1887

Chapter 35 : 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.

Preview this chapter:
Zoom in
Zoomout

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

| /docserver/preview/fulltext/10.1128/9781555819583/9781555819576_Chap35-1.gif /docserver/preview/fulltext/10.1128/9781555819583/9781555819576_Chap35-2.gif

Abstract:

Mycorrhizal fungi are a heterogeneous group of diverse taxa associated with the roots of over 90% of all plant species, from liverworts to angiosperms. Although they can spend part of their life cycle in the rhizosphere, mycorrhizal fungi always associate with the roots of plants, including forest trees, wild grasses, and many crops, and colonize environments such as alpine and boreal zones, tropical forests, grasslands, and croplands. Both partners benefit from the relationship: mycorrhizal fungi improve the fitness of their host plants by influencing mineral nutrition and water absorption and by increasing tolerance to biotic and abiotic stresses. The host plant rewards the fungal symbiont with carbon compounds derived from the photosynthetic process ( ).

Citation: Lanfranco L, Bonfante P, Genre A. 2017. The Mutualistic Interaction between Plants and Arbuscular Mycorrhizal Fungi, p 727-747. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0012-2016
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of Figure 1
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 ( ) with permission of the publisher.

Citation: Lanfranco L, Bonfante P, Genre A. 2017. The Mutualistic Interaction between Plants and Arbuscular Mycorrhizal Fungi, p 727-747. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0012-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
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.

Citation: Lanfranco L, Bonfante P, Genre A. 2017. The Mutualistic Interaction between Plants and Arbuscular Mycorrhizal Fungi, p 727-747. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0012-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3
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 ( ) with permission of the publisher.

Citation: Lanfranco L, Bonfante P, Genre A. 2017. The Mutualistic Interaction between Plants and Arbuscular Mycorrhizal Fungi, p 727-747. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0012-2016
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555819583.chap35
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.[CrossRef]
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 : 14061423.[CrossRef]
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 : 519530.[CrossRef]
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.[CrossRef]
7. Miller RM,, Reinhardt DR,, Jastrow JD . 1995. External hyphal production of vesicular-arbuscular mycorrhizal fungi in pasture and tallgrass prairie communities. Oecologia 103 : 1723.[CrossRef]
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 : 227250.[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 : 11151126.[CrossRef]
10. Bonfante P, . 1984. Anatomy and morphology of VA mycorrhizae, p 533. 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 : 593617.[CrossRef]
12. Lanfranco L,, Young JPW . 2012. Genetic and genomic glimpses of the elusive arbuscular mycorrhizal fungi. Curr Opin Plant Biol 15 : 454461.[CrossRef]
13. Bago B,, Pfeffer PE,, Shachar-Hill Y . 2000. Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol 124 : 949958.[CrossRef]
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 : 880882.[CrossRef]
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 : 13851388.[CrossRef]
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 : 6972.[CrossRef]
17. Pozo MJ,, Azcón-Aguilar C . 2007. Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10 : 393398.[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 : 651664.[CrossRef]
19. Porcel R,, Aroca R,, Ruiz-Lozano JM . 2011. Salinity stress alleviation using arbuscular mycorrhizal fungi. Agron Sustainable Dev 32 : 181200.[CrossRef]
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 : 1324.[CrossRef]
21. Redecker D,, Kodner R,, Graham LE . 2000. Glomalean fungi from the Ordovician. Science 289 : 19201921.[CrossRef]
22. Remy W,, Taylor TN,, Hass H,, Kerp H . 1994. Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci USA 91 : 1184111843.[CrossRef]
23. Janse JM . 1896. Les endophytes radicaux de quelques plantes Javanese. Ann Jardin Bot Buitenzorg 15 : 53212.
24. Gallaud I . 1905. Études sur les mycorrhizes endotrophes. Rev Générale Bot 17 : 548, 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 : 5563.
26. Schüßler A,, Schwarzott D,, Walker C . 2001. A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105 : 14131421.[CrossRef]
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 : 411430.[CrossRef]
28. Davison J,, Moora M,, Öpik M,, Adholeya A,, Ainsaar L,, 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 : 970973.[CrossRef]
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 : 970984.[CrossRef]
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 : 200211.[CrossRef]
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 : 836845.[CrossRef]
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 : 21992210.[CrossRef]
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 : 950958.[CrossRef]
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 : 2011720122. (Erratum, http://www.pnas.org/content/111/1/562.3.full.)[CrossRef]
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.[CrossRef]
36. Young JPW . 2015. Genome diversity in arbuscular mycorrhizal fungi. Curr Opin Plant Biol 26 : 113119.[CrossRef]
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 : 574577.[CrossRef]
38. Field KJ,, Pressel S,, Duckett JG,, Rimington WR,, Bidartondo MI . 2015. Symbiotic options for the conquest of land. Trends Ecol Evol 30 : 477486.[CrossRef]
39. Hosny M,, Gianinazzi-Pearson V,, Dulieu H . 1998. Nuclear DNA content of 11 fungal species in Glomales. Genome 41 : 422428.[CrossRef]
40. Jany JL,, Pawlowska TE . 2010. Multinucleate spores contribute to evolutionary longevity of asexual glomeromycota. Am Nat 175 : 424435.[CrossRef]
41. Lanfranco L,, Delpero M,, Bonfante P . 1999. Intrasporal variability of ribosomal sequences in the endomycorrhizal fungus Gigaspora margarita . Mol Ecol 8 : 3745.[CrossRef]
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 : 225234.[CrossRef]
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 : 11761187.[CrossRef]
44. Hijri M,, Sanders IR . 2005. Low gene copy number shows that arbuscular mycorrhizal fungi inherit genetically different nuclei. Nature 433 : 160163.[CrossRef]
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 : 31793186.[CrossRef]
46. Ropars J,, Corradi N . 2015. Homokaryotic vs heterokaryotic mycelium in arbuscular mycorrhizal fungi: different techniques, different results? New Phytol 208 : 638641.[CrossRef]
47. Pawlowska TE,, Taylor JW . 2004. Organization of genetic variation in individuals of arbuscular mycorrhizal fungi. Nature 427 : 733737.[CrossRef]
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 : 717724.[CrossRef]
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 : 175181.[CrossRef]
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 : 924937.[CrossRef]
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 : 616624.[CrossRef]
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 : 257270.[CrossRef]
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 : 136145.[CrossRef]
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 : 77857790. (Erratum, http://www.pnas.org/content/112/38/E5376.full.)[CrossRef]
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 : 77917796.[CrossRef]
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 : 130144.[CrossRef]
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 : 265275.[CrossRef]
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 : 10051012.[CrossRef]
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 : 21572160.[CrossRef]
60. Martin F,, Tuskan GA,, DiFazio SP,, Lammers P,, Newcombe G,, Podila GK . 2004. Symbiotic sequencing for the Populus mesocosm. New Phytol 161 : 330335.[CrossRef]
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 : 15431546.
62. Martin F , , et al . 2010. Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464 : 10331038.[CrossRef]
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.[CrossRef]
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 : 34893499.[CrossRef]
65. Harrison MJ . 2012. Cellular programs for arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 15 : 691698.[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 : 14071420.[CrossRef]
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 : 514525.[CrossRef]
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 : 1339013395.[CrossRef]
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 : 693698.[CrossRef]
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 : 10791088.[CrossRef]
71. Al-Babili S,, Bouwmeester HJ . 2015. Strigolactones, a novel carotenoid-derived plant hormone. Annu Rev Plant Biol 66 : 161186.[CrossRef]
72. Ruyter-Spira C,, Al-Babili S,, van der Krol S,, Bouwmeester H . 2013. The biology of strigolactones. Trends Plant Sci 18 : 7283.[CrossRef]
73. Akiyama K,, Matsuzaki K,, Hayashi H . 2005. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435 : 824827.[CrossRef]
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.[CrossRef]
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 : 402413.[CrossRef]
76. Akiyama K,, Ogasawara S,, Ito S,, Hayashi H . 2010. Structural requirements of strigolactones for hyphal branching in AM fungi. Plant Cell Physiol 51 : 11041117.[CrossRef]
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 : 10121020.[CrossRef]
78. Bonfante P,, Genre A . 2015. Arbuscular mycorrhizal dialogues: do you speak ‘plantish’ or ‘fungish’? Trends Plant Sci 20 : 150154.[CrossRef]
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 : 451457.[CrossRef]
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 : 952962.[CrossRef]
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 : 195207.[CrossRef]
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 : 716733.[CrossRef]
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 : 347355.[CrossRef]
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 : 260270.[CrossRef]
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 : 5863.[CrossRef]
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 : 190202.[CrossRef]
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 : 265273.[CrossRef]
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 : 16711685.[CrossRef]
89. Oldroyd GED . 2013. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11 : 252263.[CrossRef]
90. Gobbato E . 2015. Recent developments in arbuscular mycorrhizal signaling. Curr Opin Plant Biol 26 : 17.[CrossRef]
91. Genre A,, Russo G . 2016. Does a common pathway transduce symbiotic signals in plant-microbe interactions? Front Plant Sci 7 : 96.[CrossRef]
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 : 823838.[CrossRef]
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 : 97819786. (Erratum, http://www.pnas.org/content/112/38/E5378.full.)[CrossRef]
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 : 359364.[CrossRef]
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 : 610624.[CrossRef]
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 : 25092526.[CrossRef]
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 : 208216.[CrossRef]
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 : 1434814353.[CrossRef]
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 : 13641367.[CrossRef]
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 : 527531.[CrossRef]
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 : 25282545.[CrossRef]
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 : 48974901.[CrossRef]
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 : 81268132.[CrossRef]
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 : 13611364.[CrossRef]
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 : 47014705.[CrossRef]
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 : 883894.[CrossRef]
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 : 912921.[CrossRef]
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 : 2054020545.[CrossRef]
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 : 17861789.[CrossRef]
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 : 17891791.[CrossRef]
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 : 17391750.[CrossRef]
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 : 255265.[CrossRef]
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 : 324335.[CrossRef]
114. Schauser L,, Roussis A,, Stiller J,, Stougaard J . 1999. A plant regulator controlling development of symbiotic root nodules. Nature 402 : 191195.[CrossRef]
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 : 22362241.[CrossRef]
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 : 587593.[CrossRef]
117. Nagahashi G,, Douds DD Jr . 1997. Appressorium formation by AM fungi on isolated cell walls of carrot roots. New Phytol 136 : 299304.[CrossRef]
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 : 22422246.[CrossRef]
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 : 15211524.[CrossRef]
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 : 244255.[CrossRef]
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 : 810822.[CrossRef]
122. Bonfante P, . 2001. At the interface between mycorrhizal fungi and plants: the structural organization of cell wall, plasma membrane and cytoskeleton, p 4561. In Hock B (ed), The Mycota, IX: Fungal Associations. Springer, Berlin, Germany.[CrossRef]
123. Balestrini R,, Bonfante P . 2014. Cell wall remodeling in mycorrhizal symbiosis: a way towards biotrophism. Front Plant Sci 5 : 237.[CrossRef]
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 : 809819.[CrossRef]
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 : 482494.[CrossRef]
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 : 83168321.[CrossRef]
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 : 21892195.[CrossRef]
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 : 766777.[CrossRef]
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 : 711725.[CrossRef]
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 : 18081817.[CrossRef]
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 : 18181830.[CrossRef]
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 : 14831497.[CrossRef]
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 : 17201725.[CrossRef]
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 : 42364251.[CrossRef]
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 : E665E672.[CrossRef]
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 : 13451358.[CrossRef]
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 : E5025E5034.[CrossRef]
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 : 545557.[CrossRef]
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 : 854871.[CrossRef]
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.[CrossRef]
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 : 130133.[CrossRef]
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 : 27742788.
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 : 341353.[CrossRef]
144. Kloppholz S,, Kuhn H,, Requena N . 2011. A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr Biol 21 : 12041209.[CrossRef]
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 : 513545.[CrossRef]
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 : 277286.[CrossRef]
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 : 609621.[CrossRef]
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 : 755769.[CrossRef]
149. Sędzielewska-Toro K,, Delaux P-M . 2016. Mycorrhizal symbioses: today and tomorrow. New Phytol 209 : 917920.[CrossRef]
150. Bapaume L,, Reinhardt D . 2012. How membranes shape plant symbioses: signaling and transport in nodulation and arbuscular mycorrhiza. Front Plant Sci 3 : 223.[CrossRef]
151. Smith SE,, Smith FA . 2012. Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth. Mycologia 104 : 113.[CrossRef]
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 : 597625.[CrossRef]
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 : 10501061.[CrossRef]
154. Harrison MJ,, van Buuren ML . 1995. A phosphate transporter from the mycorrhizal fungus Glomus versiforme . Nature 378 : 626629.[CrossRef]
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 : 11401148.[CrossRef]
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 : 620627.[CrossRef]
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 : 387392.[CrossRef]
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 : 533546.[CrossRef]
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 : 285289.[CrossRef]
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 : 638649.[CrossRef]
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.[CrossRef]
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 : 555563.
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 : 1422.[CrossRef]
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 : 24132429.[CrossRef]
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 : 660671.[CrossRef]
166. Bücking H,, Kafle A . 2015. Role of arbuscular mycorrhizal fungi in the nitrogen uptake of plants: current knowledge and research gaps. Agronomy 5 : 587612.[CrossRef]
167. Lanfranco L,, Guether M,, Bonfante P, . 2011. Arbuscular mycorrhizas and N acquisition by plants, p 5268. In Polacco JC,, Todd CD (ed), Ecological Aspects of Nitrogen Metabolism in Plants. Wiley, Chichester, United Kingdom.