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Transcription factors network in root endosymbiosis establishment and development


Root endosymbioses are mutualistic interactions between plants and the soil microorganisms (Fungus, Frankia or Rhizobium) that lead to the formation of nitrogen-fixing root nodules and/or arbuscular mycorrhiza. These interactions enable many species to survive in different marginal lands to overcome the nitrogen-and/or phosphorus deficient environment and can potentially reduce the chemical fertilizers used in agriculture which gives them an economic, social and environmental importance. The formation and the development of these structures require the mediation of specific gene products among which the transcription factors play a key role. Three of these transcription factors, viz., CYCLOPS, NSP1 and NSP2 are well conserved between actinorhizal, legume, non-legume and mycorrhizal symbioses. They interact with DELLA proteins to induce the expression of NIN in nitrogen fixing symbiosis or RAM1 in mycorrhizal symbiosis. Recently, the small non coding RNA including micro RNAs (miRNAs) have emerged as major regulators of root endosymbioses. Among them, miRNA171 targets NSP2, a TF conserved in actinorhizal, legume, non-legume and mycorrhizal symbioses. This review will also focus on the recent advances carried out on the biological function of others transcription factors during the root pre-infection/pre-contact, infection or colonization. Their role in nodule formation and AM development will also be described.

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Root nodule symbiosis


Arbuscular mycorhizal symbiosis


Transcription factor


  1. Akiyama K, Hayashi H (2006) Strigolactones: chemical signals for fungal symbionts and parasitic weeds in plant roots. Ann Bot 97:925–931. https://doi.org/10.1093/aob/mcl063

  2. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827. https://doi.org/10.1038/nature03608

  3. 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. https://doi.org/10.1093/pcp/pcq058

  4. Alder A, Jamil M, Marzorati M et al (2012) The path from β-carotene to carlactone, a strigolactone-like plant hormone. Science 335:1348–1351

  5. Alloisio N, Queiroux C, Fournier P et al (2010) The Frankia alni symbiotic transcriptome. Mol Plant-Microbe Interact MPMI 23:593–607. https://doi.org/10.1094/MPMI-23-5-0593

  6. Andriankaja A, Boisson-Dernier A, Frances L et al (2007) AP2-ERF transcription factors mediate Nod factor dependent Mt ENOD11 activation in root hairs via a novel cis-regulatory motif. Plant Cell 19:2866–2885. https://doi.org/10.1105/tpc.107.052944

  7. Ariel F, Brault-Hernandez M, Laffont C et al (2012) Two direct targets of cytokinin signaling regulate symbiotic nodulation in Medicago truncatula. Plant Cell. 24:3838–3852. https://doi.org/10.1105/tpc.112.103267

  8. Ariel F, Romero-Barrios N, Jégu T, Benhamed M, Crespi M (2015) Battles and hijacks: noncoding transcription in plants. Trends Plant Sci 20:362–371

  9. Asamizu E, Shimoda Y, Kouchi H et al (2008) A positive regulatory role for LjERF1 in the nodulation process is revealed by systematic analysis of nodule-associated transcription factors of Lotus japonicus. Plant Physiol 147:2030–2040. https://doi.org/10.1104/pp.108.118141

  10. Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15:2730–2741

  11. Baluška F, Parker JS, Barlow PW (1993) A role for gibberellicacid in orienting microtubules and regulating cell-growth polarity in the maize root cortex. Planta 191:149–157. https://doi.org/10.1007/BF00199744

  12. Barker SJ, Tagu D (2000) The roles of auxins and cytokinins in mycorrhizal symbioses. J Plant Growth Regul 19:144–154

  13. Bassa C, Mila I, Bouzayen M, Audran-Delalande C (2012) Phenotypes associated with down-regulation of Sl-IAA27 support functional diversity among Aux/IAA family members in tomato. Plant Cell Physiol 53:1583–1595

  14. Bassa C, Etemadi M, Combier J-P et al (2013) Sl-IAA27 gene expression is induced during arbuscular mycorrhizal symbiosis in tomato and in Medicago truncatula. Plant Signal Behav 8:e25637

  15. Battaglia M, Rípodas C, Clúa J et al (2014) A nuclear factor Y interacting protein of the GRAS family Is required for nodule organogenesis, infection thread progression, and lateral root growth. Plant Physiol 164:1430–1442. https://doi.org/10.1104/pp.113.230896

  16. Baudin M, Laloum T, Lepage A et al (2015) A phylogenetically conserved group of nuclear factor-Y Transcription factors interact to control nodulation in legumes. Plant Physiol 169:2761–2773. https://doi.org/10.1104/pp.15.01144

  17. Bazin J, Bustos-Sanmamed P, Hartmann C, Lelandais-Brière C, Crespi M (2017) Complexity of miRNA-dependent regulation in root symbiosis. Phil Trans R Soc B 367:1570–1579. https://doi.org/10.1098/rstb.2011.0228

  18. Besserer A, Bécard G, Jauneau A et al (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

  19. Beveridge CA, Kyozuka J (2010) New genes in the strigolactone-related shoot branching pathway. Curr Opin Plant Biol 13:34–39. https://doi.org/10.1016/j.pbi.2009.10.003

  20. Boualem A, Laporte P, Jovanovic M et al (2008) MicroRNA166 controls root and nodule development in Medicago truncatula. Plant J 54:876–887. https://doi.org/10.1111/j.1365-313X.2008.03448.x

  21. Breakspear A, Liu C, Roy S et al (2014) The root hair “infectome” of Medicago truncatula uncovers changes in cell cycle genes and reveals a requirement for auxin signaling in rhizobial infection. Plant Cell 26:4680–4701

  22. Bustos-Sanmamed P, Mao G, Deng Y et al (2013) miR160 overexpression affects root growth and nitrogen-fixing nodule number in Medicago truncatula. Funct Plant Biol 40:1208–1220

  23. Carretero-Paulet L, Galstyan A, Roig-Villanova I et al (2010) Genome-wide classification and evolutionary analysis of the bHLH family of transcription factors in Arabidopsis, poplar, rice, moss, and algae. Plant Physiol 153:1398–1412

  24. Catoira R, Galera C, de Billy F et al (2000) Four genes of Medicago truncatula controlling components of a nod factor transduction pathway. Plant Cell 12:1647–1666

  25. Cerri MR, Frances L, Laloum T et al (2012) Medicago truncatula ERN transcription factors: regulatory interplay with NSP1/NSP2 GRAS factors and expression dynamics throughout rhizobial infection. Plant Physiol 160:2155–2172. https://doi.org/10.1104/pp.112.203190

  26. Cerri MR, Frances L, Kelner A, Fournier J, Middleton PH et al (2016) The symbiosis-related ERN transcription factors act in concert to coordinate rhizobial host root infection. Plant Physiol 171:1037–1054. https://doi.org/10.1104/pp.16.00230

  27. Chabaud M, Gherbi H, Pirolles E et al (2016) Chitinase-resistant hydrophilic symbiotic factors secreted by Frankia activate both Ca2+ spiking and NIN gene expression in the actinorhizal plant Casuarina glauca. New Phytol 209:86–93. https://doi.org/10.1111/nph.13732

  28. Champion A, Lucas M, Tromas A et al (2015) Inhibition of auxin signaling in Frankia-infected cells in Casuarina glauca nodules leads to increased nodulation. Plant Physiol 114. https://doi.org/10.1104/pp.114.255307

  29. Chekanova JA (2015) Long non-coding RNAs and their functions in plants. Curr Opin Plant Biol 27:207–216

  30. Chiasson DM, Loughlin PC, Mazurkiewicz D et al (2014) Soybean SAT1 (symbiotic ammonium transporter 1) encodes a bHLH transcription factor involved in nodule growth and NH4+ transport. Proc Natl Acad Sci 111:4814–4819

  31. Clavijo F, Diédhiou I, Vaissayre V et al (2015) The Casuarina NIN gene is transcriptionally activated throughout Frankia root infection as well as in response to bacterial diffusible signals. New Phytol. https://doi.org/10.1111/nph.13506

  32. Couzigou JM, Combier JP (2016) Plant microRNAs: key regulators of root architecture and biotic interactions. New Phytol 212:22–35. https://doi.org/10.1111/nph.14058

  33. Czaja LF, Hogekamp C, Lamm P et al (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. https://doi.org/10.1104/pp.112.195990

  34. De Luis A, Markmann K, Cognat V et al (2012) Two microRNAs linked to nodule infection and nitrogen-fixing ability in the legume Lotus japonicus. Plant Physiol 160:2137–2154

  35. Delaux P-M, Bécard G, Combier J-P (2013) NSP1 is a component of the Myc signaling pathway. New Phytol 199:59–65. https://doi.org/10.1111/nph.12340

  36. Demina IV, Persson T, Santos P et al (2013) Comparison of the nodule vs. root transcriptome of the actinorhizal plant Datisca glomerata: actinorhizal nodules contain a specific class of defensins. PLoS ONE 8:e72442. https://doi.org/10.1371/journal.pone.0072442

  37. Dénarié J, Debellé F, Promé J-C (1996) Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu Rev Biochem 65:503–535

  38. Devers EA, Teply J, Reinert A et al (2013) An endogenous artificial microRNA system for unraveling the function of root endosymbioses related genes in Medicago truncatula. BMC Plant Biol 13:82. https://doi.org/10.1186/1471-2229-13-82

  39. Diédhiou I, Tromas A, Cissoko M et al (2014) Identification of potential transcriptional regulators of actinorhizal symbioses in Casuarina glauca and Alnus glutinosa. BMC Plant Biol 14:342

  40. Ei-D AMSE., Salama A, Wareing PF (1979) Effects of mineralnutrition on endogenous cytokinins in plants of sunflower (Helianthus annuus L.). J Exp Bot 30:971–981

  41. Etemadi M, Gutjahr C, Couzigou J-M et al (2014) Auxin perception is required for arbuscule development in arbuscular mycorrhizal symbiosis. Plant Physiol 166:281–292

  42. Feddermann N, Reinhardt D (2011) Conserved residues in the ankyrin domain of VAPYRIN indicate potential protein-protein interaction surfaces. Plant Signal Behav 6:680–684

  43. Floss DS, Levy JG, Lévesque-Tremblay V et al (2013) DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci 110:E5025–E5034. https://doi.org/10.1073/pnas.1308973110

  44. Foo E, Ross JJ, Jones WT, Reid JB (2013) Plant hormones in arbuscular mycorrhizal symbioses: an emerging role for gibberellins. Ann Bot 111:769–779. https://doi.org/10.1093/aob/mct041

  45. Fournier J, Timmers AC, Sieberer BJ et al (2008) Mechanism of infection thread elongation in root hairs of Medicago truncatula and dynamic interplay with associated rhizobial colonization. Plant Physiol 148:1985–1995

  46. Frugier F, Poirier S, Satiat-Jeunemaître B et al (2000) A Krüppel-like zinc finger protein is involved in nitrogen-fixing root nodule organogenesis. Genes Dev 14:475–482

  47. Gaude N, Schulze WX, Franken P, Krajinski F (2012) Cell type-specific protein and transcription profiles implicate periarbuscular membrane synthesis as an important carbon sink in the mycorrhizal symbiosis. Plant Signal Behav 7:461–464. https://doi.org/10.4161/psb.19650

  48. Genre A, Russo G (2016) Does a Common pathway transduce symbiotic signals in plant-microbe interactions? Plant Biot Interact. https://doi.org/10.3389/fpls.2016.00096

  49. Genre A, Chabaud M, Timmers T et al (2005) Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17:3489–3499

  50. Genre A, Chabaud M, Faccio A et al (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. https://doi.org/10.1105/tpc.108.059014

  51. Ghodhbane-Gtari F, Beauchemin N, Bruce D et al (2013) Draft genome sequence of Frankia sp. strain CN3, an atypical, noninfective (Nod-) ineffective (Fix-) isolate from Coriaria nepalensis. Genome Announc 1:e00085-13

  52. Gobbato E (2015) Recent developments in arbuscular mycorrhizal signaling. Curr Opin Plant Biol 26:1–7. https://doi.org/10.1016/j.pbi.2015.05.006

  53. Gobbato E, Marsh JF, Vernié T et al (2012) A GRAS-Type transcription factor with a specific function in mycorrhizal signaling. Curr Biol 22:2236–2241. https://doi.org/10.1016/j.cub.2012.09.044

  54. Gobbato E, Wang E, Higgins G et al (2013) RAM1 and RAM2 function and expression during Arbuscular Mycorrhizal Symbiosis and Aphanomyces euteiches colonization. Plant Signal Behav 8:10e26049

  55. Godiard L, Lepage A, Moreau S et al (2011) MtbHLH1, a bHLH transcription factor involved in Medicago truncatula nodule vascular patterning and nodule to plant metabolic exchanges. New Phytol 191:391–404

  56. Gomez-Roldan V, Fermas S, Brewer PB et al (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194

  57. Gough C, Cullimore J (2011) Lipo-chitooligosaccharide signaling in endosymbiotic plant-microbe interactions. Mol Plant Microbe Interact 24:867–878. https://doi.org/10.1094/MPMI-01-11-0019

  58. Granqvist E, Sun J, Op den Camp R et al (2015) Bacterial-induced calcium oscillations are common to nitrogen-fixing associations of nodulating legumes and nonlegumes. New Phytol, 207:551–558

  59. Gutjahr C (2014) Phytohormone signaling in arbuscular mycorhiza development. Curr Opin Plant Biol 20:26–34

  60. Gutjahr C, Parniske M (2013) Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annu Rev Cell Dev Biol 29:593–617. https://doi.org/10.1146/annurev-cellbio-101512-122413

  61. Gutjahr C, Radovanovic D, Geoffroy J et al (2012) The half-size ABC transporters STR1 and STR2 are indispensable for mycorrhizal arbuscule formation in rice. Plant J 69:906–920

  62. 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

  63. Heck C, Kuhn H, Heidt S, Walter S, Rieger N, Requena N (2016) Symbiotic fungi control plant root cortex development through the novel GRAS transcription factor MIG1. Curr Biol 26:2770–2778

  64. Hirsch S, Oldroyd GE (2009) GRAS-domain transcription factors that regulate plant development. Plant Signal Behav 4:698–700

  65. Hirsch S, Kim J, Muñoz A et al (2009) GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell 21:545–557

  66. Hocher V, Alloisio N, Auguy F et al (2011) Transcriptomics of actinorhizal symbioses reveals homologs of the whole common symbiotic signaling cascade. Plant Physiol 156:700–711. https://doi.org/10.1104/pp.111.174151

  67. Hofferek V, Mendrinna A, Gaude N et al (2014) MiR171h restricts root symbioses and shows like its target NSP2 a complex transcriptional regulation in Medicago truncatula. BMC Plant Biol 14:199

  68. Hogekamp C, Küster H (2013) A roadmap of cell-type specific gene expression during sequential stages of the arbuscular mycorrhiza symbiosis. BMC Genom 14:306. https://doi.org/10.1186/1471-2164-14-306

  69. Hogekamp C, Arndt D, Pereira PA et al (2011) Laser microdissection unravels cell-type-specific transcription in arbuscular mycorrhizal roots, including CAAT-box transcription factor gene expression correlating with fungal contact and spread. Plant Physiol 157:2023–2043. https://doi.org/10.1104/pp.111.186635

  70. Holt DB, Gupta V, Meyer D et al (2015) micro RNA 172 (miR172) signals epidermal infection and is expressed in cells primed for bacterial invasion in Lotus japonicus roots and nodules. New Phytol 208:241–256

  71. Huijser P, Schmid M (2011) The control of developmental phase transitions in plants. Development 138:4117–4129

  72. Javot H, Pumplin N, Harrison MJ (2007) Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant Cell Environ 30:310–322

  73. Jones KM, Kobayashi H, Davies BW et al (2007) How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nat Rev Microbiol 5:619–633. https://doi.org/10.1038/nrmicro1705

  74. Kaló P, Gleason C, Edwards A et al (2005) Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 308:1786–1789. https://doi.org/10.1126/science.1110951

  75. Kang H, Chu X, Wang C et al (2014) A MYB coiled-coil transcription factor interacts with NSP2 and is involved in nodulation in Lotus japonicus. New Phytol 201:837–849. https://doi.org/10.1111/nph.12593

  76. Khan GA, Declerck M, Sorin C et al (2011) MicroRNAs as regulators of root development and architecture. Plant Mol Biol 77:47–58

  77. Kistner C, Parniske M (2002) Evolution of signal transduction in intracellular symbiosis. Trends Plant Sci 7:511–518

  78. Koltai H (2011) Strigolactones are regulators of root development. New Phytol 190:545–549

  79. Koltai H, LekKala SP, Bhattacharya C et al (2010) A tomato strigolactone-impaired mutant displays aberrant shoot morphology and plant interactions. J Exp Bot 61(6):1739–1749. https://doi.org/10.1093/jxb/erq041

  80. Kosuta S, Chabaud M, Lougnon G et al (2003) A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiol 131:952–962

  81. Kretzschmar T, Kohlen W, Sasse J et al (2012) A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature 483:341–344

  82. Laloum T, Baudin M, Frances L et al (2014) Two CCAAT-box-binding transcription factors redundantly regulate early steps of the legume-rhizobia endosymbiosis. Plant J 79:757–768. https://doi.org/10.1111/tpj.12587

  83. Laplaze L, Lucas M, Champion A (2015) Rhizobial root hair infection requires auxin signaling. Trends Plant Sci 20:332–334

  84. Laporte P, Lepage A, Fournier J et al (2013) The CCAAT box-binding transcription factor NF-YA1 controls rhizobial infection. J Exp Bot. https://doi.org/10.1093/jxb/ert392

  85. Laporte P, Lepage A, Fournier J et al (2014) The CCAAT box-binding transcription factor NF-YA1 controls rhizobial infection. J of Exp Bot 65:481–494. https://doi.org/10.1093/jxb/ert392

  86. Lauressergues D, Delaux P-M, Formey D et al (2012) The microRNA miR171h modulates arbuscular mycorrhizal colonization of Medicago truncatula by targeting NSP2. Plant J 72:512–522. https://doi.org/10.1111/j.1365-313X.2012.05099.x

  87. Lelandais-Briére C, Moreau J, Hartmann C et al (2016) Noncoding RNAs, emerging regulators in root endosymbioses. Mol Plant Micro Int 29:170–180. https://doi.org/10.1094/MPMI-10-15-0240-FI

  88. Li H, Sun J, Xu Y et al (2007) The bHLH-type transcription factor AtAIB positively regulates ABA response in Arabidopsis. Plant Mol Biol 65:655–665

  89. Liu J, Blaylock LA, Endre G et al (2003) Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. Plant Cell Online 15:2106–2123. https://doi.org/10.1105/tpc.014183

  90. Liu W, Kohlen W, Lillo A et al (2011) Strigolactone biosynthesis in Medicago truncatula and rice requires the symbiotic GRAS-type transcription factors NSP1 and NSP2. Plant Cell 23:3853–3865

  91. Madsen LH, Tirichine L, Jurkiewicz A et al (2010) The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat Commun 1:10. https://doi.org/10.1038/ncomms1009

  92. Maillet F, Poinsot V, André O et al (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469:58–63. https://doi.org/10.1038/nature09622

  93. Mao G, Turner M, Yu O, Subramanian S (2013) miR393 and miR164 influence indeterminate but not determinate nodule development. Plant Signal Behav 8:e26753

  94. Marsh JF, Rakocevic A, Mitra RM et al (2007) Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase. Plant Physiol 144:324–335. https://doi.org/10.1104/pp.106.093021

  95. Mazziotta L, Reynoso MA, Aguilar OM et al (2013) Transcriptional and functional variation of NF-YC1 in genetically diverse accessions of Phaseolus vulgaris during the symbiotic association with Rhizobium etli. Plant Biol 15:808–818

  96. Middleton PH, Jakab J, Penmetsa RV et al (2007) An ERF transcription factor in Medicago truncatula that is essential for Nod factor signal transduction. Plant Cell 19:1221–1234. https://doi.org/10.1105/tpc.106.048264

  97. Murray JD, Muni RRD, Torres-Jerez I et al (2011) Vapyrin, a gene essential for intracellular progression of arbuscular mycorrhizal symbiosis, is also essential for infection by rhizobia in the nodule symbiosis of Medicago truncatula. Plant J 65:244–252

  98. Normand P, Lapierre P, Tisa LS et al (2007) Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography. Genome Res 17:7–15. https://doi.org/10.1101/gr.5798407

  99. Nouioui I, Beauchemin N, Cantor MN et al (2013) Draft genome sequence of Frankia sp. strain BMG5. 12, a nitrogen-fixing actinobacterium isolated from Tunisian soils. Genome Announc 1:e00468-13

  100. Nova-Franco B, ĺniguez LP, Valdés-Lopez O et al (2015) The micro-RNA72c-APETALA2-1 node as a key regulator of the common bean-Rhizobium etli nitrogen fixation symbiosis. Plant Physiol 168:273–291

  101. Obertello M, Sy MO, Laplaze L et al (2004) Actinorhizal nitrogen fixing nodules: infection process, molecular biology and genomics. Afr J Biotechnol 2:528–538. https://doi.org/10.4314/ajb.v2i12.14883

  102. Oldroyd GED (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11:252–263. https://doi.org/10.1038/nrmicro2990

  103. Oldroyd GED, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519–546. https://doi.org/10.1146/annurev.arplant.59.032607.092839

  104. Ovchinnikova E, Journet E-P, Chabaud M et al (2011) IPD3 controls the formation of nitrogen-fixing symbiosomes in pea and Medicago Spp. Mol Plant Microbe Interact 24:1333–1344

  105. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775. https://doi.org/10.1038/nrmicro1987

  106. Parry G, Calderon-Villalobos LI, Prigge M et al (2009) Complex regulation of the TIR1/AFB family of auxin receptors. Proc Natl Acad Sci USA 106:22540–22545

  107. Pawlowski K, Sprent JI (2007) Comparison between actinorhizal and legume symbiosis. In: Nitrogen-fixing actinorhizal symbioses. Springer, New York, pp 261–288

  108. Persson T, Battenberg K, Demina IV et al (2014) Candidatus Frankia Datiscae Dg1, the actinobacterial microsymbiont of Datisca glomerata, expresses the canonical nod genes nodABC in symbiosis with its host plant. PLoS ONE 10:e0127630–e0127630

  109. Pimprikar P, Carbonnel S, Paries M et al (2016) A CCaMK-CYCLOPS-DELLA complex activates transcription of RAM1 to regulate arbuscule branching. Curr Biol 26:987–998

  110. 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

  111. Pumplin N, Mondo SJ, Topp S et al (2010) Medicago truncatula Vapyrin is a novel protein required for arbuscular mycorrhizal symbiosis. Plant J 61:482–494

  112. 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

  113. Reddy DMR, Schorderet M, Feller U, Reinhardt D (2007) A petunia mutant affected in intracellular accommodation and morphogenesis of arbuscular mycorrhizal fungi. Plant J 51:739–750

  114. Shive JB, Sisler HD (1976) Effects of ancymidol (a growth retardant) and triarimol (a fungicide) on the growth, sterols, and gibberellins of Phaseolus vulgaris (L.). Plant Physiol 57:640–644. https://doi.org/10.1104/pp.57.4.640

  115. Rich MK, Schorderet M, Reinhardt D (2014) The role of the cell wall compartment in mutualistic symbioses of plants. Plant-Microbe Interact 5:238

  116. Rich MK, Courty PM, Roux C, Reinhardt D (2017) Role of the GRAS transcription factor ATA/RAM1 in the transcriptional reprogramming of arbuscular mycorrhiza in Petunia hybrida. BMC Genom 18:589. https://doi.org/10.1186/s12864-017-3988-8

  117. Samad AFA, Sajad M, Nazaruddin N, Fauzi IA, Murad AMA, Zainal Z, Ismail I (2017) MicroRNA and Transcription factor: key players in plant regulatory network. Front Plant Sci 8:565. https://doi.org/10.3389/fpls.2017.00565

  118. Sandal N, Petersen TR, Murray J et al (2006) Genetics of symbiosis in Lotus japonicus: recombinant inbred lines, comparative genetic maps, and map position of 35 symbiotic loci. Mol Plant Microbe Interact 19:80–91

  119. Santi C, Bogusz D, Franche C (2013) Biological nitrogen fixation in non-legume plants. Ann Bot 111:743–767. https://doi.org/10.1093/aob/mct048

  120. Schauser L, Roussis A, Stiller J, Stougaard J (1999) A plant regulator controlling development of symbiotic root nodules. Nature 402:191–195. https://doi.org/10.1038/46058

  121. Schmitz AM, Harrison MJ (2014) Signaling events during initiation of arbuscular mycorrhizal symbiosis. J Integr Plant Biol 56:250–261

  122. Si-Ammour A, Windels D, Arn-Bouldoires E et al (2011) miR393 and secondary siRNAs regulate expression of the TIR1/AFB2 auxin receptor clade and auxinrelated development of Arabidopsis leaves. Plant Physiol 157:683–691

  123. Sieberer BJ, Chabaud M, Fournier J et al (2012) A switch in Ca2+ spiking signature is concomitant with endosymbiotic microbe entry into cortical root cells of Medicago truncatula. Plant J 69:822–830

  124. Singh S, Katzer K, Lambert J et al (2014) CYCLOPS, a DNA-binding transcriptional activator, orchestrates symbiotic root nodule development. Cell Host Microbe 15:139–152. https://doi.org/10.1016/j.chom.2014.01.011

  125. Sinharoy S, Torres-Jerez I, Bandyopadhyay K et al (2013) The C2H2 transcription factor regulator of symbiosome differentiation represses transcription of the secretory pathway gene VAMP721a and promotes symbiosome development in Medicago truncatula. Plant Cell 25:3584–3601. https://doi.org/10.1105/tpc.113.114017

  126. Smit P, Raedts J, Portyanko V et al (2005) NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308:1789–1791. https://doi.org/10.1126/science.1111025

  127. Soyano T, Kouchi H, Hirota A, Hayashi M (2013) NODULE INCEPTION directly targets NF-Y subunit genes to regulate essential processes of root nodule development in Lotus japonicus. PLoS Genet 9:e1003352. https://doi.org/10.1371/journal.pgen.1003352

  128. Suzaki T, Ito M, Kawaguchi M (2013) Genetic basis of cytokinin and auxin functions during root nodule development. Front Plant Sci 4:42

  129. Svistoonoff S, Hocher V, Gherbi H (2014) Actinorhizal root nodule symbioses: what is signalling telling on the origins of nodulation? Curr Opin Plant Biol 20:11–18. https://doi.org/10.1016/j.pbi.2014.03.001

  130. Takeda N, Tsuzuki S, Suzaki T et al (2013) CERBERUS and NSP1 of Lotus japonicus are Common symbiosis genes that modulate arbuscular mycorrhiza development. Plant Cell Physiol 54:1711–1723. https://doi.org/10.1093/pcp/pct114

  131. Tanimoto E (1987) Gibberellin-dependent root elongation in lactuca-sativa: recovery from growth retardant-suppressed elongation with thickening by low concentration of Ga3. Plant Cell Physiol. 28:963–973. https://doi.org/10.1093/oxfordjournals.pcp.a077399

  132. Tisa LS, Beauchemin N, Cantor MN et al (2015) Draft genome sequence of Frankia sp. strain DC12, an atypical, noninfective, ineffective isolate from Datisca cannabina. Genome Announc 3:e00889–15. https://doi.org/10.1128/genomeA.00889-15

  133. Tisa LS, Beauchemin N, Gtari M et al (2013) What stories can the Frankia genomes start to tell us? J Biosci 38:719–726

  134. Turner M, Nizampatnam NR, Baron M et al (2013) Ectopic expression of miR160 results in auxin hypersensitivity, cytokinin hyposensitivity, and inhibition of symbiotic nodule development in soybean. Plant Physiol 162:2042–2055

  135. van Brussel AAN, Bakhuizen R, Spronsen PC van et al (1992) Induction of pre-infection thread structures in the leguminous host plant by mitogenic lipo-oligosaccharides of Rhizobium. Science 257:70–72. https://doi.org/10.1126/science.257.5066.70

  136. Vernié T, Moreau S, De Billy F et al (2008) EFD is an ERF transcription factor involved in the control of nodule number and differentiation in Medicago truncatula. Plant Cell 20:2696–2713

  137. Vernié T, Kim J, Frances L et al (2015) The NIN transcription factor coordinates diverse nodulation programs in different tissues of the Medicago truncatula root. Plant Cell 27:3410–3424. https://doi.org/10.1105/tpc.15.00461

  138. Vessey JK, Pawlowski K, Bergman B (2005) Root-based N2-fixing symbioses: legumes, actinorhizal plants, Parasponia sp. and cycads. In: Root physiology: from gene to function. Springer, New York, pp 51–78

  139. Vidal EA, Araus V, Lu C et al (2010) Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proc Natl Acad Sci USA 107:4477–4482

  140. Wall LG, Berry AM (2008) Early interactions, infection and nodulation in actinorhizal symbiosis. In: Pawlowski K, Newton WE (eds) Nitrogen-fixing actinorhizal symbioses. Springer, Netherlands, pp 147–166

  141. Wall LG, Beauchemin N, Cantor MN et al (2013) Draft genome sequence of Frankia sp. strain BCU110501, a nitrogen-fixing actinobacterium isolated from nodules of Discaria trinevis. Genome Announc 1:e00503–e00513

  142. Wang GL, Que F, Xu ZS et al (2015) Exogenous gibberellin altered morphology, anatomic and transcriptional regulatory networks of hormones in carrot root and shoot. BMC Plant Biol. 15:290. https://doi.org/10.1186/s12870-015-0679-y

  143. Wang E, Schornack S, Marsh JF et al (2012) A common signaling process that promotes mycorrhizal and oomycete colonization of plants. Curr Biol 22:2242–2246

  144. Wang Y, Wang L, Zou Y et al (2014) Soybean miR172c targets the repressive AP2 transcription factor NNC1 to activate ENOD40 expression and regulate nodule initiation. Plant Cell 26:4782–4801

  145. Wu G, Park MY, Conway SR et al (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138:750–759

  146. Xie F, Murray JD, Kim J et al (2012) Legume pectate lyase required for root infection by rhizobia. Proc Natl Acad Sci 109:633–638

  147. Xue L, Cui H, Buer B et al (2015) Network of GRAS transcription factors involved in the control of arbuscule development in Lotus japonicus. Plant Physiol 167:854–871

  148. Yan Z, Hossain MS, Arikit S et al (2015) Identification of microRNAs and their mRNA targets during soybean nodule development: functional analysis of the role of miR393j-3p in soybean nodulation. New Phytol. 207:748–759. https://doi.org/10.1111/nph.13365

  149. Yan Z, Hossain MS, Wang J et al (2013) miR172 regulates soybean nodulation. Mol Plant-Microbe Interact 26:1371–1377

  150. Yano K, Yoshida S, Müller J et al (2008) CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc Natl Acad Sci 105:20540–20545

  151. Yano K, Aoki S, Liu M, Umehara Y et al (2017) Function and evolution of a Lotus japonicus AP2/ERF family transcription factor that is required for development of infection threads. DNA Res 24(2):193–203. https://doi.org/10.1093/dnares/dsw052

  152. Yu N, Luo D, Zhang X et al (2014) A DELLA protein complex controls the arbuscular mycorrhizal symbiosis in plants. Cell Res 24:130–133. https://doi.org/10.1038/cr.2013.167

  153. Zanetti ME, Blanco FA, Beker MP et al (2010) AC subunit of the plant nuclear factor NF-Y required for rhizobial infection and nodule development affects partner selection in the common bean-Rhizobium etli symbiosis. Plant Cell 22:4142–4157

  154. 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

  155. 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

  156. Zhu H, Chen T, Zhu M et al (2008) A novel ARID DNA-binding protein interacts with SymRK and is expressed during early nodule development in Lotus japonicus. Plant Physiol 148:337–347

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We thank Dr Laurent LAPLAZE and Dr Valérie HOCHER from IRD (Institut de Recherche pour le Développement) for their suggestions, comments, and critical reviews, Dr Mathish NAMBIAR-VEETIL from IFGTB (Institute of Forest Genetics and Tree Breeding) for English correction, and the anonymous reviewers for their valuable comments.

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Diédhiou, I., Diouf, D. Transcription factors network in root endosymbiosis establishment and development. World J Microbiol Biotechnol 34, 37 (2018). https://doi.org/10.1007/s11274-018-2418-7

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  • Transcription factors
  • Micro RNA
  • Root endosymbiosis
  • Root nodule symbiosis
  • Actinorhizal symbiosis
  • Mycorrhizal symbiosis