ROLE OF SIGNAL EXCHANGE IN CONTROL OF RHIZOBIUM - LEGUME SYMBIOSIS SPECIFICITY



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Abstract

The signal molecules produced by legume plants and soil bacteria rhizobia and involved in early steps of symbiosis regulation were identified through the evaluation of molecular mechanisms of plant-rhizobia communication. The molecular dialog between plants and rhizobia is initiated by plant flavanoids inducing the synthesis and secretion of lipochitooligosaccharide molecules Nod factors by rhizobial bacteria. Nod factors are N-acetylglucosamine oligomers, modified by fatty acid and certain chemical groups. Nod factors trigger a set of plant reactions resulting in a formation of root nodules - nitrogen fixing symbiotic organs. Fine chemical structure of signal molecules determines host specificity of the symbiosis. Nod factors are active in low concentrations and possess mitogenic and morphogenic activity, therefore they are recognized as the new class of growth regulators. In this paper the modern data about study of Nod factor perception mechanisms and signal transduction pathway in legume plants are presented and considered with perspective for future application of these knowledge for practical increasing of symbiosis efficiency from plant side. This work was supported by RFBR 07-08-00700a (Russian Foundation of Basic Research), CRDF RUXO-012-ST-06 (BP2M12) and HIII-5399. 2008. 4, RFBR-NWO (06-04-89000-НВОЦ-а) grants.

About the authors

Elena A Dolgikh

All-Russia Research Institute for Agricultural Microbiology, St. Petersburg, RF

Email: dol2helen@yahoo.com

Irina V Leppyanen

All-Russia Research Institute for Agricultural Microbiology, Saint-Petersburg, RF

Email: leppyanen_irina@rambler.ru

Maria A Osipova

Saint Petersburg State University, Saint-Petersburg, RF

Email: mary_osipova@mail.ru Universitetskaya nab., 7/9, Saint-Petersburg, 199034, Russia

Igor A Tikhonovich

All-Russia Research Institute for Agricultural Microbiology, Saint-Petersburg, RF

Email: arriam@arriam.spb.ru. contact@arriam.spb.ru Podbelskiy Ch., 3, Saint-Petersburg, Pushkin-8

References

  1. Ane J.M., Kiss G.B., Riely B.K. et al., 2004. Medicago trancatula DMI1 required for bacterial and fungal symbioses in legumes//Science. Vol. 303, P. 1364-1367.
  2. Albrecht C., Geurts R., Lapeyrie F., Bisseling T., 1998. Endomycorrhizae and rhizobial Nod factors both require SYM8 to induce the expression of the early nodulin genes PseNOD5 and PseNOD12A//The Plant Journal. Vol. 15, N 5, P. 605-614.
  3. Ardourel M., Demont N., Debelle F.D. et al., 1994. 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, P. 1357-1374.
  4. Arrighi J.F., barre A., ben Amor B. et al., 2006. The Medicago trancatula lysine motif-receptorlike kinase gene family includes NFP and new noduleexpressed genes//Plant Physiology. Vol. 142, P. 265-279.
  5. Ben Amor B., Shaw S.L., Oldroyd G.E.D. et al., 2003. The NFP locus of Medicago trancatula controls an early step of Nod factor signal transduction upstream of a rapid calcium flux and root hair deformation//Plant J. Vol. 34, P. 1-12.
  6. Bateman A, Bycroft M., 2000. The structure of a LysM domain from E. coli membrane bound lytic murein transglycosylase D (MltD)//J. Mol Biol. Vol. 299, P. 1113-1119.
  7. Borisov A.Y., Barmicheva E.M., Jacobi L.M. et al., 2000. Pea (Pisum sativum L.) mendelian genes controlling development of nitrogen-fixing nodules and arbuscular mycorrhiza//Czech J. Genet Plant Breed. Vol. 36, P. 106-110.
  8. Borisov A.Y., Danilova T.N., Koroleva T.A. et al., 2007. Regulatory genes of garden pea (Pisum sativum L.) controlling the development of nitrogen-fixing nodules and arbuscular mycorrhiza: a review of basic and applied aspects//Applied Biochemistry and Microbiology. Vol. 43, N 3, P. 237-243.
  9. Boller T., 1995. Chemoperception of microbial signals in plant cells//Annual Review of Plant Physiology and Plant Molecular Biology. Vol. 46, P. 189-214.
  10. Caetano-Anolles G., Gresshoff P.M., 1991. Plant genetic control of nodulation//Annu. Rev. Microbiol. Vol. 45. P. 345-382.
  11. 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. Vol. 12, P. 1647-1665.
  12. Charron D., Pingret J.L., Chabaud M., et al., 2004. Pharmacological evidence that multiple phospholipid signaling pathways link Rhizobium nodulation factor perception in Medicago trancatula root hairs to intracellular responses, including Ca2+ spiking and specific ENOD gene expression//Plant Physiol. Vol. 136, P. 3582-3593.
  13. Cook D., Dreyer D., Bonnet D. et al., 1995. Transient induction of a peroxidase gene in Medicago trancatula precedes infection by Rhizobium meliloti//Plant Cell. Vol. 7, P. 43-55.
  14. Denarie J., Debelle F., Prome J.C., 1996. Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis//Annu. Rev. Biochem. Vol. 65, P. 503-535.
  15. De Ruijter N.C. A., Bisseling T., Emons A.M. C., 1999. Rhizobium Nod factors induce an increase in sub-apical fine bundles of actin filaments in Vicia sativa root hairs within minutes//Mol. Plant Microbe Interact. Vol. 12, P. 829-832.
  16. Ehrhardt D.W., Atkinson E.M., Long S.R., 1992. Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors//Science. Vol. 256, P. 998-1000.
  17. Ehrhardt D.W., Wais R., Long S.R., 1996. Calcium spiking in plant root hairs responding to Rhizobium nodulation signals//Cell. Vol, 85. P. 673-681.
  18. Endre G., Kereszt A., Kevei Z. et al., 2002. A receptor kinase gene regulating symbiotic nodule development//Nature. Vol. 417, P. 962-966.
  19. Engstrom E.M., Ehrhardt D.W., Mitra R.M., Long S.R., 2002. Pharmacological analysis of Nod factor-induced calcium spiking in Medicago truncatula: evidence for the requirement of type IIA calcium pumps and phosphoinositide signaling//Plant Physiol. Vol. 128, P. 1390-1401.
  20. Felle H.H., Kondorosi E., Kondorosi A., Schultze M. 1999. Nod factors modulate the concentration of cyto solic free calcium differently in growing and non-growing root hairs of Medicago sativa L.//Planta. Vol. 209, P. 207-212.
  21. Geurts R., Heidstra R., Hadri A-E. et al., 1997. Sym2 of Pisum sativum is involved in Nod factor perception mechanism that controls the infection process in the epidermis//Plant Physiology. Vol. 115, P. 351-359.
  22. Geurts R., Fedorova E., Bisseling T., 2005. Nod factor signaling genes and their functioning in early stages of Rhizobium infection//Curr. Opin. Plant Biol. Vol. 8, P. 346-352.
  23. Gleason C., Chaudhuri S., Yang T.B., 2006. Nodulation independent of rhizobia induced by a calcium activated kinase lacking autoinhibition//Nature. Vol. 441, P. 1149-1152.
  24. Gianinazzi-Pearson V., 1996. Plant cell responses to arbuscular mycorrhizal fungi: getting to the roots of the symbiosis//Plant Cell. Vol. 8, P. 1871-1883.
  25. Harris J.M., Wais R., Long S.R., 2003. Rhizobium-induced calcium spiking in Lotus japonicus//Mol. Plant Microbe Interact. Vol. 16, P. 335-341.
  26. Heckmann A.B., Lombardo F., Miwa H. et al., 2006. Lotus japonicus nodulation requires two GRAS domain regulators, one of which is functionally conserved in a non-legume//Plant Physiology. Vol. 142, P. 1739-1750.
  27. Horvath B., Heidstra R., Lados M., et al., 1993. Lipooligosaccharides of Rhizobium induce infection related early nodulin gene expression in pea root hairs//Plant J. Vol. 4, P. 727-733.
  28. Imaizumi-Anraku H., Takeda N., Charpentier M. et al., 2005. Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots//Nature. Vol. 433, P. 527-531.
  29. Journet E.P., El-Gachtouli N., Vernoud V. et al., 2001. Medicago trancatula ENOD11: A novel RPRP-encoding early nodulin gene expressed during mycorrhization in arbuscule-containing cells//Mol. Plant Microbe Interact. Vol. 14, N 6, P. 737-748.
  30. Kalo P., Gleason C., Edwards A. et al., 2005. Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators//Science. Vol. 308, P. 1786-1789.
  31. Kanamori N., Madsen L.H., Radutoiu S. et al., 2006. A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis//Proc. Natl. Acad. Sci. USA. Vol. 103, N 2, P. 359-364.
  32. Kistner C., Winzer T., Pitzschke A. et al., 2005. Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis//Plant Cell. Vol. 17, P. 2217-2229.
  33. Lerouge P., Roche P., Faucher C. et al., 1990. Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal//Nature. Vol. 19, P. 781-784.
  34. Levy J., Bres C., Geurts R. et al., 2004. A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses//Science. Vol. 303, P. 1361-1363.
  35. Limpens E., Franken C., Smit P. et al., 2003. LysM domain receptor kinases regulating rhizobial Nod factorinduced infection//Science. Vol. 302, P. 630-633.
  36. Long S.R., 1996. Rhizobium symbiosis: Nod factors in perspective//Plant Cell. Vol. 8, P. 1885-1898.
  37. Lombardo F., Heckmann A.B., Miwa H. et al., 2006. Identification of symbiotically defective mutants of Lotus japonicus affected in infection thread growth//Mol. Plant Microbe Interact. Vol. 19, N 12, P. 1444-1450.
  38. Madsen E.B., Madsen L.H., Radutoiu S. et al., 2003. A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals//Nature. Vol. 425, P. 637-640.
  39. Marsh J.F., Rakocevic A., Mitra R.M. et al., 2007. Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase//Plant Physiology. Vol. 144, P. 324-335.
  40. Mitra R.M., Shaw S.L., Long S.R., 2004. Six nonnodulating plant mutants defective for Nod factor-induced transcriptional changes associated with the legumerhizobia symbiosis//Proc. Natl. Acad. Sci. USA. Vol. 101, P. 4701-4705.
  41. Miwa H., Sun J., Oldroyd G.E. D., Downie J.A., 2006. Analysis of Nod-factor-induced calcium signaling in root hairs of symbiotically defective mutants of Lotus japonicus//Mol. Plant Microbe Interact. Vol. 19, N 8, P. 914-923.
  42. Mulder L., Lefebvre B., Cullimore J., Imberty A., 2006. LysM domains of Medicago truncatula NFP protein involved in Nod factor perception. Glycosylation state, molecular modeling and docking of chitooligosaccharides and Nod factors//Glycobiology. Vol. 16, N 9, P. 801-809.
  43. Oldroyd G.E., engstrom E.M., Long S.R., 2001. Ethylene inhibits the Nod factor signal transduction pathway of of Medicago trancatula//Plant Cell. Vol. 13, P. 1835-1849.
  44. Oldroyd G.E., Long S.R., 2003. Identification and characterization of Nodulation-Signaling Pathway 2, a gene of Medicago truncatula involved in Nod factor signaling//Plant Physiol. Vol. 131, P. 1027-1032.
  45. Parniske M., 2004. Molecular genetics of the arbuscular mycorrhizal symbiosis//Curr. Opin. Plant Biol. Vol. 7, P. 414-421.
  46. Perret X., Staehelin C., Broughton W.J., 2000. Molecular basis of symbiotic promiscuity//Microbiol Mol Biol Rev. Vol. 64, N 1, P. 180-201.
  47. Radutoiu S., Madsen L.H., Madsen E.B., 2003. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases//Nature. Vol. 425, P. 569-570.
  48. Schauser L., Wieloch W., Stougaard J., 1999. A plant regulator controlling development of symbiotic root nodules//Nature. Vol. 402. P. 191-195.
  49. Schneider A., Walker S.A., Poyser S. et al., 1999. Genetic mapping and functional analysis of a nodulationdefective mutant (sym19) of pea (Pisum sativum L.)//Mol. Gen. Genet. Vol. 262, P. 1-11.
  50. Schultze M., Kondorosi A., 1998. Regulation of symbiotic root nodule development//Annu Rev. Genet. Vol. 32, P. 33-57.
  51. Smit P., Raedts J., Portyanko V. et al., 2005. NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription//Science. Vol. 308, P. 1789-1790.
  52. Smit P., Limpens E., Geurts R. et al., 2007. Medicago LYK3 an Entry Receptor in Rhizobial Nod Factor Signaling//Plant Physiology. Vol. 145, N 1, P. 183-191.
  53. Spaink H.P., Sheeley D.M., van Brussel A.A.N. et al., 1991. A novel highly unsaturated fatty acid moiety of lipooligosaccharide signals determines host specificity of Rhizobium//Nature. Vol. 354, P. 125-130.
  54. Stokkermans T.J. W., Peters N.K., 1994. Bradyrhizobium elkanii lipo-oligosaccharide signals induce complete nodule structures on Glycine soja Siebold et. Zucc.//Planta. Vol. 193, P. 413-420.
  55. Stracke S., Kistner C., Yoshida S. et al., 2002. A plant receptor-like kinase required for both bacterial and fungal symbiosis//Nature. Vol. 417. P. 959-961.
  56. Tirichine L., Imaizumi-Anraku H., Yoshida S. et al.,, 2006. Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development//Nature. Vol. 441, P. 1153-1156.
  57. Tsyganov V.E., Voroshilova V.A., Priefer U.B. et al., 2002. Genetic dissection of the initiation of the infection process and nodule tissue development in the Rhizobiumpea (Pisum sativum L.) symbiosis//Annals of Botany. Vol. 89, P. 357-366.
  58. Truchet G., Roche P., Lerouge P. et al., 1991. Sulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa//Nature. Vol. 351. P. 670-673.
  59. Van Brussel A.A. N., Bakhuizen R., Van Spronsen P.C. et al., 1992. Induction of preinfection thread structures in the leguminous host plant by mitogenic lipooligosaccharides of Rhizobium//Science. Vol. 257, P. 70-72.
  60. Wais R.J., Galera C., Oldroyd G. et al., 2000. Genetic analysis of calcium spiking responses in nodulation mutants of Medicago trancatula//Proc. Natl. Acad. Sci. USA. Vol. 97. P. 13407-13412.
  61. Walker S.A., Viprey V., Downie J.A. 2000. Dissection of nodulation signaling using pea mutants defective for calcium spiking induced by Nod factors and chitin oligomers//Proc. Natl. Acad. Sci. USA. Vol. 97, P. 13413-14418.
  62. Yahyaoui F.E., Kuster H., Ben Amor B. et al., 2004. Expression profiling in Medicago trancatula identifies more than 750 genes differently expressed during nodulation, including many potential regulators of the symbiotic program//Plant Physiology. Vol. 136, P. 3159-3176.
  63. Yano K., Tansengco M.L., Hio T. et al., 2006. New nodulation mutants responsible for infection thread development in Lotus japonicus//Mol. Plant Microbe Interact. Vol. 19, N 7, P. 801-810.
  64. Zhukov V.A., Borisov A.Y., Kuznetsova E.V., et al., 2007. Genome synteny of pea and model legumes: from mutations through genetic mapping to the genes//15th International Congress on Nitrogen Fixation & 12th International Conference of the African Association for Biological Nitrogen Fixation, Book of abstracts, Cape Town, South Africa. P. 62.

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Copyright (c) 2008 Dolgikh E.A., Leppyanen I.V., Osipova M.A., Tikhonovich I.A.

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