Inter- and Intraspecific Fungal Diversity in the Arbuscular Mycorrhizal Symbiosis

  • Brandon Monier
  • Vincent Peta
  • Jerry Mensah
  • Heike BückingEmail author


The 450-million-year-old arbuscular mycorrhizal (AM) symbiosis plays a critical role for the nutrient uptake and abiotic (drought, salinity, and heavy metals) and biotic stress resistance of the majority of land plants. The fungal extraradical mycelium takes up nutrients, such as phosphate and nitrogen, and delivers them to the intraradical mycelium, where the fungus exchanges these nutrients against carbon from the host. It is known for decades that AM fungi can improve the nutrient acquisition of many important crops under low input conditions and are able to increase plant productivity in stressful environments. However, despite their application potential as biofertilizers and bioprotectors, AM fungi have so far not been widely adopted. This is mainly due to the high variability and context dependency of mycorrhizal growth and nutrient uptake responses that make benefits by AM fungal communities difficult to predict. In this review, we summarize our current understanding of interspecific and intraspecific fungal diversity in mycorrhizal growth benefits and discuss the role of fungal genetic variability and host and fungal compatibility in this functional diversity. A better understanding of these processes is key to exploit the whole potential of AM fungi for agricultural applications and to increase the nutrient acquisition efficiency and productivity of economically important crop species.


Host Plant Arbuscular Mycorrhizal Fungal Species Fungal Community Mycorrhizal Colonization 
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.



The authors wish to acknowledge the financial support of the National Science Foundation (Award: 1051397), the South Dakota Soybean Research and Promotion Council, the USDA NIFA Hatch project SD00H423-12, and the South Dakota Oilseed Initiative.


  1. Agnolucci M, Battini F, Cristani C, Giovannetti M (2015) Diverse bacterial communities are recruited on spores of different arbuscular mycorrhizal fungal isolates. Biol Fertil Soils 51:379–389. doi: 10.1007/s00374-014-0989-5 CrossRefGoogle Scholar
  2. Aira M, Gomez-Brandon M, Lazcano C, Baath E, Dominguez J (2010) Plant genotype strongly modifies the structure and growth of maize rhizosphere microbial communities. Soil Biol Biochem 42:2276–2281. doi: 10.1016/j.soilbio.2010.08.029 CrossRefGoogle Scholar
  3. Akiyama K, Hayashi H (2006) Strigolactones: chemical signals for fungal symbionts and parasitic weeds in plant roots. Ann Bot 97:925–931. doi: 10.1093/aob/mcl063 PubMedPubMedCentralCrossRefGoogle Scholar
  4. Akiyama K, Matsuzaki KI, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827. doi: 10.1038/nature03608 PubMedCrossRefGoogle Scholar
  5. Angelard C, Sanders IR (2011) Effect of segregation and genetic exchange on arbuscular mycorrhizal fungi in colonization of roots. New Physician 189:652–657. doi: 10.1111/j.1469-8137.2010.03602.x CrossRefGoogle Scholar
  6. Angelard C, Colard A, Niculita-Hirzel H, Croll D, Sanders IR (2010) Segregation in a mycorrhizal fungus alters rice growth and symbiosis-specific gene transcription. Curr Biol 20:1216–1221. doi: 10.1016/j.cub.2010.05.031 PubMedCrossRefGoogle Scholar
  7. Antunes PM, Koch AM, Morton JB, Rillig MC, Klironomos JN (2011) Evidence for functional divergence in arbuscular mycorrhizal fungi from contrasting climatic origins. New Physician 189:507–514. doi: 10.1111/j.1469-8137.2010.03480.x CrossRefGoogle Scholar
  8. Avio L, Pellegrino E, Bonari E, Giovannetti M (2006) Functional diversity of arbuscular mycorrhizal fungal isolates in relation to extraradical mycelial networks. New Physician 172:347–357. doi: 10.1111/j.1469-8137.2006.01839.x CrossRefGoogle Scholar
  9. Avio L, Cristani C, Strani P, Giovannetti M (2009) Genetic and phenotypic diversity of geographically different isolates of Glomus mosseae. Can J Microbiol 55:242–253. doi: 10.1139/w08-129 PubMedCrossRefGoogle Scholar
  10. Battini F, Cristani C, Giovannetti M, Agnolucci M (2016) Multifunctionality and diversity of culturable bacterial communities strictly associated with spores of the plant beneficial symbiont Rhizophagus intraradices. Microbiol Res 183:68–79. doi: 10.1016/j.micres.2015.11.012 PubMedCrossRefGoogle Scholar
  11. Bentivenga SP, Bever JD, Morton JB (1997) Genetic variation of morphological characters within a single isolate of the endomycorrhizal fungus Glomus clarum. Am J Bot 84:1211–1216PubMedCrossRefGoogle Scholar
  12. Besserer A, Puech-Pagès V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S, Portais JC, Roux C, Bécard G, Séjalon-Delmas N (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol 4:1239–1247. doi: 10.1371/journal.pbio.0040226 CrossRefGoogle Scholar
  13. Börstler B, Raab PA, Thiery O, Morton JB, Redecker D (2008) Genetic diversity of the arbuscular mycorrhizal fungus Glomus intraradices as determined by mitochondrial large subunit rRNA gene sequences is considerably higher than previously expected. New Physician 180:452-465 doi: 10.1111/j.1469-8137.2008.02574.x
  14. Börstler B, Thiéry O, Sýkorova Z, Berner A, Redecker D (2010) Diversity of mitochondrial large subunit rDNA haplotypes of Glomus intraradices in two agricultural field experiments and two semi-natural grasslands. Mol Ecol 19:1497–1511. doi: 10.1111/j.1365-294X.2010.04590.x PubMedCrossRefGoogle Scholar
  15. Breuillin-Sessoms F, Floss DS, Gomez SK, Pumplin N, Ding Y, Levesque-Tremblay V, Noar RD, Daniels DA, Bravo A, Eaglesham JB, Benedito VA, Udvardi MK, Harrison MJ (2015) Suppression of arbuscule degeneration in Medicago truncatula phosphate transporter 4 mutants is dependent on the ammonium transporter 2 family protein AMT2;3. Plant Cell. doi: 10.1105/tpc.114.131144. pii:tpc.114.131144
  16. Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77. doi: 10.1007/s11104-008-9877-9 CrossRefGoogle Scholar
  17. Bücking H, Shachar-Hill Y (2005) Phosphate uptake, transport and transfer by the arbuscular mycorrhizal fungus Glomus intraradices is stimulated by increased carbohydrate availability. New Physician 165:899–912. doi: 10.1111/j.1469-8137.2004.01274.x CrossRefGoogle Scholar
  18. Bücking H, Abubaker J, Govindarajulu M, Tala M, Pfeffer PE, Nagahashi G, Lammers PJ, Shachar-Hill Y (2008) Root exudates stimulate the uptake and metabolism of organic carbon in germinating spores of Glomus intraradices. New Physician 180:684–695. doi: 10.1111/j.1469-8137.2008.02590.x CrossRefGoogle Scholar
  19. Bücking H, Mensah JA, Fellbaum CR (2016) Common mycorrhizal networks and their effect on the bargaining power of the fungal partner in the arbuscular mycorrhizal symbiosis. Commun Integr Biol 9(1):e1107684. doi: 10.1080/19420889.2015.1107684 PubMedPubMedCentralCrossRefGoogle Scholar
  20. Buée M, Rossignol M, Jauneau A, Ranjeva R, Bécard G (2000) The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Mol Plant Microbe Interact 13:693–698. doi: 10.1094/MPMI.2000.13.6.693 PubMedCrossRefGoogle Scholar
  21. Buée M, Maurice J-P, Zeller B, Andrianarisoa S, Ranger J, Courtecuisse R, Marçais B, Le Tacon F (2011) Influence of tree species on richness and diversity of epigeous fungal communities in a French temperate forest stand. Fungal Ecol 4:22–31. doi: 10.1016/j.funeco.2010.07.003 CrossRefGoogle Scholar
  22. Campagnac E, Khasa DP (2014) Relationship between genetic variability in Rhizophagus irregularis and tolerance to saline conditions. Mycorrhiza 24:121–129. doi: 10.1007/s00572-013-0517-8 PubMedCrossRefGoogle Scholar
  23. Corradi N, Bonfante P (2012) The arbuscular mycorrhizal symbiosis: origin and evolution of a beneficial plant infection. PLoS Pathog 8:3. doi: 10.1371/journal.ppat.1002600 CrossRefGoogle Scholar
  24. Croll D, Giovannetti M, Koch AM, Sbrana C, Ehinger M, Lammers PJ, Sanders IR (2009) Nonself vegetative fusion and genetic exchange in the arbuscular mycorrhizal fungus Glomus intraradices. New Physician 181:924–937. doi: 10.1111/j.1469-8137.2008.02726.x CrossRefGoogle Scholar
  25. Cruz C, Egsgaard H, Trujillo C, Ambus P, Requena N, Martins-Loucao MA, Jakobsen I (2007) Enzymatic evidence for the key role of arginine in nitrogen translocation by arbuscular mycorrhizal fungi. Plant Physiol 144:782–792. doi: 10.1104/pp.106.090522 PubMedPubMedCentralCrossRefGoogle Scholar
  26. Czaja LF, Hogekamp C, Lamm P, Maillet F, Martinez EA, Samain E, Dénarié J, Küster H, Hohnjec N (2012) Transcriptional responses toward diffusible signals from symbiotic microbes reveal MtNFP- and MtDMI3-dependent reprogramming of host gene expression by arbuscular mycorrhizal fungal lipochitooligosaccharides. Plant Physiol 159:1671–1685. doi: 10.1104/pp.112.195990 PubMedPubMedCentralCrossRefGoogle Scholar
  27. Daubois L, Beaudet D, Hijri M, de la Providencia I (2016) Independent mitochondrial and nuclear exchanges arising in Rhizophagus irregularis crossed-isolates support the presence of a mitochondrial segregation mechanism. BMC Microbiol 16:12. doi: 10.1186/s12866-016-0627-5 CrossRefGoogle Scholar
  28. de Novais CB, Borges WL, Jesus ED, Saggin OJ, Siqueira JO (2014) Inter- and intraspecific functional variability of tropical arbuscular mycorrhizal fungi isolates colonizing corn plants. Appl Soil Ecol 76:78–86. doi: 10.1016/j.apsoil.2013.12.010 CrossRefGoogle Scholar
  29. Ehinger M, Koch AM, Sanders IR (2009) Changes in arbuscular mycorrhizal fungal phenotypes and genotypes in response to plant species identity and phosphorus concentration. New Physician 184:412–423. doi: 10.1111/j.1469-8137.2009.02983.x CrossRefGoogle Scholar
  30. Ehinger MO, Croll D, Koch AM, Sanders IR (2012) Significant genetic and phenotypic changes arising from clonal growth of a single spore of an arbuscular mycorrhizal fungus over multiple generations. New Physician 196:853–861. doi: 10.1111/j.1469-8137.2012.04278.x CrossRefGoogle Scholar
  31. Fellbaum CR, Gachomo EW, Beesetty Y, Choudhari S, Strahan GD, Pfeffer PE, Kiers ET, Bücking H (2012) Carbon availability triggers fungal nitrogen uptake and transport in the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 109:2666–2671. doi: 10.1073/pnas.1118650109 PubMedPubMedCentralCrossRefGoogle Scholar
  32. Fellbaum CR, Mensah JA, Cloos AJ, Strahan GD, Pfeffer PE, Kiers ET, Bücking H (2014) Fungal nutrient allocation in common mycelia networks is regulated by the carbon source strength of individual host plants. New Phytol 203:645–656. doi: 10.1111/nph.12827 CrossRefGoogle Scholar
  33. Fitter AH (2005) Darkness visible: reflections on underground ecology. J Ecol 93:231–243. doi: 10.1111/j.0022-0477.2005.00990.x CrossRefGoogle Scholar
  34. Genre A, Chabaud M, Timmers T, Bonfante P, Barker DG (2005) Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Mol Plant Microbe Interact 17:3489–3499. doi: 10.1105/tpc.105.035410 Google Scholar
  35. Gherbi H, Markmann K, Svistoonoff S, Estevan J, Autran D, Giczey G, Auguy F, Péret B, Laplaze L, Franche C, Parniske M, Bogusz D (2008) SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhizal fungi, rhizobia, and Frankia bacteria. Proc Natl Acad Sci USA 105:4928–4932. doi: 10.1073/pnas.0710618105 PubMedPubMedCentralCrossRefGoogle Scholar
  36. Ghignone S, Salvioli A, Anca I, Lumini E, Ortu G, Petiti L, Cruveiller S, Bianciotto V, Piffanelli P, Lanfranco L, Bonfante P (2012) The genome of the obligate endobacterium of an AM fungus reveals an interphylum network of nutritional interactions. ISME J 6:136–145. doi: 10.1038/ismej.2011.110 PubMedCrossRefGoogle Scholar
  37. Giovannetti M, Sbrana C, Strani P, Agnolucci M, Rinaudo V, Avio L (2003) Genetic diversity of isolates of Glomus mosseae from different geographic areas detected by vegetative compatibility testing and biochemical and molecular analysis. Appl Environ Microbiol 69:616–624. doi: 10.1128/aem.69.1.616-624.2003 PubMedPubMedCentralCrossRefGoogle Scholar
  38. Gomez SK, Javot H, Deewatthanawong P, Torres-Jerez I, Tang Y, Blancaflor EB, Udvardi MK, Harrison MJ (2009) Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis. BMC Plant Biol 9(10). doi: 10.1186/1471-2229-9-10
  39. Gosling P, Jones J, Bending GD (2016) Evidence for functional redundancy in arbuscular mycorrhizal fungi and implications for agroecosystem management. Mycorrhiza 26:77–83. doi: 10.1007/s00572-015-0651-6 PubMedCrossRefGoogle Scholar
  40. Grunwald U, Guo WB, Fischer K, Isayenkov S, Ludwig-Müller J, Hause B, Yan XL, Küster H, Franken P (2009) Overlapping expression patterns and differential transcript levels of phosphate transporter genes in arbuscular mycorrhizal, Pi-fertilised and phytohormone-treated Medicago truncatula roots. Planta 229:1023–1034. doi: 10.1007/s00425-008-0877-z PubMedPubMedCentralCrossRefGoogle Scholar
  41. Guether M, Neuhauser B, Balestrini R, Dynowski M, Ludewig U, Bonfante P (2009) A mycorrhizal-specific ammonium transporter from Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiol 150:73–83. doi: 10.1104/pp.109.136390 PubMedPubMedCentralCrossRefGoogle Scholar
  42. Halary S, Malik S-B, Lildhar L, Slamovits CH, Hijri M, Corradi N (2011) Conserved meiotic machinery in Glomus spp., a putatively ancient asexual fungal lineage. Genome Biol Evol 3:950–958. doi: 10.1093/gbe/evr089 PubMedPubMedCentralCrossRefGoogle Scholar
  43. Halary S, Daubois L, Terrat Y, Ellenberger S, Wostemeyer J, Hijri M (2013) Mating type gene homologues and putative sex pheromone-sensing pathway in arbuscular mycorrhizal fungi, a presumably asexual plant root symbiont. PLoS One 8(11):12. doi: 10.1371/journal.pone.0080729 CrossRefGoogle Scholar
  44. Hammer EC, Pallon J, Wallander H, Olsson PA (2011) Tit for tat? A mycorrhizal fungus accumulates phosphorus under low plant carbon availability. FEMS Microbiol Ecol 76:236–244. doi: 10.1111/j.1574-6941.2011.01043.x PubMedCrossRefGoogle Scholar
  45. Hart MM, Reader RJ (2002) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Physician 153:335–344. doi: 10.1046/j.0028-646X.2001.00312.x CrossRefGoogle Scholar
  46. Helber N, Wippel K, Sauer N, Schaarschmidt S, Hause B, Requena N (2011) A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus sp. is crucial for the symbiotic relationship with plants. Plant Cell 23:3812–3823. doi: 10.1105/tpc.111.089813 PubMedPubMedCentralCrossRefGoogle Scholar
  47. Henkel TW, Aime MC, Chin MML, Miller SL, Vilgalys R, Smith ME (2012) Ectomycorrhizal fungal sporocarp diversity and discovery of new taxa in Dicymbe monodominant forests of the Guiana Shield. Biodivers Conserv 21:2195–2220. doi: 10.1007/s10531-011-0166-1 CrossRefGoogle Scholar
  48. Hijri M, Sanders IR (2005) Low gene copy number shows that arbuscular mycorrhizal fungi inherit genetically different nuclei. Nature 433:160–163. doi: 10.1038/nature03069 PubMedCrossRefGoogle Scholar
  49. Hijri M, Hosny M, van Tuinen D, Dulieu H (1999) Intraspecific ITS polymorphism in Scutellospora castanea (Glomales, Zygomycota) is structured within multinucleate spores. Fungal Genet Biol 26:141–151. doi: 10.1006/fgbi.1998.1112 PubMedCrossRefGoogle Scholar
  50. Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabinski C, Bever JD, Moore JC, Wilson GWT, Klironomos JN, Umbanhowar J (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407. doi: 10.1111/j.1461-0248.2009.01430.x PubMedCrossRefGoogle Scholar
  51. Jakobsen I, Abbott LK, Robson AD (1992) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. I. Spread of hyphae and phosphorus inflow into roots. New Physician 120:371–380. doi: 10.1111/j.1469-8137.1992.tb01077.x CrossRefGoogle Scholar
  52. Jansa J, Smith FA, Smith SE (2008) Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytol 177:779–789. doi: 10.1111/j.1469-8137.2007.02294.x
  53. Javot H, Penmetsa RV, Terzaghi N, Cook DR, Harrison MJ (2007) A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 104:1720–1725. doi: 10.1073/pnas.0608136104 PubMedPubMedCentralCrossRefGoogle Scholar
  54. Javot H, Penmetsa RV, Breuillin F, Bhattarai KK, Noar RD, Gomez SK, Zhang Q, Cook DR, Harrison MJ (2011) Medicago truncatula Mtpt4 mutants reveal a role for nitrogen in the regulation of arbuscule degeneration in arbuscular mycorrhizal symbiosis. Plant J 68:954–965PubMedCrossRefGoogle Scholar
  55. Johnson NC, Graham JH (2013) The continuum concept remains a useful framework for studying mycorrhizal functioning. Plant Soil 363:411–419. doi: 10.1007/s11104-012-1406-1 CrossRefGoogle Scholar
  56. Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Physician 135:575–585. doi: 10.1046/j.1469-8137.1997.00729.x CrossRefGoogle Scholar
  57. Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A, Palmer TM, West SA, Vandenkoornhuyse P, Jansa J, Bücking H (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882. doi: 10.1126/science.1208473 PubMedCrossRefGoogle Scholar
  58. Kikuchi Y, Hijikata N, Yokoyama K, Ohtomo R, Handa Y, Kawaguchi M, Saito K, Ezawa T (2014) Polyphosphate accumulation is driven by transcriptome alterations that lead to near-synchronous and near-equivalent uptake of inorganic cations in an arbuscular mycorrhizal fungus. New Physician 204:638–649. doi: 10.1111/nph.12937 CrossRefGoogle Scholar
  59. Kistner C, Winzer T, Pitzschke A, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Webb KJ, Szczyglowski K, Parniske M (2005) Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis. Plant Cell 17:2217–2229. doi: 10.1105/tpc.105.032714 PubMedPubMedCentralCrossRefGoogle Scholar
  60. Kivlin SN, Hawkes CV, Treseder KK (2011) Global diversity and distribution of arbuscular mycorrhizal fungi. Soil Biol Biochem 43:2294–2303. doi: 10.1016/j.soilbio.2011.07.012 CrossRefGoogle Scholar
  61. Klironomos JN (2000) Host-specificity and functional diversity among arbuscular mycorrhizal fungi. In: Bell CR, Brylinsky M, Johnson-Green P (eds) Microbial biosystems: new frontiers. Proceedings of the 8th International Symposium on microbial ecology. Atlantic Canada Society for Microbial Ecology, Halifax, Canada, pp 845–851Google Scholar
  62. Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301. doi: 10.1890/02-0413 CrossRefGoogle Scholar
  63. Koch AM, Antunes PM, Maherali H, Hart MM, Klironomos JN (2017) Evolutionary assymmetry in the arbuscular mycorrhizal symbiosis: conservatism in fungal morphology does not pretict host plant growth. New Phytol. doi: 10.1111/nph.1446
  64. Koch AM, Kuhn G, Fontanillas P, Fumagalli L, Goudet J, Sanders IR (2004) High genetic variability and low local diversity in a population of arbuscular mycorrhizal fungi. Proc Natl Acad Sci USA 101:2369–2374. doi: 10.1073/pnas.0306441101 PubMedPubMedCentralCrossRefGoogle Scholar
  65. Koch AM, Croll D, Sanders IR (2006) Genetic variability in a population of arbuscular mycorrhizal fungi causes variation in plant growth. Ecol Lett 9:103–110. doi: 10.1111/j.1461-0248.2005.00853.x PubMedCrossRefGoogle Scholar
  66. Kuhn G, Hijri M, Sanders IR (2001) Evidence for the evolution of multiple genomes in arbuscular mycorrhizal fungi. Nature 414:745–748. doi: 10.1038/414745a PubMedCrossRefGoogle Scholar
  67. Lekberg Y, Gibbons SM, Rosendahl S (2014) Will different OTU delineation methods change interpretation of arbuscular mycorrhizal fungal community patterns? New Physician 202:1101–1104. doi: 10.1111/nph.12758 CrossRefGoogle Scholar
  68. Maherali H, Klironomos JN (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316(5832):1746–1748. doi: 10.1126/science.1143082
  69. Maillet F, Poinsot V, André O, Puech-Pagès V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A, Martinez EA, Driguez H, Bécard G, Dénarié J (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469:58–63PubMedCrossRefGoogle Scholar
  70. Marleau J, Dalpé Y, St-Arnaud M, Hijri M (2011) Spore development and nuclear inheritance in arbuscular mycorrhizal fungi. BMC Evol Biol 11:1–11. doi: 10.1186/1471-2148-11-51 CrossRefGoogle Scholar
  71. Mayr E (1942) Systematics and the origin of species, from the viewpoint of a zoologist. Harvard University Press, LondonGoogle Scholar
  72. Mayr E (2000) The biological species concept. In: Wheeler QD, Meier R (eds) Species concepts and phylogenetic theory: a debate. Columbia University Press, New York, pp 17–29Google Scholar
  73. Mensah JA, Koch AM, Antunes PM, Hart MM, Kiers ET, Bücking H (2015) High functional diversity within arbuscular mycorrhizal fungal species is associated with differences in phosphate and nitrogen uptake and fungal phosphate metabolism. Mycorrhiza 7:533–546. doi: 10.1007/s00572-015-0631-x CrossRefGoogle Scholar
  74. Merryweather J, Fitter A (1998) The arbuscular mycorrhizal fungi of hyacinthoides non-scripta. II. Seasonal and spatial patterns of fungal populations. New Phytol 138:131–142CrossRefGoogle Scholar
  75. Mondo SJ, Toomer KH, Morton JB, Lekberg Y, Pawlowska TE (2012) Evolutionary stability in a 400-million-year-old heritable facultative mutualism. Evolution 66:2564–2576. doi: 10.1111/j.1558-5646.2012.01611.x PubMedCrossRefGoogle Scholar
  76. Moore D, Robson GD, Trinci AP (2011) 21st century guidebook to fungi. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  77. Morton JB (1985) Variation in mycorrhizal and spore morphology of Glomus occultum and Glomus diaphanum as influenced by plant host and soil environment. Mycologia 77:192–204. doi: 10.2307/3793068 CrossRefGoogle Scholar
  78. Morton JB, Benny GL (1990) Revised classification of arbuscular mycorrhizal fungi (Zygomycetes): a new order, Glomales, two new suborders, Glomineae and Gigasporineae, and two new families, Acaulosporaceae and Gigasporaceae, with an emendation of Glomaceae. Mycotaxon 37:471–491Google Scholar
  79. Mosse B, Bowen G (1968) The distribution of Endogone spores in some Australian and New Zealand soils, and in an experimental field soil at Rothamsted. Trans Br Mycol Soc 51:485–492. doi: 10.1016/S0007-1536(68)80015-4 CrossRefGoogle Scholar
  80. Munkvold L, Kjoller R, Vestberg M, Rosendahl S, Jakobsen I (2004) High functional diversity within species of arbuscular mycorrhizal fungi. New Physician 164:357–364. doi: 10.1111/j.1469-8137.2004.01169.x CrossRefGoogle Scholar
  81. Naito M, Pawlowska TE (2016) Defying Muller’s ratchet: ancient heritable endobacteria escape extinction through retention of recombination and genome plasticity. mBIO 7(3):e02057–e02015. doi: 10.1128/mBio.02057-15 PubMedPubMedCentralCrossRefGoogle Scholar
  82. Naito M, Morton JB, Pawlowska TE (2015) Minimal genomes of mycoplasma-related endobacteria are plastic and contain host-derived genes for sustained life within Glomeromycota. Proc Natl Acad Sci USA 112:7791–7796. doi: 10.1073/pnas.1501676112 PubMedPubMedCentralCrossRefGoogle Scholar
  83. Newton A, Haigh J (1998) Diversity of ectomycorrhizal fungi in Britain: a test of the species–area relationship, and the role of host specificity. New Physician 138:619–627. doi: 10.1046/j.1469-8137.1998.00143.x CrossRefGoogle Scholar
  84. Ohtomo R, Saito M (2005) Polyphosphate dynamics in mycorrhizal roots during colonization of an arbuscular mycorrhizal fungus. New Physician 167:571–578. doi: 10.1111/j.1469-8137.2005.01425.x CrossRefGoogle Scholar
  85. Öpik M, Moora M, Zobel M, Saks U, Wheatley R, Wright F, Daniell T (2008) High diversity of arbuscular mycorrhizal fungi in a boreal herb-rich coniferous forest. New Physician 179:867–876. doi: 10.1111/j.1469-8137.2008.02515.x CrossRefGoogle Scholar
  86. Öpik M, Metsis M, Daniell TJ, Zobel M, Moora M (2009) Large-scale parallel 454 sequencing reveals host ecological group specificity of arbuscular mycorrhizal fungi in a boreonemoral forest. New Physician 184:424–437. doi: 10.1111/j.1469-8137.2009.02920.x CrossRefGoogle Scholar
  87. Öpik M, Zobel M, Cantero JJ, Davison J, Facelli JM, Hiiesalu I, Jairus T, Kalwij JM, Koorem K, Leal ME (2013) Global sampling of plant roots expands the described molecular diversity of arbuscular mycorrhizal fungi. Mycorrhiza 23:411–430. doi: 10.1007/s00572-013-0482-2 PubMedCrossRefGoogle Scholar
  88. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775. doi: 10.1038/nrmicro1987 PubMedCrossRefGoogle Scholar
  89. Pawlowska TE, Taylor JW (2004) Organization of genetic variation in individuals of arbuscular mycorrhizal fungi. Nature 427:733–737. doi: 10.1038/nature02290 PubMedCrossRefGoogle Scholar
  90. Peng S, Eissenstat DM, Graham JH, Williams K, Hodge NC (1993) Growth depression in mycorrhizal citrus at high-phosphorus supply. Plant Physiol 101:1063–1071PubMedPubMedCentralCrossRefGoogle Scholar
  91. Pepe A, Giovannetti M, Sbrana C (2016) Different levels of hyphal self-incompatibility modulate interconnectedness of mycorrhizal networks in three arbuscular mycorrhizal fungi within the Glomeraceae. Mycorrhiza 26:325–332. doi: 10.1007/s00572-015-0671-2 PubMedCrossRefGoogle Scholar
  92. Powell JR, Parrent JL, Hart MM, Klironomos JN, Rillig MC, Maherali H (2009) Phylogenetic trait conservatism and the evolution of functional trade-offs in arbuscular mycorrhizal fungi. Proc R Soc Biol Sci 276:4237–4245. doi: 10.1098/rspb.2009.1015 CrossRefGoogle Scholar
  93. Pressel S, Bidartondo MI, Ligrone R, Duckett JG (2010) Fungal symbioses in bryophytes: new insights in the twenty first century. Phytotaxa 9:238-253 doi: 10.11646/phytotaxa.9.1.13Google Scholar
  94. Purin S, Morton J (2013) Anastomosis behavior differs between asymbiotic and symbiotic hyphae of Rhizophagus clarus. Mycologia:12-135. doi:  10.3852/12-135
  95. Redecker D, Schüßler A, Stockinger H, Stürmer SL, Morton JB, Walker C (2013) An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza 23:515–531. doi: 10.1007/s00572-013-0486-y PubMedCrossRefGoogle Scholar
  96. Rinaldi AC, Comandini O, Kuyper TW (2008) Ectomycorrhizal fungal diversity: separating the wheat from the chaff. Fungal Divers 33:1–45Google Scholar
  97. Rodriguez A, Sanders IR (2015) The role of community and population ecology in applying mycorrhizal fungi for improved food security. ISME J 9:1053–1061. doi: 10.1038/ismej.2014.207 PubMedCrossRefGoogle Scholar
  98. Roger A, Colard A, Angelard C, Sanders IR (2013) Relatedness among arbuscular mycorrhizal fungi drives plant growth and intraspecific fungal coexistence. ISME J 7:2137–2146. doi: 10.1038/ismej.2013.112
  99. Rosendahl S (2008) Communities, populations and individuals of arbuscular mycorrhizal fungi. New Physician 178:253–266. doi: 10.1111/j.1469-8137.2008.02378.x CrossRefGoogle Scholar
  100. Salvioli A, Chiapello M, Fontaine J, Hadj-Sahraoui AL, Grandmougin-Ferjani A, Lanfranco L, Bonfante P (2010) Endobacteria affect the metabolic profile of their host Gigaspora margarita, an arbuscular mycorrhizal fungus. Environ Microbiol 12:2083–2095. doi: 10.1111/j.1462-2920.2010.02246.x PubMedGoogle Scholar
  101. Salvioli A, Ghignone S, Novero M, Navazio L, Venice F, Bagnaresi P, Bonfante P (2016) Symbiosis with an endobacterium increases the fitness of a mycorrhizal fungus, raising its bioenergetic potential. ISME J 10:130–144. doi: 10.1038/ismej.2015.91 PubMedCrossRefGoogle Scholar
  102. Sanders IR (1999) No sex please, we’re fungi. Nature 399:737–739. doi: 10.1038/21544 PubMedCrossRefGoogle Scholar
  103. Sanders IR (2002) Ecology and evolution of multigenomic arbuscular mycorrhizal fungi. Am Nat 160:128–141. doi: 10.1086/342085 CrossRefGoogle Scholar
  104. Sanders IR (2011) Fungal sex: meiosis machinery in ancient symbiotic fungi. Curr Biol 21:896–897. doi: 10.1016/j.cub.2011.09.021 CrossRefGoogle Scholar
  105. Schüßler A, Walker C (2010) The Glomeromycota. A species list with new families and new genera. In: Libraries at the Royal Botanic Garden Edinburgh, The Royal Botanic Garden Kew, Botanische Staatssammlung Munich, and Oregon State University, GloucesterGoogle Scholar
  106. Smith SE, Read D (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, New YorkGoogle Scholar
  107. Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250. doi: 10.1146/annurev-arplant-042110-103846 PubMedCrossRefGoogle Scholar
  108. Smith FA, Smith SE (2013) How useful is the mutualism-parasitism continuum of arbuscular mycorrhizal functioning? Plant Soil 363:7–18. doi: 10.1007/s11104-012-1583-y CrossRefGoogle Scholar
  109. Smith SE, Jakobsen I, Grønlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156:1050–1057. doi: 10.1104/pp.111.174581 PubMedPubMedCentralCrossRefGoogle Scholar
  110. Stockinger H, Walker C, Schussler A (2009) ‘Glomus intraradices DAOM197198’, a model fungus in arbuscular mycorrhiza research, is not Glomus intraradices. New Physician 183(4):1176–1187. doi: 10.1111/j.1469-8137.2009.02874.x CrossRefGoogle Scholar
  111. Stukenbrock EH, Rosendahl S (2005) Clonal diversity and population genetic structure of arbuscular mycorrhizal fungi (Glomus spp.) studied by multilocus genotyping of single spores. Mol Ecol 14:743–752. doi: 10.1111/j.1365-294X.2005.02453.x PubMedCrossRefGoogle Scholar
  112. Takanishi I, Ohtomo R, Hayatsu M, Saito M (2009) Short-chain polyphosphate in arbuscular mycorrhizal roots colonized by Glomus spp.: a possible phosphate pool for host plants. Soil Biol Biochem 41:1571–1573. doi: 10.1016/j.soilbio.2009.04.002 CrossRefGoogle Scholar
  113. Tamasloukht M, Séjalon-Delmas N, Kluever A, Jauneau A, Roux C, Bécard G, Franken P (2003) Root factors induce mitochondrial related gene expression and fungal respiration during developmental switch from asymbiosis to presymbiosis in the arbuscular mycorrhizal fungus Gigaspora rosea. Plant Physiol 131:1468–1478. doi: 10.1104/pp.012898 PubMedPubMedCentralCrossRefGoogle Scholar
  114. Tamasloukht M, Waschke A, Franken P (2007) Root exudate-stimulated RNA accumulation in the arbuscular mycorrhizal fungus Gigaspora rosea. Soil Biol Biochem 39:1824–1827. doi: 10.1016/j.soilbio.2007.01.031 CrossRefGoogle Scholar
  115. Taylor TN, Remy W, Hass H, Kerp H (1995) Fossil arbuscular mycorrhizae from the early devonian. Mycologia 87:560–573. doi: 10.2307/3760776 CrossRefGoogle Scholar
  116. Tedersoo L, May TW, Smith ME (2010) Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20:217–263. doi: 10.1007/s00572-009-0274-x PubMedCrossRefGoogle Scholar
  117. Tisserant E, Kohler A, Dozolme-Seddas P, Balestrini R, Benabdellah K, Colard A, Croll D, Da Silva C, Gomez SK, Koul R, Ferrol N, Fiorilli V, Formey D, Franken P, Helber N, Hijri M, Lanfranco L, Lindquist E, Liu Y, Malbreil M, Morin E, Poulain J, Shapiro H, van Tuinen D, Waschke A, Azcón-Aguilar C, Bécard G, Bonfante P, Harrison MJ, Küster H, Lammers P, Paszkowski U, Requena N, Rensing SA, Roux C, Sanders IR, Shachar-Hill Y, Tuskan G, Young JPW, Gianinazzi-Pearson V, Martin F (2012) The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices (DAOM 197198) reveals functional tradeoffs in an obligate symbiont. New Physician 193:755–769. doi: 10.1111/j.1469-8137.2011.03948.x CrossRefGoogle Scholar
  118. Toomer KH, Chen XH, Naito M, Mondo SJ, den Bakker HC, VanKuren NW, Lekberg Y, Morton JB, Pawlowska TE (2015) Molecular evolution patterns reveal life history features of mycoplasma-related endobacteria associated with arbuscular mycorrhizal fungi. Mol Ecol 24:3485–3500. doi: 10.1111/mec.13250 PubMedCrossRefGoogle Scholar
  119. Torrecillas E, Alguacil MM, Roldán A (2012) Host preferences of arbuscular mycorrhizal fungi colonizing annual herbaceous plant species in semiarid Mediterranean Prairies. Appl Environ Microbiol 78:6180–6186. doi: 10.1128/AEM.01287-12 PubMedPubMedCentralCrossRefGoogle Scholar
  120. Treseder KK (2013) The extent of mycorrhizal colonization of roots and its influence on plant growth and phosphorus content. Plant Soil 371:1–13. doi: 10.1007/s11104-013-1681-5 CrossRefGoogle Scholar
  121. Tripathi P, Rabara RC, Reese RN, Miller MA, Rohila JS, Subramanian S, Shen QJ, Morandi D, Bücking H, Shulaev V, Rushton PJ (2016) A toolbox of genes, proteins, metabolites and promoters for improving drought tolerance in soybean includes the metabolite coumestrol and stomatal development genes. BMC Genomics 17:1–22. doi: 10.1186/s12864-016-2420-0 CrossRefGoogle Scholar
  122. Valyi K, Rillig MC, Hempel S (2015) Land-use intensity and host plant identity interactively shape communities of arbuscular mycorrhizal fungi in roots of grassland plants. New Physician 205:1577–1586. doi: 10.1111/nph.13236 CrossRefGoogle Scholar
  123. Vannini C, Carpentieri A, Salvioli A, Novero M, Marsoni M, Testa L, de Pinto MC, Amoresano A, Ortolani F, Bracale M, Bonfante P (2016) An interdomain network: the endobacterium of a mycorrhizal fungus promotes antioxidative responses in both fungal and plant hosts. New Phytol 211:265–275. doi: 10.1111/nph.13895 PubMedCrossRefGoogle Scholar
  124. Violi HA, Treseder KK, Menge JA, Wright SF, Lovatt CJ (2007) Density dependence and interspecific interactions between arbuscular mycorrhizal fungi mediated plant growth, glomalin production, and sporulation. Can J Bot 85:63–75. doi: 10.1139/b06-151 CrossRefGoogle Scholar
  125. Walder F, Niemann H, Natarajan M, Lehmann MF, Boller T, Wiemken A (2012) Mycorrhizal networks: common goods of plants shared under unequal terms of trade. Plant Physiol 159:789–797. doi: 10.1104/pp.112.195727 PubMedPubMedCentralCrossRefGoogle Scholar
  126. Wang X, Bücking H (2015) Arbuscular mycorrhizal growth and phosphate uptake responses are fungal specific but do not differ between a soybean genotype with a high and a low phosphate acquisition efficiency. Ann Bot. doi: 10.1093/aob/mcw074. pii:mcw074
  127. Wang B, Qiu Y-L (2006) Phylogenetic distribution and evolution of mycorrhizae in land plants. Mycorrhiza 16:2. doi:10.1007/s00572-005-0033-699-363Google Scholar
  128. Wright DP, Read DJ, Scholes JD (1998) Mycorrhizal sink strength influences whole plant carbon balance of Trifolium repens L. Plant Cell Environ 21:881–891. doi: 10.1046/j.1365-3040.1998.00351.x CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Brandon Monier
    • 1
  • Vincent Peta
    • 1
  • Jerry Mensah
    • 1
  • Heike Bücking
    • 1
    Email author
  1. 1.Biology and Microbiology DepartmentSouth Dakota State UniversityBrookingsUSA

Personalised recommendations