Skip to main content
Log in

Lichens toGunnera — with emphasis onAzolla

  • Biology of Interactions between Plants and Diazotrophic Bacteria
  • Published:
Plant and Soil Aims and scope Submit manuscript

Summary

N2-fixing cyanobacteria occur in symbiotic associations with fungi (ascomycetes) as lichens and with a few green plants. The associated cyanobacterium is always a species ofNostoc orAnabaena. Only a small number of plant genera are involved but there is a remarkable range of host diversity. Associations occur with several bryophytes (e.g.Anthoceros, Blasia, Cavicularia), a pteridophyte (Azolla), cycads (nine genera includingMacrozamia andEncephalartos) and an angiosperm (Gunnera). Except forGunnera, where the cyanobacterium penetrates the plant cells, the cyanobacteria are extracellular with specialized morphological modifications and/or structures of the host plant organs providing an environment which facilitates interaction with the prokaryote.

Salient aspects of current knowledge pertaining to the establishment, perpetuation, and functioning of the individual symbioses are summarized. Where possible this includes information concerning recognition and specificity, mode(s) of infection, morphological modifications/adaptations of the host plant and a synopsis of morphological, physiological and biochemical changes common to the symbiotic cyanobacteria. The latter encompasses heterocyst frequencies, enzymes involved in ammonia assimilation, photosynthetic capability and metabolic interaction with the host.

TheAzolla-Anabaena symbioses, which have potential agronomic significance as an alternative nitrogen source and maintain continuity with the endophyte through the sexual cycle, are emphasized.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Ahmadjian V and Jacobs J B 1983 Algal-fungal relationships in lichens: recognition, synthesis, and development.In Algal Symbiosis. Ed. L J Goff. Cambridge University Press, New York. pp 147–172.

    Google Scholar 

  2. Alexander V 1981 Nitrogen-fixing lichens in tundra and teiga ecosystems.In Current Perspectives in Nitrogen Fixation. Eds. A H Gibson and W E Newton Australian Academy of Science Canberra. p. 257.

    Google Scholar 

  3. Allen E K and Allen O N 1965 Nonleguminous Plant Symbiosis.In Microbiology and Soil Fertility (Proc. 25th Annual Biology Colloquium). Eds C M Gilmour and O N Allen. Oregon State University Press. Corvallis. pp 7–106.

    Google Scholar 

  4. Ashton P J 1974 The effect of some environmental factors on the growth ofAzolla filiculoides Lam.In The Organe River Progress Report. Ed. E M Zinderen-Bakker Bloemfontein, South Africa. pp 123–138.

    Google Scholar 

  5. Ashton P J and Walmsley R D 1976 The aquatic fernAzolla and itsAnabaena symbiont. Endeavour 35, 39–43.

    Google Scholar 

  6. Becking J H 1978 Ecology and physiological adaptations ofAnabaena in theAzolla-Anabaena symbiosis. Ecol. Bull. (Stockholm) 26, 258–273.

    Google Scholar 

  7. Becking J H 1979 Environmental requirements ofAzolla for use in tropical rice production.In Nitrogen and Rice. IRRI (eds.) International Rice Research Institute, Los Banos, Laguna, Philippines. pp 245–274.

    Google Scholar 

  8. Bergersen F J, Kennedy G S and Wittman W 1965 Nitrogen fixation in the coralloid roots ofMacrozamia communis L. Johnson. Aust. J. Biol. Sci. 18, 1135–1142.

    Google Scholar 

  9. Bond G and Scott G D 1955 An examination of some symbiotic systems for fixation of nitrogen. Ann. Bot. 19, 67–77.

    Google Scholar 

  10. Bonnett H T and Silvester W B 1981 Specificity in theGunnera-Nostoc endosymbiosis. New Phytol. 89, 121–128.

    Google Scholar 

  11. Bothe H, Nelles H, Häger K-P, Papen H, and Neuer G 1984 Physiology and biochemistry of N2-fixation by cyanobacteria.In Advances in Nitrogen Fixation Research. Eds C Veeger and W E Newton. Martinus Nijhoff, The Hague, pp 199–210.

    Google Scholar 

  12. Bottomley P J and Van Baalen C 1978 Characteristics of heterotrophic growth in the bluegreen algaNostoc sp. strain. Mac. J. Gen. Microbiol. 107, 309–318.

    Google Scholar 

  13. Bottomley P J and Van Baalen C 1978 Dark hexose metabolism by photoautotrophically and heterotrophically grown cells of the blue-green alga (cyanobacteria)Nostoc sp. strain Mac. J. Bacteriol. 135, 888–894.

    Google Scholar 

  14. Brasell H M 1984 Nitrogen fixation associated with colonizing bryophytes.In Advances in Nitrogen Fixation Research. Eds C Veeger and W E Newton. Martinus Nijhoff, The Hague. p 48.

    Google Scholar 

  15. Calvert H E and Peters G A 1981 TheAzolla-Anabaena relationship. IX. Morphological analysis of leaf cavity hair population. New Phytol. 89, 327–335.

    Google Scholar 

  16. Calvert H E, Perkins S K and Peters, G A 1983 Sporocarp structure in the heterosporous water fernAzolla mexicana Presl. SEM III, 1499–1510.

    Google Scholar 

  17. Duckett J G, Prasad A K S K, Davies D A and Walker S 1977 A cytological analysis of theNostoc-bryophyte relationship. New Phytol. 79, 349–362.

    Google Scholar 

  18. Duckett J G, Toth R and Soni S L 1975 An ultrastructural study of theAzolla-Anabaena azollae relationship. New Phytol. 75, 111–118.

    Google Scholar 

  19. Enderlin C S and Meeks J C 1983 Pure culture and reconstitution of theAnthoceros-Nostoc symbiotic association. Planta 158, 157–165.

    Google Scholar 

  20. Fogg G E and Stewart W D P 1968In situ determinations of biological nitrogen fixation in Antarctica. Br. Antarct. Sur. Bull. 15, 39–46.

    Google Scholar 

  21. Fogg G E, Stewart W D P, Fay P and Walsby A E 1973 The Blue-Green Algae. Academic Press, New York. 459 p.

    Google Scholar 

  22. Gallon J R 1980 Nitrogen fixation by photoautotrophs.In Nitrogen Fixation. Eds (W D P Stewart and J R Gallon. Academic Press, London. pp 199–238.

    Google Scholar 

  23. Gates J E, Fisher R W, Goggin T W and Azrolan N I 1980 Antigenic differences betweenAnabaena azollae fresh from theAzolla fern leaf cavity and free-living cyanobacteria. Arch. Microbiol. 128, 126–129.

    Google Scholar 

  24. Granhall U and Hofsten A V 1976 Nitrogenase activity in relation to intracellular organisms inSphagnum mosses. Physiol. Plant. 36, 88–94.

    Google Scholar 

  25. Grilli Caiola M 1980 On the phycobionts of the cycad coralloid roots. New Phytol. 85, 537–544.

    Google Scholar 

  26. Grobbelaar N, Small J G C, Marshall J and Hattingh W 1984 Metabolic studies on the coralloid roots ofEncephalartos transvenosus and its endophyte.In Advances in Nitrogen Fixation Research. Eds. C Veeger and W E Newton. Martinus Nijhoff, The Hague. p 54.

    Google Scholar 

  27. Grobbellar N, Strauss J M and Groenewald E G 1971 Non-leguminous seed plants in southern Africa which fix nitrogen symbiotically. Plant and Soil Spec. Vol. 325–341.

  28. Gunning B E S and Pate J S 1974 Transfer cells.In Dynamic Aspects of Plant Ultrastructure. Ed. A W Robards. McGraw Hill, U.K. pp 441–480.

    Google Scholar 

  29. Halliday J and Pate J S 1976 Symbiotic nitrogen fixation by coralloid roots of cycadMacrozamia riedlei: Physiological characteristics and ecological significance. Aust. J. Plant Physiol. 3, 349–358.

    Google Scholar 

  30. Haselkorn R, Mazur B, Orr J, Rice D, Wood N and Rippka R 1980 Heterocysts differentiation and nitrogen fixation in cyanobacteria (blue-green algae)In Nitrogen Fixation, Vol. II. Eds W E Newton and W H Orme-Johnson. University Park Press, Baltimore. pp 259–278.

    Google Scholar 

  31. Hill D J 1975 The pattern of development ofAnabaena in theAzolla-Anabaena symbiosis. Planta 122, 179–184.

    Google Scholar 

  32. Hill D J 1977 The role ofAnabaena in theAzolla-Anabaena symbiosis. New Phytol. 78, 611–616.

    Google Scholar 

  33. Hitch J B and Millbank J W 1975 Nitrogen metabolism in lichens. VII. Nitrogenase activity and heterocyst frequency in lichens with blue-green phycobionts. New Phytol. 75, 239–244.

    Google Scholar 

  34. Hitch C J B and Stewart W D P 1973 Nitrogen fixation by lichens in Scotland. New Phytol. 72, 509–524.

    Google Scholar 

  35. Kaplan D and Peters G A 1981Azolla-Anabaena reltionship. X.15N2 fixation and transport in main stem axes. New Phytol. 89, 337–346.

    Google Scholar 

  36. Kershaw K A Millbank J W 1970 Nitrogen metabolism in lichens. II. The partition of cephalodial-fixed nitrogen between the mycobiont and phycobionts ofPeltigera aphthosa. New Phytol. 69, 75–79.

    Google Scholar 

  37. Kobiler D, Cohen-Sharon A and Tel-Or E 1981 Recognition between the N2-fixingAnabaena and the water fernAzolla. FEBS Lett. 133, 157–160.

    Google Scholar 

  38. Ladha J K and Watanabe I 1982 Antigenic similarity amongAnabaena azollae separated from different species ofAzolla. Biochem. Biophys. Res. Commun. 109, 675–682.

    Google Scholar 

  39. Ladha J K and Watanabe I 1984 Antigenic analysis ofAnabaena azollae and presence of lectin inAzolla-Anabaena association.In Advances in Nitrogen Fixation Research. Eds. C Veeger and W E Newton. Martinus Nijhoff, The Hague. p. 421.

    Google Scholar 

  40. Lindbald P 1984 Diversion between C2H2 reduction and heterocyst frequency in a cycad root.In Advances in Nitrogen Fixation Research. Eds C Veeger and W E Newton. Martinus Nijhoff, The Hague. p. 511.

    Google Scholar 

  41. Liu C C 1979 Use ofAzolla in rice production in China.In Nitrogen and Rice. IRRI (eds). International Rice Research Institute, Los Banos, Laguna, Philippines. pp 375–394

    Google Scholar 

  42. Liu C C, Wei W-C and Zheng D-Y 1984 Some advances inAzolla Research.In Advances in Nitrogen Fixation Research. Eds C Veeger and W E Newton. Martinus Nijhoff, The Hague. p. 57.

    Google Scholar 

  43. Lockhart C M, Rowell P and Stewart W D P 1978 Phytohaemagglutinins from the nitrogenfixing lichensPeltigera canina andP. polydactyla. FEMS Microbiol Lett. 3, 127–130.

    Google Scholar 

  44. Lumpkin T A 1983 Taxonomy, physiology and agronomic potential ofAzolla spp. Thesis, University of Hawaii. 179 pp.

  45. Lumpkin T A and Plucknett D L 1982Azolla as a Green Manure: Use and Management in Crop Production. Westview Press, Boulder, Colorado. 230 pp.

    Google Scholar 

  46. Meeks J C, Enderlin C S, Wycoff K L, Chapman J S and Joseph C M 1983 Assimilation of13NH +4 byAnthoceros grown with and without symbioticNostoc. Planta 158, 384–391.

    Google Scholar 

  47. Mellor R B, Gadd G M, Rowell P and Stewart W D P 1981 A phytohaemagglutinin from theAzolla-Anabaena symbiosis. Biochem. Biophys. Res. Commun. 99, 1348–1353.

    Google Scholar 

  48. Milindasuta B-E 1975 Developmental anatomy of coralloid roots in cycads. Am. J. Bot. 62, 468–472.

    Google Scholar 

  49. Millbank J W 1974 Associations with blue-green algae.In The Biology of Nitrogen Fixation. Ed. A Quispel. Elsevier, New York. pp. 238–264.

    Google Scholar 

  50. Millbank J W 1977 Lower plant associations.In A Treatise on Dinitrogen Fixation, Sec III. Eds R W F Hardy and W S Silver. John Wiley and Sons, Inc., New York. pp 125–152.

    Google Scholar 

  51. Millbank J W and Olsen J D 1981 The assessment of nitrogen fixation and throughput by lichens. I. The use of a controlled environment chamber to relate acetylene reduction estimates to nitrogen fixation. New Phytol. 89, 657–665.

    Google Scholar 

  52. Misra S B 1984 Use ofAzolla biofertilizer as dual cropping in rice cultivation. Thesis, Berhampur University, India. 350 p.

    Google Scholar 

  53. Moore A W 1969Azolla: Biology and agronomic significance. Bot. Rev. 35, 17–34

    Google Scholar 

  54. Nathanielsz C P and Staff I A 1975 A mode of entry of blue-green algae into the apogeotropic roots ofMacrozamia communis. Am. J. Bot. 62, 232–235.

    Google Scholar 

  55. Newton J W and Herman A I 1979 Isolation of cyanobacteria from the aquatic fern,Azolla. Arch. Microbiol. 120, 161–165.

    Google Scholar 

  56. Nguyen T H and Nguyen N H 1984 Isolation and culture ofAnabaena azollae in vitro.In Advances in Nitrogen Fixation Research. Eds C Veeger and W E Newton. Martinus Nijhoff. The Hague. p. 517.

    Google Scholar 

  57. Orr J and Haselkorn R 1982 Regulation of glutamine synthetase activity and synthesis in free-living and symbioticAnabaena spp. J. Bacteriol. 152, 626–635.

    Google Scholar 

  58. Peters G A and Calvert H E 1982 TheAzolla-Anabaena symbioses.In Advances in Agricultural Microbiology. Ed. N S Subba Rao. Oxford and IBH Publ. Co., Bombay. pp 191–218.

    Google Scholar 

  59. Peters G A and Calvert H E 1983 TheAzolla-Anabaena azollae symbiosis.In Algal Symbiosis. Ed. L J Goff. Cambridge University Press, New York. pp 109–145.

    Google Scholar 

  60. Peters G A, Toia Jr R E, Evans W R, Crist D K, Mayne B C and Poole R E 1980 Characterization and comparisons of five N2-fixingAzolla-Anabaena associations. I. Optimization of growth conditions for biomass increase and N content in a controlled environment. Plant Cell Environ. 3, 261–269.

    Google Scholar 

  61. Peters G A, Ito O, Tyagi V V S, and Kaplan D 1981 Physiological studies on N2-fixingAzolla.In Genetic Engineering of Symbiotic Nitrogen Fixation and Conservation of Fixed Nitrogen. Ed. J M Lyons, Plenum Publishing Corporation, New York. pp 342–362.

    Google Scholar 

  62. Peters G A, Calvert H E, Kaplan D, Ito O and Toia Jr R E 1982 TheAzolla-Anabaena symbiosis: Morphology, physiology and use. Israel J. Bot. 31, 305–323.

    Google Scholar 

  63. Peters G A, Kaplan D, Meeks J C, Buzby K M, Marsh B H and Corbin J L 1984 Aspects of nitrogen and carbon interchange in theAzolla-Anabaena symbiosis.In Nitrogen Fixation and CO2 Metabolism. Eds P L Ludden and J E Burris. Elsevier, New York. pp 213–222.

    Google Scholar 

  64. Rai A N, Rowell P and Stewart W D P 1980 NH +4 assimilation and nitrogenase regulation in the lichenPeltigera aphthosa Willd. New Phytol. 85, 545–555.

    Google Scholar 

  65. Rai A N, Rowell P and Stewart W D P 1981 Glutamate synthase activity in symbiotic cyanobacteria. J. Gen. Microbiol. 126, 515–518.

    Google Scholar 

  66. Rai A N, Rowell P and Stewart W D P 1981 Nitrogenase activity and dark CO2 fixation in the lichenPeltigera aphthosa Willd. Planta 151, 256–264.

    Google Scholar 

  67. Ray T B, Peters G A, Toia Jr R E and Mayne B C 1978Azolla-Anabaena relationship. VII. Distribution of ammonia-assimilating enzymes, protein, and chlorophyll between host and symbiont. Plant Physiol 62, 463–467.

    Google Scholar 

  68. Ray T B, Mayne B C, Toia Jr R E and Peters G A 1979Azolla-Anabaena relationship. VIII. Photosynthetic characterization of the association and individual partners. Plant Physiol. 64, 791–795.

    Google Scholar 

  69. Ridgeway J E 1967 The biotic relationship ofAnthoceros andPhaeoceros to certain cyanophyta. Ann. Mo. Bot. Gdn. 54, 95–102.

    Google Scholar 

  70. Rodgers G A and Stewart W D P 1977 The cyanophyte-hepatic symbiosis. I. Morphology and physiology. New Phytol. 78, 441–458.

    Google Scholar 

  71. Schopf J W 1970 Precambrian microorganisms and evolutionary events prior to the origin of vascular plants. Biol. Rev. 45, 319–352.

    Google Scholar 

  72. Silvester W B 1975 Endophyte adaptation inGunnera-Nostoc symbiosis.In Symbiotic Nitrogen Fixation in Plants. Ed. P S Nutman. Cambridge University Press, Cambridge. pp. 521–538.

    Google Scholar 

  73. Silvester W B 1977 Dinitrogen fixation by plant associations excluding legumes.In A Treatise on Dinitrogen Fixation, Section IV. Eds R W F Hardy and A H Gibson. John Wiley and Sons Inc., New York. pp 141–150.

    Google Scholar 

  74. Silvester W B and McNamara P J 1976 The infection process and ultrastructure of theGunnera-Nostoc symbiosis. New Phytol. 77, 135–141.

    Google Scholar 

  75. Silvester W B and Smith D R 1969 Nitrogen fixation byGunnera-Nostoc symbiosis. Nature 224, 1231.

    Google Scholar 

  76. Singh P K 1977 Multiplication and utilization of fernAzolla containing nitrogen-fixing algal symbiont as green manure in rice cultivation. Il Riso 26, 125–137.

    Google Scholar 

  77. Singh P K 1979 Symbiotic algal N2-fixation and crop productivity.In Annual Review of Plant Sciences. Ed. C P Malik. Kalyani Publishers, New Delhi, India. pp. 37–65.

    Google Scholar 

  78. Singh P K 1980 Introduction of greenAzolla biofertilizer in India. Curr. Sci. 49, 155–156.

    Google Scholar 

  79. Singh P K and Misra S P 1982 Effects of herbicides on growth and N2 fixation ofAzolla pinnata under field conditions. J. Biol. Res. 2, 91–96.

    Google Scholar 

  80. Spratt E R 1915 The root nodules of the Cycadaceae. Ann. Bot. 29, 619–626.

    Google Scholar 

  81. Stewart W D P 1980 Some aspects of structure and function in N2-fixing cyanobacteria. Annu. Rev. Microbiol. 34, 497–536.

    Google Scholar 

  82. Stewart W D P and Rogers G A 1977 The cyanophyte-hepatic symbiosis. II. Nitrogen fixation and the interchange of nitrogen and carbon. New Phytol. 78, 459–471.

    Google Scholar 

  83. Stewart W D P and Rodgers G A 1978 Studies on the symbiotic blue-green algae ofAnthoceros, Blasia andPeltigera. Ecol. Bull. (Stockholm) 26, 247–259.

    Google Scholar 

  84. Stewart W D P and Rowell P 1977 Modifications of nitrogen-fixing algae in lichen symbioses. Nature 265, 371–372.

    Google Scholar 

  85. Stewart W D P, Rowell P and Rai A N 1980 Symbiotic nitrogen-fixing cyanobacteria.In Nitrogen Fixation. Eds. W D P Stewart and J R Gallon. Academic Press, London. pp. 239–277.

    Google Scholar 

  86. Stewart W D P, Rai A N, Reed R H, Creach E, Codd G A and Rowell P 1981 Studies on the N2 fixing lichenPeltigera aphthosa.In Current Perspectives in Nitrogen Fixation. Eds. A H Gibson and W E Newton. Australian Academy of Science, Canberra. pp 237–243.

    Google Scholar 

  87. Subudhi B P R and Watanabe I 1981 Differential phosphorus requirements ofAzolla species and strains in phosphorus-limited continuous culture. Soil Sci. Plant Nutr. 27, 237–247.

    Google Scholar 

  88. Talley S N and Rains D W 1980Azolla as a nitrogen source for temperate rice.In Nitrogen Fixation, Vol. II. Eds W E Newton and W H Orme-Johnson. University Park Press, Baltimore. pp 311–320.

    Google Scholar 

  89. Talley S N and Rains D W 1980Azolla filiculoides Lam. as a fallow-season green manure for rice in temperate climate. Agron. J. 72, 11–18.

    Google Scholar 

  90. Talley S N, Talley B J and Rains D W 1977 Nitrogen fixation byAzolla in rice fields.In Genetic Engineering for Nitrogen Fixation. Ed. A Hollaender. Plenum Press, New York. pp 259–281.

    Google Scholar 

  91. Tel-Or E and Sandovsky T 1982 The response of the nitrogen-fixing cyanobacteriumAnabaena azollae to combined nitrogen compounds and sugar. Israel J. Bot. 31, 329–336.

    Google Scholar 

  92. Tel-Or E, Sandovsky T, Arad H, Keysary A and Kobiler D 1984 The unique properties of the symbioticAnabaena azollae in the water fernAzolla: Metabolism and intercellular recognition.In Advances in Nitrogen Fixation Research. Eds C Veeger and W E Newton. Martinus Nijhof, The Hague, pp 461–465.

    Google Scholar 

  93. Tuan D T and Thuyet T Q 1979 Use ofAzolla in rice production in Vietnam.In Nitrogen and Rice. IRRI (eds). International Rice Research Institute. Los Banos Philippines. pp 395–406.

    Google Scholar 

  94. Tung H F and Thuyet T Q 1979 Use ofAzolla in rice production in Vietnam.In Nitrogen and Rice. IRRI (eds) International Rice Research Institute. Los Banos, Philippines. pp 395–406.

    Google Scholar 

  95. Tyagi V V S, Mayne B C and Peters G A 1980 Purification and initial characterization of phycobiliproteins from the endophytic cyanobacterium ofAzolla. Arch. Microbiol. 128, 41–44.

    Google Scholar 

  96. Tyagi V V S, Ray T B, Mayne B C and Peters G A 1981 TheAzolla-Anabaena relationship. XI. Phycobiliproteins in the action spectrum for nitrogenase-catalyzed acetylene reduction. Plant Physiol. 68, 1479–1484.

    Google Scholar 

  97. Venkataraman G S 1962 Studies on nitrogen fixation by blue-green algae. III. Nitrogen fixation byAnabaena azollae. Ind. J. Agri. Sci. 32, 22–24.

    Google Scholar 

  98. Watanabe I 1982Azolla-Anabaena symbiosis — its physiology and use in tropical agriculture.In Microbiology of Tropical Soils and Plant Productivity. Eds Y R Dommergues and H G Diem. Martinus Nijhoff, The Hague. pp 169–185.

    Google Scholar 

  99. Watanabe I, Berja N S and Alimagno B V 1977 Utilization of theAzolla-Anabaena complex as a nitrogen fertilizer for rice. IIR Research Paper Series 11, 1–15.

    Google Scholar 

  100. Watanabe I, Berja N S and Del Rosario D C 1980 Growth ofAzolla in paddy field as affected by phosphorus fertilizer. Soil Sci. Plant Nutr. 26, 301–307.

    Google Scholar 

  101. Whitton B A 1973 Interactions with other organisms.In The Biology of the Blue-Green Algae. Eds N G Carr and B A Whitton. University of California Press, Berkeley. pp 415–433.

    Google Scholar 

  102. Wieringa K T 1968 A new method for obtaining bacteria-free cultures of blue-green algae. Antonie Van Leeuwenhoek 34, 54–56.

    Google Scholar 

  103. Wittman W, Bergersen F J and Kennedy G S 1965 The coralloid roots ofMacrozamia communis L. Johnson. Aust. J. Biol. Sci. 18, 1129–1134.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Peters, G.A., Toia, R.E., Calvert, H.E. et al. Lichens toGunnera — with emphasis onAzolla . Plant Soil 90, 17–34 (1986). https://doi.org/10.1007/BF02277384

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02277384

Key words

Navigation