No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

The Mutualistic Interaction between Plants and Arbuscular Mycorrhizal Fungi

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
Buy this Microbiology Spectrum Article
Price Non-Member $15.00
  • Authors: Luisa Lanfranco1, Paola Bonfante2, Andrea Genre3
  • Editors: Joseph Heitman4, Barbara J. Howlett5
    Affiliations: 1: Department of Life Sciences and Systems Biology, University of Torino, Torino, 10125, Italy; 2: Department of Life Sciences and Systems Biology, University of Torino, Torino, 10125, Italy; 3: Department of Life Sciences and Systems Biology, University of Torino, Torino, 10125, Italy; 4: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710; 5: School of Biosciences, The University of Melbourne, Victoria, NSW 3010, Australia
  • Source: microbiolspec November 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.FUNK-0012-2016
  • Received 13 May 2016 Accepted 08 July 2016 Published 18 November 2016
  • Luisa Lanfranco, luisa.lanfranco@unito.it
image of The Mutualistic Interaction between Plants and Arbuscular Mycorrhizal Fungi
    Preview this microbiology spectrum article:
    Zoom in

    The Mutualistic Interaction between Plants and Arbuscular Mycorrhizal Fungi, Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/4/6/FUNK-0012-2016-1.gif /docserver/preview/fulltext/microbiolspec/4/6/FUNK-0012-2016-2.gif
  • Abstract:

    Mycorrhizal fungi belong to several taxa and develop mutualistic symbiotic associations with over 90% of all plant species, from liverworts to angiosperms. While descriptive approaches have dominated the initial studies of these fascinating symbioses, the advent of molecular biology, live cell imaging, and “omics” techniques have provided new and powerful tools to decipher the cellular and molecular mechanisms that rule mutualistic plant-fungus interactions. In this article we focus on the most common mycorrhizal association, arbuscular mycorrhiza (AM), which is formed by a group of soil fungi belonging to Glomeromycota. AM fungi are believed to have assisted the conquest of dry lands by early plants around 450 million years ago and are found today in most land ecosystems. AM fungi have several peculiar biological traits, including obligate biotrophy, intracellular development inside the plant tissues, coenocytic multinucleate hyphae, and spores, as well as unique genetics, such as the putative absence of a sexual cycle, and multiple ecological functions. All of these features make the study of AM fungi as intriguing as it is challenging, and their symbiotic association with most crop plants is currently raising a broad interest in agronomic contexts for the potential use of AM fungi in sustainable production under conditions of low chemical input.

  • Citation: Lanfranco L, Bonfante P, Genre A. 2016. The Mutualistic Interaction between Plants and Arbuscular Mycorrhizal Fungi. Microbiol Spectrum 4(6):FUNK-0012-2016. doi:10.1128/microbiolspec.FUNK-0012-2016.


1. Smith VSE, Read DJ. 2008. Mycorrhizal Symbiosis, 3rd ed. Academic Press, New York, NY.
2. van der Heijden MGA, Sanders IR. 2002. Mycorrhizal Ecology. Springer-Verlag, Berlin, Germany.
3. Bonfante P, Genre A. 2010. Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat Commun 1:48. http://dx.doi.org/10.1038/ncomms1046.
4. van der Heijden MGA, Martin FM, Selosse MA, Sanders IR. 2015. Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423 http://dx.doi.org/10.1111/nph.13288.
5. Gianinazzi S, Gollotte A, Binet MN, van Tuinen D, Redecker D, Wipf D. 2010. Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530 http://dx.doi.org/10.1007/s00572-010-0333-3.
6. Berruti A, Lumini E, Balestrini R, Bianciotto V. 2016. Arbuscular mycorrhizal fungi as natural biofertilizers: let’s benefit from past successes. Front Microbiol 6:1559. http://dx.doi.org/10.3389/fmicb.2015.01559.
7. Miller RM, Reinhardt DR, Jastrow JD. 1995. External hyphal production of vesicular-arbuscular mycorrhizal fungi in pasture and tallgrass prairie communities. Oecologia 103:17–23 http://dx.doi.org/10.1007/BF00328420.
8. 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 http://dx.doi.org/10.1146/annurev-arplant-042110-103846. [CrossRef]
9. Finlay RD. 2008. Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. J Exp Bot 59:1115–1126 http://dx.doi.org/10.1093/jxb/ern059.
10. Bonfante P. 1984. Anatomy and morphology of VA mycorrhizae, p 5–33. In Powell CL, Bagyaraj DJ (ed), VA Mycorrhizae. CRC Press, Boca Raton, FL.
11. Gutjahr C, Parniske M. 2013. Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annu Rev Cell Dev Biol 29:593–617 http://dx.doi.org/10.1146/annurev-cellbio-101512-122413.
12. Lanfranco L, Young JPW. 2012. Genetic and genomic glimpses of the elusive arbuscular mycorrhizal fungi. Curr Opin Plant Biol 15:454–461 http://dx.doi.org/10.1016/j.pbi.2012.04.003.
13. Bago B, Pfeffer PE, Shachar-Hill Y. 2000. Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol 124:949–958 http://dx.doi.org/10.1104/pp.124.3.949.
14. 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 http://dx.doi.org/10.1126/science.1208473.
15. Rillig MC, Aguilar-Trigueros CA, Bergmann J, Verbruggen E, Veresoglou SD, Lehmann A. 2015. Plant root and mycorrhizal fungal traits for understanding soil aggregation. New Phytol 205:1385–1388 http://dx.doi.org/10.1111/nph.13045.
16. van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR. 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72 http://dx.doi.org/10.1038/23932.
17. Pozo MJ, Azcón-Aguilar C. 2007. Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398 http://dx.doi.org/10.1016/j.pbi.2007.05.004. [CrossRef]
18. 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 http://dx.doi.org/10.1007/s10886-012-0134-6.
19. Porcel R, Aroca R, Ruiz-Lozano JM. 2011. Salinity stress alleviation using arbuscular mycorrhizal fungi. Agron Sustainable Dev 32:181–200 http://dx.doi.org/10.1007/s13593-011-0029-x.
20. Augé RM, Toler HD, Saxton AM. 2015. Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis. Mycorrhiza 25:13–24 http://dx.doi.org/10.1007/s00572-014-0585-4.
21. Redecker D, Kodner R, Graham LE. 2000. Glomalean fungi from the Ordovician. Science 289:1920–1921 http://dx.doi.org/10.1126/science.289.5486.1920.
22. Remy W, Taylor TN, Hass H, Kerp H. 1994. Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci USA 91:11841–11843 http://dx.doi.org/10.1073/pnas.91.25.11841.
23. Janse JM. 1896. Les endophytes radicaux de quelques plantes Javanese. Ann Jardin Bot Buitenzorg 15:53–212.
24. Gallaud I. 1905. Études sur les mycorrhizes endotrophes. Rev Générale Bot 17:5–48, 66–83, 123–135, 223–239, 313–325, 425–433, 479–500.
25. Tulasne LR, Tulasne C. 1844. Fungi nonnulli hipogaei, novi v. minus cogniti auct. G Bot Ital (Florence, Italy) 2:55–63.
26. Schüßler A, Schwarzott D, Walker C. 2001. A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421 http://dx.doi.org/10.1017/S0953756201005196.
27. Öpik M, Zobel M, Cantero JJ, Davison J, Facelli JM, Hiiesalu I, Jairus T, Kalwij JM, Koorem K, Leal ME, Liira J, Metsis M, Neshataeva V, Paal J, Phosri C, Põlme S, Reier Ü, Saks Ü, Schimann H, Thiéry O, Vasar M, Moora M. 2013. Global sampling of plant roots expands the described molecular diversity of arbuscular mycorrhizal fungi. Mycorrhiza 23:411–430 http://dx.doi.org/10.1007/s00572-013-0482-2.
28. Davison J, Moora M, Öpik M, Adholeya A, Ainsaar L, Bâ A, Burla S, Diedhiou AG, Hiiesalu I, Jairus T, Johnson NC, Kane A, Koorem K, Kochar M, Ndiaye C, Pärtel M, Reier Ü, Saks Ü, Singh R, Vasar M, Zobel M. 2015. Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science 349:970–973 http://dx.doi.org/10.1126/science.aab1161.
29. Krüger M, Krüger C, Walker C, Stockinger H, Schüssler A. 2012. Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytol 193:970–984 http://dx.doi.org/10.1111/j.1469-8137.2011.03962.x.
30. Lee J, Young JPW. 2009. The mitochondrial genome sequence of the arbuscular mycorrhizal fungus Glomus intraradices isolate 494 and implications for the phylogenetic placement of Glomus. New Phytol 183:200–211 http://dx.doi.org/10.1111/j.1469-8137.2009.02834.x.
31. Pelin A, Pombert JF, Salvioli A, Bonen L, Bonfante P, Corradi N. 2012. The mitochondrial genome of the arbuscular mycorrhizal fungus Gigaspora margarita reveals two unsuspected trans-splicing events of group I introns. New Phytol 194:836–845 http://dx.doi.org/10.1111/j.1469-8137.2012.04072.x.
32. Nadimi M, Beaudet D, Forget L, Hijri M, Lang BF. 2012. Group I intron-mediated trans-splicing in mitochondria of Gigaspora rosea and a robust phylogenetic affiliation of arbuscular mycorrhizal fungi with Mortierellales. Mol Biol Evol 29:2199–2210 http://dx.doi.org/10.1093/molbev/mss088.
33. Halary S, Malik SB, 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 http://dx.doi.org/10.1093/gbe/evr089.
34. Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A, Balestrini R, Charron P, Duensing N, Frei dit Frey N, Gianinazzi-Pearson V, Gilbert LB, Handa Y, Herr JR, Hijri M, Koul R, Kawaguchi M, Krajinski F, Lammers PJ, Masclaux FG, Murat C, Morin E, Ndikumana S, Pagni M, Petitpierre D, Requena N, Rosikiewicz P, Riley R, Saito K, San Clemente H, Shapiro H, van Tuinen D, Bécard G, Bonfante P, Paszkowski U, Shachar-Hill YY, Tuskan GA, Young JP, Sanders IR, Henrissat B, Rensing SA, Grigoriev IV, Corradi N, Roux C, Martin F. 2013. Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc Natl Acad Sci USA 110:20117–20122 http://dx.doi.org/10.1073/pnas.1313452110. (Erratum, http://www.pnas.org/content/111/1/562.3.full.)
35. Lin K, Limpens E, Zhang Z, Ivanov S, Saunders DGO, Mu D, Pang E, Cao H, Cha H, Lin T, Zhou Q, Shang Y, Li Y, Sharma T, van Velzen R, de Ruijter N, Aanen DK, Win J, Kamoun S, Bisseling T, Geurts R, Huang S. 2014. Single nucleus genome sequencing reveals high similarity among nuclei of an endomycorrhizal fungus. PLoS Genet 10:e1004078. http://dx.doi.org/10.1371/journal.pgen.1004078.
36. Young JPW. 2015. Genome diversity in arbuscular mycorrhizal fungi. Curr Opin Plant Biol 26:113–119 http://dx.doi.org/10.1016/j.pbi.2015.06.005.
37. Bidartondo MI, Read DJ, Trappe JM, Merckx V, Ligrone R, Duckett JG. 2011. The dawn of symbiosis between plants and fungi. Biol Lett 7:574–577 http://dx.doi.org/10.1098/rsbl.2010.1203.
38. Field KJ, Pressel S, Duckett JG, Rimington WR, Bidartondo MI. 2015. Symbiotic options for the conquest of land. Trends Ecol Evol 30:477–486 http://dx.doi.org/10.1016/j.tree.2015.05.007.
39. Hosny M, Gianinazzi-Pearson V, Dulieu H. 1998. Nuclear DNA content of 11 fungal species in Glomales. Genome 41:422–428 http://dx.doi.org/10.1139/g98-038.
40. Jany JL, Pawlowska TE. 2010. Multinucleate spores contribute to evolutionary longevity of asexual glomeromycota. Am Nat 175:424–435 http://dx.doi.org/10.1086/650725.
41. Lanfranco L, Delpero M, Bonfante P. 1999. Intrasporal variability of ribosomal sequences in the endomycorrhizal fungus Gigaspora margarita. Mol Ecol 8:37–45 http://dx.doi.org/10.1046/j.1365-294X.1999.00535.x.
42. Jansa J, Mozafar A, Anken T, Ruh R, Sanders IR, Frossard E. 2002. Diversity and structure of AMF communities as affected by tillage in a temperate soil. Mycorrhiza 12:225–234 http://dx.doi.org/10.1007/s00572-002-0163-z.
43. Stockinger H, Walker C, Schüssler A. 2009. ‘Glomus intraradices DAOM197198’, a model fungus in arbuscular mycorrhiza research, is not Glomus intraradices. New Phytol 183:1176–1187 http://dx.doi.org/10.1111/j.1469-8137.2009.02874.x.
44. Hijri M, Sanders IR. 2005. Low gene copy number shows that arbuscular mycorrhizal fungi inherit genetically different nuclei. Nature 433:160–163 http://dx.doi.org/10.1038/nature03069.
45. Rosendahl S, Stukenbrock EH. 2004. Community structure of arbuscular mycorrhizal fungi in undisturbed vegetation revealed by analyses of LSU rDNA sequences. Mol Ecol 13:3179–3186 http://dx.doi.org/10.1111/j.1365-294X.2004.02295.x.
46. Ropars J, Corradi N. 2015. Homokaryotic vs heterokaryotic mycelium in arbuscular mycorrhizal fungi: different techniques, different results? New Phytol 208:638–641 http://dx.doi.org/10.1111/nph.13448.
47. Pawlowska TE, Taylor JW. 2004. Organization of genetic variation in individuals of arbuscular mycorrhizal fungi. Nature 427:733–737 http://dx.doi.org/10.1038/nature02290.
48. Giovannetti M, Fortuna P, Citernesi AS, Morini S, Nuti MP. 2001. The occurrence of anastomosis formation and nuclear exchange in intact arbuscular mycorrhizal networks. New Phytol 151:717–724 http://dx.doi.org/10.1046/j.0028-646x.2001.00216.x.
49. Giovannetti M, Sbrana C, Avio L, Strani P. 2004. Patterns of below-ground plant interconnections established by means of arbuscular mycorrhizal networks. New Phytol 164:175–181 http://dx.doi.org/10.1111/j.1469-8137.2004.01145.x.
50. 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 Phytol 181:924–937 http://dx.doi.org/10.1111/j.1469-8137.2008.02726.x.
51. 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 http://dx.doi.org/10.1128/AEM.69.1.616-624.2003.
52. Desirò A, Salvioli A, Ngonkeu EL, Mondo SJ, Epis S, Faccio A, Kaech A, Pawlowska TE, Bonfante P. 2014. Detection of a novel intracellular microbiome hosted in arbuscular mycorrhizal fungi. ISME J 8:257–270 http://dx.doi.org/10.1038/ismej.2013.151.
53. 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 http://dx.doi.org/10.1038/ismej.2011.110.
54. Torres-Cortés G, Ghignone S, Bonfante P, Schüßler A. 2015. Mosaic genome of endobacteria in arbuscular mycorrhizal fungi: transkingdom gene transfer in an ancient mycoplasma-fungus association. Proc Natl Acad Sci USA 112:7785–7790 http://dx.doi.org/10.1073/pnas.1501540112. (Erratum, http://www.pnas.org/content/112/38/E5376.full.)
55. 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 http://dx.doi.org/10.1073/pnas.1501676112.
56. 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 http://dx.doi.org/10.1038/ismej.2015.91.
57. 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 http://dx.doi.org/10.1111/nph.13895.
58. Ikeda Y, Shimura H, Kitahara R, Masuta C, Ezawa T. 2012. A novel virus-like double-stranded RNA in an obligate biotroph arbuscular mycorrhizal fungus: a hidden player in mycorrhizal symbiosis. Mol Plant Microbe Interact 25:1005–1012 http://dx.doi.org/10.1094/MPMI-11-11-0288.
59. Kitahara R, Ikeda Y, Shimura H, Masuta C, Ezawa T. 2014. A unique mitovirus from Glomeromycota, the phylum of arbuscular mycorrhizal fungi. Arch Virol 159:2157–2160 http://dx.doi.org/10.1007/s00705-014-1999-1.
60. Martin F, Tuskan GA, DiFazio SP, Lammers P, Newcombe G, Podila GK. 2004. Symbiotic sequencing for the Populus mesocosm. New Phytol 161:330–335 http://dx.doi.org/10.1111/j.1469-8137.2004.00982.x.
61. Spanu PD, Abbott JC, Amselem J, Burgis TA, Soanes DM, Stüber K.. Ver Loren van, Themaat E, Brown JK, Butcher SA, Gurr SJ, Lebrun MH, Ridout CJ, Schulze-Lefert P, Talbot NJ, Ahmadinejad N, Ametz C, Barton GR, Benjdia M, Bidzinski P, Bindschedler LV, Both M, Brewer MT, Cadle-Davidson L, Cadle-Davidson MM, Collemare J, Cramer R, Frenkel O, Godfrey D, Harriman J, Hoede C, King BC, Klages S, Kleemann J, Knoll D, Koti PS, Kreplak J, López-Ruiz FJ, Lu X, Maekawa T, Mahanil S, Micali C, Milgroom MG, Montana G, Noir S, O’Connell RJ, Oberhaensli S, Parlange F, Pedersen C, Quesneville H, Reinhardt R, Rott M, Sacristán S, Schmidt SM, Schön M, Skamnioti P, Sommer H, Stephens A, Takahara H, Thordal-Christensen H, Vigouroux M, Wessling R, Wicker T, Panstruga R. 2010. Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330:1543–1546.
62. Martin F, et al. 2010. Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464:1033–1038 http://dx.doi.org/10.1038/nature08867.
63. Ropars J, Kinga Sędzielewska Toro K, Noel J, Pelin A, Charron P, Farinelli L, Marton T, Krüger M, Fuchs J, Brachmann A, Corradi N. 2016. Evidence for the sexual origin of heterokaryosis in arbuscular mycorrhizal fungi. Nat Microbiol 1:16033. doi:10.1038/nmicrobiol.2016.33.
64. 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. Plant Cell 17:3489–3499 http://dx.doi.org/10.1105/tpc.105.035410.
65. Harrison MJ. 2012. Cellular programs for arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 15:691–698 http://dx.doi.org/10.1016/j.pbi.2012.08.010. [CrossRef]
66. Genre A, Chabaud M, Faccio A, Barker DG, Bonfante P. 2008. Prepenetration apparatus assembly precedes and predicts the colonization patterns of arbuscular mycorrhizal fungi within the root cortex of both Medicago truncatula and Daucus carota. Plant Cell 20:1407–1420 http://dx.doi.org/10.1105/tpc.108.059014.
67. Wang B, Yeun LH, Xue JY, Liu Y, Ané JM, Qiu YL. 2010. Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonization of land by plants. New Phytol 186:514–525 http://dx.doi.org/10.1111/j.1469-8137.2009.03137.x.
68. Delaux PM, Radhakrishnan GV, Jayaraman D, Cheema J, Malbreil M, Volkening JD, Sekimoto H, Nishiyama T, Melkonian M, Pokorny L, Rothfels CJ, Sederoff HW, Stevenson DW, Surek B, Zhang Y, Sussman MR, Dunand C, Morris RJ, Roux C, Wong GK-S, Oldroyd GED, Ané J-M. 2015. Algal ancestor of land plants was preadapted for symbiosis. Proc Natl Acad Sci USA 112:13390–13395 http://dx.doi.org/10.1073/pnas.1515426112.
69. 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 http://dx.doi.org/10.1094/MPMI.2000.13.6.693.
70. Nagahashi G, Douds DD Jr. 2004. Isolated root caps, border cells, and mucilage from host roots stimulate hyphal branching of the arbuscular mycorrhizal fungus, Gigaspora gigantea. Mycol Res 108:1079–1088 http://dx.doi.org/10.1017/S0953756204000693.
71. Al-Babili S, Bouwmeester HJ. 2015. Strigolactones, a novel carotenoid-derived plant hormone. Annu Rev Plant Biol 66:161–186 http://dx.doi.org/10.1146/annurev-arplant-043014-114759.
72. Ruyter-Spira C, Al-Babili S, van der Krol S, Bouwmeester H. 2013. The biology of strigolactones. Trends Plant Sci 18:72–83 http://dx.doi.org/10.1016/j.tplants.2012.10.003.
73. Akiyama K, Matsuzaki K, Hayashi H. 2005. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827 http://dx.doi.org/10.1038/nature03608.
74. Besserer A, Puech-Pagès V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S, Portais J-C, Roux C, Bécard G, Séjalon-Delmas N. 2006. Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol 4:e226. http://dx.doi.org/10.1371/journal.pbio.0040226.
75. Besserer A, Bécard G, Jauneau A, Roux C, Séjalon-Delmas N. 2008. GR24, a synthetic analog of strigolactones, stimulates the mitosis and growth of the arbuscular mycorrhizal fungus Gigaspora rosea by boosting its energy metabolism. Plant Physiol 148:402–413 http://dx.doi.org/10.1104/pp.108.121400.
76. Akiyama K, Ogasawara S, Ito S, Hayashi H. 2010. Structural requirements of strigolactones for hyphal branching in AM fungi. Plant Cell Physiol 51:1104–1117 http://dx.doi.org/10.1093/pcp/pcq058.
77. Moscatiello R, Sello S, Novero M, Negro A, Bonfante P, Navazio L. 2014. The intracellular delivery of TAT-aequorin reveals calcium-mediated sensing of environmental and symbiotic signals by the arbuscular mycorrhizal fungus Gigaspora margarita. New Phytol 203:1012–1020 http://dx.doi.org/10.1111/nph.12849.
78. Bonfante P, Genre A. 2015. Arbuscular mycorrhizal dialogues: do you speak ‘plantish’ or ‘fungish’? Trends Plant Sci 20:150–154 http://dx.doi.org/10.1016/j.tplants.2014.12.002.
79. Bonfante P, Requena N. 2011. Dating in the dark: how roots respond to fungal signals to establish arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 14:451–457 http://dx.doi.org/10.1016/j.pbi.2011.03.014.
80. Kosuta S, Chabaud M, Lougnon G, Gough C, Dénarié J, Barker DG, Bécard G. 2003. A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiol 131:952–962 http://dx.doi.org/10.1104/pp.011882.
81. Oláh B, Brière C, Bécard G, Dénarié J, Gough C. 2005. Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signalling pathway. Plant J 44:195–207 http://dx.doi.org/10.1111/j.1365-313X.2005.02522.x.
82. Kuhn H, Küster H, Requena N. 2010. Membrane steroid-binding protein 1 induced by a diffusible fungal signal is critical for mycorrhization in Medicago truncatula. New Phytol 185:716–733 http://dx.doi.org/10.1111/j.1469-8137.2009.03116.x.
83. Chabaud M, Genre A, Sieberer BJ, Faccio A, Fournier J, Novero M, Barker DG, Bonfante P. 2011. Arbuscular mycorrhizal hyphopodia and germinated spore exudates trigger Ca2+ spiking in the legume and nonlegume root epidermis. New Phytol 189:347–355 http://dx.doi.org/10.1111/j.1469-8137.2010.03464.x.
84. Mukherjee A, Ané J-M. 2011. Germinating spore exudates from arbuscular mycorrhizal fungi: molecular and developmental responses in plants and their regulation by ethylene. Mol Plant Microbe Interact 24:260–270 http://dx.doi.org/10.1094/MPMI-06-10-0146.
85. 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 469:58–63 http://dx.doi.org/10.1038/nature09622.
86. Genre A, Chabaud M, Balzergue C, Puech-Pagès V, Novero M, Rey T, Fournier J, Rochange S, Bécard G, Bonfante P, Barker DG. 2013. Short-chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytol 198:190–202 http://dx.doi.org/10.1111/nph.12146.
87. Chabaud M, Venard C, Defaux-Petras A, Bécard G, Barker DG. 2002. Targeted inoculation of Medicago truncatula in vitro root cultures reveals MtENOD11 expression during early stages of infection by arbuscular mycorrhizal fungi. New Phytol 156:265–273 http://dx.doi.org/10.1046/j.1469-8137.2002.00508.x.
88. 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 http://dx.doi.org/10.1104/pp.112.195990.
89. Oldroyd GED. 2013. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11:252–263 http://dx.doi.org/10.1038/nrmicro2990.
90. Gobbato E. 2015. Recent developments in arbuscular mycorrhizal signaling. Curr Opin Plant Biol 26:1–7 http://dx.doi.org/10.1016/j.pbi.2015.05.006. [CrossRef]
91. Genre A, Russo G. 2016. Does a common pathway transduce symbiotic signals in plant-microbe interactions? Front Plant Sci 7:96 http://dx.doi.org/10.3389/fpls.2016.00096.
92. Chen T, Zhu H, Ke D, Cai K, Wang C, Gou H, Hong Z, Zhang Z. 2012. A MAP kinase kinase interacts with SymRK and regulates nodule organogenesis in Lotus japonicus. Plant Cell 24:823–838 http://dx.doi.org/10.1105/tpc.112.095984.
93. Venkateshwaran M, Jayaraman D, Chabaud M, Genre A, Balloon AJ, Maeda J, Forshey K, den Os D, Kwiecien NW, Coon JJ, Barker DG, Ané J-M. 2015. A role for the mevalonate pathway in early plant symbiotic signaling. Proc Natl Acad Sci USA 112:9781–9786. (Erratum, http://www.pnas.org/content/112/38/E5378.full.) http://dx.doi.org/10.1073/pnas.1413762112.
94. Kanamori N, Madsen LH, Radutoiu S, Frantescu M, Quistgaard EM, Miwa H, Downie JA, James EK, Felle HH, Haaning LL, Jensen TH, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J. 2006. A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc Natl Acad Sci USA 103:359–364 http://dx.doi.org/10.1073/pnas.0508883103.
95. Saito K, Yoshikawa M, Yano K, Miwa H, Uchida H, Asamizu E, Sato S, Tabata S, Imaizumi-Anraku H, Umehara Y, Kouchi H, Murooka Y, Szczyglowski K, Downie JA, Parniske M, Hayashi M, Kawaguchi M. 2007. NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus. Plant Cell 19:610–624 http://dx.doi.org/10.1105/tpc.106.046938.
96. Groth M, Takeda N, Perry J, Uchida H, Dräxl S, Brachmann A, Sato S, Tabata S, Kawaguchi M, Wang TL, Parniske M. 2010. NENA, a Lotus japonicus homolog of Sec13, is required for rhizodermal infection by arbuscular mycorrhiza fungi and rhizobia but dispensable for cortical endosymbiotic development. Plant Cell 22:2509–2526 http://dx.doi.org/10.1105/tpc.109.069807.
97. Riely BK, Lougnon G, Ané JM, Cook DR. 2007. The symbiotic ion channel homolog DMI1 is localized in the nuclear membrane of Medicago truncatula roots. Plant J 49:208–216 http://dx.doi.org/10.1111/j.1365-313X.2006.02957.x.
98. Capoen W, Sun J, Wysham D, Otegui MS, Venkateshwaran M, Hirsch S, Miwa H, Downie JA, Morris RJ, Ané JM, Oldroyd GE. 2011. Nuclear membranes control symbiotic calcium signaling of legumes. Proc Natl Acad Sci USA 108:14348–14353 http://dx.doi.org/10.1073/pnas.1107912108.
99. Ané J-M, Kiss GB, Riely BK, Penmetsa RV, Oldroyd GE, Ayax C, Lévy J, Debellé F, Baek JM, Kalo P, Rosenberg C, Roe BA, Long SR, Dénarié J, Cook DR. 2004. Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303:1364–1367 http://dx.doi.org/10.1126/science.1092986.
100. Imaizumi-Anraku H, Takeda N, Charpentier M, Perry J, Miwa H, Umehara Y, Kouchi H, Murakami Y, Mulder L, Vickers K, Pike J, Downie JA, Wang T, Sato S, Asamizu E, Tabata S, Yoshikawa M, Murooka Y, Wu GJ, Kawaguchi M, Kawasaki S, Parniske M, Hayashi M. 2005. Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature 433:527–531 http://dx.doi.org/10.1038/nature03237.
101. Venkateshwaran M, Cosme A, Han L, Banba M, Satyshur KA, Schleiff E, Parniske M, Imaizumi-Anraku H, Ané JM. 2012. The recent evolution of a symbiotic ion channel in the legume family altered ion conductance and improved functionality in calcium signaling. Plant Cell 24:2528–2545 http://dx.doi.org/10.1105/tpc.112.098475.
102. Patil S, Takezawa D, Poovaiah BW. 1995. Chimeric plant calcium/calmodulin-dependent protein kinase gene with a neural visinin-like calcium-binding domain. Proc Natl Acad Sci USA 92:4897–4901 http://dx.doi.org/10.1073/pnas.92.11.4897.
103. Takezawa D, Ramachandiran S, Paranjape V, Poovaiah BW. 1996. Dual regulation of a chimeric plant serine/threonine kinase by calcium and calcium/calmodulin. J Biol Chem 271:8126–8132 http://dx.doi.org/10.1074/jbc.271.14.8126.
104. Lévy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet EP, Ané JM, Lauber E, Bisseling T, Dénarié J, Rosenberg C, Debellé F. 2004. A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303:1361–1364 http://dx.doi.org/10.1126/science.1093038.
105. Mitra RM, Gleason CA, Edwards A, Hadfield J, Downie JA, Oldroyd GE, Long SR. 2004. A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development: gene identification by transcript-based cloning. Proc Natl Acad Sci USA 101:4701–4705 http://dx.doi.org/10.1073/pnas.0400595101.
106. Miwa H, Sun J, Oldroyd GE, Downie JA. 2006. Analysis of calcium spiking using a cameleon calcium sensor reveals that nodulation gene expression is regulated by calcium spike number and the developmental status of the cell. Plant J 48:883–894 http://dx.doi.org/10.1111/j.1365-313X.2006.02926.x.
107. Messinese E, Mun JH, Yeun LH, Jayaraman D, Rougé P, Barre A, Lougnon G, Schornack S, Bono JJ, Cook DR, Ané JM. 2007. A novel nuclear protein interacts with the symbiotic DMI3 calcium- and calmodulin-dependent protein kinase of Medicago truncatula. Mol Plant Microbe Interact 20:912–921 http://dx.doi.org/10.1094/MPMI-20-8-0912.
108. Yano K, Yoshida S, Müller J, Singh S, Banba M, Vickers K, Markmann K, White C, Schuller B, Sato S, Asamizu E, Tabata S, Murooka Y, Perry J, Wang TL, Kawaguchi M, Imaizumi-Anraku H, Hayashi M, Parniske M. 2008. CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc Natl Acad Sci USA 105:20540–20545 http://dx.doi.org/10.1073/pnas.0806858105.
109. Kaló P, Gleason C, Edwards A, Marsh J, Mitra RM, Hirsch S, Jakab J, Sims S, Long SR, Rogers J, Kiss GB, Downie JA, Oldroyd GE. 2005. Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 308:1786–1789 http://dx.doi.org/10.1126/science.1110951.
110. Smit P, Raedts J, Portyanko V, Debellé F, Gough C, Bisseling T, Geurts R. 2005. NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308:1789–1791 http://dx.doi.org/10.1126/science.1111025.
111. Heckmann AB, Lombardo F, Miwa H, Perry JA, Bunnewell S, Parniske M, Wang TL, Downie JA. 2006. Lotus japonicus nodulation requires two GRAS domain regulators, one of which is functionally conserved in a non-legume. Plant Physiol 142:1739–1750 http://dx.doi.org/10.1104/pp.106.089508.
112. Murakami Y, Miwa H, Imaizumi-Anraku H, Kouchi H, Downie JA, Kawaguchi M, Kawasaki S. 2006. Positional cloning identifies Lotus japonicus NSP2, a putative transcription factor of the GRAS family, required for NIN and ENOD40 gene expression in nodule initiation. DNA Res 13:255–265 http://dx.doi.org/10.1093/dnares/dsl017.
113. Marsh JF, Rakocevic A, Mitra RM, Brocard L, Sun J, Eschstruth A, Long SR, Schultze M, Ratet P, Oldroyd GE. 2007. Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase. Plant Physiol 144:324–335 http://dx.doi.org/10.1104/pp.106.093021.
114. Schauser L, Roussis A, Stiller J, Stougaard J. 1999. A plant regulator controlling development of symbiotic root nodules. Nature 402:191–195 http://dx.doi.org/10.1038/46058.
115. Gobbato E, Marsh JF, Vernié T, Wang E, Maillet F, Kim J, Miller JB, Sun J, Bano SA, Ratet P, Mysore KS, Dénarié J, Schultze M, Oldroyd GE. 2012. A GRAS-type transcription factor with a specific function in mycorrhizal signaling. Curr Biol 22:2236–2241 http://dx.doi.org/10.1016/j.cub.2012.09.044.
116. Giovannetti M, Sbrana C, Avio L, Citernesi AS, Logi C. 1993. Differential hyphal morphogenesis in arbuscular mycorrhizal fungi during pre-infection stages. New Phytol 125:587–593 http://dx.doi.org/10.1111/j.1469-8137.1993.tb03907.x.
117. Nagahashi G, Douds DD Jr. 1997. Appressorium formation by AM fungi on isolated cell walls of carrot roots. New Phytol 136:299–304 http://dx.doi.org/10.1046/j.1469-8137.1997.00739.x.
118. Wang E, Schornack S, Marsh JF, Gobbato E, Schwessinger B, Eastmond P, Schultze M, Kamoun S, Oldroyd GE. 2012. A common signaling process that promotes mycorrhizal and oomycete colonization of plants. Curr Biol 22:2242–2246 http://dx.doi.org/10.1016/j.cub.2012.09.043.
119. Gutjahr C, Gobbato E, Choi J, Riemann M, Johnston MG, Summers W, Carbonnel S, Mansfield C, Yang S-Y, Nadal M, Acosta I, Takano M, Jiao W-B, Schneeberger K, Kelly KA, Paszkowski U. 2015. Rice perception of symbiotic arbuscular mycorrhizal fungi requires the karrikin receptor complex. Science 350:1521–1524 http://dx.doi.org/10.1126/science.aac9715.
120. Genre A, Ivanov S, Fendrych M, Faccio A, Zársky V, Bisseling T, Bonfante P. 2012. Multiple exocytotic markers accumulate at the sites of perifungal membrane biogenesis in arbuscular mycorrhizas. Plant Cell Physiol 53:244–255 http://dx.doi.org/10.1093/pcp/pcr170.
121. Takeda N, Maekawa T, Hayashi M. 2012. Nuclear-localized and deregulated calcium- and calmodulin-dependent protein kinase activates rhizobial and mycorrhizal responses in Lotus japonicus. Plant Cell 24:810–822 http://dx.doi.org/10.1105/tpc.111.091827.
122. Bonfante P. 2001. At the interface between mycorrhizal fungi and plants: the structural organization of cell wall, plasma membrane and cytoskeleton, p 45–61. In Hock B (ed), The Mycota, IX: Fungal Associations. Springer, Berlin, Germany. http://dx.doi.org/10.1007/978-3-662-07334-6_4
123. Balestrini R, Bonfante P. 2014. Cell wall remodeling in mycorrhizal symbiosis: a way towards biotrophism. Front Plant Sci 5:237 http://dx.doi.org/10.3389/fpls.2014.00237.
124. Pumplin N, Harrison MJ. 2009. Live-cell imaging reveals periarbuscular membrane domains and organelle location in Medicago truncatula roots during arbuscular mycorrhizal symbiosis. Plant Physiol 151:809–819 http://dx.doi.org/10.1104/pp.109.141879.
125. Pumplin N, Mondo SJ, Topp S, Starker CG, Gantt JS, Harrison MJ. 2010. Medicago truncatula Vapyrin is a novel protein required for arbuscular mycorrhizal symbiosis. Plant J 61:482–494 http://dx.doi.org/10.1111/j.1365-313X.2009.04072.x.
126. Ivanov S, Fedorova EE, Limpens E, De Mita S, Genre A, Bonfante P, Bisseling T. 2012. Rhizobium-legume symbiosis shares an exocytotic pathway required for arbuscule formation. Proc Natl Acad Sci USA 109:8316–8321 http://dx.doi.org/10.1073/pnas.1200407109.
127. Zhang X, Pumplin N, Ivanov S, Harrison MJ. 2015. EXO70I is required for development of a sub-domain of the periarbuscular membrane during arbuscular mycorrhizal symbiosis. Curr Biol 25:2189–2195 http://dx.doi.org/10.1016/j.cub.2015.06.075.
128. Takeda N, Sato S, Asamizu E, Tabata S, Parniske M. 2009. Apoplastic plant subtilases support arbuscular mycorrhiza development in Lotus japonicus. Plant J 58:766–777 http://dx.doi.org/10.1111/j.1365-313X.2009.03824.x.
129. Rech SS, Heidt S, Requena N. 2013. A tandem Kunitz protease inhibitor (KPI106)-serine carboxypeptidase (SCP1) controls mycorrhiza establishment and arbuscule development in Medicago truncatula. Plant J 75:711–725 http://dx.doi.org/10.1111/tpj.12242.
130. Krajinski F, Courty PE, Sieh D, Franken P, Zhang H, Bucher M, Gerlach N, Kryvoruchko I, Zoeller D, Udvardi M, Hause B. 2014. The H+-ATPase HA1 of Medicago truncatula is essential for phosphate transport and plant growth during arbuscular mycorrhizal symbiosis. Plant Cell 26:1808–1817 http://dx.doi.org/10.1105/tpc.113.120436.
131. Wang E, Yu N, Bano SA, Liu C, Miller AJ, Cousins D, Zhang X, Ratet P, Tadege M, Mysore KS, Downie JA, Murray JD, Oldroyd GE, Schultze M. 2014. A H+-ATPase that energizes nutrient uptake during mycorrhizal symbioses in rice and Medicago truncatula. Plant Cell 26:1818–1830 http://dx.doi.org/10.1105/tpc.113.120527.
132. Zhang Q, Blaylock LA, Harrison MJ. 2010. Two Medicago truncatula half-ABC transporters are essential for arbuscule development in arbuscular mycorrhizal symbiosis. Plant Cell 22:1483–1497 http://dx.doi.org/10.1105/tpc.110.074955.
133. 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 http://dx.doi.org/10.1073/pnas.0608136104.
134. Yang SY, Grønlund M, Jakobsen I, Grotemeyer MS, Rentsch D, Miyao A, Hirochika H, Kumar CS, Sundaresan V, Salamin N, Catausan S, Mattes N, Heuer S, Paszkowski U. 2012. Nonredundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the phosphate transporter1 gene family. Plant Cell 24:4236–4251 http://dx.doi.org/10.1105/tpc.112.104901.
135. Pumplin N, Zhang X, Noar RD, Harrison MJ. 2012. Polar localization of a symbiosis-specific phosphate transporter is mediated by a transient reorientation of secretion. Proc Natl Acad Sci USA 109:E665–E672 http://dx.doi.org/10.1073/pnas.1110215109.
136. Horváth B, Yeun LH, Domonkos A, Halász G, Gobbato E, Ayaydin F, Miró K, Hirsch S, Sun J, Tadege M, Ratet P, Mysore KS, Ané JM, Oldroyd GE, Kaló P. 2011. Medicago truncatula IPD3 is a member of the common symbiotic signaling pathway required for rhizobial and mycorrhizal symbioses. Mol Plant Microbe Interact 24:1345–1358 http://dx.doi.org/10.1094/MPMI-01-11-0015.
137. Floss DS, Levy JG, Lévesque-Tremblay V, Pumplin N, Harrison MJ. 2013. DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 110:E5025–E5034 http://dx.doi.org/10.1073/pnas.1308973110.
138. Takeda N, Handa Y, Tsuzuki S, Kojima M, Sakakibara H, Kawaguchi M. 2015. Gibberellins interfere with symbiosis signaling and gene expression and alter colonization by arbuscular mycorrhizal fungi in Lotus japonicus. Plant Physiol 167:545–557 http://dx.doi.org/10.1104/pp.114.247700.
139. Xue L, Cui H, Buer B, Vijayakumar V, Delaux PM, Junkermann S, Bucher M. 2015. Network of GRAS transcription factors involved in the control of arbuscule development in Lotus japonicus. Plant Physiol 167:854–871 http://dx.doi.org/10.1104/pp.114.255430.
140. Devers EA, Teply J, Reinert A, Gaude N, Krajinski F. 2013. An endogenous artificial microRNA system for unraveling the function of root endosymbioses related genes in Medicago truncatula. BMC Plant Biol 13:82. http://dx.doi.org/10.1186/1471-2229-13-82.
141. Yu N, Luo D, Zhang X, Liu J, Wang W, Jin Y, Dong W, Liu J, Liu H, Yang W, Zeng L, Li Q, He Z, Oldroyd GE, Wang E. 2014. A DELLA protein complex controls the arbuscular mycorrhizal symbiosis in plants. Cell Res 24:130–133 http://dx.doi.org/10.1038/cr.2013.167.
142. Park H-J, Floss DS, Levesque-Tremblay V, Bravo A, Harrison MJ. 2015. Hyphal branching during arbuscule development requires Reduced Arbuscular Mycorrhiza1. Plant Physiol 169:2774–2788.
143. Kobae Y, Hata S. 2010. Dynamics of periarbuscular membranes visualized with a fluorescent phosphate transporter in arbuscular mycorrhizal roots of rice. Plant Cell Physiol 51:341–353 http://dx.doi.org/10.1093/pcp/pcq013.
144. Kloppholz S, Kuhn H, Requena N. 2011. A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr Biol 21:1204–1209 http://dx.doi.org/10.1016/j.cub.2011.06.044.
145. Lo Presti L, Lanver D, Schweizer G, Tanaka S, Liang L, Tollot M, Zuccaro A, Reissmann S, Kahmann R. 2015. Fungal effectors and plant susceptibility. Annu Rev Plant Biol 66:513–545 http://dx.doi.org/10.1146/annurev-arplant-043014-114623.
146. Tsuzuki S, Handa Y, Takeda N, Kawaguchi M. 2016. Strigolactone-induced putative secreted protein 1 is required for the establishment of symbiosis by the arbuscular mycorrhizal fungus Rhizophagus irregularis. Mol Plant Microbe Interact 29:277–286 http://dx.doi.org/10.1094/MPMI-10-15-0234-R.
147. Fiorilli V, Belmondo S, Khouja HR, Abbà S, Faccio A, Daghino S, Lanfranco L. 2016. RiPEIP1, a gene from the arbuscular mycorrhizal fungus Rhizophagus irregularis, is preferentially expressed in planta and may be involved in root colonization. Mycorrhiza 26:609–621 http://dx.doi.org/10.1007/s00572-016-0697-0.
148. 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 JP, 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 Phytol 193:755–769 http://dx.doi.org/10.1111/j.1469-8137.2011.03948.x.
149. Sędzielewska-Toro K, Delaux P-M. 2016. Mycorrhizal symbioses: today and tomorrow. New Phytol 209:917–920 http://dx.doi.org/10.1111/nph.13820.
150. Bapaume L, Reinhardt D. 2012. How membranes shape plant symbioses: signaling and transport in nodulation and arbuscular mycorrhiza. Front Plant Sci 3:223 http://dx.doi.org/10.3389/fpls.2012.00223.
151. Smith SE, Smith FA. 2012. Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth. Mycologia 104:1–13 http://dx.doi.org/10.3852/11-229.
152. Casieri L, Ait Lahmidi N, Doidy J, Veneault-Fourrey C, Migeon A, Bonneau L, Courty PE, Garcia K, Charbonnier M, Delteil A, Brun A, Zimmermann S, Plassard C, Wipf D. 2013. Biotrophic transportome in mutualistic plant-fungal interactions. Mycorrhiza 23:597–625 http://dx.doi.org/10.1007/s00572-013-0496-9.
153. Facelli E, Smith SE, Facelli JM, Christophersen HM, Andrew Smith F. 2010. Underground friends or enemies: model plants help to unravel direct and indirect effects of arbuscular mycorrhizal fungi on plant competition. New Phytol 185:1050–1061 http://dx.doi.org/10.1111/j.1469-8137.2009.03162.x.
154. Harrison MJ, van Buuren ML. 1995. A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378:626–629 http://dx.doi.org/10.1038/378626a0.
155. Maldonado-Mendoza IE, Dewbre GR, Harrison MJ. 2001. A phosphate transporter gene from the extra-radical mycelium of an arbuscular mycorrhizal fungus Glomus intraradices is regulated in response to phosphate in the environment. Mol Plant Microbe Interact 14:1140–1148 http://dx.doi.org/10.1094/MPMI.2001.14.10.1140.
156. Benedetto A, Magurno F, Bonfante P, Lanfranco L. 2005. Expression profiles of a phosphate transporter gene (GmosPT) from the endomycorrhizal fungus Glomus mosseae. Mycorrhiza 15:620–627 http://dx.doi.org/10.1007/s00572-005-0006-9.
157. Ezawa T, Cavagnaro TR, Smith SE, Smith FA, Ohtomo R. 2003. Rapid accumulation of polyphosphate in extraradical hyphae of an arbuscular mycorrhizal fungus as revealed by histochemistry and a polyphosphate kinase/luciferase system. New Phytol 161:387–392 http://dx.doi.org/10.1046/j.1469-8137.2003.00966.x.
158. Mensah JA, Koch AM, Antunes PM, Kiers ET, Hart M, Bücking H. 2015. High functional diversity within species of arbuscular mycorrhizal fungi is associated with differences in phosphate and nitrogen uptake and fungal phosphate metabolism. Mycorrhiza 25:533–546 http://dx.doi.org/10.1007/s00572-015-0631-x.
159. Hijikata N, Murase M, Tani C, Ohtomo R, Osaki M, Ezawa T. 2010. Polyphosphate has a central role in the rapid and massive accumulation of phosphorus in extraradical mycelium of an arbuscular mycorrhizal fungus. New Phytol 186:285–289 http://dx.doi.org/10.1111/j.1469-8137.2009.03168.x.
160. 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 Phytol 204:638–649 http://dx.doi.org/10.1111/nph.12937.
161. Kikuchi Y, Hijikata N, Ohtomo R, Handa Y, Kawaguchi M, Saito K, Masuta C, Ezawa T. 2016. Aquaporin-mediated long-distance polyphosphate translocation directed towards the host in arbuscular mycorrhizal symbiosis: application of virus-induced gene silencing. New Phytol http://dx.doi.org/10.1111/nph.14016.
162. Ezawa T, Smith SE, Smith FA. 2001. Differentiation of polyphosphate metabolism between the extra- and intraradical hyphae of arbuscular mycorrhizal fungi. New Phytol 149:555–563.
163. Liu H, Trieu AT, Blaylock LA, Harrison MJ. 1998. Cloning and characterization of two phosphate transporters from Medicago truncatula roots: regulation in response to phosphate and to colonization by arbuscular mycorrhizal (AM) fungi. Mol Plant Microbe Interact 11:14–22 http://dx.doi.org/10.1094/MPMI.1998.11.1.14.
164. Harrison MJ, Dewbre GR, Liu J. 2002. A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14:2413–2429 http://dx.doi.org/10.1105/tpc.004861.
165. Volpe V, Giovannetti M, Sun X-G, Fiorilli V, Bonfante P. 2016. The phosphate transporters LjPT4 and MtPT4 mediate early root responses to phosphate status in non mycorrhizal roots. Plant Cell Environ 39:660–671 http://dx.doi.org/10.1111/pce.12659.
166. Bücking H, Kafle A. 2015. Role of arbuscular mycorrhizal fungi in the nitrogen uptake of plants: current knowledge and research gaps. Agronomy 5:587–612 http://dx.doi.org/10.3390/agronomy5040587.
167. Lanfranco L, Guether M, Bonfante P. 2011. Arbuscular mycorrhizas and N acquisition by plants, p 52–68. In Polacco, JC, Todd CD (ed), Ecological Aspects of Nitrogen Metabolism in Plants. Wiley, Chichester, United Kingdom.
168. Mader P, Vierheilig H, Streitwolf-Engel R, Boller T, Frey B, Christie P, Wiemken A. 2000. Transport of 15N from a soil compartment separated by a polytetrafluoro-ethylene membrane to plant roots via the hyphae of arbuscular mycorrhizal fungi. New Phytol 146:155–161 http://dx.doi.org/10.1046/j.1469-8137.2000.00615.x.
169. López-Pedrosa A, González-Guerrero M, Valderas A, Azcón-Aguilar C, Ferrol N. 2006. GintAMT1 encodes a functional high-affinity ammonium transporter that is expressed in the extraradical mycelium of Glomus intraradices. Fungal Genet Biol 43:102–110 http://dx.doi.org/10.1016/j.fgb.2005.10.005.
170. Pérez-Tienda J, Testillano PS, Balestrini R, Fiorilli V, Azcón-Aguilar C, Ferrol N. 2011. GintAMT2, a new member of the ammonium transporter family in the arbuscular mycorrhizal fungus Glomus intraradices. Fungal Genet Biol 48:1044–1055 http://dx.doi.org/10.1016/j.fgb.2011.08.003.
171. Cruz C, Egsgaard H, Trujillo C, Ambus P, Requena N, Martins-Loução MA, Jakobsen I. 2007. Enzymatic evidence for the key role of arginine in nitrogen translocation by arbuscular mycorrhizal fungi. Plant Physiol 144:782–792 http://dx.doi.org/10.1104/pp.106.090522.
172. Jin H, Pfeffer PE, Douds DD, Piotrowski E, Lammers PJ, Shachar-Hill Y. 2005. The uptake, metabolism, transport and transfer of nitrogen in an arbuscular mycorrhizal symbiosis. New Phytol 168:687–696 http://dx.doi.org/10.1111/j.1469-8137.2005.01536.x.
173. Govindarajulu M, Pfeffer PE, Jin H, Abubaker J, Douds DD, Allen JW, Bücking H, Lammers PJ, Shachar-Hill Y. 2005. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819–823 http://dx.doi.org/10.1038/nature03610.
174. Willis A, Rodrigues BF, Harris PJC. 2013. The ecology of arbuscular mycorrhizal fungi. Crit Rev Plant Sci 32:1–20 http://dx.doi.org/10.1080/07352689.2012.683375.
175. 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 arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 109:2666–2671 http://dx.doi.org/10.1073/pnas.1118650109.
176. Guether M, Neuhäuser 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 http://dx.doi.org/10.1104/pp.109.136390.
177. Kobae Y, Tamura Y, Takai S, Banba M, Hata S. 2010. Localized expression of arbuscular mycorrhiza-inducible ammonium transporters in soybean. Plant Cell Physiol 51:1411–1415 http://dx.doi.org/10.1093/pcp/pcq099.
178. Koegel S, Ait Lahmidi N, Arnould C, Chatagnier O, Walder F, Ineichen K, Boller T, Wipf D, Wiemken A, Courty PE. 2013. The family of ammonium transporters (AMT) in Sorghum bicolor: two AMT members are induced locally, but not systemically in roots colonized by arbuscular mycorrhizal fungi. New Phytol 198:853–865 http://dx.doi.org/10.1111/nph.12199.
179. 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 68:954–965 http://dx.doi.org/10.1111/j.1365-313X.2011.04746.x.
180. 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 27:1352–1366 http://dx.doi.org/10.1105/tpc.114.131144.
181. Balestrini R, Gómez-Ariza J, Lanfranco L, Bonfante P. 2007. Laser microdissection reveals that transcripts for five plant and one fungal phosphate transporter genes are contemporaneously present in arbusculated cells. Mol Plant Microbe Interact 20:1055–1062 http://dx.doi.org/10.1094/MPMI-20-9-1055.
182. Fiorilli V, Lanfranco L, Bonfante P. 2013. The expression of GintPT, the phosphate transporter of Rhizophagus irregularis, depends on the symbiotic status and phosphate availability. Planta 237:1267–1277 http://dx.doi.org/10.1007/s00425-013-1842-z.
183. Hodge A, Campbell CD, Fitter AH. 2001. An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413:297–299 http://dx.doi.org/10.1038/35095041.
184. Leigh J, Hodge A, Fitter AH. 2009. Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytol 181:199–207 http://dx.doi.org/10.1111/j.1469-8137.2008.02630.x.
185. Hodge A, Fitter AH. 2010. Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proc Natl Acad Sci USA 107:13754–13759 http://dx.doi.org/10.1073/pnas.1005874107.
186. Whiteside MD, Digman MA, Gratton E, Treseder KK. 2012. Organic nitrogen uptake by arbuscular mycorrhizal fungi in a boreal forest. Soil Biol Biochem 55:7–13 http://dx.doi.org/10.1016/j.soilbio.2012.06.001.
187. Cappellazzo G, Lanfranco L, Fitz M, Wipf D, Bonfante P. 2008. Characterization of an amino acid permease from the endomycorrhizal fungus Glomus mosseae. Plant Physiol 147:429–437 http://dx.doi.org/10.1104/pp.108.117820.
188. Belmondo S, Fiorilli V, Pérez-Tienda J, Ferrol N, Marmeisse R, Lanfranco L. 2014. A dipeptide transporter from the arbuscular mycorrhizal fungus Rhizophagus irregularis is upregulated in the intraradical phase. Front Plant Sci 5:436 http://dx.doi.org/10.3389/fpls.2014.00436.
189. Casieri L, Gallardo K, Wipf D. 2012. Transcriptional response of Medicago truncatula sulphate transporters to arbuscular mycorrhizal symbiosis with and without sulphur stress. Planta 235:1431–1447 http://dx.doi.org/10.1007/s00425-012-1645-7.
190. Giovannetti M, Tolosano M, Volpe V, Kopriva S, Bonfante P. 2014. Identification and functional characterization of a sulfate transporter induced by both sulfur starvation and mycorrhiza formation in Lotus japonicus. New Phytol 204:609–619 http://dx.doi.org/10.1111/nph.12949.
191. Garcia K, Zimmermann SD. 2014. The role of mycorrhizal associations in plant potassium nutrition. Front Plant Sci 5:337 http://dx.doi.org/10.3389/fpls.2014.00337.
192. Drigo B, Pijl AS, Duyts H, Kielak AM, Gamper HA, Houtekamer MJ, Boschker HT, Bodelier PL, Whiteley AS, van Veen JA, Kowalchuk GA. 2010. Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2. Proc Natl Acad Sci USA 107:10938–10942 http://dx.doi.org/10.1073/pnas.0912421107.
193. 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 http://dx.doi.org/10.1105/tpc.111.089813.
194. 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 http://dx.doi.org/10.1111/j.1574-6941.2011.01043.x.
195. Walder F, van der Heijden MG. 2015. Regulation of resource exchange in the arbuscular mycorrhizal symbiosis. Nat Plants 1:15159. http://dx.doi.org/10.1038/nplants.2015.159.
196. 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 http://dx.doi.org/10.1111/j.1365-313X.2007.03069.x.
197. de Wit PJGM, Testa AC, Oliver RP. 2016. Fungal plant pathogenesis mediated by effectors. Microbiol Spectrum 4(6):FUNK-0021-2016. http://dx.doi.org/10.1128/microbiolspec.FUNK-0021-2016.
198. Fiorilli V, Catoni M, Miozzi L, Novero M, Accotto GP, Lanfranco L. 2009. Global and cell-type gene expression profiles in tomato plants colonized by an arbuscular mycorrhizal fungus. New Phytol 184:975–987 http://dx.doi.org/10.1111/j.1469-8137.2009.03031.x.
199. Cervantes-Gámez RG, Bueno-Ibarra MA, Cruz-Mendívil A, Calderón-Vázquez CL, Ramírez-Douriet CM, Maldonado-Mendoza IE, Villalobos-López MÁ, Valdez-Ortíz Á, López-Meyer M. 2016. Arbuscular mycorrhizal symbiosis-induced expression changes in Solanum lycopersicum leaves revealed by RNA-seq analysis. Plant Mol Biol Report 34:89–102 http://dx.doi.org/10.1007/s11105-015-0903-9.
200. 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 http://dx.doi.org/10.1111/pce.12508.
201. Giovannetti M, Avio L, Barale R, Ceccarelli N, Cristofani R, Iezzi A, Mignolli F, Picciarelli P, Pinto B, Reali D, Sbrana C, Scarpato R. 2012. Nutraceutical value and safety of tomato fruits produced by mycorrhizal plants. Br J Nutr 107:242–251 http://dx.doi.org/10.1017/S000711451100290X.
202. Hart M, Ehret DL, Krumbein A, Leung C, Murch S, Turi C, Franken P. 2015. Inoculation with arbuscular mycorrhizal fungi improves the nutritional value of tomatoes. Mycorrhiza 25:359–376 http://dx.doi.org/10.1007/s00572-014-0617-0.
203. Salvioli A, Zouari I, Chalot M, Bonfante P. 2012. The arbuscular mycorrhizal status has an impact on the transcriptome profile and amino acid composition of tomato fruit. BMC Plant Biol 12:44. http://dx.doi.org/10.1186/1471-2229-12-44.
204. Zouari I, Salvioli A, Chialva M, Novero M, Miozzi L, Tenore GC, Bagnaresi P, Bonfante P. 2014. From root to fruit: RNA-Seq analysis shows that arbuscular mycorrhizal symbiosis may affect tomato fruit metabolism.BMC Genomics 15:221. http://dx.doi.org/10.1186/1471-2164-15-221.
205. Foo E, Ross JJ, Jones WT, Reid JB. 2013. Plant hormones in arbuscular mycorrhizal symbioses: an emerging role for gibberellins. Ann Bot (Lond) 111:769–779 http://dx.doi.org/10.1093/aob/mct041.
206. Gutjahr C. 2014. Phytohormone signaling in arbuscular mycorhiza development. Curr Opin Plant Biol 20:26–34 http://dx.doi.org/10.1016/j.pbi.2014.04.003. [CrossRef]
207. Pozo MJ, López-Ráez JA, Azcón-Aguilar C, García-Garrido JM. 2015. Phytohormones as integrators of environmental signals in the regulation of mycorrhizal symbioses. New Phytol 205:1431–1436 http://dx.doi.org/10.1111/nph.13252.
208. Hause B, Mrosk C, Isayenkov S, Strack D. 2007. Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry 68:101–110 http://dx.doi.org/10.1016/j.phytochem.2006.09.025.
209. López-Ráez JA, Verhage A, Fernández I, García JM, Azcón-Aguilar C, Flors V, Pozo MJ. 2010. Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. J Exp Bot 61:2589–2601 http://dx.doi.org/10.1093/jxb/erq089.
210. Ludwig-Müller J. 2010. Hormonal responses in host plants triggered by arbuscular mycorrhizal fungi, p 169–190. In Kaltai H, Kapulnik Y (ed), Arbuscular Mycorrhizas: Physiology and Function. Springer Verlag, Heidelberg, Germany. http://dx.doi.org/10.1007/978-90-481-9489-6_8
211. Miozzi L, Catoni M, Fiorilli V, Mullineaux PM, Accotto GP, Lanfranco L. 2011. Arbuscular mycorrhizal symbiosis limits foliar transcriptional responses to viral infection and favors long-term virus accumulation. Mol Plant Microbe Interact 24:1562–1572 http://dx.doi.org/10.1094/MPMI-05-11-0116.
212. Martín-Rodríguez JA, Ocampo JA, Molinero-Rosales N, Tarkowská D, Ruíz-Rivero O, García-Garrido JM. 2015. Role of gibberellins during arbuscular mycorrhizal formation in tomato: new insights revealed by endogenous quantification and genetic analysis of their metabolism in mycorrhizal roots. Physiol Plant 154:66–81 http://dx.doi.org/10.1111/ppl.12274.
213. Martín-Rodríguez JÁ, León-Morcillo R, Vierheilig H, Ocampo JA, Ludwig-Müller J, García-Garrido JM. 2011. Ethylene-dependent/ethylene-independent ABA regulation of tomato plants colonized by arbuscular mycorrhiza fungi. New Phytol 190:193–205 http://dx.doi.org/10.1111/j.1469-8137.2010.03610.x.
214. Etemadi M, Gutjahr C, Couzigou J-M, Zouine M, Lauressergues D, Timmers A, Audran C, Bouzayen M, Bécard G, Combier J-P. 2014. Auxin perception is required for arbuscule development in arbuscular mycorrhizal symbiosis. Plant Physiol 166:281–292 http://dx.doi.org/10.1104/pp.114.246595.
215. Wasternack C, Hause B. 2013. Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann Bot (Lond) 111:1021–1058 http://dx.doi.org/10.1093/aob/mct067.
216. Singh LP, Gill SS, Tuteja N. 2011. Unraveling the role of fungal symbionts in plant abiotic stress tolerance. Plant Signal Behav 6:175–191 http://dx.doi.org/10.4161/psb.6.2.14146.
217. Azcón R, Medina A, Aroca R, Ruiz-Lozano JM. 2013. Abiotic stress remediation by the arbuscular mycorrhizal symbiosis and rhizosphere bacteria/yeast interactions, p 991–1002. In de Bruijn FJ (ed), Molecular Microbial Ecology of the Rhizosphere. John Wiley and Sons, Hoboken, NJ. http://dx.doi.org/10.1002/9781118297674.ch93
218. Pozo MJ, Jung SC, Lòpez-Ràez J, Azcón-Aguilar C. 2010. Impact of arbuscular mycorrhizal symbiosis on plant response to biotic stress: the role of plant defence mechanisms, p 193–207. In Koltai H, Kapulnik Y (ed), Arbuscular Mycorrhizas: Physiology and Function, 2nd ed. Springer Verlag, Heidelberg, Germany. http://dx.doi.org/10.1007/978-90-481-9489-6_9
219. Pozo MJ, Cordier C, Dumas-Gaudot E, Gianinazzi S, Barea JM, Azcón-Aguilar C. 2002. Localized versus systemic effect of arbuscular mycorrhizal fungi on defence responses to Phytophthora infection in tomato plants. J Exp Bot 53:525–534 http://dx.doi.org/10.1093/jexbot/53.368.525.
220. Whipps JM. 2004. Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Can J Bot 82:1198–1227 http://dx.doi.org/10.1139/b04-082.
221. Ismail Y, Hijri M. 2012. Arbuscular mycorrhization with Glomus irregularis induces expression of potato PR homologues genes in response to infection by Fusarium sambucinum. Funct Plant Biol 39:236–245 http://dx.doi.org/10.1071/FP11218.
222. Campos-Soriano L, García-Martínez J, San Segundo B. 2012. The arbuscular mycorrhizal symbiosis promotes the systemic induction of regulatory defence-related genes in rice leaves and confers resistance to pathogen infection. Mol Plant Pathol 13:579–592 http://dx.doi.org/10.1111/j.1364-3703.2011.00773.x.
223. Vos C, Schouteden N, van Tuinen D, Chatagnier O, Elsen A, De Waele D, Panis B, Gianinazzi-Pearson V. 2013. Mycorrhiza-induced resistance against the rootknot nematode Meloidogyne incognita involves priming of defense gene responses in tomato. Soil Biol Biochem 60:45–54 http://dx.doi.org/10.1016/j.soilbio.2013.01.013.
224. Simard SW, Beiler KJ, Bingham MA, Deslippe JR, Philip LJ, Teste FP. 2012. Mycorrhizal networks: mechanisms, ecology and modelling. Fungal Biol Rev 26:39–60 http://dx.doi.org/10.1016/j.fbr.2012.01.001.
225. Voets L, Goubau I, Olsson PA, Merckx R, Declerck S. 2008. Absence of carbon transfer between Medicago truncatula plants linked by a mycorrhizal network, demonstrated in an experimental microcosm. FEMS Microbiol Ecol 65:350–360 http://dx.doi.org/10.1111/j.1574-6941.2008.00503.x.
226. Selosse M-A, Roy M. 2009. Green plants that feed on fungi: facts and questions about mixotrophy. Trends Plant Sci 14:64–70 http://dx.doi.org/10.1016/j.tplants.2008.11.004.
227. Jalonen R, Nygren P, Sierra J. 2009. Transfer of nitrogen from a tropical legume tree to an associated fodder grass via root exudation and common mycelial networks. Plant Cell Environ 32:1366–1376 http://dx.doi.org/10.1111/j.1365-3040.2009.02004.x.
228. Lekberg Y, Hammer EC, Olsson PA. 2010. Plants as resource islands and storage units: adopting the mycocentric view of arbuscular mycorrhizal networks. FEMS Microbiol Ecol 74:336–345 http://dx.doi.org/10.1111/j.1574-6941.2010.00956.x.
229. Zabinski CA, Quinn L, Callaway RM. 2002. Phosphorus uptake, not carbon transfer, explains arbuscular mycorrhizal enhancement of Centaurea maculosa in the presence of native grassland species. Funct Ecol 16:758–765 http://dx.doi.org/10.1046/j.1365-2435.2002.00676.x.
230. van der Heijden MGA, Wiemken A, Sanders IR. 2003. Different arbuscular mycorrhizal fungi alter coexistence and resource distribution between co-occurring plant. New Phytol 157:569–578 http://dx.doi.org/10.1046/j.1469-8137.2003.00688.x.
231. Wagg C, Jansa J, Stadler M, Schmid B, van der Heijden MGA. 2011. Mycorrhizal fungal identity and diversity relaxes plant-plant competition. Ecology 92:1303–1313 http://dx.doi.org/10.1890/10-1915.1.
232. 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 http://dx.doi.org/10.1104/pp.112.195727.
233. Wang ZG, Jin X, Bao XG, Li XF, Zhao JH, Sun JH, Christie P, Li L. 2014. Intercropping enhances productivity and maintains the most soil fertility properties relative to sole cropping. PLoS One 9:e113984. http://dx.doi.org/10.1371/journal.pone.0113984.
234. Song YY, Zeng RS, Xu JF, Li J, Shen X, Yihdego WG. 2010. Interplant communication of tomato plants through underground common mycorrhizal networks. PLoS One 5:e13324. http://dx.doi.org/10.1371/journal.pone.0013324.
235. Babikova Z, Gilbert L, Bruce TJA, Birkett M, Caulfield JC, Woodcock C, Pickett JA, Johnson D. 2013. Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack. Ecol Lett 16:835–843 http://dx.doi.org/10.1111/ele.12115.
236. Song YY, Ye M, Li C, He X, Zhu-Salzman K, Wang RL, Su YJ, Luo SM, Zeng RS. 2014. Hijacking common mycorrhizal networks for herbivore-induced defence signal transfer between tomato plants. Sci Rep 4:3915 http://dx.doi.org/10.1038/srep03915.
237. Johnson D, Gilbert L. 2015. Interplant signalling through hyphal networks. New Phytol 205:1448–1453 http://dx.doi.org/10.1111/nph.13115. [CrossRef]

Citations loading...


Article metrics loading...



Mycorrhizal fungi belong to several taxa and develop mutualistic symbiotic associations with over 90% of all plant species, from liverworts to angiosperms. While descriptive approaches have dominated the initial studies of these fascinating symbioses, the advent of molecular biology, live cell imaging, and “omics” techniques have provided new and powerful tools to decipher the cellular and molecular mechanisms that rule mutualistic plant-fungus interactions. In this article we focus on the most common mycorrhizal association, arbuscular mycorrhiza (AM), which is formed by a group of soil fungi belonging to Glomeromycota. AM fungi are believed to have assisted the conquest of dry lands by early plants around 450 million years ago and are found today in most land ecosystems. AM fungi have several peculiar biological traits, including obligate biotrophy, intracellular development inside the plant tissues, coenocytic multinucleate hyphae, and spores, as well as unique genetics, such as the putative absence of a sexual cycle, and multiple ecological functions. All of these features make the study of AM fungi as intriguing as it is challenging, and their symbiotic association with most crop plants is currently raising a broad interest in agronomic contexts for the potential use of AM fungi in sustainable production under conditions of low chemical input.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of FIGURE 1

Root colonization in ectomycorrhizal (blue) and arbuscular mycorrhizal (pink) interactions. Ectomycorrhizal fungi envelop root tips with a thick mycelial mantle. From this mantle, intercellular hyphae generate the so-called Hartig net around epidermal cells. In the case of arbuscular mycorrhizae, the root tip is usually not colonized; hyphae developed from a germinated spore produce a hyphopodium on the root epidermis. Intraradical colonization proceeds both inter- and intracellularly, culminating with the development of highly branched arbuscules inside inner cortical cells. Reprinted from ( 3 ) with permission of the publisher.

Source: microbiolspec November 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.FUNK-0012-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2

Fluorescence micrographs of different stages in the life cycle of the AM fungus . A spore (S) and the germination hyphae (GH) show strong cytoplasmic autofluorescence. Hyphopodia (arrows) on the surface of a host root give rise to single infection units with several arbuscules (A) in the inner root cortex. A high magnification from a root longitudinal section showing two arbuscules in adjacent cortical cells. Bars = 100 μm (a–c), 25 μm (d); fungal fluorescence was excited with 380–405 nm UV light.

Source: microbiolspec November 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.FUNK-0012-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3

Root colonization by AM fungi. Spore germination generates a short explorative mycelium. The perception of root exudates induces repeated hyphal branching, increasing the probability of direct contact between the symbionts. Concurrently, fungal exudates are also released and activate the common symbiotic signaling pathway in root cells. Signal transduction includes nuclear-associated calcium signals (spiking) and leads to the activation of cellular and transcriptional responses (green cells and nuclei). Plant-fungus contact is followed by the formation of an adhering hyphopodium on the root surface. The contacted epidermal cell then assembles a prepenetration apparatus (PPA), a broad cytoplasmic aggregation (yellow) responsible for the exocytotic biogenesis of the symbiotic interface compartment, where the intracellular hypha is hosted. Root colonization proceeds through the epidermis into the inner cortical cells with a PPA-like process. Intercellular hyphae can also develop along the root axis. Eventually, highly branched arbuscules develop in the lumen of inner cortical cells, deploying an extensive surface for nutrient exchange. Reprinted from ( 3 ) with permission of the publisher.

Source: microbiolspec November 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.FUNK-0012-2016
Permissions and Reprints Request Permissions
Download as Powerpoint

Supplemental Material

No supplementary material available for this content.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error