Glycoconjugate Journal

, Volume 32, Issue 7, pp 455–464 | Cite as

Lipo-chitooligosaccharidic nodulation factors and their perception by plant receptors

  • Judith Fliegmann
  • Jean-Jacques BonoEmail author


Lipo-chitooligosaccharides produced by nitrogen-fixing rhizobia are signaling molecules involved in the establishment of an important agronomical and ecological symbiosis with plants. These compounds, known as Nod factors, are biologically active on plant roots at very low concentrations indicating that they are perceived by specific receptors. This article summarizes the main strategies developed for the syntheses of bioactive Nod factors and their derivatives in order to better understand their mode of perception. Different Nod factor receptors and LCO-binding proteins identified by genetic or biochemical approaches are also presented, indicating perception mechanisms that seem to be more complicated than expected, probably involving multi-component receptor complexes.


Lipo-chitooligosaccharides Symbiosis Receptor Plant LysM 



We thank C. Gough and J. Cullimore (LIPM, Toulouse) for critical reading of the manuscript. We acknowledge funding on LCO signaling in our group by the the French National Research Agency contracts “SYMNALING” (ANR-12-BSV7-0001) and “NICE CROPS” (ANR-14-CE18-0008) and by the French Laboratory of Excellence project "TULIP" (ANR-10-LABX-41; ANR-11-IDEX-0002-02).

Conflict of interest

The authors declare that they have no conflict of interest.


  1. 1.
    Lerouge, P., Roche, P., Faucher, C., Maillet, F., Truchet, G., Promé, J.C., Dénarié, J.: Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344(6268), 781–784 (1990)CrossRefPubMedGoogle Scholar
  2. 2.
    Dénarié, J., Debellé, F., Rosenberg, C.: Signaling and host range variation in nodulation. Annu. Rev. Microbiol. 46, 497–531 (1992)CrossRefPubMedGoogle Scholar
  3. 3.
    Dénarié, J., Debellé, F., Promé, J.C.: Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu. Rev. Biochem. 65, 503–535 (1996)CrossRefPubMedGoogle Scholar
  4. 4.
    D’Haeze, W., Holsters, M.: Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 12(6), 79R–105R (2002)CrossRefPubMedGoogle Scholar
  5. 5.
    Maillet, F., Poinsot, V., André, O., Puech-Pages, V., Haouy, A., Gueunier, M., Cromer, L., Giraudet, D., Formey, D., Niebel, A., Martinez, E.A., Driguez, H., Bécard, G., Dénarié, J.: Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469(7328), 58–63 (2011)CrossRefPubMedGoogle Scholar
  6. 6.
    Czaja, L.F., Hogekamp, C., Lamm, P., Maillet, F., Andres Martinez, E., Samain, E., Dénarié, J., Küster, H., Hohnjec, N.: Transcriptional responses towards diffusible signals from symbiotic microbes reveal MtNFP- and MtDMI3-dependent reprogramming of host gene expression by AM fungal LCOs. Plant Physiol. 159(4), 1671–1685 (2012)PubMedCentralCrossRefPubMedGoogle Scholar
  7. 7.
    Camps, C., Jardinaud, M.-F., Rengel, D., Carrère, S., Hervé, C., Debellé, F., Gamas, P., Bensmihen, S., Gough, C.: Combined genetic and transcriptomic analysis reveals three major signalling pathways activated by Myc-LCOs in Medicago truncatula. New Phytol. (2015). doi: 10.1111/nph.13427 PubMedGoogle Scholar
  8. 8.
    Sun, J., Miller, J.B., Granqvist, E., Wiley-Kalil, A., Gobbato, E., Maillet, F., Cottaz, S., Samain, E., Venkateshwaran, M., Fort, S., Morris, R.J., Ané, J.-M., Dénarié, J., Oldroyd, G.E.D.: Activation of symbiosis signaling by arbuscular mycorrhizal fungi in legumes and rice. Plant Cell 27, 823–838 (2015)Google Scholar
  9. 9.
    Price, N.P., Relic, B., Talmont, F., Lewin, A., Prome, D., Pueppke, S.G., Maillet, F., Dénarié, J., Prome, J.C., Broughton, W.J.: Broad-host-range Rhizobium species strain NGR234 secretes a family of carbamoylated, and fucosylated, nodulation signals that are O-acetylated or sulphated. Mol. Microbiol. 6(23), 3575–3584 (1992)CrossRefPubMedGoogle Scholar
  10. 10.
    Nicolaou, K.C., Bockovich, N.J., Carcanague, D.R., Hummel, C.W., Even, L.F.: Total synthesis of the NodRm-IV factors, the rhizobium nodulation signals. J. Am. Chem. Soc. 114(22), 8701–8702 (1992)CrossRefGoogle Scholar
  11. 11.
    Bono, J.J., Riond, J., Nicolaou, K.C., Bockovich, N.J., Estevez, V.A., Cullimore, J.V., Ranjeva, R.: Characterization of a binding site for chemically synthesized lipo-oligosaccharidic NodRm factors in particulate fractions prepared from roots. Plant J. 7(2), 253–260 (1995)CrossRefPubMedGoogle Scholar
  12. 12.
    Ikeshita, S., Sakamoto, A., Nakahara, Y., Nakahara, Y., Ogawa, T.: Synthesis of the root nodule-inducing factor NodRm-IV(C16:2, S) of Rhizobium meliloti and related compounds. Tetrahedron Lett. 35(19), 3123–3126 (1994)Google Scholar
  13. 13.
    Tailler, D., Jacquinet, J.-C., Beau, J.-M.: Total synthesis of NodRm(S): a sulfated lipotetrasaccharide symbiotic signal from Rhizobium meliloti. J. Chem. Soc. Chem. Commun. 16, 1827–1828 (1994)CrossRefGoogle Scholar
  14. 14.
    Lai-Xi, W., Chuan, L., Qin-Wei, W., Yong-Zheng, H.: Total synthesis of the sulfated lipooligosaccharide signal involved in Rhizobium meliloti-alfalfa symbiosis. Tetrahedron Lett. 34(48), 7763–7766 (1993)Google Scholar
  15. 15.
    Ikeshita, S., Nakahara, Y., Ogawa, T.: Synthetic studies on the lipooligosaccharide Nod Bj-IV (C18:1, Fuc, Gro) produced by Bradyrhizobium japonicum strain USDA61. Carbohydr. Res. 266(2), C1–C6 (1995)CrossRefPubMedGoogle Scholar
  16. 16.
    Demont-Caulet, N., Maillet, F., Tailler, D., Jacquinet, J.C., Prome, J.C., Nicolaou, K.C., Truchet, G., Beau, J.M., Dénarié, J.: Nodule-inducing activity of synthetic Sinorhizobium meliloti nodulation factors and related lipo-chitooligosaccharides on alfalfa. Importance of the acyl chain structure. Plant Physiol. 120(1), 83–92 (1999)PubMedCentralCrossRefPubMedGoogle Scholar
  17. 17.
    Gressent, F., Drouillard, S., Mantegazza, N., Samain, E., Geremia, R.A., Canut, H., Niebel, A., Driguez, H., Ranjeva, R., Cullimore, J., Bono, J.J.: Ligand specificity of a high-affinity binding site for lipo-chitooligosaccharidic Nod factors in Medicago cell suspension cultures. Proc. Natl. Acad. Sci. U. S. A. 96(8), 4704–4709 (1999)PubMedCentralCrossRefPubMedGoogle Scholar
  18. 18.
    Rasmussen, M.O., Hogg, B., Bono, J.J., Samain, E., Driguez, H.: New access to lipo-chitooligosaccharide nodulation factors. Org. Biomol. Chem. 2(13), 1908–1910 (2004)CrossRefGoogle Scholar
  19. 19.
    Samain, E., Drouillard, S., Heyraud, A., Driguez, H., Geremia, R.A.: Gram-scale synthesis of recombinant chitooligosaccharides in Escherichia coli. Carbohydr. Res. 302, 35–42 (1997)CrossRefPubMedGoogle Scholar
  20. 20.
    Samain, E., Chazalet, V., Geremia, R.A.: Production of O-acetylated and sulfated chitooligosaccharides by recombinant Escherichia coli strains harboring different combinations of nod genes. J. Biotechnol. 72, 33–47 (1999)CrossRefPubMedGoogle Scholar
  21. 21.
    Despras, G., Alix, A., Urban, D., Vauzeilles, B., Beau, J.-M.: From chitin to bioactive chitooligosaccharides and conjugates: access to Lipochitooligosaccharides and the TMG-chitotriomycin. Angew. Chem. Int. Ed. 53(44), 11912–11916 (2014)CrossRefGoogle Scholar
  22. 22.
    Bek, A.S., Sauer, J., Thygesen, M.B., Duus, J.O., Petersen, B.O., Thirup, S., James, E., Jensen, K.J., Stougaard, J., Radutoiu, S.: 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. 23(1), 58–66 (2010)CrossRefPubMedGoogle Scholar
  23. 23.
    Gadella Jr., T.W., Vereb Jr., G., Hadri, A.E., Rohrig, H., Schmidt, J., John, M., Schell, J., Bisseling, T.: Microspectroscopic imaging of nodulation factor-binding sites on living Vicia sativa roots using a novel bioactive fluorescent nodulation factor. Biophys. J. 72(5), 1986–1996 (1997)Google Scholar
  24. 24.
    Goedhart, J., Rohrig, H., Hink, M.A., van Hoek, A., Visser, A.J., Bisseling, T., Gadella Jr., T.W.: Nod factors integrate spontaneously in biomembranes and transfer rapidly between membranes and to root hairs, but transbilayer flip-flop does not occur. Biochemistry 38(33), 10898–10907 (1999)CrossRefPubMedGoogle Scholar
  25. 25.
    Goedhart, J., Hink, M.A., Visser, A.J., Bisseling, T., Gadella Jr., T.W.: In vivo fluorescence correlation microscopy (FCM) reveals accumulation and immobilization of Nod factors in root hair cell walls. Plant J. 21(1), 109–119 (2000)CrossRefPubMedGoogle Scholar
  26. 26.
    Goedhart, J., Bono, J.-J., Bisseling, T., Gadella Jr., T.W.: Identical accumulation and immobilization of sulfated and nonsulfated Nod factors in host and nonhost root hair cell walls. Mol. Plant-Microbe Interact. 16(10), 884–892 (2003)CrossRefPubMedGoogle Scholar
  27. 27.
    Morando, M.A., Nurisso, A., Grenouillat, N., Vauzeilles, B., Beau, J.-M., Cañada, F.J., Jiménez-Barbero, J., Imberty, A.: NMR and molecular modelling reveal key structural features of synthetic nodulation factors. Glycobiology 21(6), 824–833 (2011)CrossRefPubMedGoogle Scholar
  28. 28.
    Ben Amor, B., Shaw, S.L., Oldroyd, G.E., Maillet, F., Penmetsa, R.V., Cook, D., Long, S.R., Dénarié, J., Gough, C.: 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. 34(4), 495–506 (2003)CrossRefGoogle Scholar
  29. 29.
    Madsen, E.B., Madsen, L.H., Radutoiu, S., Olbryt, M., Rakwalska, M., Szczyglowski, K., Sato, S., Kaneko, T., Tabata, S., Sandal, N., Stougaard, J.: A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425(6958), 637–640 (2003)CrossRefPubMedGoogle Scholar
  30. 30.
    Radutoiu, S., Madsen, L.H., Madsen, E.B., Felle, H.H., Umehara, Y., Gronlund, M., Sato, S., Nakamura, Y., Tabata, S., Sandal, N., Stougaard, J.: Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425(6958), 585–592 (2003)CrossRefPubMedGoogle Scholar
  31. 31.
    Arrighi, J.-F., Barre, A., Ben Amor, B., Bersoult, A., Soriano, L.C., Mirabella, R., de Carvalho-Niebel, F., Journet, E.-P., Ghérardi, M., Huguet, T., Geurts, R., Dénarié, J., Rougé, P., Gough, C.: The Medicago truncatula lysin motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol. 142(1), 265–279 (2006)PubMedCentralCrossRefPubMedGoogle Scholar
  32. 32.
    Buist, G., Steen, A., Kok, J., Kuipers, O.P.: LysM, a widely distributed protein motif for binding to (peptido)glycans. Mol. Microbiol. 68(4), 838–847 (2008)CrossRefPubMedGoogle Scholar
  33. 33.
    Zhang, X.-C., Wu, X., Findley, S., Wan, J., Libault, M., Nguyen, H.T., Cannon, S.B., Stacey, G.: Molecular evolution of Lysin motif-type receptor-like kinases in plants. Plant Physiol. 144(2), 623–636 (2007)PubMedCentralCrossRefPubMedGoogle Scholar
  34. 34.
    Lohmann, G.V., Shimoda, Y., Nielsen, M.W., Jörgensen, F.G., Grossmann, C., Sandal, N., Sörensen, K., Thirup, S., Madsen, L.H., Tabata, S., Sato, S., Stougaard, J., Radutoiu, S.: Evolution and regulation of the Lotus japonicus LysM receptor gene family. Mol. Plant-Microbe Interact. 23(4), 510–521 (2010)CrossRefPubMedGoogle Scholar
  35. 35.
    Zhang, X.-C., Cannon, S., Stacey, G.: Evolutionary genomics of LysM genes in land plants. BMC Evol. Biol. 9(183), 183 (2009)PubMedCentralCrossRefPubMedGoogle Scholar
  36. 36.
    Catoira, R., Timmers, A.C., Maillet, F., Galera, C., Penmetsa, R.V., Cook, D., Dénarié, J., Gough, C.: The HCL gene of Medicago truncatula controls Rhizobium-induced root hair curling. Development 128(9), 1507–1518 (2001)PubMedGoogle Scholar
  37. 37.
    Ardourel, M., Demont, N., Debellé, F., Maillet, F., de Billy, F., Prome, J.C., Dénarié, J., Truchet, G.: 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 6, 1357–1374 (1994)PubMedCentralCrossRefPubMedGoogle Scholar
  38. 38.
    Geurts, R., Heidstra, R., Hadri, A.E., Downie, J.A., Franssen, H., Van Kammen, A., Bisseling, T.: Sym2 of pea is involved in a nodulation factor-perception mechanism that controls the infection process in the epidermis. Plant Physiol. 115(2), 351–359 (1997)PubMedCentralPubMedGoogle Scholar
  39. 39.
    Limpens, E., Franken, C., Smit, P., Willemse, J., Bisseling, T., Geurts, R.: LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 302(5645), 630–603 (2003)CrossRefPubMedGoogle Scholar
  40. 40.
    Smit, P., Limpens, E., Geurts, R., Fedorova, E., Dolgikh, E., Gough, C., Bisseling, T.: Medicago LYK3, an entry receptor in rhizobial nodulation factor signaling. Plant Physiol. 145(1), 183–191 (2007)PubMedCentralCrossRefPubMedGoogle Scholar
  41. 41.
    Madsen, E.B., Antolín-Llovera, M., Grossmann, C., Ye, J., Vieweg, S., Broghammer, A., Krusell, L., Radutoiu, S., Jensen, O.N., Stougaard, J., Parniske, M.: Autophosphorylation is essential for the in vivo function of the Lotus japonicus Nod factor receptor 1 and receptor-mediated signalling in cooperation with Nod factor receptor 5. Plant J. 65(3), 404–417 (2011)CrossRefPubMedGoogle Scholar
  42. 42.
    Klaus-Heisen, D., Nurisso, A., Pietraszewska-Bogiel, A., Mbengue, M., Camut, S., Timmers, T., Pichereaux, C., Rossignol, M., Gadella, T.W.J., Imberty, A., Lefebvre, B., Cullimore, J.V.: Structure-function similarities between a plant receptor-like kinase and the human interleukin-1 receptor-associated kinase-4. J. Biol. Chem. 286, 11202–11210 (2011)PubMedCentralCrossRefPubMedGoogle Scholar
  43. 43.
    Mbengue, M., Camut, S., de Carvalho-Niebel, F., Deslandes, L., Froidure, S., Klaus-Heisen, D., Moreau, S., Rivas, S., Timmers, T., Hervé, C., Cullimore, J., Lefebvre, B.: The Medicago truncatula E3 Ubiquitin Ligase PUB1 interacts with the LYK3 symbiotic receptor and negatively regulates infection and nodulation. Plant Cell 22(10), 3474–3488 (2010)PubMedCentralCrossRefPubMedGoogle Scholar
  44. 44.
    Miwa, H., Sun, J., Oldroyd, G.E.D., Downie, J.A.: Analysis of Nod-factor-induced calcium signaling in root hairs of symbiotically defective mutants of Lotus japonicus. Mol. Plant Microbe Interact. 19(8), 914–923 (2006)CrossRefPubMedGoogle Scholar
  45. 45.
    Ehrhardt, D.W., Wais, R., Long, S.R.: Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85(5), 673–681 (1996)CrossRefPubMedGoogle Scholar
  46. 46.
    Morieri, G., Martinez, E.A., Jarynowski, A., Driguez, H., Morris, R., Oldroyd, G.E.D., Downie, J.A.: Host-specific Nod-factors associated with Medicago truncatula nodule infection differentially induce calcium influx and calcium spiking in root hairs. New Phytol. 200(3), 656–662 (2013)Google Scholar
  47. 47.
    Rival, P., de Billy, F., Bono, J.-J., Gough, C., Rosenberg, C., Bensmihen, S.: Epidermal and cortical roles of NFP and DMI3 in coordinating early steps of nodulation in Medicago truncatula. Development 139(18), 3383–3391 (2012)CrossRefPubMedGoogle Scholar
  48. 48.
    Bensmihen, S., de Billy, F., Gough, C.: Contribution of NFP LysM domains to the recognition of Nod Factors during the Medicago truncatula/Sinorhizobium meliloti symbiosis. PLoS ONE 6(11), e26114 (2011)PubMedCentralCrossRefPubMedGoogle Scholar
  49. 49.
    Hayashi, T., Shimoda, Y., Sato, S., Tabata, S., Imaizumi-Anraku, H., Hayashi, M.: Rhizobial infection does not require cortical expression of upstream common symbiosis genes responsible for the induction of Ca2+ spiking. Plant J. 77(1), 146–159 (2014)PubMedCentralCrossRefPubMedGoogle Scholar
  50. 50.
    Madsen, L.H., Tirichine, L., Jurkiewicz, A., Sullivan, J.T., Heckmann, A.B..., Bek, A.S., Ronson, C.W., James, E.K., Stougaard, J.: The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat Commun 1(10) (2010)Google Scholar
  51. 51.
    Broghammer, A., Krusell, L., Blaise, M., Sauer, J., Sullivan, J.T., Maolanon, N., Vinther, M., Lorentzen, A., Madsen, E.B., Jensen, K.J., Roepstorff, P., Thirup, S., Ronson, C.W., Thygesen, M.B., Stougaard, J.: Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding. Proc. Natl. Acad. Sci. U. S. A. 109(34), 13859–13864 (2012)PubMedCentralCrossRefPubMedGoogle Scholar
  52. 52.
    Etzler, M.E., Kalsi, G., Ewing, N.N., Roberts, N.J., Day, R.B., Murphy, J.B.: A Nod factor binding lectin with apyrase activity from legume roots. Proc. Natl. Acad. Sci. U. S. A. 96(10), 5856–5861 (1999)PubMedCentralCrossRefPubMedGoogle Scholar
  53. 53.
    Roberts, N.J., Morieri, G., Kalsi, G., Rose, A., Stiller, J., Edwards, A., Xie, F., Gresshoff, P.M., Oldroyd, G.E.D., Downie, J.A., Etzler, M.E.: Rhizobial and mycorrhizal symbioses in Lotus japonicus require lectin nucleotide phosphohydrolase, which acts upstream of calcium signaling. Plant Physiol. 161(1), 556–567 (2013)PubMedCentralCrossRefPubMedGoogle Scholar
  54. 54.
    Hogg, B.V., Cullimore, J.V., Ranjeva, R., Bono, J.J.: The DMI1 and DMI2 early symbiotic genes of Medicago truncatula are required for a high-affinity nodulation factor-binding site associated to a particulate fraction of roots. Plant Physiol. 140(1), 365–373 (2006)PubMedCentralCrossRefPubMedGoogle Scholar
  55. 55.
    Gressent, F., Mantegazza, N., Cullimore, J.V., Driguez, H., Ranjeva, R., Bono, J.J.: High-affinity Nod factor binding site from Phaseolus vulgaris cell suspension cultures. Mol. Plant Microbe Interact. 15(8), 834–839 (2002)CrossRefPubMedGoogle Scholar
  56. 56.
    Fliegmann, J., Canova, S., Lachaud, C., Uhlenbroich, S., Gasciolli, V., Pichereaux, C., Rossignol, M., Rosenberg, C., Cumener, M., Pitorre, D., Lefebvre, B., Gough, C., Samain, E., Fort, S., Driguez, H., Vauzeilles, B., Beau, J.-M., Nurisso, A., Imberty, A., Cullimore, J., Bono, J.-J.: Lipo-chitooligosaccharidic symbiotic signals are recognized by LysM receptor-like kinase LYR3 in the legume Medicago truncatula. ACS Chem. Biol. 8(9), 1900–1906 (2013)CrossRefPubMedGoogle Scholar
  57. 57.
    Genre, A., Chabaud, M., Balzergue, C., Puech-Pagès, V., Novero, M., Rey, T., Fournier, J., Rochange, S., Bécard, G., Bonfante, P., Barker, D.G.: 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. 198(1), 190–202 (2013)CrossRefPubMedGoogle Scholar
  58. 58.
    Liu, T., Liu, Z., Song, C., Hu, Y., Han, Z., She, J., Fan, F., Wang, J., Jin, C., Chang, J., Zhou, J.-M., Chai, J.: Chitin-induced dimerization activates a plant immune receptor. Science 336(6085), 1160–1164 (2012)CrossRefPubMedGoogle Scholar
  59. 59.
    Wong, J.E.M.M., Midtgaard, S.R., Gysel, K., Thygesen, M.B., Sørensen, K.K., Jensen, K.J., Stougaard, J., Thirup, S., Blaise, M.: An intermolecular binding mechanism involving multiple LysM domains mediates carbohydrate recognition by an endopeptidase. Acta Crystallogr. D Biol. Crystallogr. 71(3), 592–605 (2015)PubMedCentralCrossRefPubMedGoogle Scholar
  60. 60.
    Wan, J., Tanaka, K., Zhang, X.-C., Son, G.H., Brechenmacher, L., Nguyen, T.H.N., Stacey, G.: LYK4, a Lysin motif receptor-like kinase, is important for chitin signaling and plant innate immunity in Arabidopsis. Plant Physiol. 160(1), 396–406 (2012)PubMedCentralCrossRefPubMedGoogle Scholar
  61. 61.
    Cao, Y., Liang, Y., Tanaka, K., Nguyen, C.T., Jedrzejczak, R.P., Joachimiak, A., Stacey, G.: The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1. ELife 3, e03766 (2014)CrossRefGoogle Scholar
  62. 62.
    Sánchez-Vallet, A., Saleem-Batcha, R., Kombrink, A., Hansen, G., Valkenburg, D.-J., Thomma, B.P.H.J., Mesters, J.R.: Fungal effector Ecp6 outcompetes host immune receptor for chitin binding through intrachain LysM dimerization. ELife 2, e00790 (2013)PubMedCentralCrossRefPubMedGoogle Scholar
  63. 63.
    Kaku, H., Nishizawa, Y., Ishii-Minami, N., Akimoto-Tomiyama, C., Dohmae, N., Takio, K., Minami, E., Shibuya, N.: Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc. Natl. Acad. Sci. U. S. A. 103(29), 11086–11091 (2006)PubMedCentralCrossRefPubMedGoogle Scholar
  64. 64.
    Hayafune, M., Berisio, R., Marchetti, R., Silipo, A., Kayama, M., Desaki, Y., Arima, S., Squeglia, F., Ruggiero, A., Tokuyasu, K., Molinaro, A., Kaku, H., Shibuya, N.: Chitin-induced activation of immune signaling by the rice receptor CEBiP relies on a unique sandwich-type dimerization. Proc. Natl. Acad. Sci. U. S. A. 111(3), 404–413 (2014)CrossRefGoogle Scholar
  65. 65.
    Shimizu, T., Nakano, T., Takamizawa, D., Desaki, Y., Ishii-Minami, N., Nishizawa, Y., Minami, E., Okada, K., Yamane, H., Kaku, H., Shibuya, N.: Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J. 64(2), 204–214 (2010)PubMedCentralCrossRefPubMedGoogle Scholar
  66. 66.
    Willmann, R., Lajunen, H.M., Erbs, G., Newman, M.-A., Kolb, D., Tsuda, K., Katagiri, F., Fliegmann, J., Bono, J.-J., Cullimore, J.V., Jehle, A.K., Götz, F., Kulik, A., Molinaro, A., Lipka, V., Gust, A.A., Nürnberger, T.: Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection. Proc. Natl. Acad. Sci. U. S. A. 108(49), 19824–19829 (2011)PubMedCentralCrossRefPubMedGoogle Scholar
  67. 67.
    Miyata, K., Kozaki, T., Kouzai, Y., Ozawa, K., Ishii, K., Asamizu, E., Okabe, Y., Umehara, Y., Miyamoto, A., Kobae, Y., Akiyama, K., Kaku, H., Nishizawa, Y., Shibuya, N., Nakagawa, T.: Bifunctional plant receptor, OsCERK1, regulates both chitin-triggered immunity and arbuscular mycorrhizal symbiosis in rice. Plant Cell Physiol. 55, 1864–1872 (2014)CrossRefPubMedGoogle Scholar
  68. 68.
    Gough, C., Jacquet, C.: Nod factor perception protein carries weight in biotic interactions. Trends Plant Sci. 18(10), 566–574 (2013)CrossRefPubMedGoogle Scholar
  69. 69.
    Radutoiu, S., Madsen, L.H., Madsen, E.B., Jurkiewicz, A., Fukai, E., Quistgaard, E.M., Albrektsen, A.S., James, E.K., Thirup, S., Stougaard, J.: LysM domains mediate lipochitin-oligosaccharide recognition and Nfr genes extend the symbiotic host range. EMBO J. 26(17), 3923–3935 (2007)PubMedCentralCrossRefPubMedGoogle Scholar
  70. 70.
    De Mita, S., Streng, A., Bisseling, T., Geurts, R.: Evolution of a symbiotic receptor through gene duplications in the legume–rhizobium mutualism. New Phytol. 201(3), 961–972 (2013)CrossRefPubMedGoogle Scholar
  71. 71.
    Op den Camp, R., Streng, A., De Mita, S., Cao, Q., Polone, E., Liu, W., Ammiraju, J.S.S., Kudrna, D., Wing, R., Untergasser, A., Bisseling, T., Geurts, R.: LysM-type mycorrhizal receptor recruited for Rhizobium symbiosis in nonlegume Parasponia. Science 331(6019), 909–912 (2011)CrossRefGoogle Scholar
  72. 72.
    Gomez, S.K., Javot, H., Deewatthanawong, P., Torres-Jerez, I., Tang, Y., Blancaflor, E., Udvardi, M., Harrison, M.: Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis. BMC Plant Biol. 9(1), 10 (2009)PubMedCentralCrossRefPubMedGoogle Scholar
  73. 73.
    De Mita, S., Streng, A., Bisseling, T., Geurts, R.: Evolution of a symbiotic receptor through gene duplications in the legume-rhizobium mutualism. New Phytol. 201(3), 961–972 (2014)CrossRefPubMedGoogle Scholar
  74. 74.
    Zhang, X., Dong, W., Sun, J., Feng, F., Deng, Y., He, Z., Oldroyd, G.E.D., Wang, E.: The receptor kinase CERK1 has dual functions in symbiosis and immunity signalling. Plant J. 81(2), 258–267 (2015)CrossRefPubMedGoogle Scholar
  75. 75.
    Nakagawa, T., Kaku, H., Shimoda, Y., Sugiyama, A., Shimamura, M., Takanashi, K., Yazaki, K., Aoki, T., Shibuya, N., Kouchi, H.: From defense to symbiosis: limited alterations in the kinase domain of LysM receptor-like kinases are crucial for evolution of legume–Rhizobium symbiosis. Plant J. 65(2), 169–180 (2011)CrossRefPubMedGoogle Scholar
  76. 76.
    Delaux, P.-M., Séjalon-Delmas, N., Bécard, G., Ané, J.-M.: Evolution of the plant-microbe symbiotic “toolkit”. Trends Plant Sci. 18(6), 298–304 (2013)CrossRefPubMedGoogle Scholar
  77. 77.
    Liang, Y., Tóth, K., Cao, Y., Tanaka, K., Espinoza, C., Stacey, G.: Lipochitooligosaccharide recognition: an ancient story. New Phytol. 204(2), 289–296 (2014)CrossRefPubMedGoogle Scholar
  78. 78.
    Maolanon, N.N., Blaise, M., Sørensen, K.K., Thygesen, M.B., Cló, E., Sullivan, J.T., Ronson, C.W., Stougaard, J., Blixt, O., Jensen, K.J.: Lipochitin oligosaccharides immobilized through oximes in glycan microarrays bind LysM proteins. ChemBioChem 15, 425–434 (2014)CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.INRA, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR441Castanet-TolosanFrance
  2. 2.CNRS, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR2594Castanet-TolosanFrance

Personalised recommendations