B. Marion and . Master,

, Molecular dialogue in the nitrogen-fixing root symbiosis Casuarina/Frankia: characterization of Frankia's symbiotic signal molecules

D. Baker and B. Mullin, Actinorhizal Symbioses, Biological Nitrogen Fixation, vol.7, pp.259-292, 1992.

K. Bargali, Actinorhizal plants of Kumaun Himalaya and their ecological significance, African Journal of Plant Science, vol.5, pp.401-406, 2011.

D. R. Benson and W. B. Silvester, Biology of Frankia strains, actinomycete symbionts of actinorhizal plants, Microbiological Reviews, vol.57, issue.2, pp.293-319, 1993.

A. M. Berry, L. Mcintyre, and M. E. Mccully, Fine structure of root hair infection leading to nodulation in the Frankia-Alnus symbiosis, Canadian Journal of Botany, vol.64, issue.2, pp.292-305, 1986.

B. Buszewski and S. Noga, Hydrophilic interaction liquid chromatography (HILIC)--a powerful separation technique, Analytical and Bioanalytical Chemistry, vol.402, issue.1, pp.231-247, 2012.
DOI : 10.1007/s00216-011-5308-5

URL : https://link.springer.com/content/pdf/10.1007%2Fs00216-011-5308-5.pdf

H. Cérémonie, F. Debellé, and M. P. Fernandez, Structural and functional comparison of Frankia root hair deforming factor and rhizobia Nod factor, Canadian Journal of Botany, vol.77, issue.9, pp.1293-1301, 1999.

M. Chabaud, H. Gherbi, E. Pirolles, V. Vaissayre, J. Fournier et al., Chitinase-resistant hydrophilic symbiotic factors secreted by Frankia activate both Ca2+ spiking and NIN gene expression in the actinorhizal plant Casuarina glauca, New Phytologist, vol.209, issue.1, pp.86-93, 2016.

E. Chaia, L. G. Wall, and K. Huss-danell, Life in soil by the actinorhizal root nodule endophyte Frankia, Symbiosis, vol.51, issue.3, pp.201-226, 2010.

M. Cissoko, V. Hocher, H. Gherbi, D. Gully, A. Carre-mlouka et al., Actinorhizal signaling molecules: Frankia root hair deforming factor shares properties with NIN induction factor, 2018.

F. Clavijo, I. Diedhiou, V. Vaissayre, L. Brottier, J. Acolatse et al., The Casuarina NIN gene is transcriptionally activated throughout Frankia root infection as well as in response to bacterial diffusible signals, The New Phytologist, vol.208, issue.3, pp.887-903, 2015.

J. O. Dawson, Ecology Of Actinorhizal Plants, Nitrogen-fixing Actinorhizal Symbioses, pp.199-234, 2008.

B. Marion and . Master,

, Molecular dialogue in the nitrogen-fixing root symbiosis Casuarina/Frankia: characterization of Frankia's symbiotic signal molecules

I. V. Demina, T. Persson, P. Santos, M. Plaszczyca, and P. K. , Comparison of the nodule vs. root transcriptome of the actinorhizal plant Datisca glomerata: actinorhizal nodules contain a specific class of defensins, PloS One, vol.8, issue.8, p.72442, 2013.

J. Dénarié, F. Debellé, and J. C. Promé, Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis, Annual Review of Biochemistry, vol.65, pp.503-535, 1996.

N. Diagne, K. Arumugam, M. Ngom, M. Nambiar-veetil, C. Franche et al., Use of Frankia and actinorhizal plants for degraded lands reclamation, BioMed Research International, p.948258, 2013.

H. Gherbi, K. Markmann, S. Svistoonoff, J. Estevan, D. Autran et al., SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankiabacteria, Proceedings of the National Academy of Sciences, vol.105, issue.12, pp.4928-4932, 2008.

A. Good, Toward nitrogen-fixing plants, Science, vol.359, issue.6378, pp.869-870, 2018.

E. Granqvist, J. Sun, R. Op-den-camp, P. Pujic, L. Hill et al., Bacterial-induced calcium oscillations are common to nitrogen-fixing associations of nodulating legumes and nonlegumes, The New Phytologist, vol.207, issue.3, pp.551-558, 2015.

M. Griesmann, Y. Chang, X. Liu, Y. Song, G. Haberer et al., , p.1743, 2018.

B. Guillotin, J. Couzigou, and C. , NIN Is Involved in the Regulation of Arbuscular Mycorrhizal Symbiosis, Frontiers in Plant Science, 2016.

V. Hocher, N. Alloisio, F. Auguy, P. Fournier, P. Doumas et al., Transcriptomics of Actinorhizal Symbioses Reveals Homologs of the Whole Common Symbiotic Signaling Cascade, vol.156, pp.700-711, 2011.
URL : https://hal.archives-ouvertes.fr/halsde-00723395

V. Hocher, F. Auguy, X. Argout, L. Laplaze, C. Franche et al., Expressed sequence-tag analysis in Casuarina glauca actinorhizal nodule and root, New Phytologist, vol.169, issue.4, pp.681-688, 2006.

B. M. Hoffman, D. Lukoyanov, Z. Yang, D. R. Dean, and L. C. Seefeldt, Mechanism of nitrogen fixation by nitrogenase: the next stage, Chemical Reviews, vol.114, issue.8, pp.4041-4062, 2014.

B. Marion and . Master,

, Molecular dialogue in the nitrogen-fixing root symbiosis Casuarina/Frankia: characterization of Frankia's symbiotic signal molecules

A. Ktari, A. Gueddou, I. Nouioui, G. Miotello, I. Sarkar et al., Host Plant Compatibility Shapes the Proteogenome of Frankia coriariae, Frontiers in Microbiology, vol.8, p.720, 2017.

K. Kucho, K. Kakoi, M. Yamaura, S. Higashi, T. Uchiumi et al., Transient transformation of frankia by fusion marker genes in liquid culture, Microbes and Environments, vol.24, issue.3, pp.231-240, 2009.

P. Lerouge, P. Roche, C. Faucher, F. Maillet, G. Truchet et al., Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal, Nature, vol.344, issue.6268, pp.781-784, 1990.

K. Markmann, G. Giczey, and P. M. , Functional Adaptation of a Plant Receptor-Kinase Paved the Way for the Evolution of Intracellular Root Symbioses with Bacteria, PLOS Biology, vol.6, issue.3, p.68, 2008.

I. M. Miller and D. D. Baker, Nodulation of actinorhizal plants byFrankia strains capable of both root hair infection and intercellular penetration, Protoplasma, vol.131, issue.1, pp.82-91, 1986.

T. V. Nguyen, D. Wibberg, K. Battenberg, J. Blom, B. Vanden-heuvel et al., An assemblage of Frankia Cluster II strains from California contains the canonical nod genes and also the sulfotransferase gene nodH, BMC Genomics, vol.17, issue.1, p.796, 2016.

P. Normand, P. Lapierre, L. S. Tisa, J. P. Gogarten, N. Alloisio et al., Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography, Genome Research, vol.17, issue.1, pp.7-15, 2007.
DOI : 10.1101/gr.5798407

URL : https://hal.archives-ouvertes.fr/halsde-00140365

P. Normand, S. Orso, B. Cournoyer, P. Jeannin, C. Chapelon et al., Molecular phylogeny of the genus Frankia and related genera and emendation of the family Frankiaceae, International Journal of Systematic Bacteriology, vol.46, issue.1, pp.1-9, 1996.

I. Nouioui, F. Ghodhbane-gtari, M. D. Montero-calasanz, M. Göker, J. P. Meierkolthoff et al., Proposal of a type strain for Frankia alni (Woronin 1866) Von Tubeuf 1895, emended description of Frankia alni, and recognition of Frankia casuarinae sp. nov. and Frankia elaeagni sp. nov, International Journal of Systematic and Evolutionary Microbiology, vol.66, issue.12, pp.5201-5210, 2016.
URL : https://hal.archives-ouvertes.fr/hal-01604995

M. Obertello, O. S. Mame, L. Laurent, S. Carole, S. Sergio et al., Actinorhizal nitrogen fixing nodules: infection process, Marion BOISSEAUX Master's Thesis GEEFT, 2003.

, Molecular dialogue in the nitrogen-fixing root symbiosis Casuarina/Frankia: characterization of Frankia's symbiotic signal molecules. molecular biology and genomics, African Journal of Biotechnology, vol.2, issue.12, pp.528-538

G. E. Oldroyd, Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants, Nature Reviews. Microbiology, vol.11, issue.4, pp.252-263, 2013.

G. E. Oldroyd, J. D. Murray, P. S. Poole, and J. A. Downie, The rules of engagement in the legume-rhizobial symbiosis, Annual Review of Genetics, vol.45, pp.119-144, 2011.

J. Olivares, E. J. Bedmar, and J. Sanjuán, Biological nitrogen fixation in the context of global change, Molecular plant-microbe interactions: MPMI, vol.26, issue.5, pp.486-494, 2013.

K. Pawlowski and K. N. Demchenko, The diversity of actinorhizal symbiosis, Protoplasma, vol.249, issue.4, pp.967-979, 2012.

B. Péret, R. Swarup, L. Jansen, G. Devos, F. Auguy et al., Auxin Influx Activity Is Associated with Frankia Infection during Actinorhizal Nodule Formation in Casuarina glauca, Plant Physiology, vol.144, issue.4, pp.1852-1862, 2007.

F. Perrine-walker, H. Gherbi, L. Imanishi, V. Hocher, F. Ghodhbane-gtari et al., Symbiotic signaling in actinorhizal symbioses, Current Protein & Peptide Science, vol.12, issue.2, pp.156-164, 2011.
DOI : 10.2174/1389211213488422037

T. Persson, K. Battenberg, I. V. Demina, T. Vigil-stenman, B. V. Heuvel et al., Candidatus Frankia Datiscae Dg1, the Actinobacterial Microsymbiont of Datisca glomerata, Expresses the Canonical nod Genes nodABC in Symbiosis with Its Host Plant, PLOS ONE, vol.10, issue.5, p.127630, 2015.

;. Phenomenex, U. Phenomenex, . Hplc, G. C. Spe, and . Phenomenex, The Complete Guide to Solid Phase Extraction (SPE), 2017.

J. R. Postgate, Biological nitrogen fixation: fundamentals, Phil. Trans. R. Soc. Lond. B, vol.296, pp.375-385, 1082.

T. Rawnsley and L. S. Tisa, Development of a physical map for three Frankia strains and a partial genetic map for Frankia EuI1c, p.25, 2007.

C. Rouvier, J. Schwencke, Y. Prin, E. Navarro, P. Benoist et al., Biologie et diversité génétique des souches de Frankia associées aux Casuarinacées, Acta Botanica Gallica, vol.143, issue.7, pp.567-580, 1996.

B. Marion and . Master,

, Molecular dialogue in the nitrogen-fixing root symbiosis Casuarina/Frankia: characterization of Frankia's symbiotic signal molecules

C. Santi, D. Bogusz, and C. Franche, Biological nitrogen fixation in non-legume plants, Annals of Botany, vol.111, issue.5, pp.743-767, 2013.

P. Simonet, E. Navarro, C. Rouvier, P. Reddell, J. Zimpfer et al., Co-evolution between Frankia populations and host plants in the family Casuarinaceae and consequent patterns of global dispersal, Environmental Microbiology, vol.1, issue.6, pp.525-533, 1999.

D. E. Soltis, P. S. Soltis, D. R. Morgan, S. M. Swensen, B. C. Mullin et al., Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms, Proceedings of the National Academy of Sciences, vol.92, issue.7, pp.2647-2651, 1995.

T. Soyano, H. Kouchi, A. Hirota, and M. Hayashi, Nodule inception directly targets NF-Y subunit genes to regulate essential processes of root nodule development in Lotus japonicus, PLoS genetics, vol.9, issue.3, p.1003352, 2014.

S. Svistoonoff, F. M. Benabdoun, M. Nambiar-veetil, L. Imanishi, V. Vaissayre et al., The Independent Acquisition of Plant Root Nitrogen-Fixing Symbiosis in Fabids Recruited the Same Genetic Pathway for Nodule Organogenesis, PloS one, vol.8, issue.5, p.64515, 2013.

S. Svistoonoff, H. Gherbi, M. Nambiar-veetil, C. Zhong, Z. Michalak et al., Contribution of transgenic Casuarinaceae to our knowledge of the actinorhizal symbioses, Symbiosis, vol.50, issue.1, pp.3-11, 2010.
URL : https://hal.archives-ouvertes.fr/hal-01833620

S. Svistoonoff, V. Hocher, and H. Gherbi, Actinorhizal root nodule symbioses: what is signalling telling on the origins of nodulation?, Current Opinion in Plant Biology, vol.20, pp.11-18, 2014.

L. S. Tisa, R. Oshone, I. Sarkar, A. Ktari, A. Sen et al., Genomic approaches toward understanding the actinorhizal symbiosis: an update on the status of the Frankia genomes, Symbiosis, vol.70, issue.1, pp.5-16, 2016.

M. Valdés, N. Pérez, P. Estrada-de-los-santos, J. Caballero-mellado, J. J. Peña-cabriales et al., Non-Frankia Actinomycetes Isolated from Surface-Sterilized Roots of Casuarina equisetifolia Fix Nitrogen, Applied and Environmental Microbiology, vol.71, issue.1, pp.460-466, 2005.

K. A. Vandenbosch and J. G. Torrey, Development of Endophytic Frankia Sporangia in Field-and Laboratory-Grown Nodules of Comptonia peregrina and Myrica Gale, American Journal of Botany, vol.72, issue.1, pp.99-108, 1985.

J. Vessey, K. Pawlowski, and B. Bergman, Root-based N2-fixing Symbioses: Legumes, Actinorhizal Plants, Parasponia sp. and Cycads, Plant and Soil, pp.51-78, 2005.

B. Marion and . Master,

, Molecular dialogue in the nitrogen-fixing root symbiosis Casuarina/Frankia: characterization of Frankia's symbiotic signal molecules

E. Yoro, T. Suzaki, K. Toyokura, H. Miyazawa, H. Fukaki et al., A Positive Regulator of Nodule Organogenesis, NODULE INCEPTION, Acts as a Negative Regulator of Rhizobial Infection in Lotus japonicus1, Plant Physiology, vol.165, issue.2, pp.747-758, 2014.

X. Zhang and D. R. Benson, Utilization of amino acids by Frankia sp. strain CpI1, Archives of Microbiology, vol.158, issue.4, pp.256-261, 1992.

Z. Zhang, M. F. Lopez, and T. J. , A comparison of cultural characteristics and infectivity of Frankia isolates from root nodules of Casuarina species, Plant and Soil, vol.78, issue.1, pp.79-90, 1984.

C. Zhong, S. Mansour, M. Nambiar-veetil, D. Bogusz, and C. Franche, Casuarina glauca: a model tree for basic research in actinorhizal symbiosis, Journal of Biosciences, vol.38, issue.4, pp.815-823, 2013.

C. Zhong, Y. Zhang, Y. Chen, Q. Jiang, Z. Chen et al., Casuarina research and applications in China, Symbiosis, vol.50, pp.107-114, 2009.

B. Marion and . Master,

, Molecular dialogue in the nitrogen-fixing root symbiosis Casuarina/Frankia: characterization of Frankia's symbiotic signal molecules, p.39

. List, Arbuscular mycorrhiza AU: Arbitrary Units BD: Broughton and Dilworth CCaMK: Calcium & Calmodulin-dependent Kinase CcI3: Frankia strain CgNIN: Casuarina glauca NIN ESI: Electrospray ionization EST: Expressed Sequence Tag FcS: Frankia casuarinae supernatant GFP: Green Fluorescent Protein GUS: ?-glucuronidase enzyme HPLC: High Pressure Liquid Chromatography IPCC: Intergovernmental Panel on Climate Change IRD: Research Institute for Development LC/MS: Liquid chromatography paired with mass spectrometry ljNIN: Lotus japonicus NIN MS: Mass Spectrometry NF: Nod factors NIN: Nodule inception NINA: NIN -Activator pI: Isoelectric point PMSF: Phenylmethylsulfonyl fluoride Q-TOF: Quadruple Time Of Flight RHDF: Root Hair Deforming Factor SYMRK: SYMbiosis Receptor Kinase T-DNA: Transfer Deoxyribonucleic acid TFA: Trifluoroacetic acid USDA: United States Department of Agriculture X

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, Molecular dialogue in the nitrogen-fixing root symbiosis Casuarina/Frankia: characterization of Frankia's symbiotic signal molecules

, Chromatograms obtained using RP-C18 and RP-Polar C18 columns in HPLC. Injection consisted of X-CW elution fraction (50 µL). A: Purification using RP-C18 column with TFA 0.1 % (v:v). B: Purification using RP-C18 column with ammonium hydroxide 0.1 % (v:v). C: Purification using RP-Polar C18 column using TFA 0.1 % (v:v). D: Purification using RP-Polar C18 column using ammonium hydroxide 0.1 % (v:v). Regions circled correspond to fractions leading to the activation of ProCgNIN:GFP and ProCgNIN:GUS. The blue line corresponds to methanol gradient as described in Material and Methods. UV detection was at 254 nm in Arbitrary Units (AU), X-CW elution fractions and not in controls (red circle). A1: Positive ion mass spectra of X-CW elution fraction solubilized in 0.1% TFA. A2: positive ion mass spectra of X-CW methanol 95% / Ammonium hydroxide 5% fraction solubilized in 0.1% TFA, vol.13