 56:16–27. doi: 10.1093/pcp/pcu158 PubMedCrossRefGoogle Scholar
  180. Orrelland P, Bennett AE (2013) How can we exploit above-belowground interactions to assist in addressing the challenges of food security? Front Plant Sci 4. doi: 10.3389/fpls.2013.00432
  181. Ossler JN, Zielinski CA, Heath KD (2015) Tripartite mutualism: facilitation or trade-offs between rhizobial and mycorrhizal symbionts of legume hosts. Am J Bot 102:1332–1341. doi: 10.3732/ajb.1500007 PubMedCrossRefGoogle Scholar
  182. Pangesti N, Pineda A, Pieterse CMJ, Dicke M, van Loon JJA (2013) Two-way plant-mediated interactions between root-associated microbes and insects: from ecology to mechanisms. Front Plant Sci 4. doi: 10.3389/fpls.2013.00414
  183. Pangesti N, Pineda A, Dicke M, van Loon JJA (2015a) Variation in plant-mediated interactions between rhizobacteria and caterpillars: potential role of soil composition. Plant Biol 17:474–483. doi: 10.1111/plb.12265 PubMedCrossRefGoogle Scholar
  184. Pangesti N, Weldegergis BT, Langendorf B, van Loon JJA, Dicke M, Pineda A (2015b) Rhizobacterial colonization of roots modulates plant volatile emission and enhances the attraction of a parasitoid wasp to host-infested plants. Oecologia 178:1169–1180. doi: 10.1007/s00442-015-3277-7 PubMedPubMedCentralCrossRefGoogle Scholar
  185. Pankoke H, Höpfner I, Matuszak A, Beyschlag W, Müller C (2015) The effects of mineral nitrogen limitation, competition, arbuscular mycorrhiza, and their respective interactions, on morphological and chemical plant traits of Plantago lanceolata. Phytochemistry 118:149–161. doi:
  186. Pastore AI, Russell FL (2012) Insect herbivore effects on resource allocation to shoots and roots in Lespedeza capitata. Plant Ecol 213:843–851. doi: 10.1007/s11258-012-0046-0 CrossRefGoogle Scholar
  187. Piculell BJ, Hoeksema JD, Thompson JN (2008) Interactions of biotic and abiotic environmental factors in an ectomycorrhizal symbiosis, and the potential for selection mosaics. BMC Biol 6. doi: 10.1186/1741-7007-6-23
  188. Pieterse CMJ et al (2008) Cross-talk between signaling pathways leading to defense against pathogens and insects. In: Lorito M, Woo SL, Dicke M (eds) Biology of plant-microbe interactions. International Society for Molecular Plant-Microbe Interactions, St. Paul, pp 1–9Google Scholar
  189. Pieterse CMJ, Poelman EH, Van Wees SCM, Dicke M (2013) Induced plant responses to microbes and insects. Front Plant Sci 4. doi: 10.3389/fpls.2013.00475
  190. Pii Y, Mimmo T, Tomasi N, Terzano R, Cesco S, Crecchio C (2015) Microbial interactions in the rhizosphere: beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. A review. Biol Fertil Soils 51:403–415. doi: 10.1007/s00374-015-0996-1 CrossRefGoogle Scholar
  191. Pineda A, Zheng SJ, van Loon JJA, Pieterse CMJ, Dicke M (2010) Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci 15:507–514. doi: 10.1016/j.tplants.2010.05.007 PubMedCrossRefGoogle Scholar
  192. Pineda A, Zheng SJ, van Loon JJA, Dicke M (2012) Rhizobacteria modify plant-aphid interactions: a case of induced systemic susceptibility. Plant Biol 14:83–90. doi: 10.1111/j.1438-8677.2011.00549.x PubMedCrossRefGoogle Scholar
  193. Pineda A, Dicke M, Pieterse CMJ, Pozo MJ (2013a) Beneficial microbes in a changing environment: are they always helping plants to deal with insects? Funct Ecol 27:574–586. doi: 10.1111/1365-2435.12050 CrossRefGoogle Scholar
  194. Pineda A, Soler R, Weldegergis BT, Shimwela MM, Van Loon JJA, Dicke M (2013b) Non-pathogenic rhizobacteria interfere with the attraction of parasitoids to aphid-induced plant volatiles via jasmonic acid signalling. Plant Cell Environ 36:393–404. doi: 10.1111/j.1365-3040.2012.02581.x PubMedCrossRefGoogle Scholar
  195. Planchamp C, Glauser G, Mauch-Mani B (2015) Root inoculation with Pseudomonas putida KT2440 induces transcriptional and metabolic changes and systemic resistance in maize plants. Front Plant Sci 5. doi: 10.3389/fpls.2014.00719
  196. Pozo MJ, Azcon-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398. doi: 10.1016/j.pbi.2007.05.004 PubMedCrossRefGoogle Scholar
  197. Pozo MJ, Van Loon LC, Pieterse CMJ (2004) Jasmonates – signals in plant-microbe interactions. J Plant Growth Regul 23:211–222. doi: 10.1007/s00344-004-003105 Google Scholar
  198. Rapparini F, Llusià J, Peñuelas J (2008) Effect of arbuscular mycorrhizal (AM) colonization on terpene emission and content of Artemisia annua L. Plant Biol 10:108–122. doi: 10.1055/s-2007-964963 PubMedCrossRefGoogle Scholar
  199. Remy W, Taylor T, Hass H, Kerp H (1994) Four hundred-million-year-old vesicular mycorrhizae. Proc Natl Acad Sci 91:11841–11843PubMedPubMedCentralCrossRefGoogle Scholar
  200. Rieske LK (2001) Influence of symbiotic fungal colonization on oak seedling growth and suitability for insect herbivory. Environ Entomol 30:849–854CrossRefGoogle Scholar
  201. Roda AL, Baldwin IT (2003) Molecular technology reveals how the induced direct defenses of plants work. Basic Appl Ecol 4:15–26CrossRefGoogle Scholar
  202. Rodriguez-Echeverria S, Traveset A (2015) Putative linkages between below- and aboveground mutualisms during alien plant invasions. Aob Plants 7. doi: 10.1093/aobpla/plv062
  203. Roger A, Getaz M, Rasmann S, Sanders IR (2013) Identity and combinations of arbuscular mycorrhizal fungal isolates influence plant resistance and insect preference. Ecol Entomol 38:330–338. doi: 10.1111/een.12022 CrossRefGoogle Scholar
  204. Rostás M, Turlings TCJ (2008) Induction of systemic acquired resistance in Zea mays also enhances the plant’s attractiveness to parasitoids. Biol Control 46:178–186. doi:
  205. Sampedro L, Moreira X, Zas R (2011) Costs of constitutive and herbivore-induced chemical defences in pine trees emerge only under low nutrient availability. J Ecol 99:818–827. doi: 10.1111/j.1365-2745.2011.01814.x CrossRefGoogle Scholar
  206. Santhanam R, Luu VT, Weinhold A, Goldberg J, Oh Y, Baldwin IT (2015) Native root-associated bacteria rescue a plant from a sudden-wilt disease that emerged during continuous cropping. Proc Natl Acad Sci 112:E5013–E5020. doi: 10.1073/pnas.1505765112 PubMedPubMedCentralCrossRefGoogle Scholar
  207. Saravesi K, Ruotsalainen AL, Cahill JF (2014) Contrasting impacts of defoliation on root colonization by arbuscular mycorrhizal and dark septate endophytic fungi of Medicago sativa. Mycorrhiza 24:239–245. doi: 10.1007/s00572-013-0536-5 PubMedCrossRefGoogle Scholar
  208. Sarma BK, Yadav SK, Singh S, Singh HB (2015) Microbial consortium-mediated plant defense against phytopathogens: readdressing for enhancing efficacy. Soil Biol Biochem 87:25–33. doi:
  209. Schädler M, Jung G, Brandl R, Auge H (2004) Secondary succession is influenced by belowground insect herbivory on a productive site. Oecologia 138:242–252PubMedCrossRefGoogle Scholar
  210. Schädler M, Brandl R, Kempel A (2010) Host plant genotype determines bottom-up effects in an aphid-parasitoid-predator system. Entomol Exp Appl 135:162–169. doi: 10.1111/j.1570-7458.2010.00976.x CrossRefGoogle Scholar
  211. Schausberger P, Peneder S, Jurschik S, Hoffmann D (2012) Mycorrhiza changes plant volatiles to attract spider mite enemies. Funct Ecol 26:441–449. doi: 10.1111/j.1365-2435.2011.01947.x CrossRefGoogle Scholar
  212. Schenk PM, McGrath KC, Lorito M, Pieterse CMJ (2008) Plant-microbe and plant-insect interactions meet common grounds. New Phytol 179:251–255PubMedCrossRefGoogle Scholar
  213. Schmidt DD, Voelckel C, Hartl M, Schmidt S, Baldwin IT (2005) Specificity in ecological interactions. Attack from the same lepidopteran herbivore results in species-specific transcriptional responses in two solanaceous host plants. Plant Physiol 138:1763–1773. doi: 10.1104/pp.105.061192 PubMedPubMedCentralCrossRefGoogle Scholar
  214. Schreck TK, David SJ, Mooney KA (2013) Effects of Brassica nigra and plant-fungi interactions on the arthropod community of Deinandra fasciculata. Biol Invasions 15:2443–2454. doi: 10.1007/s10530-013-0464-5 CrossRefGoogle Scholar
  215. Selosse MA, Strullu-Derrien C, Martin FM, Kamoun S, Kenrick P (2015) Plants, fungi and oomycetes: a 400-million year affair that shapes the biosphere. New Phytol 206:501–506. doi: 10.1111/nph.13371 PubMedCrossRefGoogle Scholar
  216. Shrivastava G et al (2015) Colonization by arbuscular mycorrhizal and endophytic fungi enhanced terpene production in tomato plants and their defense against a herbivorous insect. Symbiosis 65:65–74. doi: 10.1007/s13199-015-0319-1 CrossRefGoogle Scholar
  217. Simard SW, Durall DM (2004) Mycorrhizal networks: a review of their extent, function, and importance. Can J Bot 82:1140–1165CrossRefGoogle Scholar
  218. Simard SW, Jones MD, Durall DM (2002) Carbon and nutrient fluxes within and between mycorrhizal plants. Mycorrhizal Ecol 157:33–74CrossRefGoogle Scholar
  219. Simonsen AK, Stinchcombe JR (2014) Herbivory eliminates fitness costs of mutualism exploiters. New Phytol 202:651–661. doi: 10.1111/nph.12668 PubMedCrossRefGoogle Scholar
  220. Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, New YorkGoogle Scholar
  221. Spehn EM et al (2002) The role of legumes as a component of biodiversity in a cross-European study of grassland biomass nitrogen. Oikos 98:205–218CrossRefGoogle Scholar
  222. Sprent JI (2001) Nodulation in legumes. Kew Royal Botanical Gardens, KewGoogle Scholar
  223. Stadler B, Solinger S, Michalzik B (2001) Insect herbivores and the nutrient flow from the canopy to the soil in coniferous and deciduous forests. Oecologia 126:104–113CrossRefGoogle Scholar
  224. Summers MC, Mondor EB (2011) Rhizobium alters inducible defenses in broad bean, Vicia faba. Open J Ecol 1:57–62CrossRefGoogle Scholar
  225. Sun XG, Tang M (2013) Effect of arbuscular mycorrhizal fungi inoculation on root traits and root volatile organic compound emissions of Sorghum bicolor. S Afr J Bot 88:373–379. doi: 10.1016/j.sajb.2013.09.007 CrossRefGoogle Scholar
  226. Tao L, Gowler CD, Ahmad A, Hunter MD, de Roode JC (2015) Disease ecology across soil boundaries: effects of below-ground fungi on above-ground host–parasite interactions. Proc R Soc Lond B Biol Sci 282. doi: 10.1098/rspb.2015.1993
  227. Tao L, Ahmad A, de Roode JC, Hunter MD (2016) Arbuscular mycorrhizal fungi affect plant tolerance and chemical defences to herbivory through different mechanisms. J Ecol 104:561–571. doi: 10.1111/1365-2745.12535 CrossRefGoogle Scholar
  228. Tarkka M, Hampp R (2008) Secondary metabolites of soil streptomycetes in biotic interactions. In: Karlovsky P (ed) Secondary metabolites in soil ecology. Springer, Heidelberg, pp 107–128CrossRefGoogle Scholar
  229. Tarkka MT et al (2013) OakContigDF159.1, a reference library for studying differential gene expression in Quercus robur during controlled biotic interactions: use for quantitative transcriptomic profiling of oak roots in ectomycorrhizal symbiosis. New Phytol 199:529–540. doi: 10.1111/nph.12317 PubMedCrossRefGoogle Scholar
  230. Tawaraya K et al (2012) Leaf herbivory by Spodoptera litura increases arbuscular mycorrhizal colonization in roots of soybean. Soil Sci Plant Nutr 58:445–449. doi: 10.1080/00380768.2012.704520 CrossRefGoogle Scholar
  231. Techau MEC, Bjornlund L, Christensen S (2004) Simulated herbivory effects on rhizosphere organisms in pea (Pisum sativum) depended on phosphate. Plant and Soil 264:185–194CrossRefGoogle Scholar
  232. Thamer S, Schädler M, Bonte D, Ballhorn DJ (2011) Dual benefit from a belowground symbiosis: nitrogen fixing rhizobia promote growth and defense against a specialist herbivore in a cyanogenic plant. Plant and Soil 341:209–219. doi: 10.1007/s11104-010-0635-4 CrossRefGoogle Scholar
  233. Thompson JN (2005) The geographic mosaic of coevolution. University Chicago Press, ChicagoGoogle Scholar
  234. Tkacz A, Poole P (2015) Role of root microbiota in plant productivity. J Exp Bot 66:2167–2175. doi: 10.1093/jxb/erv157 PubMedPubMedCentralCrossRefGoogle Scholar
  235. Toussaint JP, Smith FA, Smith SE (2007) Arbuscular mycorrhizal fungi can induce the production of phytochemicals in sweet basil irrespective of phosphorus nutrition. Mycorrhiza 17:291–297. doi: 10.1007/s00572-006-0104-3 PubMedCrossRefGoogle Scholar
  236. Trocha LK, Weiser E, Robakowski P (2016) Interactive effects of juvenile defoliation, light conditions, and interspecific competition on growth and ectomycorrhizal colonization of Fagus sylvatica und Pinus sylvestris seedlings. Mycorrhiza 26:47–56. doi: 10.1007/s00572-015-0645-4 PubMedCrossRefGoogle Scholar
  237. Ueda K et al (2013) Effects of arbuscular mycorrhizal fungi on the abundance of foliar-feeding insects and their natural enemy. Appl Entomol Zool 48:79–85. doi: 10.1007/s13355-012-0155-1 CrossRefGoogle Scholar
  238. Valdez Barillas JR, Paschke MW, Ralphs MH, Child RD (2007) White locoweed toxicity is facilitated by a fungal endophyte and nitrogen-fixing bacteria. Ecology 88:1850–1856PubMedCrossRefGoogle Scholar
  239. van der Heijden MGA, Boller T, Wiemken A, Sanders IR (1998a) Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology 79:2082–2091CrossRefGoogle Scholar
  240. van der Heijden MGA et al (1998b) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72CrossRefGoogle Scholar
  241. van der Heijden MGA et al (2006) Symbiotic bacteria as a determinant of plant community structure and plant productivity in dune grassland. FEMS Microbiol Ecol 56:178–187PubMedCrossRefGoogle Scholar
  242. van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310PubMedCrossRefGoogle Scholar
  243. van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483. doi: 10.1146/annurev.phyto.36.1.453 PubMedCrossRefGoogle Scholar
  244. Vannette RL, Hunter MD (2009) Mycorrhizal fungi as mediators of defence against insect pests in agricultural systems. Agric For Entomol 11:351–358. doi: 10.1111/j.1461-9563.2009.00445.x CrossRefGoogle Scholar
  245. Vannette RL, Hunter MD (2011) Plant defence theory re-examined: nonlinear expectations based on the costs and benefits of resource mutualisms. J Ecol 99:66–76. doi: 10.1111/j.1365-2745.2010.01755.x CrossRefGoogle Scholar
  246. Vannette RL, Hunter MD (2013) Mycorrhizal abundance affects the expression of plant resistance traits and herbivore performance. J Ecol 101:1019–1029. doi: 10.1111/1365-2745.12111 CrossRefGoogle Scholar
  247. Varga S, Kytöviita M-M, Siikamäki P (2009) Sexual differences in response to simulated herbivory in the gynodioecious herb Geranium sylvaticum. Plant Ecol 202:325–336. doi: 10.1007/s11258-008-9492-0 CrossRefGoogle Scholar
  248. Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant and Soil 255:571–586. doi: 10.1023/A:1026037216893 CrossRefGoogle Scholar
  249. Veyrath N, Robert CAM, Turlings TCJ, Erb M (2016) Herbivore intoxication as a potential primary function of an inducible volatile plant signal. J Ecol 104:591–600. doi: 10.1111/1365-2745.12526 CrossRefGoogle Scholar
  250. Wagner D (1997) The influence of ant nests on Acacia seed production, herbivory and soil nutrients. J Ecol 85:83–93. doi: 10.2307/2960629 CrossRefGoogle Scholar
  251. Wall L (2000) The actinorhizal symbiosis. J Plant Growth Regul 19:167–182PubMedGoogle Scholar
  252. Wang M, Bezemer TM, van der Putten WH, Biere A (2015) Effects of the timing of herbivory on plant defense induction and insect performance in ribwort plantain (Plantago lanceolata L.) depend on plant mycorrhizal status. J Chem Ecol 41:1006–1017. doi: 10.1007/s10886-015-0644-0 PubMedPubMedCentralCrossRefGoogle Scholar
  253. Wardle DA (2002) Communities and ecosystems: linking the aboveground and belowground components. Princeton University Press, PrincetonGoogle Scholar
  254. Waughman GJ, French JRJ, Jones K (1981) Nitrogen fixation in some terrestrial environments. In: Broughton WJ (ed) Nitrogen fixation, vol 1. Clarendon, Oxford, pp 135–192Google Scholar
  255. Wearn JA, Gange AC (2007) Above-ground herbivory causes rapid and sustained changes in mycorrhizal colonization of grasses. Oecologia 153:959–971PubMedCrossRefGoogle Scholar
  256. Weber MG, Keeler KH (2012) The phylogenetic distribution of extrafloral nectaries in plants. Ann Bot. doi: 10.1093/aob/mcs225 PubMedPubMedCentralGoogle Scholar
  257. Weese DJ, Heath KD, Dentinger BTM, Lau JA (2015) Long-term nitrogen addition causes the evolution of less-cooperative mutualists. Evolution 69:631–642. doi: 10.1111/evo.12594 PubMedCrossRefGoogle Scholar
  258. Whitaker MRL, Katayama N, Ohgushi T (2014) Plant-rhizobia interactions alter aphid honeydew composition. Arthropod Plant Interact 8:213–220. doi: 10.1007/s11829-014-9304-5 CrossRefGoogle Scholar
  259. Wiemken V, Boller T (2002) Ectomycorrhiza: gene expression, metabolism and the wood-wide web. Curr Opin Plant Biol 5:355–361PubMedCrossRefGoogle Scholar
  260. Wilson K, Stinner RE (1984) A potential influence of rhizobium activity on the availability of nitrogen to legume herbivores. Oecologia 61:337–341. doi: 10.1007/BF00379631 CrossRefGoogle Scholar
  261. Wink M (1988) Plant breeding: importance of plant secondary metabolites for protection against pathogens and herbivores. Theor Appl Genet 75:225–233CrossRefGoogle Scholar
  262. Wooley SC, Paine TD (2007) Can intra-specific genetic variation in arbuscular mycorrhizal fungi (Glomus etunicatum) affect a mesophyll-feeding herbivore (Tupiocoris notatus Distant)? Ecol Entomol 32:428–434CrossRefGoogle Scholar
  263. Wooley SC, Paine TD (2011) Infection by mycorrhizal fungi increases natural enemy abundance on tobacco (Nicotiana rustica). Environ Entomol 40:36–41. doi: 10.1603/en10145 PubMedCrossRefGoogle Scholar
  264. Wullschleger SD, Leakey ADB, St Clair SB (2007) Functional genomics and ecology – a tale of two scales. New Phytol 176:735–739PubMedCrossRefGoogle Scholar
  265. Yang HS, Dai YJ, Wang XH, Zhang Q, Zhu LQ, Bian XM (2014) Meta-analysis of interactions between arbuscular mycorrhizal fungi and biotic stressors of plants. Scientific World Journal. doi: 10.1155/2014/746506 Google Scholar
  266. Yao Q, Zhu HH, Zeng RS (2007) Role of phenolic compounds in plant defence: induced by arbuscular mycorrhizal fungi. Allelopathy J 20:1–13Google Scholar
  267. Zamioudis C, Pieterse CMJ (2012) Modulation of host immunity by beneficial microbes. Mol Plant Microbe Interact 25:139–150. doi: 10.1094/mpmi-06-11-0179 PubMedCrossRefGoogle Scholar
  268. Zubek S, Rola K, Szewczyk A, Majewska ML, Turnau K (2015) Enhanced concentrations of elements and secondary metabolites in Viola tricolor L. induced by arbuscular mycorrhizal fungi. Plant and Soil 390:129–142. doi: 10.1007/s11104-015-2388-6 CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department Community EcologyHelmholtz-Centre for Environmental Research (UFZ)HalleGermany
  2. 2.iDiv – German Centre for Integrative Biodiversity ResearchLeipzigGermany
  3. 3.Department of BiologyPortland State UniversityPortlandUSA

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