for intracellular progression of arbuscular mycorrhizal symbiosis, is also essential for infection by
rhizobia in the nodule symbiosis of Medicago
truncatula. Plant J 65(2):244–252
Nadal M, Sawers R, Naseem S, Bassin B, Kulicke C,
Sharman A, An G, An K, Ahern KR, Romag A,
Brutnell TP, Gutjahr C, Geldner N, Roux C, Martinoia E, Konopka JB, Paszkowski U (2017) An Nacetylglucosamine transporter required for arbuscular mycorrhizal symbioses in rice and maize.
Nat Plants 26:17073
Nagahashi G, Douds DD (2011) The effects of hydroxy
fatty acids on the hyphal branching of germinated
spores of AM fungi. Fungal Biol 115(4–5):351–358
Nagahashi G, Douds DD Jr (1997) Appressorium formation by AM fungi on isolated cell walls of carrot
roots. New Phytol 136:299–304
Nagata M, Yamamoto N, Shigeyama T, Terasawa Y,
Anai T, Sakai T, Inada S, Arima S, Hashiguchi M,
Akashi R, Nakayama H, Ueno D, Hirsch AM,
Suzuki A (2015) Red/far red light controls arbuscular mycorrhizal colonization via jasmonic acid
and strigolactone signaling. Plant Cell Physiol
56:2100–2109
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 U S A 112:7791–7796
Navazio L, Moscatiello R, Genre A, Novero M, Baldan B,
Bonfante P, Mariani P (2007) A diffusible signal
from arbuscular mycorrhizal fungi elicits a transient cytosolic calcium elevation in host plant cells.
Plant Physiol 144:673–681
Nelson DC, Flematti GR, Riseborough JA, Ghisalberti
EL, Dixon KW, Smith SM (2010) Karrikins
enhance light responses during germination and
seedling development in Arabidopsis thaliana.
Proc Natl Acad Sci U S A 107:7095–7100
Ola ´h B, Brie `re C, Be ´card G, De ´narie ´ 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
Oldroyd GED (2013) Speak, friend, and enter: signalling
systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11(4):252–263
Oldroyd GED, Downie JA (2006) Nuclear calcium
changes at the core of symbiosis signalling. Curr
Opin Plant Biol 9:351–357
Op Den Camp R, Streng A, De Mita S, Cao Q, Polone E,
Liu W, Ammiraju JS, Kudrna D, Wing R, Untergasser A, Bisseling T, Geurts R (2011) LysM-type
mycorrhizal receptor recruited for rhizobium
symbiosis in non legume Parasponia. Science
331:909–912
Orchard S, Hilton S, Bending GD, Dickie IA, Standish
RJ, Gleeson RD, Jeffery P, Powell JR, Walker C,
Bass D, Monk J, Simonin A, Ryan MH (2017) Fine
endophytes (Glomus tenue) are related to Mucoromycotina not Glomeromycota. New Phytol
213:481–486
Pan HR, Oztas O, Zhang XW, Wu XY, Stonoha C, Wang
E, Wang B, Wang D (2016) A symbiotic SNARE
protein generated by alternative termination of
transcription. Nat Plants 2:15197
Pandey P, Wang M, Baldwin IT, Pandey SP, Groten K
(2018) Complex regulation of microRNAs in roots
of competitively-grown isogenic Nicotiana attenuata plants with different capacities to interact with
arbuscular mycorrhizal fungi. BMC Genomics 19
(1):937
Park H-J, Floss DS, Levesque-Tremblay V, Bravo A,
Harrison MJ (2015) Hyphal branching during
arbuscule development requires RAM1. Plant
Physiol 169:2774–2788
Parniske M (2004) Molecular genetics of the arbuscular
mycorrhizal symbiosis. Curr Opin Plant Biol
7:414–421
Parniske M (2008) Arbuscular mycorrhiza: the mother
of plant root endosymbioses. Nat Rev Microbiol 6
(10):763–775
Pellegrin C, Morin E, Martin FM, Veneault-Fourrey C
(2015) Comparative analysis of secretomes from
ectomycorrhizal fungi with an emphasis on smallsecreted proteins. Front Microbiol 6:1278
Pfeffer PE, Douds DD, Be ´card G, Shachar-Hill Y (1999)
Carbon uptake and the metabolism and transport
of lipids in an arbuscular mycorrhiza. Plant
Physiol 120:587–598
Pimprikar P, Gutjahr C (2018) Transcriptional regulation of arbuscular mycorrhiza development. Plant
Cell Physiol 59:673–690
Pimprikar P, Carbonnel S, Paries M, Katzer K, Klingl V,
Bohmer MJ, Karl L, Floss DS, Harrison MJ, Parniske M, Gutjahr C (2016) A CCaMK-CYCLOPSDELLA complex activates transcription of RAM1
to regulate arbuscule branching. Curr Biol
26:987–998
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
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
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
Ramirez-Flores MR, Rellan-Alvarez R, Wozniak B, Gebreselassie MN, Jakobsen I, Olalde-Portugal V, Baxter I, Paszkowski U, RJH S (2017) Coordinated
changes in the accumulation of metal ions in
maize (Zea mays ssp. mays L.) in response to
168
L. Lanfranco et al.
rhizobia in the nodule symbiosis of Medicago
truncatula. Plant J 65(2):244–252
Nadal M, Sawers R, Naseem S, Bassin B, Kulicke C,
Sharman A, An G, An K, Ahern KR, Romag A,
Brutnell TP, Gutjahr C, Geldner N, Roux C, Martinoia E, Konopka JB, Paszkowski U (2017) An Nacetylglucosamine transporter required for arbuscular mycorrhizal symbioses in rice and maize.
Nat Plants 26:17073
Nagahashi G, Douds DD (2011) The effects of hydroxy
fatty acids on the hyphal branching of germinated
spores of AM fungi. Fungal Biol 115(4–5):351–358
Nagahashi G, Douds DD Jr (1997) Appressorium formation by AM fungi on isolated cell walls of carrot
roots. New Phytol 136:299–304
Nagata M, Yamamoto N, Shigeyama T, Terasawa Y,
Anai T, Sakai T, Inada S, Arima S, Hashiguchi M,
Akashi R, Nakayama H, Ueno D, Hirsch AM,
Suzuki A (2015) Red/far red light controls arbuscular mycorrhizal colonization via jasmonic acid
and strigolactone signaling. Plant Cell Physiol
56:2100–2109
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 U S A 112:7791–7796
Navazio L, Moscatiello R, Genre A, Novero M, Baldan B,
Bonfante P, Mariani P (2007) A diffusible signal
from arbuscular mycorrhizal fungi elicits a transient cytosolic calcium elevation in host plant cells.
Plant Physiol 144:673–681
Nelson DC, Flematti GR, Riseborough JA, Ghisalberti
EL, Dixon KW, Smith SM (2010) Karrikins
enhance light responses during germination and
seedling development in Arabidopsis thaliana.
Proc Natl Acad Sci U S A 107:7095–7100
Ola ´h B, Brie `re C, Be ´card G, De ´narie ´ 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
Oldroyd GED (2013) Speak, friend, and enter: signalling
systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11(4):252–263
Oldroyd GED, Downie JA (2006) Nuclear calcium
changes at the core of symbiosis signalling. Curr
Opin Plant Biol 9:351–357
Op Den Camp R, Streng A, De Mita S, Cao Q, Polone E,
Liu W, Ammiraju JS, Kudrna D, Wing R, Untergasser A, Bisseling T, Geurts R (2011) LysM-type
mycorrhizal receptor recruited for rhizobium
symbiosis in non legume Parasponia. Science
331:909–912
Orchard S, Hilton S, Bending GD, Dickie IA, Standish
RJ, Gleeson RD, Jeffery P, Powell JR, Walker C,
Bass D, Monk J, Simonin A, Ryan MH (2017) Fine
endophytes (Glomus tenue) are related to Mucoromycotina not Glomeromycota. New Phytol
213:481–486
Pan HR, Oztas O, Zhang XW, Wu XY, Stonoha C, Wang
E, Wang B, Wang D (2016) A symbiotic SNARE
protein generated by alternative termination of
transcription. Nat Plants 2:15197
Pandey P, Wang M, Baldwin IT, Pandey SP, Groten K
(2018) Complex regulation of microRNAs in roots
of competitively-grown isogenic Nicotiana attenuata plants with different capacities to interact with
arbuscular mycorrhizal fungi. BMC Genomics 19
(1):937
Park H-J, Floss DS, Levesque-Tremblay V, Bravo A,
Harrison MJ (2015) Hyphal branching during
arbuscule development requires RAM1. Plant
Physiol 169:2774–2788
Parniske M (2004) Molecular genetics of the arbuscular
mycorrhizal symbiosis. Curr Opin Plant Biol
7:414–421
Parniske M (2008) Arbuscular mycorrhiza: the mother
of plant root endosymbioses. Nat Rev Microbiol 6
(10):763–775
Pellegrin C, Morin E, Martin FM, Veneault-Fourrey C
(2015) Comparative analysis of secretomes from
ectomycorrhizal fungi with an emphasis on smallsecreted proteins. Front Microbiol 6:1278
Pfeffer PE, Douds DD, Be ´card G, Shachar-Hill Y (1999)
Carbon uptake and the metabolism and transport
of lipids in an arbuscular mycorrhiza. Plant
Physiol 120:587–598
Pimprikar P, Gutjahr C (2018) Transcriptional regulation of arbuscular mycorrhiza development. Plant
Cell Physiol 59:673–690
Pimprikar P, Carbonnel S, Paries M, Katzer K, Klingl V,
Bohmer MJ, Karl L, Floss DS, Harrison MJ, Parniske M, Gutjahr C (2016) A CCaMK-CYCLOPSDELLA complex activates transcription of RAM1
to regulate arbuscule branching. Curr Biol
26:987–998
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
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
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
Ramirez-Flores MR, Rellan-Alvarez R, Wozniak B, Gebreselassie MN, Jakobsen I, Olalde-Portugal V, Baxter I, Paszkowski U, RJH S (2017) Coordinated
changes in the accumulation of metal ions in
maize (Zea mays ssp. mays L.) in response to
168
L. Lanfranco et al.