Signals and responses: Choreographing the complex interaction between legumes and α- and β-rhizobia

Plant Signaling and Behavior

Volumn 1, Issue 4, 2006, Pages 161-168

  Lee, Angie ^a   Hirsch, Ann M ^a,b  

^a Cellular and Developmental Biology ^*  (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

rhizobia; rhizobia; Biological nitrogen fixation; Recognition; Specificity

Indexed keywords

EID: 39449107186     PISSN: 15592316     EISSN: 15592324     Source Type: Journal    
DOI: 10.4161/psb.1.4.3143     Document Type: Review

References (74)

1. Sprent JI. Nodulation in Legumes. Royal Botanic Gardens, Kew: The Cromwell Press Ltd., 2001:146.
2. Sy A, Giraud E, Samba R, de Lajudie P, Gillis M, Dreyfus B. Certaines légumineuses du genre Crotalaria sont spécifiquement nodulées par une nouvelle espèce de Methylobacterium. Can J Microbiol 2001; 47:503-8.
3. Sy A, Giraud E, Jourand P, Garcia N, Willems A, de Lajudie P, Prin Y, Neyra M, Gillis M, Boivin-Masson C, Dreyfus B. Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. J Bacteriol 2001; 183:214-20.
4. Jaftha JB, Strijdom BW, Steyn PL. Characterization of pigmented methylotrophic bacteria which nodulate Lotononis bainesii. Syst Appl Microbiol 2002; 25:440-49.
5. Van Berkum P, Eardly BD. The aquatic budding bacterium Blastobacter denitrificans is a nitrogen-fixing symbiont of Aeschynomene indica. Appl Environ Microbiol 2002; 68:1132-6.
6. Rivas R, Willems A, Subba-Rao NS, Mateos PF, Dazzo FB, Kroppenstedt RM, Martinez-Molina E, Gillis M, Velazquez E. Description of Devosia neptuniae sp. nov. that nodulates and fixes nitrogen in symbiosis with Neptunia natans, an aquatic legume from India. Syst Appl Microbiol 2003; 26:47-53.
7. Vandamme P, Coenye T. Taxonomy of the genus Cupriavidus: A tale of lost and found. J Syst Evol Microbiol 2004; 54:2285-9.
8. Moulin L, Chen WM, Béna G, Dreyfus B, Boivin-Masson C. Rhizobia: The family is expanding. In: Finan T, O'Brian M, Layzell D, Vessey K, Newton W, eds. Nitrogen Fixation. Global Perspectives. New York: CABI Publishing, 2002:61-5.
9. Chen WM, Laevens S, Lee TM, Coenye T, De Vos P, Mergeay M, Vandamme P. Ralstonia taiwanensis sp. nov., isolated from root nodules of Mimosa species and sputum of a cystic fibrosis patient. Int J Syst Evol Microbiol 2001; 51:1729-35.
10. Chen WM, James EK, Prescott AR, Kierans M, Sprent JI. Nodulation of Mimosa spp. by the b-Proteobacterium Ralstonia taiwanensis. Mol Plant-Microbe Inter 2003; 16:1051-61.
11. Chen WM, Moulin L, Bontemps C, Vandamme P, Béna G, Boivin-Masson C. Legume symbiotic nitrogen fixation by b-Proteobacteria is widespread in nature. J Bacteriol 2003; 185:7266-72.
12. Barrett CF, Parker MA. Prevalence of Burkholderia sp. nodule symbionts on four mimosoid legumes from Barro Colorado Island, Panama. Syst Appl Microbiol 2005; 28:57-65.
13. Valverde A, Velázquez E, Gutiérrez C, Cervantes E, Ventosa A, Igual JM. Herbaspirillum lusitanum sp. nov., a novel nitrogen-fixing bacterium associated with root nodules of Phaseolus vulgaris. Int J Syst Evol Microbiol 2003; 53:1979-83.
14. Pueppke SG, Broughton WJ. Rhizobium sp. strain NGR234 and R. fredii USDA257 share exceptionally broad, nested host ranges. Mol Plant-Microbe Inter 1999; 12:293-318.
15. Long SR. Genes and signals in the Rhizobium-legume symbiosis. Plant Physiol 2001; 125:69-72.
16. Moulin L, Mundive A, Dreyfus B, Boivin-Masson C. Nodulation of legumes by members of the beta-subclass of Proteobacteria. Nature 2001; 411:948-50.
17. Chen WM, James EK, Chou JH, Sheu SY, Yang SZ, Sprent JI. b-Rhizobia from Mimosa pigra, a newly discovered invasive plant in Taiwan. New Phytol 2005; 168:661-75.
18. Chen WM, de Faria SM, Straliotto R, Pitard RM, Simões-Araùjo JL, Chou JS, Chou YJ, Barrios E, Prescott AR, Elliott GN, Sprent JI, Young JPW, James EK. Proof that Burkholderia strains form effective symbioses with legumes: A study of novel Mimosa-nodulating strains from South America. Appl Environ Microbiol 2005; 71:7461-71.
19. Barrett CF, Parker MA. Coexistence of Burkholderia, Cupriavidus, and Rhizobium sp. nodule bacteria on two Mimosa spp. in Costa Rica. Appl Environ Microbiol 2006; 72:1198-206.
20. Atkinson EM, Palcic MM, Hindsgaul O, Long SR. Biosynthesis of Rhizobium meliloti lipooligosaccharide Nod factors: NodA is required for an N-acyltransferase activity. Proc Nat Acad Sci USA 1994; 91:8418-22.
21. Röhrig 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 chitooligosaccharide backbone. Proc Nat Acad Sci USA 1994; 91:3122-6.
22. Vandamme P, Goris J, Chen WM, de Vos P, Willem A. Burkholderia tuberum sp. nov. and Burkholderia phymatum sp. nov., nodulate the roots of tropical legumes. Syst Appl Microbiol 2002; 25:507-12.
23. Zhang XX, Turner SL, Guo XW, Yang HJ, Debellé F, Yang GP, Dénarié J, Young JPW, Li FD. The common nodulation genes of Astragalus sinicus rhizobia are conserved despite chromosomal diversity. Appl Environ Microbiol 2000; 66:2988-95.
24. Boone CM, Olsthoorn MMA, Dakora FD, Spaink HP, Thomas-Oates JE. Structural characterisation of lipo-chitin oligosaccharides isolated from Bradyrhizobium aspalati, microsymbionts of commercially important South African legumes. Carb Res 1999; 317:155-63.
25. D'Haeze W, Holsters M. Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 2002; 12:79R-105R.
26. Felle HH, Kondorosi E, Kondorosi A, Schultze M. The role of ion fluxes in Nod factor signaling in Medicago sativa. Plant J 1998; 13:455-63.
27. Cárdenas L, Vidali L, Dominguez J, Perez H, Sanchez F, Hepler PK, Quinto C. Rearrangement of actin microfilaments in plant root hairs responding to Rhizobium etli nodulation signals. Plant Physiol 1998; 116:871-7.
28. Lerouge P, Roche P, Faucher C, Maillet F, Truchet G, Promé JC, Dénarié J. Symbiotic host-specificity of Rhizobium meliloti is determined by a sulfated and acylated glucosamine oligosaccharide signal. Nature 1990; 344:781-4.
29. Foucher F, Kondorosi E. Cell cycle regulation in the course of nodule organogenesis in Medicago. Plant Mol Biol 2000; 43:773-86.
30. Geurts R, Heidstra R, Hadri AE, Downie JA, 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 1997; 115:351-9.
31. Felle HH, Kondorosi E, Kondorosi A, Schultze M. Elevation of the cytosolic free Ca2+ is indispensable for the transduction of the Nod factor signal in alfalfa. Plant Physiol 1999; 121:273-9.
32. Felle HH, Kondorosi E, Kondorosi A, Schultze M. Rapid alkalinization in alfalfa root hairs in response to rhizobial lipochitooligosaccharide signals. Plant J 1996; 10:295-301.
33. Ehrhardt DW, Wais R, Long SR. Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 1996; 85:673-81.
34. Cárdenas L, Feijo JA, Kunkel JG, Sanchez F, Holdaway-Clarke T, Hepler PK, Quinto C. Rhizobium Nod factors induce increases in intracellular free calcium and extracellular calcium influxes in bean root hairs. Plant J 1999; 19:347-52.
35. Walker SA, Viprey V, Downie JA. Dissection of nodulation signaling using pea mutants defective for calcium spiking induced by Nod factors and chitin oligomers. Proc Nat Acad Sci USA 2000; 97:13413-8.
36. Shaw SL, Long SR. Nod factor elicits two separable calcium responses in Medicago truncatula root hair cells. Plant Physiol 2003; 131:976-84.
37. Wais RJ, Galera C, Oldroyd G, Catoira R, Penmetsa RV, Cook D, Gough C, Dénarié J, Long SR. Genetic analysis of calcium spiking responses in nodulation mutants of Medicago truncatula. Proc Nat Acad Sci USA 2000; 97:13407-12.
38. Harris JM, Wais R, Long SR. Rhizobium-induced calcium spiking in Lotus japonicus. Mol Plant-Microbe Inter 2003; 16:335-41.
39. Dolmetsch RE, Xu K, Lewis RS. Calcium oscillations increase the efficiency and specificity of gene expression. Nature 1998; 392:933-6.
40. Allen GJ, Chu SP, Harrington CL, Schumacher K, Hoffman T, Tang YY, Grill E, Schroeder JI. A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature 2001; 411:1053-7.
41. Pingret JL, Journet EP, Barker DG. Rhizobium Nod factor signaling: Evidence for a G protein-mediated transduction mechanism. Plant Cell 1998; 10:659-71.
42. Miller DD, de Ruijter NCA, Bisseling T, Emons AMC. The role of actin in root hair morphogenesis: Studies with lipochito-oligosaccharide as a growth stimulator and cytochalasin as an actin perturbing drug. Plant J 1999; 17:141-54.
43. De Almeida Engler J, Ruijter NCA, Rook MB, Bisseling T, Emons AMC. Lipochito-oligosaccharides reinitiate root hair tip growth in Vicia sativa with high calcium and spectrin-like antigen at the tip. Plant J 1998; 13:341-50.
44. Hirsch AM, Asad S, Fang Y, Wycoff K, Löbler M. Molecular interactions during nodule development. In: Palacios R, Mora J, Newton WE, eds. New Horizons in Nitrogen Fixation. Dordrecht: Kluwer Academic Publishers, 1993:291-7.
45. Relic' B, Talmont F, Kopcinska J, Golinowski W, Promé JC, Broughton WJ. Biological activity of Rhizobium sp. NGR234 Nod-factors on Macroptilium atropurpureum. Mol Plant-Microbe Inter 1993; 6:764-74.
46. Relic' B, Perret X, Estrada-García MT, Kopcinska J, Golinowski W, Krishnan HB, Pueppke SJ, Broughton WJ. Nod factors of Rhizobium are a key to the legume door. Mol Microbiol 1994; 13:171-8.
47. Schauser L, Roussis A, Stiller J, Stougaard J. A plant regulator controlling development of symbiotic root nodules. Nature 1999; 402:191-5.
48. Kaló P, Gleason C, Edwards A, Marsh J, Mitra RM, Hirsch S, Jakab J, Sims S, Long SR, Rogers J, Kiss GB, Downie, Oldroyd GED. Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 2005; 308:1786-9.
49. Smit P, Raedts J, Portyanko V, Debellé, Gough C, Bisseling T, Guerts R. NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 2005; 308:1789-91.
50. Endre G, Kereszt A, Kevei Z, Mihacea S, Kalo P, Kiss GB. A receptor kinase gene regulating symbiotic nodule development. Nature 2002; 417:962-6.
51. Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Szczyglowski K, Parniske M. A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 2002; 417:959-62.
52. 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 AM. 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 Nat Acad Sci USA 1997; 94:5467-72.
53. Albrecht C, Geurts R, Lapeyrie F, Bisseling T. Endomycorrhizae and rhizobial Nod factors both require SYM8 to induce the expression of the early nodulin genes PsENOD5 and PsENOD12A. Plant J 1998; 15:605-14.
54. Ané JM, Kiss GB, Riely BK, Penmetsa RV, Oldroyd GED, Ayax C, Levy J, Debellé F, Baek JM, Kalo P, Rosenberg C, Roe BA, Long SR, Dénarié J, Cook DR. Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 2004; 303:1364-7.
55. Imaizumi-Anraku H, Takeda N, Charpentier M, Perry J, Miwa H, Umehara Y, Kouchi H, Murakami Y, Mulder L, Vickers K, Pike J, Downie JA, Wang T, Sato S, Asamizu E, Tabata S, Yoshikawa M, Murooka Y, Wu GJ, Kawaguchi M, Kawasaki S, Parniske M, Hayashi M. Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature 2005; 422:527-31.
56. Levy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet EP, Ané JM, Lauber E, Bisseling T, Dénarié J, Rosenberg C, Debellé F. A putative Ca2+ and calmodulindependent protein kinase required for bacterial and fungal symbioses. Science 2004; 303:1361-4.
57. Madsen EB, Madsen LH, Radutoiu S, Olbry M, Rakwalska M, Szczyglowski K, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J. A receptor kinase of the LysM type is involved in legume perception of rhizobial signals. Nature 2003; 425:637-40.
58. Radutoiu S, Madsen LH, Madsen EB, Felle HH, Umehara Y, Grønlund M, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 2003; 425:585-92.
59. Limpens E, Franken C, Smit P, Willemse J, Bisseling T, Geurts R. LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 2003; 302:630-3.
60. Bateman A, Bycroft M. The structure of a LysM domain from E. coli membrane-bound lytic murein transglycosylase D (Mltd). J Mol Biol 2000; 299:1113-9.
61. Butler AR, O'Donnell RW, Martin VJ, Gooday GW, Stark MJR. Kluyveromyces lactis toxin has an essential chitinase activity. Eur J Biochem 1991; 199:483-8.
62. Oldroyd GED, Downie JA. Calcium, kinases and nodulation signaling in legumes. Nat Rev Mol Cell Biol 2004; 5:566-76.
63. Geurts R, Fedorova E, Bisseling T. Nod factor signaling genes and their function in the early stages of Rhizobium infection. Curr Opin Plant Biol 2005; 8:346-52.
64. Stacey G, Libault M, Brechenmacher L, Wan J, May GD. Genetics and functional genomics of legume nodulation. Curr Opin Plant Biol 2006; 9:110-121.
65. Zhu H, Riely BK, Burns NJ, Ané JM. Tracing nonlegume orthologs of legume genes required for nodulation and arbuscular mycorrhizal symbiosis. Genetics 2006; 172:2491-9.
66. Franco AA, de Faria SM. The contribution of N2-fixing tree legumes to land reclamation and sustainability in the tropics. Soil Biol Biochem 1997; 29:897-903.
67. Rasolomampianina R, Bailly X, Fetiarison R, Rabevohitra R, Béna G, Ramaroson L, Raherimandimy M, Moulin L, De Lajudie P, Dreyfus B. Nitrogen-fixing nodules from rose wood legume trees (Dalbergia spp.) endemic to Madagascar host seven different genera belonging to a- and b-Proteobacteria. Mol Ecol 2005; 14:4135-46.
68. Lynch JM, Hobbie JE. Microorganisms in Action: Concepts and Applications in Microbial Ecology. 2nd ed. Oxford, UK: Blackwell Scientific Publications, 1988:241-54.
69. Smil V. Enriching the Earth. Cambridge, MA: The MIT Press, 2001:338.
70. Kinzing AP, Socolow RH. Human impact on the nitrogen cycle. Physics Today 1994; 47:24-35.
71. Smil V. How many billions to go? Nature 1999; 409:429.
72. Haber F. The synthesis of ammonia from its elements. Nobel Lecture 1920, (http://nobelprize. org/chemistry/laureates/1918/haber-lecture.pdf).
73. Van Berkum P, Leibold JM, Eardly BD. Proposal for combining Bradyrhizobium spp. (Aeschynomene indica) with Blastobacter denitrificans and to transfer Blastobacter denitrificans (Hirsch and Muller, 1985) to the genus Bradyrhizobium as Bradyrhizobium denitrificans (comb. nov.) Syst Appl Microbiol 2006; 29:207-15.
74. Niner BM, Hirsch AM. How many Rhizobium genes, in addition to nod, nif/fix, and exo, are needed for nodule development and function? Symbiosis 1998; 24:51-102.