, Algal ancestor of land plants was preadapted for symbiosis, Proc. Natl. Acad. Sci. USA, vol.112, pp.13390-13395, 2015.
, Diet of Arbuscular Mycorrhizal Fungi: Bread and Butter?, Trends Plant Sci, vol.22, pp.652-660, 2017.
URL : https://hal.archives-ouvertes.fr/hal-02626473
, Arbuscular mycorrhiza: the mother of plant root endosymbioses, Nat. Rev. Microbiol, vol.6, pp.763-775, 2008.
, Invasion by invitation: rhizobial infection in legumes, Mol. Plant Microbe Interact, vol.24, pp.631-639, 2011.
, Lipo-chitooligosaccharidic nodulation factors and their perception by plant receptors, Glycoconj. J, vol.32, pp.455-464, 2015.
URL : https://hal.archives-ouvertes.fr/hal-02632878
, Lipo-chitooligosaccharidic symbiotic signals are recognized by LysM receptor-like kinase LYR3 in the legume Medicago truncatula, ACS Chem. Biol, vol.8, pp.1900-1906, 2013.
URL : https://hal.archives-ouvertes.fr/hal-00903488
, Molecular basis of lipochitooligosaccharide recognition by the lysin motif receptor-like kinase LYR3 in legumes, Biochem. J, vol.473, pp.1369-1378, 2016.
URL : https://hal.archives-ouvertes.fr/hal-02636928
, , 2012.
, Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding, Proc. Natl. Acad. Sci. USA, vol.109, pp.13859-13864
, , 2018.
, LysM Receptor-Like Kinase and LysM Receptor-Like Protein Families: An Update on Phylogeny and Functional Characterization, vol.9, p.1531
, The Medicago truncatula lysin [corrected] motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes, Plant Physiol, vol.142, pp.265-279, 2006.
, Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases, Nature, vol.425, pp.585-592, 2003.
, Inactivation of duplicated nod factor receptor 5 (NFR5) genes in recessive loss-of-function non-nodulation mutants of allotetraploid soybean (Glycine max L, Merr.). Plant Cell Physiol, vol.51, pp.201-214, 2010.
, Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza, Nature, vol.469, pp.58-63, 2011.
URL : https://hal.archives-ouvertes.fr/hal-00577122
, Activation of symbiosis signaling by arbuscular mycorrhizal fungi in legumes and rice, Plant Cell, vol.27, pp.823-838, 2015.
URL : https://hal.archives-ouvertes.fr/hal-02119231
, Combined genetic and transcriptomic analysis reveals three major signalling pathways activated by Myc-LCOs in Medicago truncatula, New Phytol, vol.208, pp.224-240, 2015.
URL : https://hal.archives-ouvertes.fr/hal-02632553
, 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, vol.198, pp.190-202, 2013.
, , 2011.
, LysM-type mycorrhizal receptor recruited for rhizobium symbiosis in nonlegume Parasponia, Science, vol.331, pp.909-912
, Evaluation of the Role of the LysM Receptor-Like Kinase, OsNFR5/OsRLK2 for AM Symbiosis in Rice, Plant Cell Physiol, vol.57, pp.2283-2290, 2016.
, Role of N-glycosylation sites and CXC motifs in trafficking of medicago truncatula Nod factor perception protein to plasma membrane, J. Biol. Chem, vol.287, pp.10812-10823, 2012.
, Receptor-mediated exopolysaccharide perception controls bacterial infection, Nature, vol.523, pp.308-312, 2015.
URL : https://hal.archives-ouvertes.fr/hal-02137607
, Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution, Cell, vol.134, pp.25-36, 2008.
, Two genetic changes in cis-regulatory elements caused evolution of petal spot position in Clarkia, Nat. Plants, vol.4, pp.14-22, 2018.
, Multiple control levels of root system remodeling in arbuscular mycorrhizal symbiosis, Front. Plant Sci, vol.4, p.204, 2013.
, Dynamics of periarbuscular membranes visualized with a fluorescent phosphate transporter in arbuscular mycorrhizal roots of rice, Plant Cell Physiol, vol.51, pp.341-353, 2010.
, Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis, BMC Plant Biol, vol.9, p.10, 2009.
, Phylogenomics reveals multiple losses of nitrogen-fixing root nodule symbiosis, Science, vol.361, p.1743, 2018.
URL : https://hal.archives-ouvertes.fr/hal-02479077
, Ligand-receptor co-evolution shaped the jasmonate pathway in land plants, Nat. Chem. Biol, vol.14, pp.480-488, 2018.
, Contribution of NFP LysM domains to the recognition of Nod factors during the Medicago truncatula/Sinorhizobium meliloti symbiosis, PLoS ONE, vol.6, 2011.
, Spontaneous symbiotic reprogramming of plant roots triggered by receptor-like kinases, vol.3, 2014.
, 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, vol.159, pp.1671-1685, 2012.
URL : https://hal.archives-ouvertes.fr/hal-00743307
, Lipo-chitooligosaccharides promote lateral root formation and modify auxin homeostasis in Brachypodium distachyon, New Phytol, vol.221, pp.2190-2202, 2019.
URL : https://hal.archives-ouvertes.fr/hal-02336134
, The NFP locus of Medicago truncatula controls an early step of Nod factor signal transduction upstream of a rapid calcium flux and root hair deformation, Plant J, vol.34, pp.495-506, 2003.
, Preannouncement of symbiotic guests: transcriptional reprogramming by mycorrhizal lipochitooligosaccharides shows a strict co-dependency on the GRAS transcription factors NSP1 and RAM1, BMC Genomics, vol.16, p.994, 2015.
, Intraradical colonization by arbuscular mycorrhizal fungi triggers induction of a lipochitooligosaccharide receptor, Sci. Rep, vol.6, p.29733, 2016.
, Partner communication and role of nutrients in the arbuscular mycorrhizal symbiosis, New Phytol, vol.220, pp.1031-1046, 2018.
, Intracellular accommodation of microbes by plants: a common developmental program for symbiosis and disease?, Curr. Opin. Plant Biol, vol.3, pp.320-328, 2000.
, A single evolutionary innovation drives the deep evolution of symbiotic N2-fixation in angiosperms, Nat. Commun, vol.5, p.4087, 2014.
, Comparative genomics of the nonlegume Parasponia reveals insights into evolution of nitrogen-fixing rhizobium symbioses, Proc. Natl. Acad. Sci. USA, vol.115, pp.4700-4709, 2018.
, Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal, Nature, vol.344, pp.781-784, 1990.
, Improved characterization of nod factors and genetically based variation in LysM Receptor domains identify amino acids expendable for nod factor recognition in Lotus spp, Mol. Plant Microbe Interact, vol.23, pp.58-66, 2010.
, Evolution of a symbiotic receptor through gene duplications in the legume-rhizobium mutualism, New Phytol, vol.201, pp.961-972, 2014.
URL : https://hal.archives-ouvertes.fr/hal-01268605
, A plant plasma membrane H + -ATPase expressed in yeast is activated by phosphorylation at its penultimate residue and binding of 14-3-3 regulatory proteins in the absence of fusicoccin, J. Biol. Chem, vol.275, pp.17762-17770, 2000.
, Transgenic root-nodules of Vicia-hirsuta: a fast and efficient system for the study of gene-expression in indeterminate-type nodules, Mol. Plant Microbe Interact, vol.6, pp.699-706, 1993.
, Rhizobium meliloti lipooligosaccharide nodulation factors: different structural requirements for bacterial entry into target root hair cells and induction of plant symbiotic developmental responses, Plant Cell, vol.6, pp.1357-1374, 1994.
, The temperature-sensitive brush mutant of the legume Lotus japonicus reveals a link between root development and nodule infection by rhizobia, Plant Physiol, vol.149, pp.1785-1796, 2009.
, The ternary transformation system: constitutive virG on a compatible plasmid dramatically increases Agrobacterium-mediated plant transformation, Plant Mol. Biol, vol.43, pp.495-502, 2000.
, Cytoplasmic autofluorescence of an arbuscular mycorrhizal fungus Gigaspora gigantea and nondestructive fungal observations in planta, Mycologia, vol.90, pp.921-926, 1998.
, Nodulation factors from Rhizobium tropici are sulfated or nonsulfated chitopentasaccharides containing an N-methyl-N-acylglucosaminyl terminus, Biochemistry, vol.32, pp.10430-10435, 1993.
, Stable two-element control of dTph1 transposition in mutator strains of Petunia by an inactive ACT1 introgression from a wild species, Plant J, vol.41, pp.945-955, 2005.
, A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals, Nature, vol.425, pp.637-640, 2003.
, Interaction of Medicago truncatula lysin motif receptor-like kinases, NFP and LYK3, produced in Nicotiana benthamiana induces defence-like responses, PLoS ONE, vol.8, p.65055, 2013.
URL : https://hal.archives-ouvertes.fr/hal-02645629
, Role of a receptor-like kinase K1 in pea Rhizobium symbiosis development, Planta, vol.248, pp.1101-1120, 2018.
URL : https://hal.archives-ouvertes.fr/hal-02621748
, Targeting of a Nicotiana plumbaginifolia H+ -ATPase to the plasma membrane is not by default and requires cytosolic structural determinants, Plant Cell, vol.16, pp.1772-1789, 2004.
, BLAST+: architecture and applications, BMC Bioinformatics, vol.10, p.421, 2009.
, MAFFT multiple sequence alignment software version 7: improvements in performance and usability, Mol. Biol. Evol, vol.30, pp.772-780, 2013.
, trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses, Bioinformatics, vol.25, pp.1972-1973, 2009.
, ModelFinder: fast model selection for accurate phylogenetic estimates, Nat. Methods, vol.14, pp.587-589, 2017.
, IQ-TREE: a fast and effective stochastic algorithm for estimating maximumlikelihood phylogenies, Mol. Biol. Evol, vol.32, pp.268-274, 2015.
, New algorithms and methods to estimate maximumlikelihood phylogenies: assessing the performance of PhyML 3.0, Syst. Biol, vol.59, pp.307-321, 2010.
URL : https://hal.archives-ouvertes.fr/lirmm-00511784
, Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees, Nucleic Acids Res, vol.44, issue.W1, pp.242-245, 2016.
, Fitting a mixture model by expectation maximization to discover motifs in biopolymers, Proc. Int. Conf. Intell. Syst. Mol. Biol, vol.2, pp.28-36, 1994.
, Development of a GAL4-VP16/UAS trans-activation system for tissue specific expression in Medicago truncatula, PLoS ONE, vol.12, 2017.
URL : https://hal.archives-ouvertes.fr/hal-02336312
, A remorin protein interacts with symbiotic receptors and regulates bacterial infection, Proc. Natl. Acad. Sci. USA, vol.107, pp.2343-2348, 2010.
, A modular plasmid assembly kit for multigene expression, gene silencing and silencing rescue in plants, PLoS ONE, vol.9, p.88218, 2014.
, Agrobacterium rhizogenes-mediated root transformation, The Medicago truncatula handbook, pp.1-8, 2006.
, Lotus japonicus CASTOR and POLLUX are ion channels essential for perinuclear calcium spiking in legume root endosymbiosis, Plant Cell, vol.20, pp.3467-3479, 2008.
, Early events of vesicular-arbuscular mycorrhiza formation on Ri T-DNA transformed roots, New Phytol, vol.108, pp.211-218, 1988.
, The Medicago truncatula E3 ubiquitin ligase PUB1 interacts with the LYK3 symbiotic receptor and negatively regulates infection and nodulation, Plant Cell, vol.22, pp.3474-3488, 2010.
, Radiolabeling of lipo-chitooligosaccharides using the NodH sulfotransferase: a two-step enzymatic procedure, BMC Biochem, vol.5, p.4, 2004.
, The Petunia GRAS Transcription Factor ATA/RAM1 Regulates Symbiotic Gene Expression and Fungal Morphogenesis in Arbuscular Mycorrhiza, Plant Physiol, vol.168, pp.788-797, 2015.
URL : https://hal.archives-ouvertes.fr/hal-02633688
, with the primers listed in the key resources table) from genomic DNA isolated from S. lycopersicum, P. hybrida and M. pudica, respectively, and cloned in transcriptional fusion with a GUS reporter containing a plant intron, in a pCambia 2200 modified for Golden gate cloning and containing a ProUbi:DsRed reporter as in [73]. Note that the PhLYK10 sequence in P. hybrida originates from the P. axillaris parent. 240 and 185 bp sequences preceding the SlLYK10 or MtNFP start codons were synthesized and cloned as described previously. ProSlLYK10:MtNFP-YFP was made by Golden gate cloning in a pCambia 2200 modified for Golden gate as in [6]. ProMtNFP:MtNFP-YFP was made as in [30] excepted that MtNFP was in translation fusion with YFP instead that of FLAG. SlLYK10 and PhLYK10 coding sequences were amplified by PCR from genomic DNA isolated from S. lycopersicum and P. hybrida respectively and cloned, Cloning 1.8, 1.5 and 1.9 kbp corresponding to the non-coding region between SlLYK10, PhLYK10, and MpNFP and the preceding genes, including the 5 0 UTR were amplified by PCR
, for SlLYK10 or in a pCambia 2200 modified for Golden gate cloning as in [6] for PhLYK10. For expression in M. truncatula, SlLYK10 sequence was optimized with a M. truncatula codon usage and cloned in translational fusion with YFP under the control of Pro35S in a pCambia 2200 modified for Golden gate cloning as in [6]. For expression in L. japonicus, PhLYK10 coding sequence was amplified by PCR from genomic DNA isolated from P. hybrida and cloned in translational fusion with mOrange under the control of LjUbiquitin promoter into a pCambia
, For SlLYK10c and PhLYK10c constructs, the sequences coding the extracellular region of SlLYK10 or PhLYK10 were amplified by PCR (with the primers listed in the key resources table) and cloned in translational fusion with the sequences coding TM/ICR of MtNFP and YFP under the control of Pro35S in a pCambia 2200 modified for Golden gate cloning as in, vol.6
, G 460 A) was identified by sequencing (NGS) an amplicon (key resources table) obtained on tomato (cv M82) EMS-mutagenized lines. Homozygous mutant or WT SlLYK10 alleles were identified by sequencing (Sanger) a similar amplicon on the progeny. The Phlyk10-1 mutant allele (line LY0882, dTph1 insertion 116 bp from the start codon) was identified by BLAST-searching in a Petunia dTPh1 transposon flanking sequence database [29] with the full PhLYK10 coding sequence. This line was crossed with the stabilizer line W5 [60], to segregate out the activator locus required for dTph1 transposition, S. lycopersicum and P. hybrida mutant identification and genotyping The Sllyk10-1 mutant allele (line 1051
, Agrobacterium rhizogenes mediated transformation Tomato (cv Marmande) seeds were surface sterilized and germinated in vitro for 7 to 10 days until cotyledons were fully expanded. Plantlets were cut at the hypocotyl level, immerged in a A. rhizogenes ARqua1 suspension at OD 600nm = 0.3 and grown for 3 days at 25 C on MS, then on MS supplemented with 50 mg/l kanamycin and 200 mg/l cefotaxim until emergence of transgenic roots. Transgenic roots were selected by fluorescence microscopy
, ROC lines derived from transformed roots were grown in dark, on MS medium supplemented with 50 mg/l kanamycin
, Mtnfp-2 plants were produced as described in [76] for analysis of promoter expression pattern and for complementation experiment, respectively. Chimeric L. japonicus Gifu and Ljnfr5-2 plants were produced as described in, vol.77
, Roots were harvested, washed and stained between 3 and 4 weeks post inoculation. For analysis of GUS activity in tomato roots, sterilized Gigantea gigaspora spores, harvested from a leek nurse culture, were pregerminated 5 days on M medium [78] in a 3% CO 2 incubator at 32 C. Two spores and one fragment of a transgenic tomato ROC line were then co-cultured on a Petri dish containing M medium supplemented with 50 mg/l kanamycin. Petri dishes were placed vertically with ROC lines above the fungal spores for 4 weeks. For analysis of GUS activity in M. truncatula transgenic roots, chimeric plantlets were transferred in 50 mL containers filled with a mix 1:1 of attapulgite and sand, watered with 20 mL of 0.5x modified Long ashton medium and inoculated with 200 spores of R. irregularis DAOM 197198. Roots were harvested, washed and stained 2 weeks post inoculation. Inoculation with rhizobia and spontaneous nodulation M. truncatula chimeric plantlets were transferred in 250 mL containers filled with attapulgite, watered with 20 mL of Farhaeus medium supplemented with 1 mM NH 4 NO 3 . After 4 days, 2.5 mL of a suspension at OD 600nm = 0.025 of a S. meliloti strains 2011 harboring the hemA-lacZ plasmid (pXLGD4) was added around the hypocotyl. Roots were harvested, washed and stained 4 weeks post inoculation. For complementation experiments, L. japonicus chimeric plantlets were transferred to Weck jars containing 300 mL of a mix of sand and vermiculite and inoculated with 20 mL of a M. loti MAFF303099 DsRED suspension in FP medium, Inoculation with AMF For AM phenotyping, petunia seeds were germinated on a sterilized potting soil until cotyledons were fully expanded. Tomato seeds were surface sterilized and germinated in sterile water. Petunia and tomato plantlets were then transferred in 50 mL containers filled with attapulgite, watered with 20 mL of 0.5x modified Long ashton (7.5 mM NaH 2 PO 4 ), and inoculated with 500 spores of R. irregularis DAOM, 197198.
, Root systems were analyzed 60 days post transformation. Transient Expression in N. benthamiana Leaves of N. benthamiana were infiltrated with A. tumefaciens LBA4404 virGN54D strains as described in [79]. Leaves were harmannitol. Tomato ROC and chimeric M. truncatula plants expressing the GUS reporter were stained with 0.1% X-Gluc or Magenta-Gluc (20 min under vacuum followed by incubation at 37 C). AMF were stained by treating root tissues with 100% ethanol for 4 h, then with 10% KOH for 8 min at 95 C (tomato ROC and P. hybrida roots) or 1,5 days at room temperature (M. truncatula roots) and finally with 0.2 M PBS pH 7.2, Triton X-100 0.01%, 1 mg/mL WGA CF488A conjugate overnight at room temperature. For analysis of subcellular localization, tomato ROC and N. benthamiana leaves were imaged using a SP8 confocal microscope. Arbuscules in P. hybrida were imaged with a SP2 confocal microscope. Overlay corresponds to merge of green fluorescence channel images with differential interference contrast images. GUS and WGA staining were imaged using an Axiozoom V16 microscope (Figure 4) or an Axioplan 2 microscope (Figure 5), L. japonicus chimeric plantlets were transferred to Fahraeus medium plates containing 0.1 mM of the ethylene biosynthesis inhibitor L-a-(2-aminoethoxyvinyl)-glycine 2.5 weeks after transformation
, nodulated roots systems expressing the GUS reporter were stained with 0.1% mangenta-gluc and then fixed with glutaraldehyde 1.25% in 0.1 M PBS pH7.2 (30 min under vacuum). In case of Mtnfp-2 complementation, nodulated roots systems were first fixed with glutaraldehyde 1.25% and then stained with 2% X-Gal
, Western blotting and membrane fraction preparation Immunobloting of YFP fusions in M. truncatula roots was performed on 20 mg of a total extract of a pool of 10 root systems inoculated by S. meliloti. For LCO binding assays, approximately 20 g of leaves were homogenized at 4 C in a blender in the presence of 40 mL of extraction buffer (25 mM Tris, pH 8.5, 0.47 M sucrose, 5 mM EDTA, 10 mM DTT, 0.6% PVPP and protease inhibitors (0.1 mM AEBSF, and 1 mg/mL each of leupeptin, aprotinin, antipain, chymostatin, and pepstatin), Nodules were sectioned after inclusion in 6% agarose low gelling temperature using a vribratome VT 1000S and sections were imaged with an Axioplan 2 microscope. Nodules of M. truncatula roots expressing the GUS reporter under the control of the minimal promoters were stained 0.1% X-Gluc and directly imaged with an Axiozoom V16 microscope, vol.29, pp.4249-4259, 2019.
, Labeling of LCO-V(C18:1D11,NMe) was performed as described in [80]. LCO binding assays on membrane fractions containing 20 mg or 40 mg of proteins were performed as in [6] using between 1 and 2 nM of radiolabeled LCO and ranges of unlabeled LCO between 1 nM to 1 mM. Similar amount of membrane fraction from leaves expressing PhLYK10-YFP, PhLYK10-YFPc, SlLYK10c-YFP or from untransformed leaves were used in each experiment. Competition with COs were performed with 1 mM of unlabeled pure CO4 and CO8. PNGaseF treatment and immunoblotting PNGaseF treatment, LCO binding assays LCO-V(C18:1D11,NMe) and LCO-V(C18:1D11,NMe,S) were purified from the rhizobial strain Rhizobium tropici
, RNA extraction, cDNA synthesis was performed as described in [21]. Relative expression levels were calculated using glyceraldehyde-3-phosphate dehydrogenase (GAPDH) as a reference gene
, Putative orthologs were aligned with MAFFT with default parameters and aligned positions with more than 50% of gaps were removed using TrimAl. The best-fitting evolutionary model was tested using ModelFinder and according to the Bayesian Information Criteria. The model TVM+F+R5 was further used for Maximum Likelihood (ML) analysis using IQ-TREE. Branch support was tested using 10,000 replicates of SH-alrt. The resulting tree was annotated using the iTOL platform. For each ortholog, 600 bp promoter sequences were extracted upstream of the gene start using a custom Python script. Promoters were searched for enriched motif using MEME with following parameters: zero or one occurrence of motif per site, Promoter investigation MtNFP orthologs were retrieved from genomes of 71 dicotyledonous species (list in Table S2) using tBLASTn and an e-value threshold of 1 e-10
, ANALYSIS Number of independent biological replicates and individuals analyzed, as well as the statistical tests used to analyze the data are indicated in the figure legends, All statistical analyses were performed using the R software
, Current Biology, vol.29, pp.4249-4259, 2019.