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Equipe de Recherche Symbiose actinorhizienne

Nicole Alloisio

Chargée de recherche CNRS


  • Thèmes de recherches :
    1. Mécanismes moléculaires dans la symbiose fixatrice d’azote Frankia-Alnus glutinosa

Parcours scientifique






  • Pujic, P., Alloisio, N., Fournier, P., Roche, D., Sghaier, H., Miotello, G., et al. (2019). Omics of the early molecular dialogue between <i>Frankia alni</i> and <i>Alnus glutinosa</i> and the cellulase synton. Environmental Microbiology. doi:10.1111/1462-2920.14606
    Résumé : The early Frankia-Alnus symbiotic molecular exchanges were analyzed in detail by protein and RNA omics. For this, Frankia cells were placed in the presence of Alnus roots but separated by a dialysis membrane for 64 h. The bacterial cells were then harvested and analyzed by high-throughput proteomics and transcriptomics (RNA-seq). The most upregulated gene clusters were found to be the potassium transporter operon kdp and an ABC transporter operon of uncharacterized function. The most upregulated proteins were found to be acyl dehydrogenases and the potassium transporter Kdp. These suggest a preadaptation to the impending stresses linked to the penetration into isotonic host tissues and a possible rearrangement of the membrane. Another cluster among the 60 most upregulated ones that comprised two cellulases and a cellulose synthase was conserved among the Frankia and other actinobacteria such as Streptomyces. Cellulase activity was detected on CMC all along the length of the root but not away from it. Frankia alni ACN14a was found to be unable to respire or grow on glucose as sole carbon source. The cellulose synthase was found active at the tip of hyphae in response to Alnus root exudates, resulting in a calcofluor stained tip.
    Mots-clés : #1.
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  • Griesmann, M., Chang, Y., Liu, X., Song, Y., Haberer, G., Crook, M. B., et al. (2018). Phylogenomics reveals multiple losses of nitrogen-fixing root nodule symbiosis. Science (New York, N.y.). doi:10.1126/science.aat1743
    Résumé : The root nodule symbiosis of plants with nitrogen-fixing bacteria impacts global nitrogen cycles and food production but is restricted to a subset of genera within a single clade of flowering plants. To explore the genetic basis for this scattered occurrence, we sequenced the genomes of ten plant species covering the diversity of nodule morphotypes, bacterial symbionts and infection strategies. In a genome-wide comparative analysis of a total of 37 plant species, we discovered signatures of multiple independent loss-of-function events in the indispensable symbiotic regulator NODULE INCEPTION (NIN) in ten out of 13 genomes of non-nodulating species within this clade. The discovery that multiple independent losses shaped the present day distribution of nitrogen-fixing root nodule symbiosis in plants reveals a phylogenetically wider distribution in evolutionary history and a so far underestimated selection pressure against this symbiosis.
    Mots-clés : #1.

  • Lurthy, T., Alloisio, N., Fournier, P., Anchisi, S., Ponsero, A., Normand, P., et al. (2018). Molecular response to nitrogen starvation by Frankia alni ACN14a revealed by transcriptomics and functional analysis with a fosmid library in Escherichia coli. Research In Microbiology, 169(2), 90-100. doi:10.1016/j.resmic.2017.12.002
    Résumé : The transcriptome of Frankia alni strain ACN14a was compared between in vitro ammonium-replete (N-replete) and ammonium-free dinitrogen-fixing (N-fixing) conditions using DNA arrays. A Welch-test (p < 0.05) revealed significant upregulation of 252 genes under N-fixing vs. N-replete (fold-change (FC) ≥ 2), as well as significant downregulation of 48 other genes (FC ≤ 0.5). Interestingly, there were 104 Frankia genes upregulated in vitro that were also significantly upregulated in symbiosis with Alnus glutinosa, while the other 148 genes were not, showing that the physiology of in vitro fixation is markedly different from that under symbiotic conditions. In particular,in vitro fixing cells were seen to upregulate genes identified as coding for a nitrite reductase, and amidases that were not upregulated in symbiosis. Confirmatory assays for nitrite reductase showed that Frankia indeed reduced nitrite and used it as a nitrogen source. An Escherichia coli fosmid clone carrying the nirB region was able to grow better in the presence of 5 mM nitrite than without it, confirming the function of the genome region. The physiological pattern that emerges shows that Frankia undergoes nitrogen starvation that induces a molecular response different from that seen in symbiosis.
    Mots-clés : #1, fosmid library, Nitrite reductase, nitrogen fixation, nitrogen stress.


  • Carro, L., Persson, T., Pujic, P., Alloisio, N., Fournier, P., Boubakri, H., et al. (2016). Organic acids metabolism in Frankia alni. Symbiosis, 70(1-3), 37–48. doi:10.1007/s13199-016-0404-0
    Résumé : Trophic exchanges constitute the bases of the symbiosis between the nitrogen-fixing actinomycete Frankia and its host plant Alnus, but the identity of the compounds exchanged is still poorly known. In the current work, previously published transcriptomic studies of Alnus nodules and of symbiotic Frankia were reexamined for TCA cycle related genes. The bacterial TCA enzyme genes were all upregulated, especially the succinyl-CoA synthase and the citrate synthase while on the plant side, none was significantly modified in nodules relative to non-inoculated roots. A preliminary metabolomics approach permitted to see that citrate, 2-oxoglutarate, succinate, malate and fumarate were all more abundant (FC (Fold change) = 5–70) in mature nitrogen-fixing nodules than in roots. In the evaluation of the uptake and metabolism of these organic acids, a significant change was observed in the morphology of nitrogen fixing vesicles in vitro: the dicarboxylates malate, succinate and fumarate induced the formation of larger vesicles than was the case with propionate. Moreover, the production of spores was also modified depending on the organic acid present. The assays showed that most C4 dicarboxylates were taken up while C6 tricarboxylates were not and citrate even partially blocked catabolism of reserve carbon. Tests were performed to determine if the change in membrane permeability induced by Ag5, a peptide previously shown to modify the membranes of Frankia, increased the uptake of specific organic acids. No effect was observed with citrate while an increase in nitrogen fixation was seen with propionate.
    Mots-clés : #1, developmental biology, Dicarboxylates, ecology, evolutionary biology, Frankia, Microbiology, nitrogen fixation, Plant Sciences, Propionate, Respiration, Vesicles.

  • Persson, T., Van Nguyen, T., Alloisio, N., Pujic, P., Berry, A. M., Normand, P., & Pawlowski, K. (2016). The N-metabolites of roots and actinorhizal nodules from Alnus glutinosa and Datisca glomerata: can D. glomerata change N-transport forms when nodulated? Symbiosis, 70(1-3), 149–157. doi:10.1007/s13199-016-0407-x
    Résumé : To gain more insight in nitrogen metabolism in actinorhizal nodules, a comparison between the N metabolite profiles in roots vs. nodules was initiated for one host plant from the best-examined order of actinorhizal plants, Fagales, A. glutinosa (Betulaceae), a temperate tree, and one host plant from the Cucurbitales order, Datisca glomerata (Datiscaceae). For both symbioses, the symbiotic transcriptomes have been published and can be used to assess the expression of genes representing specific metabolic pathways in nodules. The amino acid profiles of roots in this study suggest that A. glutinosa transported aspartate, glutamate and citrulline in the xylem, a combination of nitrogenous solutes not published previously for this species. The amino acid profiles of D. glomerata roots depended on whether the plants were nodulated or grown on nitrate; roots of nodulated plants contained increased amounts of arginine. Although bacterial transcriptome data showed no symbiotic auxotrophy for branched chain amino acids (leucine, isoleucine, valine) in either symbiosis, D. glomerata nodules contained comparatively high levels of these amino acids. This might represent a response to osmotic stress.
    Mots-clés : #1, Actinorhiza, Arginine, Citrulline, developmental biology, ecology, evolutionary biology, Frankia, Gamma-aminobutyrate (GABA), Microbiology, Nitrogen-fixation, Plant Sciences.


  • Carro-Garcia, L., Pujic, P., Alloisio, N., Fournier, P., Boubakri, H., Hay, A. E., et al. (2015). Alnus peptides modify membrane porosity and induce the release of nitrogen-rich metabolites from nitrogen-fixing Frankia. The Isme Journal, 9(8), 1723–1733. doi:10.1038/ismej.2014.257
    Mots-clés : #1, #5, #cesn.

  • Svistoonoff, S., Tromas, A., Diagne, N., Alloisio, N., Laplaze, L., Champion, A., et al. (2015). How Transcriptomics Revealed New Information on Actinorhizal Symbioses Establishment and Evolution. Biological Nitrogen Fixation, 2 Volume Set, 425. Consulté de
    Mots-clés : #1.


  • Pujic, P., Fournier, P., Alloisio, N., Hay, A. E., Maréchal, J., Anchisi, S., & Normand, P. (2012). Lectin genes in the <i>Frankia alni</i> genome. Archives Of Microbiology, 194, 1–10. Consulté de
    Mots-clés : #1, #cesn.


  • Hocher, V., Alloisio, N., Auguy, F., Fournier, P., Doumas, P., Pujic, P., et al. (2011). Transcriptomics of Actinorhizal Symbioses Reveals Homologs of the Whole Common Symbiotic Signaling Cascade. Plant Physiology, 156(2), 700-711. doi:10.1104/pp.111.174151
    Résumé : Comparative transcriptomics of two actinorhizal symbiotic plants, Casuarina glauca and Alnus glutinosa, was used to gain insight into their symbiotic programs triggered following contact with the nitrogen-fixing actinobacterium Frankia. Approximately 14,000 unigenes were recovered in roots and 3-week-old nodules of each of the two species. A transcriptomic array was designed to monitor changes in expression levels between roots and nodules, enabling the identification of up- and down-regulated genes as well as root- and nodule-specific genes. The expression levels of several genes emblematic of symbiosis were confirmed by quantitative polymerase chain reaction. As expected, several genes related to carbon and nitrogen exchange, defense against pathogens, or stress resistance were strongly regulated. Furthermore, homolog genes of the common and nodule-specific signaling pathways known in legumes were identified in the two actinorhizal symbiotic plants. The conservation of the host plant signaling pathway is all the more surprising in light of the lack of canonical nod genes in the genomes of its bacterial symbiont, Frankia. The evolutionary pattern emerging from these studies reinforces the hypothesis of a common genetic ancestor of the Fabid (Eurosid I) nodulating clade with a genetic predisposition for nodulation.
    Mots-clés : #1, #5.

  • Hocher, V., Alloisio, N., Bogusz, D., & Normand, P. (2011). Early signaling in actinorhizal symbioses. Plant Signaling & Behavior, 6(9), 1377–1379. Consulté de
    Mots-clés : #1.


  • Alloisio, N., Queiroux, C., Fournier, P., Pujic, P., Normand, P., Vallenet, D., et al. (2010). The <i>Frankia alni</i> symbiotic transcriptome. Molecular Plant-Microbe Interactions, 23(5), 593–607. Consulté de
    Mots-clés : #1, #5, #ibio.

  • Popovici, J., Comte, G., Bagnarol, É., Alloisio, N., Fournier, P., Bellvert, F., et al. (2010). Differential effects of rare specific flavonoids on compatible and incompatible strains in the <i>Myrica</i> gale-<i>Frankia</i> actinorhizal symbiosis. Applied And Environmental Microbiology, 76(8), 2451–2460. doi:10.1128/AEM.02667-09
    Résumé : Plant secondary metabolites, and specifically phenolics, play important roles when plants interact with their environment and can act as weapons or positive signals during biotic interactions. One such interaction, the establishment of mutualistic nitrogen-fixing symbioses, typically involves phenolic-based recognition mechanisms between host plants and bacterial symbionts during the early stages of interaction. While these mechanisms are well studied in the rhizobia-legume symbiosis, little is known about the role of plant phenolics in the symbiosis between actinorhizal plants and Frankia genus strains. In this study, the responsiveness of Frankia strains to plant phenolics was correlated with their symbiotic compatibility. We used Myrica gale, a host species with narrow symbiont specificity, and a set of compatible and noncompatible Frankia strains. M. gale fruit exudate phenolics were extracted, and 8 dominant molecules were purified and identified as flavonoids by high-resolution spectroscopic techniques. Total fruit exudates, along with two purified dihydrochalcone molecules, induced modifications of bacterial growth and nitrogen fixation according to the symbiotic specificity of strains, enhancing compatible strains and inhibiting incompatible ones. Candidate genes involved in these effects were identified by a global transcriptomic approach using ACN14a strain whole-genome microarrays. Fruit exudates induced differential expression of 22 genes involved mostly in oxidative stress response and drug resistance, along with the overexpression of a whiB transcriptional regulator. This work provides evidence for the involvement of plant secondary metabolites in determining symbiotic specificity and expands our understanding of the mechanisms, leading to the establishment of actinorhizal symbioses.
    Mots-clés : #1, #3, #cesn.
  • Popovici, J., Comte, G., Bagnarol, E., Alloisio, N., Fournier, P., Bellvert, F., et al. (2010). Rare specific flavonoids affect differentially compatible and incompatible strains in the <i>Myrica</i> gale-<i>Frankia</i> actinorhizal symbiosis. Applied And Environmental Microbiology, 76, 2451-2460.
    Mots-clés : #1, #3, #cesn.


  • Alloisio, N., Félix, S., Maréchal, J., Pujic, P., Rouy, Z., Vallenet, D., et al. (2007). <i>Frankia alni</i> proteome under nitrogen-fixing and nitrogen-replete conditions. Physiologia Plantarum, 130(3), 440–453. Consulté de
    Mots-clés : #1.

  • Bagnarol, E., Popovici, J., Alloisio, N., Maréchal, J., Pujic, P., Normand, P., & Fernandez, M. (2007). Differential Frankia protein patterns induced by phenolic extracts from <i>Myricaceae</i> seeds. Physiologia Plantarum, 130(3), 380–390. Consulté de
    Mots-clés : #1.

  • Normand, P., Lapierre, P., Tisa, L. S., Gogarten, J. P., Alloisio, N., Bagnarol, E., et al. (2007). Genome characteristics of facultatively symbiotic <i>Frankia</i> sp. strains reflect host range and host plant biogeography. Genome Research, 17(1), 7-15. doi:10.1101/gr.5798407
    Résumé : Soil bacteria that also form mutualistic symbioses in plants encounter two major levels of selection. One occurs during adaptation to and survival in soil, and the other occurs in concert with host plant speciation and adaptation. Actinobacteria from the genus Frankia are facultative symbionts that form N2-fixing root nodules on diverse and globally distributed angiosperms in the “actinorhizal” symbioses. Three closely related clades of Frankia sp. strains are recognized; members of each clade infect a subset of plants from among eight angiosperm families. We sequenced the genomes from three strains; their sizes varied from 5.43 Mbp for a narrow host range strain (Frankia sp. strain HFPCcI3) to 7.50 Mbp for a medium host range strain (Frankia alni strain ACN14a) to 9.04 Mbp for a broad host range strain (Frankia sp. strain EAN1pec.) This size divergence is the largest yet reported for such closely related soil bacteria (97.8%–98.9% identity of 16S rRNA genes). The extent of gene deletion, duplication, and acquisition is in concert with the biogeographic history of the symbioses and host plant speciation. Host plant isolation favored genome contraction, whereas host plant diversification favored genome expansion. The results support the idea that major genome expansions as well as reductions can occur in facultative symbiotic soil bacteria as they respond to new environments in the context of their symbioses.
    Mots-clés : #1, #4, #6, #cesn.

  • Pawlowski, K., Jacobsen, K. R., Alloisio, N., Ford Denison, R., Klein, M., Tjepkema, J. D., et al. (2007). Truncated hemoglobins in actinorhizal nodules of <i>Datisca glomerata</i>. Plant Biology, 9(6), 776–785. Consulté de
    Mots-clés : #1.

Chapitre d’ouvrages


  • Alloisio, N., Kucho, K., Pujic, P., & Normand, P. (2015). The <i>Frankia alni</i> Symbiotic Transcriptome. Dans F. J. de Bruijn (Éd.), Biological Nitrogen Fixation (p. 757-768). Hoboken, NJ, USA: John Wiley & Sons, Inc. Consulté de
    Mots-clés : #1.


Communications Orales