Skip to main content
NCBI home page
Wiley - PMC COVID-19 Collection logoLink to Wiley - PMC COVID-19 Collection
. 2006 Apr 28;130(4):531–544. doi: 10.1111/j.1469-8137.1995.tb04330.x

Stem and root nodules on the tropical wetland legume Aeschynomene fluminensis

M F LOUREIRO 1, E K JAMES 2,✉, J I SPRENT 3, A A FRANCO 4
PMCID: PMC7168032  PMID: 33874487

SUMMARY

Aeschynomene fluminensis Veil., originally obtained from flooded areas of the Pantanal Matogrossense region of Brazil, was grown under stem‐flooded or non‐flooded conditions for 70 d after inoculation with isolates of photosynthetic stem nodule rhizobia obtained from native A. fluminensis. Stem nodules formed only on submerged stems of flooded plants (mean of 25 per plant), and did not form on aerial parts, although they were capable of growing and fixing N2 after drainage of the stems. Root nodules formed on both non‐flooded and flooded plants but were usually decreased in number by flooding (from means of 124 to 51 per plant, respectively). Flooding (and stem‐nodulation) resulted in an increase in shoot (and a decrease in root) dry weight, regardless of rhizobial isolate.

Stem nodules were attached by a wide collar of aerenchymatous tissue at the base of the nodule. There were large air spaces in the stem where nodules were subtended and these were continuous with nodule aerenchyma/outer cortex. In addition, aerenchyma and spongy tissue at the base of the nodule connected both flooded and non‐flooded root nodules to large intercellular spaces in the root cortex. The stem and root nodules were ovoid in shape, and essentially aeschynomenoid in type, i.e. the central infected tissue was without uninfected, interstitial cells. Root nodules had a similar structure to stem nodules (although stem nodules were generally larger), and flooded root nodules were approximately twice the size of non‐flooded nodules. The infected tissue of root and stem nodules consisted of spherical, bacteroid‐containing cells containing one or two rod‐shaped bacteroids per peribacteroid unit and prominent organelles. Infection threads were observed in root but not in stem nodules.

The cortex of stem and root nodules had an apparent oxygen diffusion barrier, consisting of concentric layers of small cells with interlocking cell walls and few intercellular spaces. Cell layers external to these consisted of larger cells and intercellular spaces, with some spaces being occluded with an electron‐dense material that contained a glycoprotein recognized by the monoclonal antibodies MAC236 and MAC265. The amount of glycoprotein occlusions did not appear to differ between nodule types or treatments, although stem nodules contained intracellular glycoprotein vesicles adjacent to cell walls. The exterior of the nodules consisted of an epidermis of thin flattened cells with occasional lenticels. Amyloplasts were common in lower stem and hypocotyl nodules, but fewer in flooded or non‐flooded root nodules. Upper stem nodules (i.e. those within 6 cm of the water surface) differed from more profoundly submerged stem nodules by having chloroplasts throughout the cortex. Root nodules did not contain chloroplasts, and undifferentiated plastids were found mainly in lower stem nodules.

Keywords: Aeschynomene fluminensis, stem nodules, nitrogen fixation, wetlands, oxygon

REFERENCES

  1. Alazard D. 1985. Stem and root nodulation in Aeschynomene spp. Applied and Environmental Microbiology 50: 732–734. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Alazard D, Duhoux E. 1987. Nitrogen‐fixing stem nodules on Aeschynomene afraspera . Biology and Fertility of Soils 4: 61–66. [Google Scholar]
  3. Alazard D, Duhoux E. 1988. Diversity of stem nodulation sites in Aeschynomene spp. Journal of Plant Physiology 132: 123–125. [Google Scholar]
  4. Alazard D, Duhoux E. 1990. Development of stem nodules in a tropical forage legume, Aeschynomene afraspera . Journal of Experimental Botany 41: 1199–1206. [Google Scholar]
  5. Allem AC, Vails JFM. 1987. Recursos Forrageiros Nativos do Pantanal Matogrossense. Brasilia : EMBRAPA/CENARGEN, Documentos 8. Deparmento de Difusao de Tecnologia. [Google Scholar]
  6. Arora N. 1954. Morphological development of the root and stem nodules of Aeschynomene indica L. Phytomorphology 4: 211–216. [Google Scholar]
  7. Brown S, Walsh KB. 1994. Anatomy of the legume nodule cortex with respect to nodule permeability. Australian Journal of Plant Physiology 21: 49–68. [Google Scholar]
  8. Bruijn FJ de. 1989. The unusual symbiosis between the diazotrophic stem‐nodulating bacterium Astorhisobium caitlinoittins ORS5721 and its host, the tropical legume Sesbania rostrata. In: Kosuge T, Nester EW, eds. Plant‐Microbe Interactions, Molecular and Genetic Perspectives. Vol. 3, New York , NY : McGraw‐Hill, 457–504. [Google Scholar]
  9. Corby HDL. 1988. Types of rhizobial nodules and their distribution among the Leguminosae. Kirria 13: 53–123. [Google Scholar]
  10. Dreyfus BL, Dommergues Y. 1981. Nitrogen‐fixing nodules induced by Rhizobium on the stem of the tropical legume Sesbania rostrata . FEMS Microbiology Letters 10: 313–317. [Google Scholar]
  11. Duhoux E. 1984. Ontogénèse des nodules caulinaires du Sesbania rostrata (légumineuses). Canadian Journal of Botany 62: 982–994. [Google Scholar]
  12. Eaglesham ARJ, Szalay AA. 1983. Aerial stem nodules on Aeschyinomene spp. Plant Science Letters 29: 265–272. [Google Scholar]
  13. Evans WR, Fleischman DE, Calvert HE, Pyati PV, Alter GM, Subba Rao NS. 1990. Bacteriochlorophyll and photosynthetic reaction centers in Rhizobium strain BTAi 1. Applied and Environmental Microbiology 56: 3445–3449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gallon JR. 1992. Reconciling the incompatible: N2 fixation and O2 . New Phytologist 122: 571–609. [Google Scholar]
  15. Hungria M, Eaglesham ARJ, Hardy RWF. 1992. Physiological comparisons of root and stem nodules of Aeschynomene scabra and Sesbania rostrata . Plant and Soil 139: 7–13. [Google Scholar]
  16. Hungria M, Ellis JM, Hardy RWF, Eaglesham ARJ. 1993. Light‐stimulated 14CO2 uptake and acetylene reduction by bacteriochlorophyll containing stem nodule isolate BTAil. Biology and Fertility of Soils 15: 208–214. [Google Scholar]
  17. Iannetta PPM, James EK, Sprent JI, Minchin FR. 1995. Time‐course of changes involved in the operation of the oxygen diffusion barrier in white lupin nodules. Journal of Experimental Botany 46:. [Google Scholar]
  18. James EK, Iannetta PPM, Naisbitt T, Goi SR, Sutherland JM, Sprent JI, Minchin FR, Brewin NJ. 1994. A survey of N2‐fixing nodules in the Leguminosae with particular reference to intercellular glycoproteins and the control of oxygen diffusion. Proceedings of the Royal Society of Edinburgh 102B: 429–432. [Google Scholar]
  19. James EK, Minchin FR, Sprent JI. 1992b. The physiology and nitrogen‐fixing capability of aquatically and terrestrially grown Neptunia plena: the importance of nodule oxygen supply. Annals of Botany 69: 181–187. [Google Scholar]
  20. James EK, Sprent JI, Minchin FR, Brewin NJ. 1991. Intercellular location of glycoprotein in soybean nodules: effect of altered rhizosphere oxygen concentration. Plant Cell and Environment 14: 467–476. [Google Scholar]
  21. James EK, Sprent JI, Sutherland JM, Mclnroy SG, Minchin FR. 1992a. The structure of nitrogen fixing root nodules on the aquatic mimosoid legume Neptunia plena . Annals of Botany 69: 173–180. [Google Scholar]
  22. Jayaram S, Bal AK. 1991. Oleosomes (lipid bodies) in nitrogen‐fixing peanut nodules. Plant. Cell and Environment 14: 195–205. [Google Scholar]
  23. Kwon DK, Beevers H. 1992. Growth of Sesbania rostrata (Brem) with stem nodules under controlled conditions. Plant. Cell and Environment 15: 939–945. [Google Scholar]
  24. Ladha JK, Garcia M, Pareek RP, Rarivoson G. 1992b. Relative contributions to nitrogenase (acetylene reducing) activity of stem and root nodules in Sesbania rostrata . Canadian Journal of Microbiology 38: 577–583. [Google Scholar]
  25. Ladha JK, Pareek RP, Becker M. 1992a. Stem‐nodulating legume‐Rhizobium symbiosis and its agronomic use in lowland rice. Advances in Soil Science 20: 148–192. [Google Scholar]
  26. Lorquin J, Molouba F, Dupuy N, Ndiaye S, Alazard D, Gillis M, Dreyfus B. 1993. Diversity of photosynthetic Brady‐rhizobium strains from stem nodules of Aeschynomene species. In: Palacios R, Mora J, Newton WE, eds. New Horizons in Nitrogen Fixation. Dordrecht/Boston/London : Kluwer Academic Publishers, 683–689. [Google Scholar]
  27. Loureiro MF, de Faria SM, James EK, Pott A, Franco AA. 1994. Nitrogen‐fixing stem nodules of the legume, Discolobium pulchelliim Benth. New Phytologist 128: 283–295. [DOI] [PubMed] [Google Scholar]
  28. Loureiro MF, Hungria M, Sampaio MJAM, Franco AA, Baldani JI. 1993. Photosynthetic characteristics of strains of rhizobia isolated from stem nodules of Aeschynomene fluminensis grown in the Pantanal region of Brazil. In: Palacios R, Mora J, Newton WE, eds. New Horizons in Nitrogen Fixation. Dordrecht/Boston/London : Kluwer Academic Publishers, 629. [Google Scholar]
  29. Ndoye I, Dreyfus B. 1988. N2 fixation by Sesbania rostrata and Sesbania sesban estimated using 15N and total N difference methods. Soil Biology and Biochemistry 20: 209–213. [Google Scholar]
  30. Parsons R, Day DA. 1990. Mechanism of soybean nodule adaptation to different oxygen pressures. Plant, Cell and Environment 13: 501–512. [Google Scholar]
  31. Parsons R, Raven JA, Sprent JI. 1992. A simple open flow‐system used to measure acetylene reduction activity of Sesbania rostrata stem and root nodules. Journal of Experimental Botany 43: 545–604. [Google Scholar]
  32. Parsons R, Sprent JI, Raven JA. 1993. Humidity and light affect the growth, development and nitrogenase activity of stem nodules of Sesbania rostrata (Brem). New Phytologist 125: 749–755. [DOI] [PubMed] [Google Scholar]
  33. Pugh R, Witty JF, Mytton LR, Minchin FR. 1995. The effect of waterlogging on nitrogen fixation and nodule morphology in soil‐grown white clover (Trifolium repens L.). Journal of Experimental Botany 46: 285–290. [Google Scholar]
  34. Schaede R. 1940. Die Knöllchen der adventiven Wasserwurzeln von Neptunia oleracea und ihre Bakteriensymbiose. Planta 31: 1–21. [Google Scholar]
  35. Sprent JI, Sprent P. 1990. Nitrogen fixing organisms. London : Chapman and Hall. [Google Scholar]
  36. Sprent JI, Sutherland JM, de Faria SM. 1989. Structure and function of root nodules from woody legumes. In: Stirton CH, Zarucchi JL, eds. Advances in Legume Biology. Monographs of Systematic Botany. Missouri Botanical Gardens 29, 559–578.
  37. Stam H, van Verseveld HW, de Vries W, Stouthamer AH. 1986. Utilization of poly‐β‐hydroxybutyrate in free‐living cultures of Rhizobium ORS571. FEMS Microbiology Letters 35: 215–220. [Google Scholar]
  38. Stegink SJ, Vaughn KC. 1988. Correlation between nodule ultrastructure and ability to produce stem nodules in Aeschynomene spp. Cytologia 53: 401–406. [Google Scholar]
  39. 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. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. VandenBosch 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 the immunocytochemical analysis of pea nodules and uninfected roots. European Molecular Biology Organisation Journal 8: 335–342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Vaughn KC, Elmore CD. 1985. Ultrastructural characterization of nitrogen‐fixing stem nodules on Aeschynomene indica . Cytobios 42: 49–62. [Google Scholar]
  42. Witty JF, Minchin FR. 1988. Measurement of nitrogen fixation by the acetylene reduction assay: myths and mysteries. In: Beck DP, Materon LA, eds. Nitrogen fixation by Legumes in Mediterranean Agriculture. ICARDA, 331–344. [Google Scholar]
  43. Witty JF, Minchin FR, Skøt L, Sheehy JE. 1986. Nitrogen fixation and oxygen in legume root nodules. Oxford Surveys in Plant Molecular and Cell Biology 3: 275–314. [Google Scholar]
  44. Yatazawa M, Yoshida S. 1979. Stem nodules in Aeschynomene indica and their capacity of nitrogen fixation. Physiologia Plantarum 45: 293–295. [Google Scholar]
  45. Yatazawa M, Yoshida S, Maeda E. 1984. Fine structure of root nodules of Aeschynomene indica L. Soil Science and Plant Nutrition 30: 405–416. [Google Scholar]

Articles from The New Phytologist are provided here courtesy of Wiley

RESOURCES