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Plant Molecular Evolution pp 181–194Cite as

The evolution of nodulation

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Abstract

In this review we will first describe the different steps leading to nodule formation, and these will be compared with processes of non-symbiotic plant development and growth. In general, aspects of both actinorhizal as well as rhizobial symbiosis are described, but in several cases, the emphasis will be on the Rhizobium-legume symbiosis because more knowledge of this system is available. Subsequently, the phylogeny of nodulating plants is described and a comparison is made between several aspects of legume and actinorhizal nodulation. At the end of this paper the relationship between nodule symbiosis and endomycorrhizal symbiosis is described, and it is discussed to what extent the development of root nodules involves unique properties, or whether processes and genes have been recruited from common plant development and the endomycorrhizal symbiosis.

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References

  1. Albrecht C, Geurts R, Lapeyrie F, Bisseling T: Endomyc-orrhizae and rhizobial Nod factors both require SYM8 to induce expression of the early nodulin genes PsENOD5 and PsENOD12A. Plant J 15: 605–614 (1998).

    Article  CAS  Google Scholar 

  2. Andersson CA, Llewellyn DJ, Peacock WJ, Dennis ES: Cell-specific expression of the promoters of two nonlegume haemoglobin genes in transgenic legume, Lotus corniculatus. Plant Physiol 113: 45–57 (1997).

    Article  PubMed  CAS  Google Scholar 

  3. Appleby CA, Tjepkema JD, Trinick MJ: Haemoglobin in a non-leguminous plant, Parasponia: possible genetic origin and function in nitrogen fixation. Science 220: 951–953 (1983).

    Article  PubMed  CAS  Google Scholar 

  4. Basset B, Goodman RN, Novacky A: Ultrastructure of soybean nodules. I. Release of rhizobia from the infection thread. Can J Microbiol 23: 573–582 (1977).

    Article  Google Scholar 

  5. Benson DR, Silvester WB: Biology of Frankia strains, actino-mycete symbionts of actinorhizal plants. Microbiol Rev 57: 293–319 (1993).

    PubMed  CAS  Google Scholar 

  6. Bergman B, Rai AN, Johansson C, Soderback E: Cyanobacterial-plant symbiosis. Symbiosis 14: 61–81 (1992).

    Google Scholar 

  7. Berry AM, Sunell LA: The infection process and nodule development. In: Schwintzer CR, Tjepkema JD (eds.), The Biology of Frankia and Actinorhizal Plants, pp. 61–68. Academic Press, New York (1990).

    Google Scholar 

  8. Bogusz D, Appleby CA, Landsmann J, Dennis ES, Trinick MJ, Peacock WJ: Functioning haemoglobin genes in non-nodulating plants. Nature 331: 178–180 (1988).

    Article  PubMed  CAS  Google Scholar 

  9. Carlson RW, Price NPJ, Stacey G: The biosynthesis of rhizobial lipo-oligosaccharide signal molecules. Mol Plant-Microbe Interact 7: 684–695 (1994).

    Article  PubMed  CAS  Google Scholar 

  10. Chandler MR, Date RA, Roughley RJ: Infection and root nodule development in Stylosanthes species by Rhizobium. J Exp Bot 33: 47–57 (1982).

    Article  Google Scholar 

  11. Chase MW, Soltis DE, Olmstead RG, Morgan D, Les DH, Mishler BD, et al.: Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid gene rbcL. nn Miss Bot Gard 80: 528–580 (1993).

    Article  Google Scholar 

  12. Cronquist A: An Integrated System of Classification of Flowering Plants. Columbia University Press, New York (1981).

    Google Scholar 

  13. Dart PJ: The infection process. In: Quispel A (eds), The Biology of Nitrogen Fixation, pp. 381–429. North Holland Publishing Co., Amsterdam (1974).

    Google Scholar 

  14. de Faria SM, Hay GT, Sprent JI: Entry of rhizobia into roots of Mimosa scabrella Bentham occurs between epidermal cells. J Gen Microbiol 134: 2291–2296 (1988).

    Google Scholar 

  15. de Jong AJ, Heidstra R, Spaink HP, Hartog MV, Meijer EA, Hendriks T, Lo Schiavo F, Terzi M, Bisseling T, van Kammen A, de Vries SC: Rhizobium lipo-oligosaccharides rescue a carrot somatic embryo variant. Plant Cell 5: 615–620 (1993).

    PubMed  Google Scholar 

  16. Dénarié J, Cullimore J: Lipo-oligosaccharide nodulation factors: a new class of signaling molecules mediating recognition and morphogenesis. Cell 74: 951–954 (1993).

    Article  PubMed  Google Scholar 

  17. Dénarié J, Debelle F, Prome JC: Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu Rev Biochem 65: 503–535 (1996).

    Article  PubMed  Google Scholar 

  18. Doyle JJ: Phylogenetic perspectives on nodulation: evolving views of plants and symbiotic bacteria. Trends Plant Sci 3(12): 473–478 (1998).

    Article  Google Scholar 

  19. Duc G, Trouvelot A, Gianinazzi-Pearson V, Gianinazzi S: First report of non-mycorrhizal plant mutants (myc-) obtained in pea (Pisum sativum) and fababean (Vicia faba L.). Plant Sci 60: 215–222 (1989).

    Article  Google Scholar 

  20. Fisher RF, Long SR: Rhizobium-plant signal exchange. Nature 357: 655–660 (1992).

    Article  PubMed  CAS  Google Scholar 

  21. Franche C, Diouf D, Laplaze L, Auguy F, Frutz T, Rio M, Duhoux E, Bogusz D: Soybean (lbc3), Parasponia, and Trema haemoglobin gene promoters retain symbiotic and nonsymbiotic specificity in transgenic Casuarinaceae: implications for haemoglobin gene evolution and root nodule symbiosis. Mol Plant-Microbe Interact 11: 887–894 (1998).

    Article  CAS  Google Scholar 

  22. Franssen HJ, Vijn I, Yang WC, Bisseling T: Developmental aspects of the Rhizobium-legume symbiosis. In: Schilperoort R, Dure L (eds), 10 Years Plant Molecular Biology. Plant Mol Biol 19: 89-107 (1992).

    Google Scholar 

  23. Fruhling M, Roussel H, Gianinazzi-Pearson V, Puhler A, Perlick AM: The Vicia faba leghaemoglobin gene VfLb29 is induced in root nodules and in roots colonized by the arbuscular micorrhizal fungus Glomus fasciculatum. Mol Plant-Microbe Interact 10: 124–131 (1997).

    Article  PubMed  CAS  Google Scholar 

  24. Geremia RA, Mergaert P, Geelen D, Van Montagu M, Holsters M: The NodC protein of Azorhizobium caulinodans is an N-acetylglucosaminyltransferase. Proc Natl Acad Sci USA 91: 2669–2673 (1994).

    Article  PubMed  CAS  Google Scholar 

  25. Gianinazzi-Pearson V: Plant cell responses to arbuscular mycorrhizal fungi: getting to the roots of the symbiosis. Plant Cell 8: 1871–1883 (1996).

    PubMed  Google Scholar 

  26. Hadri A-E, Spaink HP, Bisseling T, Brewin NJ: Diversity of root nodulation and rhizobial infection processes. In: Spaink HP, Kondorosi A, Hooykaas PJJ (eds), The Rhizobi-aceae, pp. 347–359. Kluwer Academic Publishers, Dordrecht, Netherlands (1998).

    Google Scholar 

  27. Harrison MJ: The arbuscular mycorrhizal symbiosis: an underground association. Trends Plant Sci 2: 54–60 (1997).

    Article  Google Scholar 

  28. Heidstra R, Bisseling T: Nod factor-induced host responses and mechanism of Nod factor perception. New Phytol 133: 25–43 (1996).

    Article  CAS  Google Scholar 

  29. Heidstra R, Yang WC, Yalcin Y, Peck S, Emons AM, van Kammen A, Bisseling T: Ethylene provides positional information on cortical cell division but is not involved in Nod factor-induced root hair tip growth in Rhizobium-legume interaction. Development 124: 1781–1787 (1997).

    PubMed  CAS  Google Scholar 

  30. Huss-Danell K, Bergman B: Nitrogenase in Frankia from root nodules of Alnus incana (L.) Moench: Immunolocalization of the Fe-and MoFe-proteins during vesicle differentiation. New Phytol 116: 443–455 (1990).

    Article  Google Scholar 

  31. Jacobsen-Lyon K, Jensen EØ, Jorgensen J, Marker KA, Peacock WJ, Dennis ES: Symbiotic and non-symbiotic haemoglobin genes of Casuarina glauca. Plant Cell 7: 213–222 (1995).

    PubMed  CAS  Google Scholar 

  32. James EK, Sprent JI, Sutherland JM, Mclnroy SG, Minchin FR: The structure of nitrogen fixing root nodules on the aquatic mimosoid legume Neptunia plena. Ann Bot 69: 173–180 (1992).

    Google Scholar 

  33. John M, Rôhring H, Schmidt J, Wieneke U, Schell J: Rhizobium NodB protein involved in nodulation signal synthesis is a chitooligosaccharide deacetylase. Proc Natl Acad Sci USA 90: 625–629 (1993).

    Article  PubMed  CAS  Google Scholar 

  34. Kijne JW: The Rhizobium infection process. In: Stacey G, Burris RH, Evans HJ (eds), Biological Nitrogen Fixation, pp. 349–398, Chapman and Hall, New York (1992).

    Google Scholar 

  35. Lancelle SA, Torrey JG: Early development of Rhizobium-induced root nodules of Parasponia rigida. II. Nodule morphogenesis and symbiotic development. Can J Bot 63: 25–35 (1984)

    Article  Google Scholar 

  36. Landsmann J, Dennis ES, Higgins TJ, Appleby CA, Kortt AA, Peacock WJ: Common evolutionary origin of legume and non-legume plant haemoglobins. Nature 324: 166–168 (1986)

    Article  CAS  Google Scholar 

  37. Laplaze L. Unpublished results.

    Google Scholar 

  38. LaRue TA, Weeden NF: The Symbiosis Genes of the Host. In: Kiss GB, Endre G (eds), Proceedings of the 1st European Nitrogen Fixation Conference, pp. 147–151. Officina Press, Szeged, Hungary (1994).

    Google Scholar 

  39. Lee KH, LaRue TA: Exogenous ethylene inhibits nodulation of Pisum sativum L. cv. Sparckle. Plant Physiol 100: 1759–1763 (1992).

    Article  CAS  Google Scholar 

  40. Libbenga KR, Harkes PAA: Initial proliferation of cortical cells in the formation of root nodules in Pisum sativum L. Planta 114: 17–28 (1973).

    Article  Google Scholar 

  41. Libbenga KR, van Iren F, Bogers RJ, Schraag-Lamers MF: The role of hormones and gradients in the initiation of cortex proliferation and nodule formation in Pisum sativum L. Planta 114: 29–39 (1973).

    Article  CAS  Google Scholar 

  42. Marvel DJ, Torrey JG, Ausubel FM: Rhizobium symbiotic genes required for nodulation of legume and nonlegume hosts. Proc Natl Acad Sci USA 84: 1319–1323 (1987).

    Article  PubMed  CAS  Google Scholar 

  43. Miller IM, Baker DD: The initiation, development and structure of root nodules in Elaeagnus angustifolia L. (Elaeagnaceae). Protoplasma 128: 107–119 (1985).

    Article  Google Scholar 

  44. Naisbitt T, James EK, Sprent JI: The evolutionary significance of the genus Chamaecrista, as determined by nodule structure. New Phytol 122: 487–492 (1992).

    Article  Google Scholar 

  45. Newcomb W: Nodule morphogenesis and differentiation. Int Rev Cytol 13 (suppl): S247–S297 (1981).

    Google Scholar 

  46. Patriarca EJ, Tate R, Riccio A, Fedorovoa E, Defez R, Iaccarino M: Down-regulation of the Rhizobium ntr system in the determinate nodule of Phaseolus vulgaris identifies a specific developmental zone. Mol Plant-Microbe Interact 9: 243–251 (1996).

    Article  CAS  Google Scholar 

  47. Pawlowsky K, Bisseling T: Rhizobial and actinorhizal symbioses: what are the shared features? Plant Cell 8: 1899–1913 (1996).

    Google Scholar 

  48. Penmetsa RV, Cook DR: A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science 275: 527–530 (1997).

    Article  PubMed  CAS  Google Scholar 

  49. Racette S, Torrey JG: Root nodule initiation in Gymnostoma (Casuarinaceae) and Shepherdia (Elaeagnaceae) induced by Frankia strain HFPGpl1. Can J Bot 67: 2873–2879 (1989).

    Article  Google Scholar 

  50. Reddy PM, Ladha JK, Ramos MC, Maillet F, Hernandez RJ, Torrizo LB, Oliva NP, Datta SK: Rhizobial lipochitooligosac-charide nodulation factors activate expression of the legume early nodulation gene ENOD12 in rice. Plant J 14: 693–702 (1998).

    Article  CAS  Google Scholar 

  51. Ribeiro A, Akkermans ADL, van Kammen A, Bisseling T, Pawlowsky K: A nodule-specific gene encoding a subtilisin-like protease is expressed in early stages of actinorhizal nodule development. Plant Cell 7: 785–794 (1995).

    PubMed  CAS  Google Scholar 

  52. Rôhring H, Schmidt J, Wieneke U, Kondorosi E, Barlier I, Schell J, John M: Biosynthesis of lipooligosaccharide nodulation factors: Rhizobium NodA protein is involved in N-acylation of the chitooligosaccaride backbone. Proc Natl Acad Sci USA 91: 3122–3126 (1994).

    Article  Google Scholar 

  53. Roth LE, Stacey G: Bacterium release into host cells of nitrogen-fixing soybean nodules: the symbiosome membrane comes from three sources. Eur J Cell Biol 49: 13–23 (1989).

    PubMed  CAS  Google Scholar 

  54. Sagan M, Morandi D, Tarenghi E, Duc G: Selection of nodulation and mycorrhizal mutants in the model plant Medicago truncatula (Gaertn.) after γ-ray mutagenesis. Plant Sci 111: 63–71 (1995).

    Article  CAS  Google Scholar 

  55. Schell J, Schmidt J, Waiden R: Notice. Trends Plant Sci 3: 130 (1998).

    Google Scholar 

  56. Schwintzer CR, Berry AM, Disney LD: Seasonal patterns of root nodule growth, endophyte morphology, nitrogenase activity and shoot development in Myrica gale. Can J Bot 60: 746–757 (1982).

    Article  Google Scholar 

  57. Shirtliffe SJ, Vessey JK: A nodulation (Nod+/Fix-) mutant of Phaseolus vulgaris L. has nodule like structures lacking peripheral vascular bundles (Pbv-) and is resistant to mycorrhyzal infection (Myc-). Plant Sci 118: 209–220 (1996).

    Article  CAS  Google Scholar 

  58. Smit G, de Koster CC, Schripsema J, Spaink HP, van Brussel AAN, Kijne JW: Uridine, a cell division factor in pea roots. Plant Mol Biol 29: 869–873 (1995).

    Article  PubMed  CAS  Google Scholar 

  59. Smith FA, Smith SE: Structural diversity in (vesicular)-arbuscular mycorrhizal symbioses. New Phytol 137: 373–388 (1997).

    Article  Google Scholar 

  60. Soltis DE, Soltis PS, Morgan DR, Swensen SM, Mullin BC, Dowd JM, Martin PG: Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proc Natl Acad Sci USA 92: 2647–2651 (1995).

    Article  PubMed  CAS  Google Scholar 

  61. Spaink HP: Rhizobial lipo-oligosaccharides: answers and questions. Plant Mol Biol 20: 977–986 (1992).

    Article  PubMed  CAS  Google Scholar 

  62. Subba-Rao NS, Mateos PF, Baker D, Pankratz HS, Palma J, Dazzo FB, Sprent JI: The unique root-nodule symbiosis between Rhizobium and the aquatic legume, Neptunia natans (L.F.) Druce. Planta 196: 311–320 (1995).

    Article  CAS  Google Scholar 

  63. Swensen SM: The evolution of actinorhizal symbiosis: evidence for multiple origins of the symbiotic association. Am J Bot 83: 1503–1512 (1996).

    Article  Google Scholar 

  64. Taylor ER, Nie XZ, MacGregor AW, Hill RD: A cereal haemoglobin gene is expressed in seed and root tissues under anaerobic conditions. Plant Mol Biol 24: 853–862 (1994).

    Article  PubMed  CAS  Google Scholar 

  65. Trevaskis JB: The characterization of haemoglobins from Arabidopsis thaliana. Ph.D. thesis, Australian National University (1997).

    Google Scholar 

  66. Trevaskis B, Watts R, Andersson CR, Llewellyn DJ, Hargrove MS, Olson JS, Dennis ES, Peacock WJ: Two haemoglobin genes in Arabidopsis thaliana: the evolutionary origins of leghaemoglobins. Proc Natl Acad Sci USA 94: 12230–12234 (1997).

    Article  PubMed  CAS  Google Scholar 

  67. Tsien HC, Dreyfus BL, Schmidt EL: Initial stages in the morphogenesis of nitrogen-fixing stem nodules of Sesbania rostrata. J Bacteriol 156: 888–897 (1983).

    PubMed  CAS  Google Scholar 

  68. Van Berkun P, Eardly BD: Molecular evolutionary systematics of the Rhizobiaceae. In: Spaink HP, Kondorosi A, Hooykaas PJJ (eds), The Rhizobiaceae, pp. 9–20. Kluwer Academic Publishers, Dordrecht, Netherlands (1998).

    Google Scholar 

  69. van Brussel AAN, Bakhuizen R, van Spronsen PC, Spaink HP, Tak T, Lugtenberg BJJ: Induction of pre-infection thread structures in the leguminous host plant by mitogenic lipooligosaccharides of Rhizobium. Science 257: 70–71 (1992).

    Article  PubMed  Google Scholar 

  70. van Kammen A: Suggested nomenclature for plant genes involved in nodulation and symbiosis. Plant Mol Biol Rep 2: 43–45 (1984).

    Article  Google Scholar 

  71. Van Rhijn P, Fang Y, Galili S, Shaul O, Atzmon N, Wininger S, Eshed Y, Lum M, Li Y, To V, Fujishige N, Kapulnik Y, Hirsch A: Expression of early nodulin genes in alfalfa mycorrhizae indicates that signal transduction pathways used in forming arbuscular mycorrhizae and Rhizobium-induced nodules may be conserved. Proc Natl Acad Sci USA 94: 5467–5472 (1997).

    Article  PubMed  Google Scholar 

  72. Vasse J, De Billy F, Camut S, Truchet G: Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules. J Bacteriol 172: 4295–4306 (1990).

    PubMed  CAS  Google Scholar 

  73. Wegel E, Schauser L, Sandal N, Stougaard J, Parniske M: Mycorrhiza mutants of Lotus japonicus define genetically independent steps during symbiotic infection. Mol Plant-Microbe Interact 11: 933–936 (1998).

    Article  CAS  Google Scholar 

  74. Wernegreen JJ, Riley MA: Comparison of the evolutionary dynamics of symbiotic housekeeping loci: a case for the genetic coherence of rhizobial linages. Mol Biol Evol 16(1): 98–113 (1999).

    Article  PubMed  CAS  Google Scholar 

  75. Wyss P, Mellor RB, Wiemken A: Vesicular-arbuscular mycorrhizas of the wild-type soybean and non-nodulating mutants with Glomus mossae contain symbiosis-specific polypeptides (micorrhizins), immunologically cross-reactive with nodulins. Planta 182: 22–26 (1990).

    Article  CAS  Google Scholar 

  76. Yang GP, Debelle F, Ferro M, Maillet F, Schütz O, Vialas C, Savagnac A, Prome JC, Dénarié J: Rhizobium Nod factor structure and the phylogeny of temperate legumes. In: Eimerich C (ed), Biological Nitrogen Fixation for the 21st Century, pp. 185–188 Kluwer Academic Publishers, Dordrecht, Netherlands (1998).

    Google Scholar 

  77. Yang WC, Horvath B, Hontelez J, van Kammen A, Bisseling T: In situ localization of Rhizobium mRNAs in pea root nodules: nifA and nifH localization. Mol Plant-Microbe Interact 7: 276–281 (1991).

    Google Scholar 

  78. Yang WC, Katinakis P, Hendriks P, Smolders A, de Vries F, Spee J, van Kammen A, Bisseling T, Franssen H: Characterization of GmENOD40, a gene showing novel patterns of cell-specific expression during soybean nodule development. Plant J 3: 573–585 (1993).

    Article  PubMed  CAS  Google Scholar 

  79. Yang WC, de Blank C, Meskiene I, Hirt H, Bakker J, van Kammen A, Franssen H, Bisseling T: Rhizobium Nod factors reactivate the cell cycle during infection and nodule primordium formation, but the cycle is only completed in primordium formation. Plant Cell 6: 1415–1426 (1994).

    CAS  Google Scholar 

  80. Young JPW: Phylogeny and taxonomy of rhizobia. Plant Soil 186: 45–52 (1996).

    Article  CAS  Google Scholar 

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  1. Department of Molecular Biology, Agricultural University, Dreijenlaan 3, 6703 HA, Wageningen, Netherlands

    Gustavo Gualtieri & Ton Bisseling

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  1. Gustavo Gualtieri
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  1. L.H. Bailey Hortorium, Cornell University, Ithaca, New York, USA

    Jeff J. Doyle

  2. Department of Ecology and Evolutionary Biology, University of California, Irvine, California, USA

    Brandon S. Gaut

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Gualtieri, G., Bisseling, T. (2000). The evolution of nodulation. In: Doyle, J.J., Gaut, B.S. (eds) Plant Molecular Evolution. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-4221-2_9

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