Azolla-Anabaena Symbioses: Basic Biology, Use, and Prospects for the Future

  • G. A. Peters
Chapter
Part of the Developments in Plant and Soil Sciences book series (DPSS, volume 13)

Abstract

For the benefit of newcomers to the area of Azolla research some introductory material is presented. Azolla is a genus of free-floating, heterosporous aquatic pteridophytes. At present the genus usually is considered to contain six extant species in two sections. The subgenus Euazolla includes A. filiculoides Lamarck, A. caroliniana Willdenow, A. mexicana Presl and A. microphylla Kaulfuss, while the subgenus Rhizosperma includes A. pinnata R. Brown and A. nilotica DeCaisne. Species identification, which is in need of further assessment and possible revision, is based primarily upon features of the reproductive structures. The four new world species in the Euazolla are characterized by three megaspore floats while the two old world species in the Rhizosperma have nine megaspore floats.

Key words

Anabaena Azolla Heterocyst Photosynthesis Sporophytes Symbiosis 
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References

  1. 1.
    Ashton P J and Walmsley R D 1976 The aquatic fern Azolla and its Anabaena symbiont. Endeavour 35; 39–43.CrossRefGoogle Scholar
  2. Becking J H 1976 Contributions of plant algal associations. In: W E Newton and C J Nyman eds. Proceedings of the 1st International Symposium on Nitrogen Fixation Vol. II. Washington State University Press. Pullman, Washington. pp. 581–591.Google Scholar
  3. 3.
    Becking J H 1979 Environmental requirements of Azolla for use in tropical rice production. In: Nitrogen and Rice. International Rice Research Institute, Los Banos, Laguna, Philippines. pp. 345–374.Google Scholar
  4. 4.
    Calvert H E and Peters G A 1981 The Azolla-Anabaena azollae relationship. IX. Morphological analysis of leaf cavity hair populations. New Phytol. 89; 327–335.CrossRefGoogle Scholar
  5. 5.
    Calvert H E and Peters G A 1982 A scanning electron microscopic view of sporulation in Azolla-mexicana Presl. (these proceedings).Google Scholar
  6. 6.
    Dao T T and Tran Q T 1979 Use of Azolla in rice production in Vietnam. In: Nitrogen and Rice. International Rice Research Institute, Los Banos, Laguna, Philippines. pp. 395–405.Google Scholar
  7. 7.
    Duckett J G, Toth R and Soni S L 1975 An ultrastructural study of the Azolla, Anabaena azollae relationship. New Phytol. 75; 111–118.CrossRefGoogle Scholar
  8. 8.
    Gunning B E S, Hughes J E and Hardham A R 1978 Formative and proliferative cell divisions, cell differentiation, and developmental changes in the meristem of Azolla roots. Planta 143; 121–144.CrossRefGoogle Scholar
  9. 9.
    Haselkorn R 1978 Heterocysts Annu. Rev. Plant Physiol. 29; 319–344.CrossRefGoogle Scholar
  10. 10.
    Haselkorn R, Mazur B, Orr J, Rice D, Wood N and Rippka R 1980 Heterocyst differentiation and nitrogen fixation in cyanobacteria (blue—green algae). In: W E Newton and W H Orme—Johnson, eds. Nitrogen Fixation, Vol. II. University Park Press, Baltimore. pp. 259–278.Google Scholar
  11. 11.
    Hill D J 1975 The pattern of developmental of Anabaena in the Azolla-Anabaena symbiosis. Planta 133; 237–242.Google Scholar
  12. 12.
    Hill D J 1977 The role of Anabaena in the Azolla-Anabaena symbiosis. New Phytol. 78; 611–616.CrossRefGoogle Scholar
  13. 13.
    International Rice Research Institute 1980 Report on the first trials of Azolla use to rice, INSFFER (1980). IRRI, Los Banos, Laguna, Philippines.Google Scholar
  14. 14.
    International Rice Research Institute 1981 Report on the second trials of Azolla use to rice, INSFFER (1980). IRRI, Los Banos, Laguna, Philippines.Google Scholar
  15. 15.
    Ito O, Toia R E, Jr., Poole R E, Crist D K, Evans W R, Mayne B C and Peters G A 1980 Physiological studies on N,-fixing Azolla species grown under three photoperiods. Plant Physiol. 65; S-109.Google Scholar
  16. 16.
    Kaplan D, Calvert H E and Peters G A 1982 Phycobiliprotein in the Azolla endophyte as a function of leaf age and cell type. Plant Physiol. 69; S-156.Google Scholar
  17. 17.
    Kaplan D and Peters G A 1981 The Azolla-Anabaena azollae relationship. X. N fixation and transport in main stem axes. New Phytol. 89; 337–36.Google Scholar
  18. 18.
    Liu C C 1979 Use of Azolla in rice production in China. In: Nitrogen and Rice. international Rice Research Institute, Los Banos, Laguna, Philippines. pp. 375–394.Google Scholar
  19. 19.
    Lumpkin T A and Plucknett D L 1980 Azolla: botany, physiology, and use as a green manure. Econ. Bot. 34; 111–153.CrossRefGoogle Scholar
  20. 20.
    Moore A W 1969 Azolla: biology and agronomic significance. Bot. Rev. 35; 17–34.Google Scholar
  21. 21.
    Newton J W 1976 Photoproduction of molecular hydrogen by a plant algal symbiotic system. Science 191; 559–561.PubMedCrossRefGoogle Scholar
  22. 22.
    Newton J W and Cavins J F 1976 Altered nitrogenous pools induced by the Azolla-Anabaena symbiosis. Plant Physiol. 58; 798–799.PubMedCrossRefGoogle Scholar
  23. 23.
    Orr J and Haselkorn R 1982 Regulation of glutamine synthetase activity and synthesis in free-living Anabaena and in symbiotic association. J. Bacteriol. 152; 626–635.PubMedGoogle Scholar
  24. 24.
    Pate J S and Gunning B E S 1972 Transfer cells. Annu. Rev. Plant Physiol. 23; 173–196.CrossRefGoogle Scholar
  25. 25.
    Petes G A 1975 The Azolla-Anabaena azollae relationship. III. Studies on metabolic capabilities and a further characterization of the symbiont. Arch. Microbiol. 103; 113–122.Google Scholar
  26. Peters G A 1976 Studies on the Azolla-Anabaena azollae symbiosis. In: W E Newton and C J Nyman, eds. Proceedings of the 1st International Symposium on Nitrogen Fixation, Vol. II. Washington State University Press, Pullman, Washington. pp. 592–610.Google Scholar
  27. 27.
    Peters G A 1977 The Azolla-Anabaena azollae symbiosis. In: A. Hollaender, ed. Genetic Engineering for Nitrogen Fixation. Plenum Press, New York. pp. 231–258.Google Scholar
  28. 28a.
    Peters G A and Kaplan D 1981 Soluble carbohydrate pool in the Azolla-Anabaena symbiosis. Plant Physiol. 67; S-37.Google Scholar
  29. 28b.
    Peters G A and Calvert H E 1982a The Azolla-Anabaena symbioses. In: N S Subba Rao, ed. Advances in Agricultural Microbiology. Oxford and IBH Publ. Co., New Delhi. pp. 191–218.Google Scholar
  30. 29.
    Peters G A and Calvert H E 1982b The Azolla-Anabaena azollae symbioses. In: Lynda Goff, ed. Algal Symbiosis: Cambridge University Press, New York. pp. 109–145.Google Scholar
  31. 30.
    Peters G A, Calvert H E, Kaplan D, Ito O and Toia R E, Jr. 1982 The Azolla-Anabaena symbiosis. Israel J. Bot. 30.Google Scholar
  32. 31.
    Peters G A, Evans W R and Toia R E, Jr. 1976 Azolla-Anabaena azollae relationship. IV. Photosynthetically-driven nitrogenase- catalyzed H2 production. Plant Physiol. 58; 119–126.PubMedCrossRefGoogle Scholar
  33. 32.
    Peters G A; and Ito O 1982 Determining N2 fixation and N input in Azolla, grown with and without combined nitrogen sources: Keeping the acetylene reduction assay in the proper perspective. (these proceedings).Google Scholar
  34. 33.
    Peters G A, Ito O, Tyagi V V S and Kaplan D 1981a Physiological studies on N2-fixing Azolla. In: J M Lyons, et al., eds. Genetic Engineering of Symbiotic Nitrogen Fixation and Conservation of Fixed Nitrogen. Plenum Press, New York. pp. 343–362.Google Scholar
  35. 34.
    Peters G A, Ito O, Tyagi V V S, Mayne B C, Kaplan D and Calvert H E 1981b Photosynthesis and N fixation in the Azolla-Anabaena symbiosis. In: A H Gibson and ~ E Newton, eds. Current Perspectives in Nitrogen Fixation. Australian Academy of Science, Canberra. pp. 121–124.Google Scholar
  36. 35.
    Peters G A and Mayne B C 1974a The Azolla, Anabaena azollae relationship. I. Initial characterization of the association. Plant Physiol. 53; 813–819.CrossRefGoogle Scholar
  37. 36.
    Peters G A and Mayne B C 1974b The Azolla, Anabaena azollae relationship. II. Localization of nitrogenase activity as assayed by acetylene reduction. Plant Physiol. 53; 820–824.CrossRefGoogle Scholar
  38. 37.
    Peters G A, Mayne B C, Ray T B and Toia R E, Jr. 1979 Physiology and biochemistry of the Azolla-Anabaena symbiosis. In: Nitrogen and Rice. International Rice Research Institute, Los Banos, Laguna, Philippines. pp. 325–344.Google Scholar
  39. 38.
    Peters G A, Ray T B, Mayne B C and Toia R E Jr. 1980a Azolla-Anabaena association: morphological and physiological studies. In: W E Newton and W H Orme-Johnson, eds. Nitrogen Fixation Vol. II. University Park Press, Baltimore. pp. 293–309.Google Scholar
  40. 39.
    Peters C A, Toia R E Jr., Evans W R, Crist D K, Mayne B C and Poole R E 1980b Characterization and comparisons of five N2-fixing Azolla-Anabaena associations. I. Optimization of growth conditions for biomass increase and N content in a controlled environment. Plant, Cell and Environ. 3; 261–269.Google Scholar
  41. 40.
    Peters G A, Toia R E Jr. Lough S M 1977 Azolla-Anabaena azollae relationship. V. N2 fixation, acetylene reduction, and H2 production. Plant Physiol. 59; 1021–1025.PubMedCrossRefGoogle Scholar
  42. 41.
    Peters G A, Toia R E Jr., Raveed D and Levine N J 1978 The Azolla-Anabaena azollae relationship. VI. Morphological aspects of the association. New Phytol. 80; 583–593.CrossRefGoogle Scholar
  43. 42.
    Ray T B, Mayne B C, Toia R E Jr. and Peters G A 1979 Azolla-Anabaena relationship. VIII. Photosynthetic characterization of the association and individual partners. Plant Physiol. 64; 791–795.PubMedCrossRefGoogle Scholar
  44. 43.
    Ray T B, Peters G A, Toia R E Jr. and Mayne B C 1978 Azolla-Anabaena relationship. VII. Distribution of ammonia-assimilating enzymes, protein, and chlorophyll between host and symbiont. Plant Physiol. 62; 463–467.PubMedCrossRefGoogle Scholar
  45. 44.
    Shi D J, Li J G, Zhung Z P, Wang F Z, Zhu L P and Peters G A 1981 Studies on nitrogen fixation and photosynthesis in Azolla imbricata (Roxb.) and Azolla filiculoides Lam. Acta Bot. Sin. 23; 306–315 (in Chinese).Google Scholar
  46. 45.
    Singh P K 1980 Introduction of “Green Azolla” biofertilizer in India. Curr. Sci. 49; 155–156.Google Scholar
  47. 46.
    Stewart W D P 1977 A botanical ramble among the blue-green algae. Br. Phycol. J. 12; 89–115.CrossRefGoogle Scholar
  48. 47.
    Subudhi B P R and Watanabe I 1981 Differential phosphorus re-quirement of Azolla species and strains in phosphorus limited continuous culture. Soil Sci. Plant Nutr. 27; 237–247.Google Scholar
  49. 48.
    Talley S N and Rains D W 1980a Azolla as a nitrogen source for temperate rice. In: W E Newton and W H Orme-Johnson eds. Nitrogen Fixation Vol. II. University Park Press, Baltimore. pp. 311–320.Google Scholar
  50. 49.
    Talley S N and Rains D W 1980b Azolla filiculoides Lam. As a fallow season green manure for rice in temperate climate. Agron. J. 72; 11–18.Google Scholar
  51. 50.
    Talley S N, Talley B J and Rains D W 1977 Nitrogen fixation by Azolla in rice fields. In: A. Hollaender ed. Genetic Engineering for Nitrogen Fixation. Plenum Press, New York. pp. 259–281.Google Scholar
  52. 51.
    Tyagi V V S, Mayne B C and Peters G A 1980 Purification and initial characterization of phycobiliproteins from the endophytic cyanobacterium of Azolla. Arch. Microbiol. 128; 41–44.Google Scholar
  53. 52.
    Tyagi V V S, Ray T B, Mayne B C and Peters G A 1981 The Azolla-Anabaena azollae relationship. XI. Phycobiliproteins in the action spectrum for nitrogenase—catalyzed acetylene reduction. Plant Physiol. 68; 1479–1484.PubMedCrossRefGoogle Scholar
  54. 53.
    Watanabe I, Espinas C R, Berja N S and Alimagno B V 1977 Utilization of the Azolla-Anabaena complex as a nitrogen fertilizer for rice. Int. Rice Res. Inst. Res. Paper Ser. 11; 1–15.Google Scholar

Copyright information

© Martinus Nijhoff/Dr W. Junk Publishers, Dordrecht 1984

Authors and Affiliations

  • G. A. Peters
    • 1
  1. 1.C.F. Kettering Research LaboratoryYellow SpringsUSA

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