An unusual infection mechanism and nodule morphogenesis in white lupin (Lupinus albus)

New Phytologist

Volumn 163, Issue 2, 2004, Pages 371-380

  González Sama, Alfonso ^a   Lucas, M Mercedes ^a   De Felipe, María R ^a   Pueyo, José J ^a  

^a INSTITUTO DE CIENCIAS AGRARIAS   (Spain)

Author keywords

Bradyrhizobium; Infection; Lupinus albus; Mesorhizobium loti; Nitrogen fixing symbiosis; Nodule; White lupin

Indexed keywords

MORPHOGENESIS;

BACTERIA (MICROORGANISMS); BRADYRHIZOBIUM; BRADYRHIZOBIUM SP.; LUPINUS; LUPINUS ALBUS; MESORHIZOBIUM; MESORHIZOBIUM LOTI; RHIZOBIACEAE;

EID: 3543038874     PISSN: 0028646X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2004.01121.x     Document Type: Article

References (49)

1. Alazard D, Duhoux E. 1990. Development of stem nodules in a tropical forage legume, Aeschynomene afraspera. Journal of Experimental Botany 41: 1199-1206.
2. Bergersen FJ. 1982. Root nodules of legumes: structure and functions. Chichester, UK: Research Studies Press.
3. Brewin NJ. 1991. Development of the legume root nodule. Annual Review of Cell Biology 7: 191-226.
4. Chandler MR. 1978. Some observations on infection of Arachis hypogaea L. by Rhizobium. Journal of Experimental Botany 29: 749-755.
5. Chandler MR, Date RA, Roughley RJ. 1982. Infection and root-nodule development in Stylosanthes species by Rhizobium. Journal of Experimental Botany 33: 47-57.
6. Chen W-M, James EK, Prescott AT, Kierans M, Sprent JI. 2003. Nodulation of Mimosa spp. by the beta-proteobacterium Ralstonia taiwanensis. Molecular Plant-Microbe Interactions 16: 1051-1061.
7. Cheng H-P, Walker GC. 1998. Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti. Journal of Bacteriology 180: 5183-5191.
8. Corby HDL, Polhill RM, Sprent JI. 1983. Taxonomy. In: Broughton WJ, ed. Nitrogen fixation, vol. 3: legumes. Oxford, UK: Oxford University Press, 1-35.
9. Davison AL, Newcomb W. 2001a. Changes in actin microfilament arrays in developing pea root nodule cells. Canadian Journal of Botany 79: 767-776.
10. Davison AL, Newcomb W. 2001b. Organization of microtubules in developing pea root nodule cells. Canadian Journal of Botany 79: 777-786.
11. Dénarié J, Debellé F, Promé JC. 1996. Rhizobium lipochitooligosaccharides nodulation factors: signalling molecules mediating recognition and morphogenesis. Annual Review of Biochemistry 65: 503-535.
12. Dreyfus BL, Dommergues YR. 1981. Nitrogen-fixing nodules induced by Rhizobium on the stem of the tropical legume Sesbania rostrata. FEMS Microbiology Letters 10: 313-317.
13. de Faria SM, Hay GT, Sprent JI. 1988. Entry of rhizobia into roots of Mimosa scabrella Bentham occurs between epidermal cells. Journal of General Microbiology 134: 2291-2296.
14. Golinowski W, Kopcinska J, Borucki W. 1987. The morphogenesis of lupine root nodules during infection by Rhizobium lupini. Acta Societatia Botanicarum Poloniae 56: 687-703.
15. Hadri A-E, Spaink HP, Bisseling T, Brewin NJ. 1998. Diversity of root nodulation and rhizobial infection processes. In: Spaink HP, Kondorosi A, Hooykaas PJJ, eds. The rhizobiaceae, molecular biology of model plant-associated bacteria. Dordrecht, The Netherlands: Kluwer Academic Publishers, 347-360.
16. Hirsch AM. 1992. Developmental biology of legume nodulation. New Phytologist 122: 211-237.
17. Hoagland DR, Arnon DI. 1938. The water culture method for growing plants without soil. California Agricultural Experimental Station Circle, no. 347.
18. Hofgen R, Willmitzer L. 1988. Storage of competent cells for Agrobacterium tumefaciens transformation. Nucleic Acid Research 16: 9877-9877.
19. James EK, Minchin FR, Iannetta PPM, Sprent JI. 1997. Temporal relationships between nitrogenase and intercellular glycoprotein in developing white lupin nodules. Annals of Botany 69: 493-503.
20. James EK, Sprent JI, Minchin FR, Brewin NJ, 1991. Intercellular location of glycoprotein in soybean nodules: effects of altered rhizosphere oxygen concentration. Plant, Cell & Environment 14: 467-476.
21. Kijne JW. 1992. The Rhizobium infection process. In: Stacey G, Burris RH, Evans HJ, eds. Biological nitrogen fixation. New York, USA: Chapman and Hall, 349-398.
22. Long SR. 1989. Rhizobium-legume nodulation: life together in the underground. Cell 56: 203-214.
23. Lotocka B, Kopcinska J, Gorecka M, Golinowski W. 2000. Formation and abortion of root nodule primordia in Lupinus luteus L. Acta Biologica Cracoviensia 42: 87-102.
24. Lucas MM. 1992. Influencia de la fertilización fosfatada sobre la simbiosis Lupinus albus L.-Bradyrhizobium sp. (Lupinus). Producción y competitividad. Madrid, Spain: Editorial Universidad Complutense de Madrid.
25. Lucas MM, Vivo A, Pozuelo JM. 1992. Application of immunolabelling techniques to Bradyrhizobium dual occupation in Lupinus nodules. Journal of Plant Physiology 140: 84-91.
26. Ndoye I, de Billy F, Vasse J, Dreyfus B, Truchet G. 1994. Root nodulation of Sesbania rostrata. Journal of Bacteriology 176: 1060-1068.
27. Patriarca EJ, Taté R, Fedorova E, Riccio A, Defez R, Iaccarino M. 1996. Down-regularion of the Rhizobium ntr system in the determinare nodule of Phaseolns vulgaris indentifies a specific developmental zone. Molecular Plant-Microbe Interactions 9: 243-251.
28. Rae AL, Bonfante-Fasolo P, Brewin NJ. 1992. Structure and growth of infection threads in the legume simbiosis with Rhizobium leguminosarum. Plant Journal 2: 385-395.
29. Reynolds ES. 1963. The use of lead citrate at high pH as an electron opaque stain in electron microscopy. Journal of Cell Biology 17: 208-213.
30. Robertson JG, Lyttleton P, Bullivant S, Grayston GF. 1978. Membranes in lupin root nodules. I. The role of Golgi bodies in the biogenesis of infection threads and peribacteroid membranes. Journal of Cell Science 30: 129-149.
31. Roth LE, Stacey G. 1989. Bacterium release into host cells of nitrogen-fixing soybean nodules: the symbiosome membrane comes from three sources. European Journal of Cell Biology 49: 13-23.
32. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd edn. New York, USA: Cold Springer Harbor Laboratory Press.
33. Sprent JI. 1989. Which steps are essential for the formation of functional legumes nodules. New Phytologist 111: 129-153.
34. van Spronsen PC, Bakhuizen R, van Brussel AAN, Kijne JN. 1994. Cell wall degradation during infection thread formation by the root nodule bacterium Rhizobium leguminosarum is a two step process. European Journal of Cell Biology 64: 88-94.
35. Subba-Rao NS, Mateos PF, Baker D, Pankratz HS, Palma J, Dazzo FB, Sprent JI. 1995. The unique root-nodule symbiosis between Rhizobium and the aquatic legume Neptunia natans (L.f.) Druce. Planta 196: 311-320.
36. Tang C, Robson AD, Dilworth MJ. 1993. Anatomical and ultrastructural observations on infection of Lupinus angustifolius L. by Bradyrhizobium sp. Journal of Computer-Assisted Microscopy 5: 47-51.
37. Tang C, Robson AD, Dilworth MJ, Kuo J. 1992. Microscopic evidence on how iron deficiency limits nodule initiation in Lupinus angustifolius L. New Phytologist 121: 457-467.
38. Taté R, Patriarca EJ, Riccio A, Defez R, Iaccarino M. 1994. Development of Phaseolus vulgaris root nodules. Molecular Plant-Microbe Interactions 7: 582-589.
39. Timmers ACJ, Auriac M-C, Truchet G. 1999. Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development 126: 3617-3628.
40. Timmers ACJ, Soupene E, Auriac MC, de Billy F, Vasse J, Boistard P, Truchet G. 2000. Saprophytic intracellular rhizobia in alfalfa nodules. Molecular Plant-Microbe Interactions 13: 1204-1213.
41. Tsien HC, Dreyfus BL, Schmidt EL. 1983. Initial stages in the morphogenesis of nitrogen-fixing stem nodules of Sesbania rostrata. Journal of Bacteriology 156: 888-897.
42. Van den Bosch KA, Bradley DJ, Knox JP, Perotto S, Butcher GW, Brewin NJ. 1989. Common components of the infection thread matrix and the intercellular space identified by immunocytochemical analysis of pea nodules and uninfected roots. EMBO Journal 8: 967-978.
43. Vasse J, de Billy F, Camut S, Truchet G. 1990. Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules. Journal of Bacteriology 172: 4295-4306.
44. Vincent JM. 1970. A manual for the practical study of root-nodule bacteria. Oxford, UK: Blackwell Scientific Publications, IBP Handbook no. 15.
45. Vivo A, Andreu JM, de la Viña S, de Felipe MR. 1989. Leghemoglobin in lupin plants (Lupinus albus L. cv. Multolupa). Plant Physiology 90: 452-457.
46. Wang T, Martínez-Romero E. 2000. Phylogeny of root and stem-nodule bacteria associated with legumes. In: Triplett EW, ed. Prokaryotic nitrogen fixation: a model system for analysis of a biology process. Wymondham, UK: Horizon Scientific Press, 177-186.
47. Warren G, Wickner W. 1996. Organelle inheritance. Cell 84: 395-400.
48. Weinstein M, Roberts RC, Helinski DR. 1992. A region of the broad-host-range plasmid RK2 causes stable in planta inheritance of plasmids in Rhizobium meliloti cells isolated from alfalfa root nodules. Journal of Bacteriology 174: 7486-7489.
49. Whitehead LF, Day DA, Hardham AR. 1998. Cytoskeleton arrays in the cells of soybean root nodules: the role of actin microfilaments in the organisation of symbiosomes. Protoplasma 203: 1194-1205.