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Structural Characteristics of the Cyanobacterium–Azolla Symbioses

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Prokaryotic Symbionts in Plants

Part of the book series: Microbiology Monographs ((MICROMONO,volume 8))

Abstract

Structure is a fundamental base for all life forms, whether plants or microbes. The development of special structures results in unique functions. Though structures of the mutualistic Azolla–cyanobacterial symbiosis are still largely un-explored, they have attracted attention of researchers in the past two decades. The occurrence of the leaf cavity and trichomes within the water-fern Azolla are hallmarks for the two cyanobacterial–plant symbiotic systems. The trichomes and the multicellular filaments are suggested to be involved in metabolic exchange between the cyanobionts and host plants due to their cell wall ingrowths, i.e., transfer cell characteristics. At the apical region of the Azolla plant, the primary branched trichomes touch each other, thereby forming linked bridge-like structures that lead to partitioning of the cyanobacteria into the young leaf cavities, thus promoting horizontal transfer of the cyanobiont during vegetative growth and asexual reproduction via sporophyte fragmentation. The trichomes developing during the sexual reproduction stages of Azolla facilitate the partitioning of the motile cyanobiont into the sporocarps, thus promoting a vertical transfer of cyanobacteria between Azolla generations, a capacity unique among cyanobacterial–plant symbioses. The cyanobionts in Azolla, Blasia and Anthoceros undergo pronounced morphological, physiological and molecular modifications to keep a synchronized development with the plant partner and to meet needs for maintaining a mutualistic symbiosis.

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References

  • Adams DG (2000) Symbiotic interaction. In: Whitton B, Potts M (eds) Ecology of Cyanobacteria: Their Diversity in Time and Space. Kluwer Academic Publishers, Dordrecht, pp 523–561

    Google Scholar 

  • Amman RI, Ludwig W, Schleifer K-H (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169

    Google Scholar 

  • Becking JH (1987) Endophyte transmission and activity in the Anabaena–Azolla association. Plant Soil 100:183–212

    Article  Google Scholar 

  • Bergman B, Matveyev A, Rasmussen U (1996) Chemical signaling in cyanobacterial–plant symbioses. Trends Plant Sci 1:191–197

    Article  Google Scholar 

  • Bergman B, Rai AN, Rasmussen U (2007) Cyanobacteria associations. In: Elmerich C, Newton WE (eds) Associative and Endophytic Nitrogen-fixing Bacteria and Cyanobacterial Associations. Springer, Dordrecht, pp 257–302

    Chapter  Google Scholar 

  • Braun-Howland EB, Lindblad P, Nierzwicki-Bauer SA (1988) Dinitrogenase reductase (Fe protein) of nitrogenase in the cyanobacterial symbints of three Azolla species: localization and sequence of appearance during heterocyst differentiation. Planta 176:319–332

    Article  CAS  Google Scholar 

  • Braun-Howland EB, Nierzwicki-Bauer SA (1990) Azolla–Anabaena symbiosis: biochemistry, physiology, ultrastructure and molecular biology. In: Rai AN (ed) CRC Handbook of Symbiotic Cyanobacteria. CRC Press, Boca Raton, FL, pp 65–117

    Google Scholar 

  • Calvert HE, Perkins SK, Peters GA (1984) Involvement of epidermal trichomes in the continuity of the Azolla–Anabaena symbiosis through the Azolla life cycle. Am J Bot 72:808 (Abstr)

    Google Scholar 

  • Calvert HE, Pence MK, Peters GA (1985) Ultrastructural ontogeny of leaf cavity trichomes in Azolla implies a functional role in metabolite exchange. Protoplasma 129:10–27

    Article  Google Scholar 

  • Calvert HE, Peters GA (1981) The Azolla–Anabaena azollae relationship. IX. Morphological analysis of leaf cavity hair populations. New Phytol 89:327–335

    Article  Google Scholar 

  • Canini A, Grilli Caiola MG, Mascini M (1990) Ammonium content, nitrogenase activity and heterocyst frequency within the leaf cavies of Azolla filiculoides Lam. FEMS Microbiol Lett 71:205–210

    Article  CAS  Google Scholar 

  • Canini A, Grilli Caiola MG, Bertocchi P, Lavagnini MG, Mascini M (1992) Ion determinations within Azolla leaf cavities by microelectrodes. Sens Actuator B 7:431–435

    Article  Google Scholar 

  • Canini A, Albertano P, Grilli Caiola MG (1993) Subcellular localization of calcium in Azolla–Anabaena symbiosis by chlorotetracycline, ESI and EELS. Bot Acta 106:146–153

    CAS  Google Scholar 

  • Carrapico F (1991) Are bacteria the 3rd partner of the Azolla–Anabaena symbiosis? Plant Soil 137:157–160

    Article  Google Scholar 

  • Duckett JG, Toth R, Soni SL (1975) An ultrastructural study of the Azolla–Anabaena relationship. New Phytol 75:111–118

    Article  Google Scholar 

  • Forni C, Grilli Caiola MG, Gentili S (1989) Bacteria in the Azolla–Anabaena symbiosis. In: Skinner AF, Boddey RM, Fendrik I (eds) Nitrogen Fixation with Non-legume. Kluwer Academic Publishers, Dordrecht, pp 83–88

    Google Scholar 

  • Forni C, Gentili S, van Hove C, Grilli Caiola MG (1990) Isolation and characterization of the bacteria living in the sporocarps of Azolla filiculoides Lam. Ann Microbiol 40:235–243

    Google Scholar 

  • Forni C, Riov J, Grilli Caiola MG, Tel-or E (1992a) Indole-3 acetic acid (IAA) production by Arthrobacter species isolated from Azolla. J Gen Microbiol 138:377–381

    PubMed  CAS  Google Scholar 

  • Forni C, Haegi A, Delogallo M, Grilli Caiola MG (1992b) Production of polysaccharides by Arthrobacter globiformis associated with Anabaena azollae in Azolla leaf cavity. FEMS Microbiol Lett 93:269–274

    Article  CAS  Google Scholar 

  • Forni C, Gaegi A, Del Gallo M (1998) Polysaccharide composition of the mucilage of Azolla algal packet. Symbiosis 24:303–313

    CAS  Google Scholar 

  • Gates JE, Fisher RW, Candle RA (1980) The occurrence of corynoforme bacteria in the leaf cavity of Azolla. Arch Microbiol 127:163–165

    Article  Google Scholar 

  • Grilli Caiola MG (1964) Infrastructure di Anabaena azollae vivente nelle foglioline di Azolla caroliniana. Ann Microbiol 14:69–90

    Google Scholar 

  • Grilli Caiola MG, Canini A, Moscone D (1989) Oxygen concentration, nitrogenase activity and heterocyst frequency in the leaf cavities of Azolla filiculoides Lam. FEMS Microbiol Lett 59:283–288

    Article  CAS  Google Scholar 

  • Grilli Caiola MG, Forni C, Castagnola M (1993) Anabaena azollae akinetes in the sporocarps of Azolla filiculoides Lam. Symbiosis 14:247–264

    Google Scholar 

  • Hill DJ (1975) The pattern of development of Anabaena in the Azolla–Anabaena symbiosis. Planta 122:179–184

    Article  Google Scholar 

  • Hill DJ (1977) The role of Anabaena in the Azolla–Anabaena symbiosis. New Phytol 78:611–616

    Article  Google Scholar 

  • Konar RN, Kapoor RK (1972) An anatomic study of Azolla pinnata. Phytomorphology 22:211–223

    Google Scholar 

  • Lang NJ (1965) Electron microscopic study of heterocyst development in Anabaena azollae Strasburger. J Phycol 1:127–134

    Article  Google Scholar 

  • Lechno-Yossef S, Nierzwicki-Bauer SA (2002) Azolla–Anabaena symbiosis. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in Symbiosis. Kluwer Academic Publishers, Dordrecht, pp 153–178

    Google Scholar 

  • Lindblad P, Bergman B, Nierzwicki-Bauer SA (1991) Immunocytochemical localization of nitrogenase in bacteria symbiotically associated with Azolla spp. Appl Environ Microbiol 57:3637–3640

    PubMed  CAS  Google Scholar 

  • Lumpkin TA, Plucknett DL (1980) Azolla: botany, physiology, and use as a green manure. Econ Bot 34:111–153

    Article  CAS  Google Scholar 

  • Meeks JC (1998) Symbiosis between nitrogen-fixing cyanobacteria and plants. Bioscience 48:266–276

    Article  Google Scholar 

  • Moore AW (1969) Azolla: biology and agronomic significance. Bot Rev 35:17–34

    Article  CAS  Google Scholar 

  • Neumüller M, Bergman B (1981) The ultrastructure of Anabaena azollae in Azolla pinnata. Physiol Plant 51:69–76

    Article  Google Scholar 

  • Nierzwicki-Bauer SA, Aulfinger H (1990) Ultrastructural characterization of eubacteria residing within leaf cavities of symbiotic and cyanobiont-free Azolla mexicana. Curr Microbiol 21:123–129

    Article  Google Scholar 

  • Nierzwicki-Bauer SA, Aulfinger H (1991) Occurrence and ultrastructural characterization of bacteria in association with Azolla. Appl Environ Microbiol 57:3629–3636

    PubMed  CAS  Google Scholar 

  • Nierzwicki-Bauer SA, Aulfinger H, Braun-Howland EB (1989) Ultrastructural characterization of an inner envelope that confines Azolla endosymbionts to the leaf cavity periphery. Can J Bot 67:2711–2719

    Article  Google Scholar 

  • Perkins SK, Peters GA (1993) The Azolla–Anabaena symbiosis: endophyte continuity in the Azolla life-cycle is facilitated by epidermal trichomes. I. Partitioning of the endophytic Anabaena into developing sporocarps. New Phytol 123:53–64

    Article  Google Scholar 

  • Peters GA (1976) Studies on the Azolla–Anabaena azollae symbiosis. In: Newton WE, Nyman CJ (eds) Proc 1st International Symposium on Nitrogen Fixation. Washington University Press, Washington DC, pp 592–610

    Google Scholar 

  • Peters GA, Calvert HE (1983) The Azolla–Anabaena azollae symbiosis. In: Goff LJ (ed) Algal Symbiosis. Combridge University Press, New York, pp 109–145

    Google Scholar 

  • Peters GA, Toia RE Jr, Raveed D, Levine NJ (1978) The Azolla–Anabaena azollae relationship. VI. Morphological aspects of the association. New Phytol 80:583–593

    Article  Google Scholar 

  • Peters GA, Meeks JC (1989) The Azolla–Anabaena symbiosis: basic biology. Annu Rev Plant Physiol Plant Mol Biol 40:193–210

    Article  Google Scholar 

  • Peters GA, Perkins SK (1993) The Azolla–Anabaena symbiosis: endophyte continuity in the Azolla life-cycle is facilitated by epidermal trichomes. II. Re-establishment of the symbiosis following gametogenesis and embryogenesis. New Phytol 123:65–75

    Article  Google Scholar 

  • Plazinski J (1990) The Azolla-Anabaena symbiosis. In: Gresshoff PM (eds) The Molecular Biology of Symbiotic Nitrogen Fixation. CRC Press, Boca Raton, pp 51–75

    Google Scholar 

  • Plazinski J, Taylor R, Shaw W, Croft L, Rolfe BG, Gunning BES (1990) Isolation of Agrobacterium sp. strain from the Azolla leaf cavity. FEMS Microbiol Lett 70:55–59

    Article  CAS  Google Scholar 

  • Sadebeck R (1902) Salviniaceae. In: Engler A, Prantl K (eds) Natürliche Pflanzenfamilien, I. Teil, 4. Abt. Wilhelm Engelmann, Leipzig, pp 383–402

    Google Scholar 

  • Schaede R (1947) Untersuchungen über Azolla und ihre Symbiose mit Blaualgen. Planta 35:319–330

    Article  Google Scholar 

  • Serrano R, Carrapico F, Vidal R (1999) The presence of lectins in bacteria associated with Azolla–Anabaena symbiosis. Symbiosis 15:169–178

    Google Scholar 

  • Shen YET (1961) Concerning Azolla imbricate. Am Fern J 51:151–155

    Article  Google Scholar 

  • Shi DJ, Hall DO (1988) The Azolla–Anabaena association: historical perspective, symbiosis and energy metabolism. Bot Rev 54:353–386

    Article  Google Scholar 

  • Smith GM (1938) Salviniaceae. In: Cryptogamic Botany, Vol 2. McGraw-Hill Inc., New York, pp 353–362

    Google Scholar 

  • Sutherland JM, Stewart WDP, Herdman M (1985) Akinetes of the cyanobacterium Nostoc PCC 7524: morphological changes during synchronous germination. Arch Microbiol 122:269–274

    Article  Google Scholar 

  • Uheda E, Kitoh S, Dohmanu T, Shiomi N (1995) Isolation and analysis of gas bubbles in the cavities of Azolla leaves. Physiol Plant 93:1–4

    Article  CAS  Google Scholar 

  • Vessey JK, Pawlowski K, Bergman B (2005) Root-based N2-fixing symbioses: legumes, actinorhizal plants, Parasponia sp. and cycads. Plant Soil 274:51–78

    Article  CAS  Google Scholar 

  • Veys P, Waterkeyn L, Lejeune A, van Hove C (1999) The pore of the leaf cavity of Azolla: morphology, cytochemistry and possible functions. Symbiosis 27:33–57

    Google Scholar 

  • Veys P, Lejeune A, van Hove C (2000) The pore of the leaf cavity of Azolla: Interspecific morphological differences and continuity between the cavity envelopes. Symbiosis 29:33–47

    Google Scholar 

  • Veys P, Lejeune A, van Hove C (2002) The of leaf cavity of Azolla: Teat-cell differentiation and cell wall projections. Protoplasma 219:31–42

    Article  PubMed  CAS  Google Scholar 

  • Walmsley RD, Breen CM, Kyle E (1973) Aspects of the fern–algal relationship in Azolla filiculoides. News Lett Limnol Soc S Afr 20:13–16

    Google Scholar 

  • Wallace WH, Gates JE (1986) Identification of eubacteria isolated from leaf cavities of 4 species the N2-fixing Azolla fern as Arthrobacter Conn and Dimmick. Appl Environ Microbiol 55:425–429

    Google Scholar 

  • Wildman RB, Loescher JH, Winger CL (1975) Development and germination of akinetes of Aphanizomenon flos-aquae. J Phycol 11:96–104

    Google Scholar 

  • Zheng WW (1991) Occurrence of bacteria in Azolla–Anabaena association and their interaction. J Electron Microsc China 15:54–56

    Google Scholar 

  • Zheng WW, Huang JH (1994) New data on the infection of the developing sporocarps with the symbionts of Azolla sporulation. J Fujian Acad Agric Sci 9:49–54

    Google Scholar 

  • Zheng WW, Huang JH, Lu PJ, Liu CC (1986) The ultrastructure of Azolla and Anabaena-free Azolla. J Fujian Agric Coll 15:211–219

    Google Scholar 

  • Zheng WW, Lin YH, Lu PJ, Liu CC (1987) Scanning electron microscopic observation of symbiotic relationship of Azolla–Anabaena azollae during the vegetative growth. Acta Bot Sinica 29:588–593

    Google Scholar 

  • Zheng WW, Lin YH, Lu PJ, Liu CC (1988) Electron microscopic observation of symbiotic relationship between Azolla and Anabaena azollae during the formation of the sporocarp of Azolla. Acta Bot Sin 30:664–666

    Google Scholar 

  • Zheng WW, Lin YH, Lin YH, Lu PJ, Liu CC (1990) Electron microscopic observation of symbiotic relationship between Azolla and Anabaena during the megaspore germination and sporeling development of Azolla. Acta Bot Sin 32:514–520

    Google Scholar 

  • Zheng WW, Liu LH, Xiu WQ (1998) The fate and ultrastrucural changes of Anabaena azollae within the developing sporocarps of Azolla. Fujian J Agric 13:1–8

    Google Scholar 

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Authors and Affiliations

  1. Biotechnology Institute, Fujian Academy of Agricultural Sciences, 350003, Fuzhou, Fujian, China

    Weiwen Zheng

  2. Department of Botany, Stockholm University, 10691, Stockholm, Sweden

    Liang Rang & Birgitta Bergman

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  1. Weiwen Zheng
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  2. Liang Rang
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  3. Birgitta Bergman
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Correspondence to Weiwen Zheng .

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Katharina Pawlowski

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Zheng, W., Rang, L., Bergman, B. (2008). Structural Characteristics of the Cyanobacterium–Azolla Symbioses. In: Pawlowski, K. (eds) Prokaryotic Symbionts in Plants. Microbiology Monographs, vol 8. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7171_2008_120

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