pathogenesis: the give-and- take in plant-bacteria
interactions. Cell Microbiol 11(3):381–388
Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith
ME, Berbee ML, Bonito G, Corradi N, Grigoriev I,
Gryganskyi A, James TY, O’Donnell K, Roberson
RW, Taylor TN, Uehling J, Vilgalys R, White MM,
Stajich JE (2016) A phylum-level phylogenetic
classification of zygomycete fungi based on
genome-scale data. Mycologia 108:1028–1046
Steinkellner S, Hage-Ahmed K, Garcia-Garrido JM, Illana A, Ocampo JA, Vierheilig H (2012) A comparison of wild-type, old and modern tomato cultivars
in the interaction with the arbuscular mycorrhizal
fungus Glomus mosseae and the tomato pathogen
Fusarium oxysporum f. sp. lycopersici. Mycorrhiza
22:189–194
Sun J, Miller JB, Granqvist E, Wiley-Kalil A, Gobbato E,
Maillet F, Cottaz S, Samain E, Venkateshwaran M,
Fort S, Morris RJ, Ane ´ JM, De ´narie ´ J, Oldroyd GED
(2015) Activation of symbiosis signaling by arbuscular mycorrhizal fungi in legumes and rice. Plant
Cell 27:823–838
Sun X, Chen W, Ivanov S, MacLean AM, Wight H,
Ramaraj T, Mudge J, Harrison MJ, Fei Z (2018)
Genome and evolution of the arbuscular mycorrhizal fungus Diversispora epigaea (formerly Glomus versiforme) and its bacterial endosymbionts.
New Phytol 221(3):1556–1573. https://doi.org/
10.1111/NPH.15472
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
Tamayo E, Go ´mez-Gallego T, Azco ´n-Aguilar C, Ferrol
N (2014) Genome-wide analysis of copper, iron
and zinc transporters in the arbuscular mycorrhizal fungus Rhizophagus irregularis. Front Plant Sci
5:547
Tanaka Y, Yano K (2005) Nitrogen delivery to maize via
mycorrhizal hyphae depends on the form of N
supplied. Plant Cell Environ 28:1247–1254
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, Azco ´nAguilar C, Be ´card G, Bonfante P, Harrison MJ,
Ku ¨ster 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(3):755–769
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, Be ´card 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 U S A 110(50):20117–20122
Torres-Corte ´s G, Ghignone S, Bonfante P, Schu ¨ßler A
(2015) Mosaic genome of endobacteria in arbuscular mycorrhizal fungi: transkingdom gene transfer in an ancient mycoplasma–fungus association.
Proc Natl Acad Sci U S A 112:7785–7790
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
Turina M, Ghignone S, Astolfi N, Silvestri A, Bonfante
P, Lanfranco L (2018) The virome of the arbuscular mycorrhizal fungus Gigaspora margarita
reveals the first report of DNA fragments
corresponding to replicating nonretroviral RNA
viruses in fungi. Environ Microbiol 20(6):2012–
2025. https://doi.org/10.1111/1462-2920.14060
Turrini A, Sbrana C, Avio L, Mugendi Njeru E, Bocci G,
Ba `rberi P, Giovannetti M (2016) Changes in the
composition of native root arbuscular mycorrhizal
fungal communities during a short-term cover
crop-maize succession. Biol Fertil Soils 52:643–653
Turrini A, Avio L, Giovannetti M, Agnolucci M (2018)
Functional complementarity of arbuscular mycorrhizal fungi and associated microbiota: the challenge of translational research. Front Plant Sci
9:1407
Uehling J, Gryganskyi A, Hameed K, Tschaplinski T,
Misztal PK, Wu S, Desiro ` A, Vande Pol N, Du Z,
Zienkiewicz A, Zienkiewicz K, Morin E, Tisserant
E, Splivallo R, Hainaut M, Henrissat B, Ohm R,
Kuo A, Yan J, Lipzen A, Nolan M, LaButti K, Barry
K, Goldstein AH, Labbe ´ J, Schadt C, Tuskan G,
Grigoriev I, Martin F, Vilgalys R, Bonito G (2017)
Comparative genomics of Mortierella elongata
and its bacterial endosymbiont Mycoavidus cysteinexigens. Environ Microbiol 19(8):2964–2983
Van Buuren ML, Maldonado-Mendoza IE, Trieu AT,
Blaylock LA, Harrison MJ (1999) Novel genes
induced during an arbuscular mycorrhizal (AM)
symbiosis formed between Medicago truncatula
and Glomus versiforme. Mol Plant-Microbe Interact 12(3):171–181
Venkateshwaran M, Cosme A, Han L, Banba M, Satyshur KA, Schleiff E, Parniske M, Imaizumi-Anraku
H, Ane ´ JM (2012) The recent evolution of a symbiotic ion channel in the legume family altered ion
170
L. Lanfranco et al.
interactions. Cell Microbiol 11(3):381–388
Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith
ME, Berbee ML, Bonito G, Corradi N, Grigoriev I,
Gryganskyi A, James TY, O’Donnell K, Roberson
RW, Taylor TN, Uehling J, Vilgalys R, White MM,
Stajich JE (2016) A phylum-level phylogenetic
classification of zygomycete fungi based on
genome-scale data. Mycologia 108:1028–1046
Steinkellner S, Hage-Ahmed K, Garcia-Garrido JM, Illana A, Ocampo JA, Vierheilig H (2012) A comparison of wild-type, old and modern tomato cultivars
in the interaction with the arbuscular mycorrhizal
fungus Glomus mosseae and the tomato pathogen
Fusarium oxysporum f. sp. lycopersici. Mycorrhiza
22:189–194
Sun J, Miller JB, Granqvist E, Wiley-Kalil A, Gobbato E,
Maillet F, Cottaz S, Samain E, Venkateshwaran M,
Fort S, Morris RJ, Ane ´ JM, De ´narie ´ J, Oldroyd GED
(2015) Activation of symbiosis signaling by arbuscular mycorrhizal fungi in legumes and rice. Plant
Cell 27:823–838
Sun X, Chen W, Ivanov S, MacLean AM, Wight H,
Ramaraj T, Mudge J, Harrison MJ, Fei Z (2018)
Genome and evolution of the arbuscular mycorrhizal fungus Diversispora epigaea (formerly Glomus versiforme) and its bacterial endosymbionts.
New Phytol 221(3):1556–1573. https://doi.org/
10.1111/NPH.15472
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
Tamayo E, Go ´mez-Gallego T, Azco ´n-Aguilar C, Ferrol
N (2014) Genome-wide analysis of copper, iron
and zinc transporters in the arbuscular mycorrhizal fungus Rhizophagus irregularis. Front Plant Sci
5:547
Tanaka Y, Yano K (2005) Nitrogen delivery to maize via
mycorrhizal hyphae depends on the form of N
supplied. Plant Cell Environ 28:1247–1254
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, Azco ´nAguilar C, Be ´card G, Bonfante P, Harrison MJ,
Ku ¨ster 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(3):755–769
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, Be ´card 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 U S A 110(50):20117–20122
Torres-Corte ´s G, Ghignone S, Bonfante P, Schu ¨ßler A
(2015) Mosaic genome of endobacteria in arbuscular mycorrhizal fungi: transkingdom gene transfer in an ancient mycoplasma–fungus association.
Proc Natl Acad Sci U S A 112:7785–7790
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
Turina M, Ghignone S, Astolfi N, Silvestri A, Bonfante
P, Lanfranco L (2018) The virome of the arbuscular mycorrhizal fungus Gigaspora margarita
reveals the first report of DNA fragments
corresponding to replicating nonretroviral RNA
viruses in fungi. Environ Microbiol 20(6):2012–
2025. https://doi.org/10.1111/1462-2920.14060
Turrini A, Sbrana C, Avio L, Mugendi Njeru E, Bocci G,
Ba `rberi P, Giovannetti M (2016) Changes in the
composition of native root arbuscular mycorrhizal
fungal communities during a short-term cover
crop-maize succession. Biol Fertil Soils 52:643–653
Turrini A, Avio L, Giovannetti M, Agnolucci M (2018)
Functional complementarity of arbuscular mycorrhizal fungi and associated microbiota: the challenge of translational research. Front Plant Sci
9:1407
Uehling J, Gryganskyi A, Hameed K, Tschaplinski T,
Misztal PK, Wu S, Desiro ` A, Vande Pol N, Du Z,
Zienkiewicz A, Zienkiewicz K, Morin E, Tisserant
E, Splivallo R, Hainaut M, Henrissat B, Ohm R,
Kuo A, Yan J, Lipzen A, Nolan M, LaButti K, Barry
K, Goldstein AH, Labbe ´ J, Schadt C, Tuskan G,
Grigoriev I, Martin F, Vilgalys R, Bonito G (2017)
Comparative genomics of Mortierella elongata
and its bacterial endosymbiont Mycoavidus cysteinexigens. Environ Microbiol 19(8):2964–2983
Van Buuren ML, Maldonado-Mendoza IE, Trieu AT,
Blaylock LA, Harrison MJ (1999) Novel genes
induced during an arbuscular mycorrhizal (AM)
symbiosis formed between Medicago truncatula
and Glomus versiforme. Mol Plant-Microbe Interact 12(3):171–181
Venkateshwaran M, Cosme A, Han L, Banba M, Satyshur KA, Schleiff E, Parniske M, Imaizumi-Anraku
H, Ane ´ JM (2012) The recent evolution of a symbiotic ion channel in the legume family altered ion
170
L. Lanfranco et al.