Skip to main content
SpringerLink
Log in
Book cover

The Prokaryotes pp 359–400Cite as

Cyanobacterial-Plant Symbioses

  • Reference work entry

Abstract

Cyanobacteria are a large group of photoautotrophic prokaryotes found in almost every environment and frequently in great abundance, particularly in the oceans. They form symbiotic relationships with a broad range of eukaryotic hosts including plants, fungi, and animals such as corals, sponges, and ascidians (sea squirts). The plant and fungal symbioses are the subject of this chapter. Within the host, the cyanobacterial symbionts (cyanobionts) are protected from environmental extremes and predation, in turn supplying the host with fixed nitrogen and, in the case of nonphotosynthetic hosts, fixed carbon. Many cyanobacteria are facultative heterotrophs, enabling them to occupy regions of the host receiving little or no light, such as the roots of plants, where they receive fixed carbon from their photosynthetic partner. In the vast majority of these symbioses, the cyanobionts are capable of independent growth, but in symbiosis they often undergo morphological and physiological modifications. In many filamentous cyanobionts, nitrogen fixation occurs in specialized cells known as heterocysts which, in free-living cyanobacteria, constitute less than 10 % of total cells. In many plant and some lichen symbioses, the heterocyst frequency is elevated four- to fivefold, as is the rate of nitrogen fixation. A number of these symbioses are of major environmental importance as suppliers of fixed nitrogen to their surroundings. For example, moss associations with epiphytic cyanobacteria are abundant in northern hemisphere forests, and cyanolichens are abundant in harsh environments where there are few other sources of fixed nitrogen.

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

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   699.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD   549.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Adams DG (2000) Symbiotic interactions. In: Whitton B, Potts M (eds) Ecology of cyanobacteria: their diversity in time and space. Kluwer, Dordrecht, pp 523–561

    Google Scholar 

  • Adams DG (2002a) Cyanobacteria in symbiosis with hornworts and liverworts. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in symbiosis. Kluwer, Dordrecht, pp 117–135

    Google Scholar 

  • Adams DG (2002b) The liverwort-cyanobacterial symbiosis. Biol Environ Proc R Ir Acad 102B:27–30

    Google Scholar 

  • Adams DG, Duggan P (1999) Heterocyst and akinete differentiation in cyanobacteria: Tansley Review No. 107. New Phytol 144:3–33

    Google Scholar 

  • Adams DG, Duggan PS (2008) Cyanobacteria-bryophyte symbioses. J Exp Bot 59:1047–1058

    PubMed  CAS  Google Scholar 

  • Adams DG, Duggan PS (2012) Signalling in cyanobacteria-plant symbioses. In: S. Perotto S, Baluska F (eds) Signaling and communication in plant symbiosis. Springer, Heidelberg, pp 93–121

    Google Scholar 

  • Adams DG, Duggan PS, Jackson O (2012) Cyanobacterial symbioses. In: Whitton B (ed) Ecology of cyanobacteria II: their diversity in time and space. Springer, Heidelberg, pp 593–647

    Google Scholar 

  • Adams DG, Bergman B, Nierzwicki-Bauer SA, Rai AN, Schussler A (2006) Cyanobacterial-plant symbioses. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes. A handbook on the biology of bacteria, vol 1, 3rd edn, Symbiotic associations, biotechnology, applied microbiology. Springer, New York, pp 331–363

    Google Scholar 

  • Ahern CP, Staff IA (1994) Symbiosis in cycads: the origin and development of coralloid roots in Macrozamia communis (Cycadaceae). Am J Bot 81:1559–1570

    Google Scholar 

  • Ahmadjian V (1993) The lichen symbiosis. Wiley, New York

    Google Scholar 

  • Anbudurai PR, Mor TS, Ohad I, Shestakov SV, Pakrasi HB (1994) The ctpA gene encodes the C-terminal processing protease for the D1 protein of the photosystem II reaction center complex. Proc Natl Acad Sci USA 91:8082–8086

    PubMed  CAS  Google Scholar 

  • Aptroot A (1998) Aspects of the integration of the taxonomy of lichenized and non-lichenized pyrenocarpoous ascomycetes. Lichenologist 30:501–514

    Google Scholar 

  • Aulfinger H, Braun-Howland EB, Kannaiyan S, Nierzwicki-Bauer SA (1991) Ultrastructural changes of the endosymbionts of Azolla microphylla during megaspore germination and early plantlet development. Can J Bot 69:2489–2496

    Google Scholar 

  • Babic S (1996) Hormogonia formation and the establishment of symbiotic associations between cyanobacteria and the bryophytes Blasia and Phaeoceros. PhD thesis, University of Leeds, Leeds

    Google Scholar 

  • Baker J, Entsch B, McKay DB (2003) The cyanobiont in an Azolla fern is neither Anabaena nor Nostoc. FEMS Microbiol Lett 229:43–47

    PubMed  CAS  Google Scholar 

  • Banack SA, Cox PA (2003) Biomagnification of cycad neurotoxins in flying foxes: implications for ALS-PDC in Guam. Neurology 61:387–389

    PubMed  CAS  Google Scholar 

  • Banack SA, Murch SJ, Cox PA (2006) Neurotoxic flying foxes as dietary items for the Chamorro people, Marianas Islands. J Ethnopharmacol 106:97–104

    PubMed  Google Scholar 

  • Banack SA, Johnson HE, Cheng R, Cox PA (2007) Production of the neurotoxin BMAA by a marine cyanobacterium. Mar Drugs 5:180–196

    PubMed  CAS  Google Scholar 

  • Banack SA, Downing TG, Spácil Z, Purdie EL, Metcalf JS, Downing S, Esterhuizen M, Codd GA, Cox PA (2010) Distinguishing the cyanobacterial neurotoxin β-N-methylamino-l-alanine (BMAA) from its structural isomer 2, 4-diaminobutyric acid (2, 4-DAB). Toxicon 56:868–879

    PubMed  CAS  Google Scholar 

  • Basile DV (1990) Morphological role of hydroxyproline containing proteins in liverworts. In: Chopra RN, Bhatia SC (eds) Bryophyte development: physiology and biochemistry. CRC Press, Boca Raton, pp 225–243

    Google Scholar 

  • Baulina OI, Lobakova ES (2003a) Atypical cell forms overproducing extracellular substances in populations of cycad cyanobionts. Microbiology 72:701–712

    CAS  Google Scholar 

  • Baulina OI, Lobakova ES (2003b) Heterocysts with reduced cell walls in populations of cycad cyanobionts. Microbiology 72:713–722

    CAS  Google Scholar 

  • Bergman B (2002) The Nostoc-Gunnera symbiosis. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in symbiosis. Kluwer, Dordrecht, pp 207–232

    Google Scholar 

  • Bergman B, Osborne B (2002) The Gunnera-Nostoc symbiosis. In: Osborne B (ed) Commentaries on cyanobacterial symbioses. Royal Irish Academy, Dublin, pp 35–39

    Google Scholar 

  • Bergman B, Rai AN (1989) The Nostoc-Nephroma symbiosis: localization, distribution pattern and levels of key proteins involved in nitrogen and carbon metabolism of the cyanobiont. Physiol Plant 77:216–224

    CAS  Google Scholar 

  • Bergman B, Lindblad P, Pettersson A, Renström E, Tiberg E (1985) Immuno-gold localization of glutamine synthetase in a nitrogen-fixing cyanobacterium (Anabaena cylindrica). Planta 166:329–334

    CAS  Google Scholar 

  • Bergman B, Lindblad P, Rai AN (1986) Nitrogenase in free-living and symbiotic cyanobacteria: immunoelectron microscopic localization. FEMS Microbiol Lett 35:75–78

    CAS  Google Scholar 

  • Bergman B, Rai AN, Johansson C, Söderbäck E (1992a) Cyanobacterial-plant symbioses. Symbiosis 14:61–81

    Google Scholar 

  • Bergman B, Johansson C, Söderbäck E (1992b) The Nostoc-Gunnera symbiosis. New Phytol 122:379–400

    Google Scholar 

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

    Google Scholar 

  • Bergman B, Rasmussen U, Rai AN (2003) Cyanobacterial associations. In: Elmerich C, Newton WE (eds) Associative nitrogen-fixing bacteria and cyanobacterial associations. Kluwer, Dordrecht

    Google Scholar 

  • Bergman B, Rasmussen U, Rai AN (2007) Cyanobacterial associations. In: Elmerich C, Newton WE (eds) Associative and endophytic nitrogen-fixing bacteria and cyanobacterial associations. Kluwer, Dordrecht, pp 257–301

    Google Scholar 

  • Bergman B, Ran L, Adams DG (2008) Cyanobacterial-plant symbioses: signaling and development. In: Herrero A, Flores E (eds) The cyanobacteria: molecular biology, Genomics and evolution. Caister Academic Press, Norfolk, pp 447–473

    Google Scholar 

  • Bhaya D (2004) Light matters: phototaxis and signal transduction in unicellular cyanobacteria. Mol Microbiol 53:745–754

    PubMed  CAS  Google Scholar 

  • Bilger W, Büdel B, Mollenhauer R, Mollenhauer D (1994) Photosynthetic activity of two developmental stages of a Nostoc strain (Cyanobacteria) isolated from Geosiphon pyriforme (Mycota). J Phycol 30:225–230

    CAS  Google Scholar 

  • Black KG, Parsons R, Osborne BA (2002) Uptake and metabolism of glucose in the Nostoc-Gunnera symbiosis. New Phytol 153:297–305

    CAS  Google Scholar 

  • Bonfante P, Grippiolo R (1984) Cytochemical and biochemical observations on the cell wall of the spore of Glomus epigaeum. Protoplasma 123:140–151

    Google Scholar 

  • Bonnett HT, Silvester WB (1981) Specificity in the Nostoc-Gunnera endosymbiosis. New Phytol 89:121–128

    CAS  Google Scholar 

  • Brasell HM, Davies SK, Mattay JP (1986) Nitrogen fixation associated with bryophytes colonizing burnt sites in Southern Tasmania, Australia. J Bryol 14:139–149

    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, pp 65–117

    Google Scholar 

  • Brenner ED, Stevenson DW, Twigg RW (2003) Cycads: evolutionary innovations and the role of plant-derived neurotoxins. Trends Plant Sci 8:446–452

    PubMed  CAS  Google Scholar 

  • Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77

    CAS  Google Scholar 

  • Burrows LL (2005) Weapons of mass retraction. Mol Microbiol 57:878–888

    PubMed  CAS  Google Scholar 

  • Bushnell T (1998) Molecular identification of endosymbionts present in the leaf cavities of Azolla caroliniana and Azolla mexicana. PhD thesis, Rensselaer Polytechnic Institute, Troy, pp 1–222

    Google Scholar 

  • Cai CY, Ouyang S, Wang Y, Fang ZJ, Rong JY, Geng LY, Li XX (1996) An Early Silurian vascular plant. Nature 379:592

    CAS  Google Scholar 

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

    Google Scholar 

  • Campbell EL, Meeks JC (1989) Characteristics of hormogonia formation by symbiotic Nostoc spp. in response to the presence of Anthoceros punctatus or its extracellular products. Appl Environ Microbiol 55:125–131

    PubMed  CAS  Google Scholar 

  • Campbell EL, Meeks JC (1992) Evidence for plant-mediated regulation of nitrogenase expression in the Anthoceros-Nostoc symbiotic association. J Gen Microbiol 138:473–480

    CAS  Google Scholar 

  • Campbell EL, Hagen KD, Cohen MF, Summers ML, Meeks JC (1996) The devR gene product is characteristic of receivers of two-component regulatory systems and is essential for heterocyst development in the filamentous cyanobacterium Nostoc sp. strain ATCC 29133. J Bacteriol 178:2037–2043

    PubMed  CAS  Google Scholar 

  • Campbell EL, Brahamsha B, Meeks JC (1998) Mutation of an alternative sigma factor in the cyanobacterium Nostoc punctiforme results in increased infection of its symbiotic plant partner, Anthoceros punctatus. J Bacteriol 180:4938–4941

    PubMed  CAS  Google Scholar 

  • Campbell EL, Wong FCY, Meeks JC (2003) DNA binding properties of the HrmR protein of Nostoc punctiforme responsible for transcriptional regulation of genes involved in the differentiation of hormogonia. Mol Microbiol 47:573–582

    PubMed  CAS  Google Scholar 

  • Campbell EL, Summers ML, Christman H, Martin ME, Meeks JC (2007) Global gene expression patterns of Nostoc punctiforme in steady state dinitrogen-grown heterocyst-containing cultures, and at single time points during the differentiation of akinetes and hormogonia. J Bacteriol 189:5247–5256

    PubMed  CAS  Google Scholar 

  • Campbell EL, Christman H, Meeks JC (2008) DNA microarray comparisons of plant factor- and nitrogen deprivation-induced hormogonia reveal decision-making transcriptional regulation patterns in Nostoc punctiforme. J Bacteriol 190:7382–7391

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    Google Scholar 

  • Carrapico F, Tavares R (1989) New data on the Azolla-Anabaena symbiosis II: cytochemical and immunocytochemical aspects. In: Skinner FA, Boddey RM, Fendrik I (eds) Nitrogen fixation with non-legumes. Kluwer, Dordrecht, pp 95–100

    Google Scholar 

  • Castillo-Guevara C, Rico-Gray V (2003) The role of macrozamin and cycasin in cycads (Cycadales) as antiherbivore defenses. J Torrey Bot Soc 130:206–217

    Google Scholar 

  • Chang DCN, Grobbelaar N, Coetzee J (1988) SEM observations on cyanobacteria-infected cycad coralloid roots. S Afr J Bot 54:491–495

    Google Scholar 

  • Chapman KE, Duggan PS, Billington NA, Adams DG (2008) Mutation at different sites in the Nostoc punctiforme cyaC gene, encoding the multiple-domain enzyme adenylate cyclase, results in different levels of infection of the host plant Blasia pusilla. J Bacteriol 190:1843–1847

    PubMed  CAS  Google Scholar 

  • Chaw S-M, Walters TW, Chang C-C, Hu S-H, Chen S-H (2005) A phylogeny of cycads (Cycadales) inferred from chloroplast matK gene, trnK intron, and nuclear rDNA ITS region. Mol Phylogenet Evol 37:214–234

    PubMed  CAS  Google Scholar 

  • Chiu WL, Peters GA, Levielle G, Still PC, Cousins S, Osborne B, Elhai J (2005) Nitrogen deprivation stimulates symbiotic gland development in Gunnera manicata. Plant Physiol 139:224–230

    PubMed  CAS  Google Scholar 

  • Cohen MF, Meeks JC (1997) A hormogonium regulating locus, hrmUA, of the cyanobacterium Nostoc punctiforme strain ATCC 29133 and its response to an extract of a symbiotic plant partner Anthoceros punctatus. Mol Plant Microbe Interact 10:280–289

    PubMed  CAS  Google Scholar 

  • Cohen MF, Yamasaki H (2000) Flavonoid-induced expression of a symbiosis-related gene in the cyanobacterium Nostoc punctiforme. J Bacteriol 182:4644–4646

    PubMed  CAS  Google Scholar 

  • Cohen MF, Wallis JG, Campbell EL, Meeks JC (1994) Transposon mutagenesis of Nostoc sp. strain ATCC 29133, a filamentous cyanobacterium with multiple cellular differentiation alternatives. Microbiology 140:3233–3240

    PubMed  CAS  Google Scholar 

  • Cohen MF, Meeks JC, Cai Y, Wolk CP (1998) Transposon mutagenesis of heterocyst-forming filamentous cyanobacteria. Methods Enzymol 297:3–17

    CAS  Google Scholar 

  • Cohen MF, Sakihama Y, Takagi YC, Ichiba T, Yamasaki H (2002) Synergistic effect of doexyanthocyanins from symbiotic fern Azolla spp. on hrmA gene induction in the cyanobacterium Nostoc punctiforme. Mol Plant Microbe Interact 15:875–882

    PubMed  CAS  Google Scholar 

  • Costa J-L, Lindblad P (2002) Cyanobacteria in symbiosis with cycads. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in symbiosis. Kluwer, Dordrecht, pp 195–205

    Google Scholar 

  • Costa JL, Paulsrud P, Lindblad P (1999) Cyanobiont diversity within coralloid roots of selected cycad species. FEMS Microbiol Ecol 28:85–91

    CAS  Google Scholar 

  • Costa J-L, Paulsrud P, Rikkinen J, Lindblad P (2001) Genetic diversity of Nostoc symbionts endophytically associated with two bryophyte species. Appl Environ Microbiol 67:4393–4396

    PubMed  CAS  Google Scholar 

  • Costa JL, Romero EM, Lindblad P (2004) Sequence based data supports a single Nostoc strain in individual coralloid roots of cycads. FEMS Microbiol Ecol 49:481–487

    PubMed  CAS  Google Scholar 

  • Cox PA, Banack SA, Murch SJ (2003) Biomagnification of cyanobacterial neurotoxins and neurodegenerative disease among the Chamorro people of Guam. Proc Natl Acad Sci USA 100:13380–13383

    PubMed  CAS  Google Scholar 

  • Cox PA, Banack SA, Murch SJ, Rasmussen U, Tien G, Bidigare RR, Metcalf JS, Morrison LF, Codd GA, Bergman B (2005) Diverse taxa of cyanobacteria produce beta-N-methylamino-l-alanine, a neurotoxic amino acid. Proc Natl Acad Sci USA 102:5074–5078

    PubMed  CAS  Google Scholar 

  • Dalton DA, Chatfield JM (1985) A new nitrogen-fixing cyanophyte-hepatic association: Nostoc and Porella. Am J Bot 72:781–784

    Google Scholar 

  • de Roissart P, Jucqued C, Watetkeyn L, Berghmans P, Van Hove C (1994) First evidence for the cutinic nature of the envelope at the interface of Azolla and its endophytes. In: Hegazi NA (ed) Nitrogen fixation with non-legumes: the sixth international symposium. The American University in Cairo Press, Cairo, pp 133–138

    Google Scholar 

  • DeLuca TH, Zackrisson O, Nilsson MC, Sellstedt A (2002) Quantifying nitrogen-fixation in feather moss carpets of boreal forests. Nature 419:917–920

    PubMed  CAS  Google Scholar 

  • DeLuca TH, Zackrisson O, Gentili F, Sellstedt A, Nilsson MC (2007) Ecosystem controls on nitrogen fixation in boreal feather moss communities. Oecologia 152:121–130

    PubMed  Google Scholar 

  • DeLuca TH, Zackrisson O, Gundale MJ, Nilsson M-C (2008) Ecosystem feedbacks and nitrogen fixation in boreal forests. Science 320:1181

    PubMed  CAS  Google Scholar 

  • Deusch O, Landan G, Roettger M, Gruenheit N, Kowallik KV et al (2008) Genes of cyanobacterial origin in plant nuclear genomes point to a heterocyst forming plastid ancestor. Mol Biol Evol 25:748–761

    PubMed  CAS  Google Scholar 

  • Do VC, Watanabe I, Zimmerman WJ, Lumpkin TA, de Waha Gaillonville T (1989) Sexual hybridization among Azolla species. Can J Bot 67:3482–3485

    Google Scholar 

  • Dotzler N, Walker C, Krings M, Hass H, Kerp H, Taylor TN, Agerer R (2009) Acaulosporoid glomeromycotan spores with a germination shield from the 400-million-year-old Rhynie chert. Mycol Prog 8:9–18

    Google Scholar 

  • Duckett JG, Prasad AKSK, Davies DA, Walker S (1977) A cytological analysis of the Nostoc-bryophyte relationship. New Phytol 79:349–362

    Google Scholar 

  • Duckett JG, Burch J, Fletcher PW, Matcham HW, Read DJ, Russell AJ, Pressel S (2004) In vitro cultivation of bryophytes: a review of practicalities, problems, progress and promise. J Bryol 26:3–20

    Google Scholar 

  • Duggan PS, Gottardello P, Adams DG (2007) Molecular analysis of genes in Nostoc punctiforme involved in pilus biogenesis and plant infection. J Bacteriol 189:4547–4551

    PubMed  CAS  Google Scholar 

  • Ekman M, Tollbäck P, Klint J, Bergman B (2006) Protein expression profiles in an endosymbiotic cyanobacterium revealed by a proteomic approach. Mol Plant Microbe Interact 19:1251–1261

    PubMed  CAS  Google Scholar 

  • Ekman M, Tollback P, Bergman B (2008) Proteomic analysis of the cyanobacterium of the Azolla symbiosis: identity, adaptation, and NifH modification. J Exp Bot 59:1023–1034

    PubMed  CAS  Google Scholar 

  • Elifio SL, Da Silva M, Iacomini M, Gorin PAJ (2000) A lectin from the lichenized basidiomycete Dictyonema glabratum. New Phytol 148:327–334

    CAS  Google Scholar 

  • Enderlin CS, Meeks JC (1983) Pure culture and reconstitution of the Anthoceros-Nostoc symbiotic association. Planta 158:157–165

    CAS  Google Scholar 

  • Erdmann N, Schiewer U (1984) Cell size changes as indicator of salt resistance of blue green algae. Arch Hydrobiol Suppl (Algol Stud) 67:431–439

    Google Scholar 

  • Esterhuizen M, Downing T (2008) β-N-methylamino-l-alanine (BMAA) in novel South African cyanobacterial isolates. Ecotoxicol Environ Saf 71:309–313

    PubMed  CAS  Google Scholar 

  • Evrard C, Van Hove C (2004) Taxonomy of the American Azolla species (Azollaceae): a critical review. Syst Geogr Plant 74:301–318

    Google Scholar 

  • Fiedler G, Muro-Pastor A, Flores E, Maldener I (2001) NtcA-dependent expression of the devBCA operon, encoding a heterocyst-specific ATP-binding cassette transporter in Anabaena spp. J Bacteriol 183:3795–3799

    PubMed  CAS  Google Scholar 

  • Fisher RF, Long SR (1992) Rhizobium-plant signal exchange. Nature 357:655–660

    PubMed  CAS  Google Scholar 

  • Flores E, Herrero A (2005) Nitrogen assimilation and nitrogen control in cyanobacteria. Biochem Soc Trans 33:164–167

    PubMed  CAS  Google Scholar 

  • Fonseca HMAC, Ferreira JIL, Berbara RLL, Zatorre NP (2009) Dominance of Paris-type morphology on mycothallus of Lunularia cruciata colonised by Glomus proliferum. Braz J Microbiol 40:96–101

    PubMed  Google Scholar 

  • Forni C, Grilli Caiola M, Gentili S (1989) Bacteria in the Azolla-Anabaena symbiosis. In: Skinner FA, Boddey RM, Fendrik I (eds) Nitrogen fixation with non-legumes. Kluwer, Dordrecht, pp 83–88

    Google Scholar 

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

    Google Scholar 

  • Galun M (1988) Handbook of lichenology. CRC Press, Boca Raton

    Google Scholar 

  • Gantar M, Kerby NW, Rowell P (1993) Colonization of wheat (Triticum vulgare L.) by N2-fixing cyanobacteria. III: the role of a hormogonia-promoting factor. New Phytol 124:505–513

    CAS  Google Scholar 

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

    Google Scholar 

  • Gebhardt JS, Nierzwicki-Bauer SA (1991) Identification of a common cyanobacterial symbiont associated with Azolla spp. through molecular and morphological characterization of free-living and symbiotic cyanobacteria. Appl Environ Microbiol 57:2141–2146

    PubMed  CAS  Google Scholar 

  • Gehrig H, Schüßler A, Kluge M (1996) Geosiphon pyriforme, a fungus forming endocytobiosis with Nostoc (Cyanobacteria), is an ancestral member of the Glomales: evidence by SSU rRNA analysis. J Mol Evol 43:71–81

    PubMed  CAS  Google Scholar 

  • Gehringer MM, Pengelly JJL, Cuddy WS, Fieker C, Forster PI, Neilan BA (2010) Host selection of symbiotic cyanobacteria in 31 species of the Australian cycad genus: Macrozamia (Zamiaceae). Mol Plant Microbe Interact 23:811–822

    PubMed  CAS  Google Scholar 

  • Gentili F, Nilsson MC, Zackrisson O, DeLuca TH, Sellstedt A (2005) Physiological and molecular diversity of feather moss associative N2-fixing cyanobacteria. J Exp Bot 56:3121–3127

    PubMed  CAS  Google Scholar 

  • Golden JW, Yoon HS (2003) Heterocyst development in Anabaena. Curr Opin Microbiol 6:557–563

    PubMed  CAS  Google Scholar 

  • Gorelova OA, Baulina OI, Shchelmanova AG, Korzhenevskaya TG, Gusev MV (1996) Heteromorphism of the cyanobacterium Nostoc sp., a microsymbiont of the Blasia pusilla moss. Microbiology 65:719–726

    Google Scholar 

  • Gratwicke B, Marshall BE (2001) The impact of Azolla filiculoides Lam. on animal biodiversity in streams in Zimbabwe. Afr J Ecol 39:216–218

    Google Scholar 

  • Grilli Caiola M (1980) On the phycobionts of the cycad coralloid roots. New Phytol 85:537–544

    Google Scholar 

  • Grilli Caiola M (1992) Cyanobacteria in symbiosis with bryophytes and tracheophytes. Biopress, Bristol

    Google Scholar 

  • Grobbelaar N, Scott WE, Hattingh W, Marshall J (1987) The identification of the coralloid endophytes of the southern African cycads and the ability of the isolates to fix dinitrogen. S Afr J Bot 53:111–118

    Google Scholar 

  • Guevara R, Armesto JJ, Caru M (2002) Genetic diversity of Nostoc microsymbionts from Gunnera tinctoria revealed by PCR-STRR fingerprinting. Microb Ecol 44:127–136

    PubMed  CAS  Google Scholar 

  • Gusev MV, Baulina OI, Gorelova OA, Lobakova ES, Korzhenevshaya TG (2002) Artificial cyanobacterium-plant symbioses. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in symbiosis. Kluwer, Dordrecht, pp 253–312

    Google Scholar 

  • Hawksworth D, Honegger R (1994) The lichen thallus: a symbiotic phenotype of nutritionally specialized fungi and its response to gall producers. In: Williams MAJ (ed) Plant galls: organisms, interactions, populations. Clarendon, Oxford, The Systematics Association, Special Volume No. 4977–98

    Google Scholar 

  • Herdman M, Rippka R (1988) Cellular differentiation: hormogonia and baeocytes. Methods Enzymol 167:232–242

    Google Scholar 

  • Herrero A, Muro-Pastor AM, Flores E (2001) Nitrogen control in cyanobacteria. J Bacteriol 183:411–425

    PubMed  CAS  Google Scholar 

  • Herrero A, Muro-Pastor AM, Valladares A, Flores E (2004) Cellular differentiation and the NtcA transcription factor in filamentous cyanobacteria. FEMS Microbiol Rev 28:469–487

    PubMed  CAS  Google Scholar 

  • Hill DJ (1975) The pattern of development of Anabaena in the Azolla-Anabaena symbiosis. Planta 122:178–184

    Google Scholar 

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

    Google Scholar 

  • Hill DJ (1989) The control of cell cycle in microbial symbionts. New Phytol 112:175–184

    Google Scholar 

  • Hill MP, Oberholzer IG (2002) Laboratory host range testing of the flea beetle, Pseudolampsis guttata (Leconte) (Coleoptera: Chrysomelidae), a potential natural enemy for red water fern, Azolla filiculoides Lamarck (Pteridophyta: Azollaceae) in South Africa. Coleopt Bull 56:79–83

    Google Scholar 

  • Houle D, Gauthier SB, Paquet S, Planas D, Warren A (2006) Identification of two genera of N2-fixing cyanobacteria growing on three feather moss species in boreal forests of Quebec, Canada. Can J Bot 84:1025–1029

    Google Scholar 

  • Jackson O, Taylor O, Adams DG, Knox JP (2012) Arabinogalactan proteins occur in the free-living cyanobacterium genus Nostoc and in plant–Nostoc symbioses. Mol Plant-Microbe Interactions 25:1338–1349

    CAS  Google Scholar 

  • Janes R (1998a) Growth and survival of Azolla filiculoides in Britain. I. Vegetative reproduction. New Phytol 138:367–375

    Google Scholar 

  • Janes R (1998b) Growth and survival of Azolla filiculoides in Britain. II. Sexual reproduction. New Phytol 138:377–384

    Google Scholar 

  • Johansson C, Bergman B (1992) Early events during the establishment of Gunnera/Nostoc symbiosis. Planta 188:403–413

    PubMed  CAS  Google Scholar 

  • Johansson C, Bergman B (1994) Reconstruction of the symbiosis of Gunnera manicata Linden: cyanobacterial specificity. New Phytol 126:643–652

    Google Scholar 

  • Joseph CM, Meeks JC (1987) Regulation of expression of glutamine synthetase in a symbiotic Nostoc strain associated with Anthoceros punctatus. J Bacteriol 169:2471–2475

    PubMed  CAS  Google Scholar 

  • Joubert L, Grobbelaar N, Coetzee J (1989) In situ studies of the ultrastructure of the cyanobacteria in the coralloid roots of Encephalartos arenarius, E. transvenosus and E. woodii (Cycadales). Phycologia 28:197–205

    Google Scholar 

  • Kaplan D, Peters GA (1988) Interaction of carbon metabolism in the Azolla-Anabaena symbiosis. Symbiosis 6:53–68

    CAS  Google Scholar 

  • Kardish N, Silberstein L, Fleminger G, Galun M (1991) Lectins from the lichen Nephroma laevigatum Ach: localization and function. Symbiosis 11:47–62

    CAS  Google Scholar 

  • Khamar HJ, Breathwaite EK, Prasse CE, Fraley ER, Secor CR, Chibane FL, Elhai J, Chiu WL (2010) Multiple roles of soluble sugars in the establishment of Gunnera-Nostoc endosymbiosis. Plant Physiol 154:1381–1389

    PubMed  CAS  Google Scholar 

  • Kimura J, Nakano T (1990) Reconstitution of a Blasia-Nostoc symbiotic association under axenic conditions. Nova Hedwig 50:191–200

    Google Scholar 

  • Klint J, Ran L, Rasmussen U, Bergman B (2006) Identification of developmentally regulated proteins in cyanobacterial hormogonia using a proteomic approach. Symbiosis 41:87–95

    CAS  Google Scholar 

  • Kluge M, Mollenhauer D, Mollenhauer R (1991) Photosynthetic carbon assimilation in Geosiphon pyriforme (Kützing) F.v. Wettstein, an endosymbiotic association of fungus and cyanobacterium. Planta 185:311–315

    PubMed  CAS  Google Scholar 

  • Kluge M, Mollenhauer D, Mollenhauer R, Kape R (1992) Geosiphon pyriforme, an endosymbiotic consortium of a fungus and a cyanobacterium (Nostoc), fixes nitrogen. Bot Acta 105:343–344

    CAS  Google Scholar 

  • Knapp E (1933) Über Geosiphon pyriformis Fr.v. Wettst., eine intrazelluläre Pilz-Algen-Symbiose. Ber Dtsch Bot Ges 51:210–217

    Google Scholar 

  • Knight CD, Adams DG (1996) A method for studying chemotaxis in nitrogen-fixing cyanobacterium-plant symbioses. Physiol Mol Plant Pathol 49:73–77

    Google Scholar 

  • Kobiler D, Cohen-Sharon A, Tel-Or E (1981) Recognition between the N2-fixing Anabaena and the water fern Azolla. FEBS Lett 133:157–160

    CAS  Google Scholar 

  • Kobiler D, Cohen-Sharon A, Tel-Or E (1982) Lectins are involved in the recognition between Anabaena and Azolla Israel. J Bot 31:324–328

    CAS  Google Scholar 

  • Komarek J, Anagnostidis K (1989) Trichormus azollae (Strasb.): modern approaches to the classification system of cyanophytes 4-nostocales. Arch Hydrobiol Algol Stud 56:303–345

    Google Scholar 

  • Krüger T, Mönch B, Oppenhäuser S, Luckas B (2010) LC-MS/MS determination of the isomeric neurotoxins BMAA (β-N-methylamino-l-alanine) and DAB (2,4-diaminobutyric acid) in cyanobacteria and seeds of Cycas revolute and Lathyrus latifolius. Toxicon 55:547–557

    PubMed  Google Scholar 

  • Kützing FT (1849) Species algarum. F.A. Brockhaus, Leipzig

    Google Scholar 

  • Lamb JR, Tugendreich S, Hieter P (1995) Tetratrico peptide repeat interactions: to TPR or not to TPR? Trends Biochem Sci 20:257–259

    PubMed  CAS  Google Scholar 

  • Large MF, Braggins JE (1993) Spore morphology of New Zealand Azolla filiculoides Lam. (Salviniaceae) New Zealand. J Bot 31:419–423

    Google Scholar 

  • Lechno-Yossef S (2002) Identification and characterization of bacteria associated with the water fern Azolla sp. PhD thesis, Rensselaer Polytechnic Institute, Troy, pp 1–132

    Google Scholar 

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

    Google Scholar 

  • Lee KY, Joseph CM, Meeks JC (1988) Glutamine synthetase specific activity and protein concentration in symbiotic Anabaena associated with Azolla caroliniana. Antonie Van Leeuwenhoek 54:345–355

    PubMed  CAS  Google Scholar 

  • Legaz M-E, Fontaniella B, Millanes A-M, Vicente C (2004) Secreted arginases from phylogenetically far-related species act as cross-recognition factors for two different algal cells. Eur J Cell Biol 83:435–446

    PubMed  CAS  Google Scholar 

  • Lehr H, Fleminger G, Galun M (1995) Lectin from the lichen Peltigera membranacea (Ach.) Nyl.: characterization and function. Symbiosis 18:1–13

    CAS  Google Scholar 

  • Lehr H, Galun M, Ott S, Jahns HM, Fleminger G (2000) Cephalodia of the lichen Peltigera aphthosa (L.) Willd.: specific recognition of the compatible photobiont. Symbiosis 29:357–365

    Google Scholar 

  • Lejeune A, Cagauan A, Van Hove C (1999) Azolla research and development: recent trends and priorities. Symbiosis 27:333–351

    Google Scholar 

  • Liaimer A, Bergman B (2003) Phytohormones in cyanobacteria: occurrence and perspectives. In: Proceedings from plant-microbe interaction conference, St. Petersburg

    Google Scholar 

  • Liaimer A, Matveyev A, Bergman B (2001) Isolation of host plant induced cDNAs from Nostoc sp. PCC 9229 forming symbiosis with the angiosperm Gunnera spp. Symbiosis 31:293–307

    CAS  Google Scholar 

  • Ligrone R (1988) Ultrastructure of a fungal endophyte in Phaeoceros laevis (L.) Prosk. (Anthocerophyta). Bot Gaz 149:92–100

    Google Scholar 

  • Ligrone R, Lopes C (1989) Cytology and development of mycorrhiza-like infection in the gametophyte of Conocephalum conicum (L.) Dum. (Marchantiales, Hepatophyta). New Phytol 111:423–433

    Google Scholar 

  • Lin C, Liu ZZ, Zheng DY, Tang LF, Watanabe I (1989) Re-establishment of symbiosis to Anabaena free Azolla. Sci China Ser B Chem 32:551–559

    Google Scholar 

  • Lindblad P (1990) Nitrogen and carbon metabolism in coralloid roots of cycads. Advances in cycad research I. Mem N Y Bot Gard 57:104–113

    Google Scholar 

  • Lindblad P (2009) Cyanobacteria in symbiosis with cycads. In: Pawlovski K (ed) Prokaryotic endosymbionts in plants, vol 8, Microbiology monographs. Springer, Berlin/Heidelberg, pp 225–233

    Google Scholar 

  • Lindblad P, Bergman B (1986) Glutamine synthetases: activity and localization in cyanobacteria of the cycads Cycas revolute and Zamia skinneri. Planta 169:1–7

    CAS  Google Scholar 

  • Lindblad P, Costa J-L (2002) The cyanobacterial-cycad symbiosis. Biol Environ Proc R Ir Acad 102B:31–33

    Google Scholar 

  • Lindblad P, Hällblom L, Bergman B (1985a) The cyanobacterium-Zamia symbiosis: C2H2 reduction and heterocyst frequency. Symbiosis 1:19–28

    CAS  Google Scholar 

  • Lindblad P, Bergman B, Hofsten AV, Hallbom L, Nylund JE (1985b) The cyanobacterium-Zamia symbiosis: an ultrastructural study. New Phytol 101:707–716

    Google Scholar 

  • Lindblad P, Rai AN, Bergman B (1987) The Cycas revoluta-Nostoc symbiosis: enzyme activities of nitrogen and carbon metabolism in the cyanobiont. J Gen Microbiol 133:1695–1699

    CAS  Google Scholar 

  • Lindblad P, Haselkorn R, Bergman B, Nierzwicki-Bauer SA (1989) Comparison of DNA restriction fragment length polymorphisms of Nostoc strains in and from cycads. Arch Microbiol 152:20–24

    PubMed  CAS  Google Scholar 

  • Lindblad P, Atkins CA, Pate JS (1991) N2-fixation by freshly isolated Nostoc from coralloid roots of the cycad Macrozamia riedlei (Firsch. ex Gand.) Garnd. Plant Physiol 96:753–759

    Google Scholar 

  • Lobakova ES, Orazova MK, Dobrovol'skaya TG (2003) Microbial complexes occurring on the apogeotropic roots and in the rhizosphere of cycad plants. Microbiology 72:628–633

    CAS  Google Scholar 

  • Lobakova ES, Dubravina GA, Zagoskina NV (2004) Formation of phenolic compounds in apogeotrophic roots of cycad plants. Russ J Plant Physiol 51:486–493

    CAS  Google Scholar 

  • Lohtander K, Oksanen I, Rikkinen J (2002) A phylogenetic study of Nephroma (lichen-forming Ascomycota). Mycol Res 106:777–787

    CAS  Google Scholar 

  • Lotti F, Giovanetti L, Margheri MC, Ventura S, Materassi R (1996) Diversity of DNA methylation pattern and total DNA restriction pattern in symbiotic Nostoc. World Microbiol Biotechnol 12:38–42

    CAS  Google Scholar 

  • Maetz M, Przybylowicz WJ, Mesjasz-Przybylowicz J, Schüßler A, Traxel K (1999a) Low-dose nuclear microscopy as a necessity for accurate quantitative microanalysis of biological samples. Nucl Instrum Methods Phys Res B 158:292–298

    CAS  Google Scholar 

  • Maetz M, Schüßler A, Wallianos A, Traxel K (1999b) Subcellular trace element distribution in Geosiphon pyriforme. Nucl Instrum Methods Phys Res B 150:200–207

    CAS  Google Scholar 

  • Maia LC, Kimbrough JW, Erdos G (1993) Problems with fixation and embedding of arbuscular mycorrhizal fungi (Glomales). Mycologia 85:323–330

    Google Scholar 

  • Malloch DW, Pirozynski KA, Raven PH (1980) Ecological and evolutionary significance of mycorrhizal symbiosis in vascular plants (a review). Proc Natl Acad Sci USA 77:2113–2118

    PubMed  CAS  Google Scholar 

  • Marler TE, Snyder LR, Shaw CA (2010) Cycas micronesica (Cycadales) plants devoid of endophytic cyanobacteria increase in beta-methylamino-l-alanine. Toxicon 56:563–568

    PubMed  CAS  Google Scholar 

  • Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159:89–102

    CAS  Google Scholar 

  • Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, Leister D, Stoebe B, Hasegawa M, Penny D (2002) Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci USA 99:12246–12251

    PubMed  CAS  Google Scholar 

  • Mattick JS (2002) Type IV pili and twitching motility. Annu Rev Microbiol 56:289–314

    PubMed  CAS  Google Scholar 

  • McConnachie AJ, Hill MP, Byrne MJ (2004) Field assessment of a frond-feeding weevil, a successful biological control agent of red waterfern, Azolla filiculoides, in southern Africa. Biol Control 29:326–331

    Google Scholar 

  • Meeks JC (1988) Symbiotic associations. Methods Enzymol 167:113–121

    Google Scholar 

  • Meeks JC (1990) Cyanobacterial-bryophyte associations. In: Rai AN (ed) CRC handbook of symbiotic cyanobacteria. CRC Press, Boca Raton, pp 43–63

    Google Scholar 

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

    Google Scholar 

  • Meeks JC (2003) Symbiotic interactions between Nostoc punctiforme, a multicellular cyanobacterium, and the hornwort Anthoceros punctatus. Symbiosis 35:55–71

    CAS  Google Scholar 

  • Meeks JC (2009) Physiological adaptations in nitrogen-fixing Nostoc-plant symbiotic associations. In: Pawlowski K (ed) Prokaryotic symbionts in plants, vol 8, Microbiol monograph. Springer, Berlin, pp 181–205

    Google Scholar 

  • Meeks JC, Elhai J (2002) Regulation of cellular differentiation in filamentous cyanobacteria in free-living and plant-associated symbiotic growth states. Microbiol Mol Biol Rev 66:94–121

    PubMed  CAS  Google Scholar 

  • Meeks JC, Enderlin CS, Wycoff KL, Chapman JS, Joseph CM (1983) Assimilation of 13NH +4 by Anthoceros grown with and without symbiotic Nostoc. Planta 158:384–391

    CAS  Google Scholar 

  • Meeks JC, Enderlin CS, Joesph CM, Chapman JS, Lollar MWL (1985a) Fixation of [13N]; N2 and transfer of fixed nitrogen in the Anthoceros-Nostoc symbiotic association. Planta 164:406–414

    CAS  Google Scholar 

  • Meeks JC, Steinberg N, Joseph CM, Enderlin CS, Jorgensen PA, Peters GA (1985b) Assimilation of exogenous and dinitrogen-derived 13NH4 + by Anabaena azollae separated from Azolla caroliniana Willd. Arch Microbiol 142:229–233

    CAS  Google Scholar 

  • Meeks JC, Campbell E, Hagen K, Hanson T, Hitzeman N, Wong F (1999) Developmental alternatives of symbiotic Nostoc punctiforme in response to its symbiotic partner Anthoceros punctatus. In: Peschek GA, Löffelhardt W, Schmetterer G (eds) The phototrophic prokaryotes. Kluwer/Plenum, New York, pp 665–678

    Google Scholar 

  • Meeks JC, Elhai J, Thiel T, Potts M, Larimer F, Lamerdin J, Predki P, Atlas R (2001) An overview of the genome of Nostoc punctiforme, a multicellular, symbiotic cyanobacterium. Photosynth Res 70:85–106

    PubMed  CAS  Google Scholar 

  • Meeks JC, Campbell EL, Summers ML, Wong FC (2002) Cellular differentiation in the cyanobacterium Nostoc punctiforme. Arch Microbiol 178:395–403

    PubMed  CAS  Google Scholar 

  • Meindl D, Loos E (1990) Release of glucose by Nostoc species isolated from the lichen Peltigera horizontalis. Plant Sci 72:283–288

    CAS  Google Scholar 

  • Mellor RB, Gadd GM, Rowell P, Stewart WDP (1981) A phytohaemagglutinin from the Azolla-Anabaena symbiosis. Biochem Biophys Res Commun 99:1348–1353

    PubMed  CAS  Google Scholar 

  • Milano V (2003) Identification of microbionts associated with the water fern Azolla. Masters thesis, Rensselaer Polytechnic Institute, Troy, pp 1–49

    Google Scholar 

  • Miura S, Yokoto A (2006) Isolation and characterization of cyanobacteria from lichen. J Gen Appl Microbiol 52:365–375

    PubMed  CAS  Google Scholar 

  • Mollenhauer D (1992) Geosiphon pyriformis. In: Reisser W (ed) Algae and symbiosis: plants, animals, fungi, viruses, interactions explored. Biopress, Bristol, pp 339–351

    Google Scholar 

  • Mollenhauer D, Mollenhauer R (1997) Endosymbiosis between Nostoc and Geosiphon pyriforme. Institut für den Wissenschaftlichen Film (IWF), Göttingen, Film-no. C1955

    Google Scholar 

  • Mollenhauer D, Mollenhauer R, Kluge M (1996) Studies on initiation and development of the partner association in Geosiphon pyriforme (Kütz.) v. Wettstein, a unique endocytobiotic system of a fungus (Glomales) and the cyanobacterium Nostoc punctiforme (Kütz.) Hariot. Protoplasma 193:3–9

    Google Scholar 

  • Muro-Pastor AM, Reyes JC, Florencio FJ (2005) Ammonium assimilation in cyanobacteria. Photosynth Res 83:135–150

    PubMed  CAS  Google Scholar 

  • Nash TH (1996) Lichen biology. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Nathanielsz CP, Staff IA (1975) A mode of entry of blue-green algae into the apogeotrophic roots of Macrozamia communis. Am J Bot 62:232–235

    Google Scholar 

  • Naumann M, Schüßler A, Bonfante P (2010) The obligate endobacteria of arbuscular mycorrhizal fungi are ancient heritable components related to the Mollicutes. ISME J 4:862–871

    PubMed  Google Scholar 

  • Newton JW, Herman AI (1979) Isolation of cyanobacteria from the aquatic fern, Azolla. Arch Microbiol 120:161–165

    Google Scholar 

  • Nierzwicki-Bauer SA, Aulfinger H (1991) Occurrence and ultrastructural characterization of bacteria in association with and isolated from Azolla caroliniana. 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

    Google Scholar 

  • Nilsson MC, Wardle DA (2005) Understory vegetation as a forest ecosystem driver: evidence from the northern Swedish boreal forest. Front Ecol Environ 3:421–428

    Google Scholar 

  • Nilsson M, Bergman B, Rasmussen U (2000) Cyanobacterial diversity in geographically related and distant host plants of the genus Gunnera. Arch Microbiol 173:97–102

    PubMed  CAS  Google Scholar 

  • Nilsson M, Rasmussen U, Bergman B (2006) Cyanobacterial chemotaxis to extracts of host and nonhost plants. FEMS Microbiol Ecol 55:382–390

    PubMed  CAS  Google Scholar 

  • Nudleman E, Kaiser D (2004) Pulling together with type IV pili. J Mol Microbiol Biotechnol 7:52–62

    PubMed  CAS  Google Scholar 

  • Obukowicz M, Schaller M, Kennedy GS (1981) Ultrastructure and phenolic histochemistry of the Cycas revoluta-Anabaena symbiosis. New Phytol 87:751–759

    Google Scholar 

  • Orr J, Haselkorn R (1982) Regulation of glutamine synthetase activity and synthesis in free-living and symbiotic Anabaena spp. J Bacteriol 152:626–635

    PubMed  CAS  Google Scholar 

  • Osborne B, Bergman B (2009) Why does Gunnera do it and other angiosperms don’t? In: Pawlowski K (ed) Prokaryotic symbionts in plants, vol 8, Microbiology monographs. Springer, Heidelberg, pp 207–224

    Google Scholar 

  • Osborne BA, Sprent JI (2002) Ecology of Nostoc-Gunnera symbiosis. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in symbiosis. Kluwer, Dordrecht, pp 207–232

    Google Scholar 

  • Osborne B, Doris F, Cullen A, McDonald R, Campbell G, Steer M (1991) Gunnera tinctoria: an unusual invader. Bioscience 41:224–234

    Google Scholar 

  • Osborne BA, Cullen A, Jones PW, Campbell GJ (1992) Use of nitrogen by the Nostoc-Gunnera tinctoria (Molina) Mirbel symbiosis. New Phytol 120:481–487

    CAS  Google Scholar 

  • Ow MC, Gantar M, Elhai J (1999) Reconstitution of a cycad-cyanobacterial association. Symbiosis 27:125–134

    Google Scholar 

  • Palmqvist K (2002) Cyanolichens: carbon metabolism. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in symbiosis. Kluwer, Dordrecht, pp 73–96

    Google Scholar 

  • Papaefthimiou D, Hrouzek P, Mugnai MA, Lukesova A, Turicchia S, Rasmussen U, Ventura S (2008) Differential patterns of evolution and distribution of the symbiotic behaviour in nostocacean cyanobacteria. Int J Syst Evol Microbiol 58:553–564

    PubMed  Google Scholar 

  • Pate JS, Lindblad P, Atkins CA (1988) Pathways of assimilation and transfer of the fixed nitrogen in coralloid roots of cycad-Nostoc symbioses. Planta 176:461–471

    CAS  Google Scholar 

  • Paulsrud P, Lindblad P (1998) Sequence variation of the tRNALeu intron as a marker for genetic diversity and specificity of symbiotic cyanobacteria in some lichens. Appl Environ Microbiol 64:310–315

    PubMed  CAS  Google Scholar 

  • Paulsrud P, Rikkinen J, Lindblad P (1998) Cyanobiont specificity in some Nostoc-containing lichens and in a Peltigera aphthosa photosymbiodeme. New Phytol 139:517–528

    CAS  Google Scholar 

  • Paulsrud P, Rikkinen J, Lindblad P (2000) Spatial patterns of photobiont diversity in some Nostoc-containing lichens. New Phytol 146:291–299

    Google Scholar 

  • Paulsrud P, Rikkinen J, Lindblad P (2001) Field experiments on cyanobacterial specificity in Peltigera aphthosa. New Phytol 152:117–123

    Google Scholar 

  • Pennell RI (1992) Cell surface arabinogalactan proteins, arabinogalactans and plant development. In: Collow JA, Green JR (eds) Perspectives in plant cell recognition. Cambridge University Press, Cambridge, UK, pp 105–121

    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

    Google Scholar 

  • Perraju BTVV, Rai AN, Kumar AR, Singh HN (1986) Cycas circinalis-Anabaena cycadeae symbiosis: photosynthesis and the enzymes of nitrogen and hydrogen metabolism in symbiotic and cultured Anabaena cycadeae. Symbiosis 1:239–251

    CAS  Google Scholar 

  • Peters GA, Calvert HE (1983) The Azolla-Anabaena azollae symbiosis. A continuum of interaction strategies. In: Goff LJ (ed) Algal symbiosis. Cambridge University Press, Cambridge, UK, pp 109–145

    Google Scholar 

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

    Google Scholar 

  • Peters GA, Kaplan D, Meeks JC, Buzby KM, Marsh BH, Corbin JL (1985) Aspects of nitrogen and carbon interchange in the Azolla-Anabaena symbiosis. In: Ludden PW, Burris JE (eds) Nitrogen fixation and CO2 metabolism. Elsevier, New York, pp 213–222

    Google Scholar 

  • Peterson RL, Howarth MJ, Whittier DP (1981) Interactions between a fungal endophyte and gametophyte cells in Psilotum nudum. Can J Bot 59:711–720

    Google Scholar 

  • Pirozynski KA, Malloch DW (1975) The origin of land plants: a matter of mycotrophism. Biosystems 6:153–164

    PubMed  CAS  Google Scholar 

  • Plazinski J (1990) The Azolla-Anabaena symbiosis. In: Gresshoff PM (ed) 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 (1990a) Isolation of Agrobacterium sp. strain from the Azolla leaf cavity. FEMS Microbiol Lett 70:55–59

    CAS  Google Scholar 

  • Plazinski J, Zheng Q, Taylor R, Croft L, Rolfe BG, Gunning BES (1990b) DNA probes show genetic variation in cyanobacterial symbionts of the Azolla fern and a closer relationship to free-living Nostoc strains than to free-living Anabaena strains. Appl Environ Microbiol 56:1263–1270

    PubMed  CAS  Google Scholar 

  • Plazinski J, Croft L, Taylor R, Zheng Q, Rolfe BG, Gunning BES (1991) Indigenous plasmids in Anabaena azollae: their taxonomic distribution and existence of regions of homology with symbiotic genes of rhizobium. Can J Microbiol 37:171–181

    CAS  Google Scholar 

  • Polsky FI, Nunn PB, Bell EA (1972) Distribution and toxicity of α-amino-β-methylaminopropionic acid. Fed Proc 31:1473–1475

    PubMed  CAS  Google Scholar 

  • Rai AN (1990) Cyanobacterial-fungal symbioses: the cyanolichens. In: Rai AN (ed) Handbook of symbiotic cyanobacteria. CRC Press, Boca Raton, pp 9–41

    Google Scholar 

  • Rai AN (2002) Cyanolichens: nitrogen metabolism. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in symbiosis. Kluwer, Dordrecht, pp 97–115

    Google Scholar 

  • Rai AN, Rowell P, Stewart WDP (1980) NH +4 assimilation and nitrogenase regulation in the lichen Peltigera aphthosa Willd. New Phytol 85:545–555

    CAS  Google Scholar 

  • Rai AN, Rowell P, Stewart WDP (1981a) Nitrogenase activity and dark CO2 fixation in the lichen Peltigera aphthosa Willd. Planta 151:256–264

    CAS  Google Scholar 

  • Rai AN, Rowell P, Stewart WDP (1981b) 15N2 incorporation and metabolism in the lichen Peltigera aphthosa Willd. Planta 152:544–552

    CAS  Google Scholar 

  • Rai AN, Rowell P, Stewart WDP (1983a) Interactions between cyanobacterium and fungus during 15N2-incorporation and metabolism in the lichen Peltigera aphthosa Willd. Arch Microbiol 134:136–142

    CAS  Google Scholar 

  • Rai AN, Rowell P, Stewart WDP (1983b) Mycobiont-cyanobiont interactions during dark nitrogen fixation by the lichen Peltigera aphthosa. Physiol Plant 57:285–290

    CAS  Google Scholar 

  • Rai AN, Borthakur M, Singh S, Bergman B (1989) Anthoceros-Nostoc symbiosis: immunoelectronmicroscopic localization of nitrogenase, glutamine synthetase, phycoerythrin and ribulose-1,5-bisphosphate carboxylase/oxygenase in the cyanobiont and the cultured (free-living) isolate Nostoc 7801. J Gen Microbiol 135:385–395

    CAS  Google Scholar 

  • Rai AN, Söderbäck E, Bergman B (2000) Tansley Review No. 116, cyanobacterium-plant symbioses. New Phytol 147:449–481

    CAS  Google Scholar 

  • Rai AN, Bergman B, Rasmussen U (eds) (2002) Cyanobacteria in symbiosis. Kluwer, Dordrecht

    Google Scholar 

  • Ran L, Larsson J, Vigil-Stenman T, Nylander J, Ininbergs K, Zheng W, Lapidus A, Lowry S, Haselkorn R, Bergman B (2010) Genome erosion in a nitrogen-fixing vertically transmitted endosymbiotic multicellular cyanobacterium. PLoS One 5:e11486

    PubMed  Google Scholar 

  • Rasmussen U, Nilsson M (2002) Cyanobacterial diversity and specificity in plant symbioses. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in symbiosis. Kluwer, Dordrecht, pp 313–328

    Google Scholar 

  • Rasmussen U, Svenning M (2001) Characterization by genotypic methods of symbiotic Nostoc strains isolated from five species of Gunnera. Arch Microbiol 176:204–210

    PubMed  CAS  Google Scholar 

  • Rasmussen U, Johansson C, Bergman B (1994) Early communication in the Gunnera-Nostoc symbiosis: plant-induced cell differentiation and protein synthesis in the cyanobacterium. Mol Plant Microbe Interact 7:696–702

    CAS  Google Scholar 

  • Rasmussen U, Johansson C, Renglin A, Petersson C, Bergman B (1996) A molecular characterization of the Gunnera-Nostoc symbiosis: comparison with Rhizobium-and Agrobacterium-plant interactions. New Phytol 133:391–398

    CAS  Google Scholar 

  • Read DJ, Duckett JG, Francis R, Ligrone R, Russel A (2000) Symbiotic fungal associations in “lower” land plants. Philos Trans R Soc Lond B 355:815–831

    CAS  Google Scholar 

  • Redecker D, Kodner R, Graham LE (2000a) Glomalean fungi from the Ordovician. Science 289:1920–1921

    PubMed  CAS  Google Scholar 

  • Redecker D, Morton JB, Bruns TD (2000b) Ancestral lineages of arbuscular mycorrhizal fungi. Mol Phylogenet Evol 14:276–284

    PubMed  CAS  Google Scholar 

  • Reinke J (1872) Ueber die anatomische Verhaltnisse einiger Arten von Gunnera L. Nachrichten der. Konigliche Gesellschaft der Wissenschaften Universitat, Gottingen, pp 100–108

    Google Scholar 

  • Reinke J (1873) Untersuchungen über die Morphologie der Vegetationsorgane von Gunnera. In: Reinke J (ed) Morphologische Abhandlungen. Verlag W. Engelman, Leipzig, pp 45–123

    Google Scholar 

  • Remy W, Taylor TN, Hass H, Kerp H (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci USA 91:11841–11843

    PubMed  CAS  Google Scholar 

  • Renzaglia KS (1982) A comparative developmental investigation of the gametophyte generation in the Metzgeriales (Hepatophyta). Bryophyt Bibl 24:1–238

    Google Scholar 

  • Renzaglia KS, Duff RJ, Nickrent DL, Garbary D (2000) Vegetative and reproductive innovations of early land plants: implications for a unified phylogeny. Trans R Soc Lond 355:769–793

    CAS  Google Scholar 

  • Rikkinen J (2002) Cyanolichens: an evolutionary overview. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in symbiosis. Kluwer, Dordrecht, pp 31–72

    Google Scholar 

  • Rikkinen J, Oksanen I, Lohtander K (2002) Lichen guilds share related cyanobacterial symbionts. Science 297:357

    PubMed  CAS  Google Scholar 

  • Rodgers GA, Stewart WDP (1974) Physiological interrelations of the blue-green alga Nostoc with the liverworts Anthoceros and Blasia. Br Phycol J 9:223

    Google Scholar 

  • Rodgers GA, Stewart WDP (1977) The cyanophyte-hepatic symbiosis. I: morphology and physiology. New Phytol 78:441–458

    Google Scholar 

  • Rosén J, Hellenäs K (2008) Determination of the neurotoxin BMAA (β-N-methylamino-l-alanine) to cycad seed and cyanobacteria by LC-MS/MS (liquid chromatography tandem mass spectrometry). Analyst 133:1785–1789

    PubMed  Google Scholar 

  • Rowell P, Rai AN, Stewart WDP (1985) Studies on the nitrogen metabolism of the lichen Peltigera aphthosa and Peltigera canina. In: Brown DH (ed) Lichen physiology and cell biology. Plenum, New York, pp 145–160

    Google Scholar 

  • Rubinstein CV, Gerrienne P, De La Puente GS, Astini RA, Steemans P (2010) Early Middle Ordovician evidence for land plants in Argentina (eastern Gondwana). New Phytol 188:365–369

    PubMed  CAS  Google Scholar 

  • Sacristan M, Millanes A-M, Legaz M-E, Vicente C (2006) A lichen lectin specifically binds to the alpha-1,4-polygalactoside moiety of urease located in the cell wall of homologous algae. Plant Signal Behav 1:23–27

    PubMed  Google Scholar 

  • Saunders RMK, Fowler K (1993) The supraspecific taxonomy and evolution of the fern genus Azolla (Azollaceae). Plant Syst Evol 184:175–193

    Google Scholar 

  • Schaede R (1951) Über die Blaualgensymbiose von Gunnera. Planta 39:154–170

    Google Scholar 

  • Scheloske S, Maetz M, Schüßler A (2001) Heavy metal uptake of Geosiphon pyriforme. Nucl Instrum Methods Phys Res Sect B 181:659–663

    CAS  Google Scholar 

  • Schenk HEA (1992) Cyanobacterial symbioses. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer K-H (eds) The prokaryotes, vol 4. Springer, Berlin, pp 3819–3854

    Google Scholar 

  • Schmid E, Oberwinkler F (1993) Mycorrhiza-like interactions between the achlorophyllous gametophyte of Lycopodium clavatum L. and its fungal endophyte studied by light and electron microscopy. New Phytol 124:69–81

    Google Scholar 

  • Schnepf E (1964) Zur Feinstruktur von Geosiphon pyriforme. Arch Mikrobiol 49:112–131

    Google Scholar 

  • Schüßler A (1999) Glomales SSU rRNA gene diversity. New Phytol 144:205–207

    Google Scholar 

  • Schüßler A (2000) Glomus claroideum forms an arbuscular mycorrhiza-like symbiosis with the hornwort Anthoceros punctatus. Mycorrhiza 10:15–21

    Google Scholar 

  • Schüßler A (2002) Molecular phylogeny, taxonomy, and evolution of Geosiphon pyriformis and arbuscular mycorrhizal fungi. Plant Soil 244:75–83

    Google Scholar 

  • Schüßler A (2012) The Geosiphon–Nostoc endosymbiosis and its role as a model for arbuscular mycorrhiza research. In: Hock B (ed) The mycota IX—fungal associations, 2nd edn. Springer, Berlin/Heidelberg (in press)

    Google Scholar 

  • Schüßler A, Walker C (2010) The Glomeromycota: a species list with new families and new genera published in libraries at The Royal Botanic Garden Edinburgh, The Royal Botanic Garden Kew, Botanische Staatssammlung Munich, and Oregon State University. Electronic version freely available online at www.amf-phylogeny.com. Gloucester

  • Schüßler A, Walker C (2011) Evolution of the ‘plant-symbiotic’ fungal phylum, Glomeromycota. In: Pöggeler S, Wöstemeyer J (eds) Evolution of fungi and fungal-like organisms. Springer, Berlin Heidelberg, pp 163–185

    Google Scholar 

  • Schüßler A, Wolf E (2005) Geosiphon pyriformis—a glomeromycotan soil fungus forming endosymbiosis with cyanobacteria. In: Declerck S, Strullu D-G, Fortin A (eds) In vitro culture of mycorrhizas. Springer, Berlin/Heidelberg, pp 271–289

    Google Scholar 

  • Schüßler A, Mollenhauer D, Schnepf E, Kluge M (1994) Geosiphon pyriforme, an endosymbiotic association of fungus and cyanobacteria: the spore structure resembles that of arbuscular mycorrhizal (AM) fungi. Bot Acta 107:36–45

    Google Scholar 

  • Schüßler A, Schnepf E, Mollenhauer D, Kluge M (1995) The fungal bladders of the endocyanosis Geosiphon pyriforme, a Glomus-related fungus: cell wall permeability indicates a limiting pore radius of only 0.5 nm. Protoplasma 185:131–139

    Google Scholar 

  • Schüßler A, Bonfante P, Schnepf E, Mollenhauer D, Kluge M (1996) Characterization of the Geosiphon pyriforme symbiosome by affinity techniques: confocal laser scanning microscopy (CLSM) and electron microscopy. Protoplasma 190:53–67

    Google Scholar 

  • Schüßler A, Meyer T, Gehrig H, Kluge M (1997) Variations of lectin binding sites in extracellular glycoconjugates during the life cycle of Nostoc punctiforme, a potentially endosymbiotic cyanobacterium. Eur J Phycol 32:233–239

    Google Scholar 

  • Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421

    Google Scholar 

  • Schüßler A, Martin H, Cohen D, Fitz M, Wipf D (2006) Characterization of a carbohydrate transporter from symbiotic glomeromycotan fungi. Nature 444:933–936

    PubMed  Google Scholar 

  • Schüßler A, Krüger M, Walker C (2011) Revealing natural relationships among arbuscular mycorrhizal fungi: culture line BEG47 represents Diversispora epigaea, not Glomus versiforme. PLoS One 6:e23333

    PubMed  Google Scholar 

  • Sergeeva E, Liaimer A, Bergman B (2002) Evidence for biosynthesis and release of the phytohormone indole-3-acetic acid by cyanobacteria. Planta 215:229–238

    PubMed  CAS  Google Scholar 

  • Serrano R, Carrapico F, Vidal R (1999) The presence of lectins in bacteria associated with the Azolla-Anabaena symbiosis. Symbiosis 27:169–178

    Google Scholar 

  • Shannon BT, Gates JE, McCowen SM (1993) DNA base composition of eubacteria isolated from 4 species of Azolla. Symbiosis 15:165–175

    CAS  Google Scholar 

  • Silvester WB (1976) Endophyte adaptation in Gunnera-Nostoc symbiosis. In: Nutman PS (ed) Symbiotic nitrogen fixation in plants. Cambridge University Press, Cambridge, UK, pp 521–541

    Google Scholar 

  • Silvester WB, McNamara PJ (1976) The infection process and ultrastructure of the Gunnera-Nostoc symbiosis. New Phytol 77:135–141

    Google Scholar 

  • Silvester WB, Smith DR (1969) Nitrogen fixation by Gunnera-Nostoc symbiosis. Nature 224:1231

    CAS  Google Scholar 

  • Silvester WB, Parsons R, Watt PW (1996) Direct measurement of release and assimilation of ammonia in the Gunnera-Nostoc symbiosis. New Phytol 132:617–625

    CAS  Google Scholar 

  • Singh P, Singh D (1997) Azolla-Anabaena symbiosis. In: Ddarwal K (ed) Biotechnological approaches in soil microorganisms for sustainable crop production. Scientific Press, Jodhpur, pp 93–107

    Google Scholar 

  • Smith DC, Douglas AE (1987) The biology of symbiosis. Edward Arnold, London

    Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London

    Google Scholar 

  • Smith SA, Beaulieu JM, Donoghue MJ (2010) An uncorrelated relaxed-clock analysis suggests an earlier origin for flowering plants. Proc Natl Acad Sci 107:5897–5902

    PubMed  CAS  Google Scholar 

  • Snyder LR, Marler TE (2011) Rethinking cycad metabolite research. Commun Integr Biol 4:86–88

    PubMed  Google Scholar 

  • Söderbäck E (1992) Developmental patterns in the Nostoc-Gunnera symbiosis. Doctoral thesis, Stockholm University, Stockholm

    Google Scholar 

  • Söderbäck E, Bergman B (1992) The Nostoc-Gunnera magellanica symbiosis: phycobiliproteins, carboxysomes and Rubisco in the microsymbiont. Physiol Plant 8:425–432

    Google Scholar 

  • Söderbäck E, Bergman B (1993) The Nostoc-Gunnera symbiosis: carbon fixation and translocation. Physiol Plant 89:125–132

    Google Scholar 

  • Söderbäck E, Lindblad P, Bergman B (1990) Developmental patterns related to nitrogen fixation in the Nostoc-Gunnera magellanica Lam symbiosis. Planta 182:355–362

    Google Scholar 

  • Solheim B, Zielke M (2002) Associations between cyanobacteria and mosses. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in symbiosis. Kluwer, Dordrecht, pp 137–152

    Google Scholar 

  • Solheim B, Wiggen H, Roberg S, Spaink HP (2004) Associations between arctic cyanobacteria and mosses. Symbiosis 37:169–187

    Google Scholar 

  • Sood A, Prasanna R, Prasanna BM, Singh PK (2008) Genetic diversity among and within cultured cyanobionts of diverse species of Azolla. Folia Microbiol 53:35–43

    CAS  Google Scholar 

  • Spáčil Z, Eriksson J, Jonasson S, Rasmussen U, Ilag LL, Bergman B (2010) Analytical protocol for identification of BMAA and DAB in biological samples. Analyst 135:127–132

    PubMed  Google Scholar 

  • Staff IA, Ahern CP (1993) Symbiosis in cycads with special reference to Macrozamia communis. In: Stevenson DW, Norstog KJ (eds) The biology, structure and systematics of the Cycadales. Palm and Cycad Societies of Australia, Queensland, pp 200–210

    Google Scholar 

  • Stahl M (1949) Die Mycorrhiza der Lebermoose mit besonderer Berücksichtigung der thallösen Formen. Planta 37:103–148

    Google Scholar 

  • Steinberg NA, Meeks JC (1989) Photosynthetic CO2 fixation and ribulose bisphosphate carboxylase/oxygenase activity of Nostoc sp. strain UCD 7801 in symbiotic association with Anthoceros punctatus. J Bacteriol 171:6227–6233

    PubMed  CAS  Google Scholar 

  • Steinberg NA, Meeks JC (1991) Physiological sources of reductant for nitrogen fixation activity in Nostoc sp. strain UCD 7801 in symbiotic association with Anthoceros punctatus. J Bacteriol 173:7324–7329

    PubMed  CAS  Google Scholar 

  • Stevenson DW (1993) The Zamiaceae in Panama with comments on phytogeography and species relationships. Brittonia 45:1–16

    Google Scholar 

  • Stewart WDP, Rogers GA (1977) The cyanophyte-hepatic symbiosis. II: nitrogen fixation and the interchange of nitrogen and carbon. New Phytol 78:459–471

    CAS  Google Scholar 

  • Stewart WDP, Rowell P (1977) Modifications of nitrogen-fixing algae in lichen symbiosis. Nature (London) 265:371–372

    CAS  Google Scholar 

  • Stewart WDP, Rowell P, Rai AN (1983) Cyanobacteria-eukaryotic plant symbioses. Ann Inst Pasteur Microbiol 134B:205–228

    CAS  Google Scholar 

  • Stock PA, Silvester WB (1994) Phloem transport of recently fixed nitrogen in the Gunnera-Nostoc symbiosis. New Phytol 126:259–266

    CAS  Google Scholar 

  • Stocker-Wörgötter E (1995) Experimental cultivation of lichens and lichen symbionts. Can J Bot 73S:579–589

    Google Scholar 

  • Stocker-Wörgötter E, Turk R (1994) Artificial resynthesis of the photosymbiodeme Peltigera leucophlebia under laboratory conditions. Cryptogam Bot 4:300–308

    Google Scholar 

  • Stucken K, John U, Cembella A, Murillo A, Soto-Liebe K et al (2010) The smallest known genomes of multicellular and toxic cyanobacteria: comparison, minimal gene sets for linked traits and the evolutionary implications. PLoS One 5:e9235

    PubMed  Google Scholar 

  • Svenning MM, Eriksson T, Rasmussen U (2005) Phylogeny of symbiotic cyanobacteria within the genus Nostoc based on 16S rDNA sequence analyses. Arch Microbiol 183:19–26

    PubMed  CAS  Google Scholar 

  • Tabita FR (1994) The biochemistry and molecular regulation of carbon dioxide metabolism in cyanobacteria. In: Bryant DA (ed) The molecular biology of cyanobacteria. Kluwer, Dordrecht, pp 437–467

    Google Scholar 

  • Tandeau de Marsac N (1994) Differentiation of hormogonia and relationships with other biological processes. In: Bryant DA (ed) The molecular biology of cyanobacteria. Kluwer, Amsterdam, pp 825–842

    Google Scholar 

  • Tehler A, Farris JS, Lipscomb DL, Kallersjo M (2000) Phylogenetic analysis of the fungi based on large rDNA data sets. Mycologia 92:459–474

    Google Scholar 

  • Tel-Or E, Sandovsky T, Kobiler D, Arad C, Weinberg R (1983) The unique symbiotic properties of Anabaena in the water fern Azolla. In: Papageorgiou GC, Packer L (eds) Prokaryotes: cell differentiation and function. Elsevier, New York, pp 303–314

    Google Scholar 

  • Thajuddin N, Muralitharan G, Sundaramoorthy M, Ramamoorthy R, Ramachandran S, Akbarsha MA, Gunasekaran M (2010) Morphological and genetic diversity of symbiotic cyanobacteria from cycads. J Basic Microbiol 50:254–265

    PubMed  CAS  Google Scholar 

  • Towata EM (1985) Morphometric and cytochemical ultrastructural analyses of the Gunnera kaalensis/Nostoc symbiosis. Bot Gaz 146:293–301

    Google Scholar 

  • Uheda E, Kitoh S (1991) Electron microscopic observations of the envelopes of isolated algal packets of Azolla. Can J Bot 69:1418–1419

    Google Scholar 

  • Uheda E, Silvester WB (2001) The role of papillae during the infection process in the Gunnera-Nostoc symbiosis. Plant Cell Physiol 42:780–783

    PubMed  CAS  Google Scholar 

  • Usher K, Bergman B, Raven J (2007) Exploring cyanobacterial mutualisms. Annu Rev Ecol Evol Syst 38:255–273

    Google Scholar 

  • Van Coppenolle B, Watanabe I, Van-Hove C, Second G, Huang N, McCouch SR (1993) Genetic diversity and phylogeny analysis of Azolla based on DNA amplification by arbitrary primers. Genome 36:686–693

    PubMed  Google Scholar 

  • Van Coppenolle B, McCouch SR, Watanabe I, Huang N, Van Hove C (1995) Genetic diversity and phylogeny analysis of Anabaena azollae based on RFLP detected in Azolla-Anabaena azollae DNA complexes using nif gene probes. Theor Appl Genet 91:589–597

    PubMed  Google Scholar 

  • Van Hove C, Lejeune A (1996) Does Azolla have any future in agriculture? In: Rahman M (ed) Biological nitrogen fixation associated with rice production. Kluwer, Dordrecht, pp 83–94

    Google Scholar 

  • Vega A, Bell EA (1967) α-Amino-β-methylaminopropionic acid, a new amino acid from seeds of Cycas circinalis. Phytochemistry 6:759–762

    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

    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 pore of the leaf cavity of Azolla: teat-cell differentiation and cell wall projections. Protoplasma 219:31–42

    PubMed  CAS  Google Scholar 

  • Villarreal JC, Renzaglia KS (2006) Structure and development of Nostoc strands in Leiosporoceros dussii (Anthocerotophyta): a novel symbiosis in land plants. Am J Bot 93:693–705

    Google Scholar 

  • Von Wettstein F (1915) Geosiphon Fr. v. Wettst., eine neue, interessante Siphonee sterr. Bot Z 65:145–156

    Google Scholar 

  • Wallace WH, Gates JE (1986) Identification of eubacteria isolated from leaf cavities of 4 species of the N-fixing Azolla fern as Arthrobacter Conn and Dimmick. Appl Environ Microbiol 52:425–429

    PubMed  CAS  Google Scholar 

  • Wang C-M, Ekman M, Bergman B (2004) Expression of cyanobacterial genes involved in heterocyst differentiation and dinitrogen fixation along a plant symbiosis development profile. Mol Plant Microbe Interact 17(4):436–443

    PubMed  CAS  Google Scholar 

  • Wang B, Yeun LH, Xue J-Y, Liu Y, Ane J-M, Qiu Y-L (2010) Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonization of land by plants. New Phytol 186:514–525

    PubMed  Google Scholar 

  • Wanntorp L, Wanntorp H-E, Oxelman B, Källersjö M (2001) Phylogeny of Gunnera. Plant Syst Evol 226:85–107

    CAS  Google Scholar 

  • Watanabe I (1994) Genetic enhancement and Azolla collection-problems in applying Azolla-Anabaena symbiosis. In: Hegazi NA, Fayez M, Monib M (eds) Nitrogen fixation with non-legumes. The American University in Cairo Press, Cairo, pp 437–450

    Google Scholar 

  • Watanabe I, Van Hove C (1996) Phylogenetic, molecular, and breeding aspects of Azolla-Anabaena symbiosis. In: Camus JM, Gibby M, Jones RJ (eds) Pteridology in perspective. Royal Botanic Gardens, Kew, pp 611–619

    Google Scholar 

  • Watanabe I, Lapis-Tenorio MT, Ventura TS, Padre BC (1993) Sexual hybrids of Azolla filiculoides with A. microphylla. Soil Sci Plant Nutr 39:669–676

    Google Scholar 

  • Watts S (2000) Signalling in the Nostoc-plant symbiosis. PhD thesis, University of Leeds, Leeds

    Google Scholar 

  • Watts SD, Knight CD, Adams DG (1999) Characterisation of plant exudates inducing chemotaxis in nitrogen-fixing cyanobacteria. In: Peschek GA, Löffelhardt W, Schmetterer G (eds) The phototrophic prokaryotes. Kluwer/Plenum, New York, pp 679–684

    Google Scholar 

  • Webb DT (1983a) Nodulation in light- and dark-grown Macrozamia communis L. Johnson seedlings in sterile culture. Ann Bot 52:545–547

    Google Scholar 

  • Webb DT (1983b) Developmental anatomy of light-induced root nodulation by Zamia pumila L. seedlings in sterile culture. Am J Bot 70:1109–1117

    Google Scholar 

  • Wei WX, Jin GY, Zhang N, Chen J (1988) Studies of hybridization in Azolla. In: Singh KH, Kramer KU (eds) Proceedings of the international symposium on systematic pteriodology. China Sciientific and Technical Press, Beijing, pp 135–139

    Google Scholar 

  • West N, Adams DG (1997) Phenotypic and genotypic comparison of symbiotic and free-living cyanobacteria from a single field site. Appl Environ Microbiol 63:4479–4484

    PubMed  CAS  Google Scholar 

  • West NJ, Adams DG, Sisson PR, Freeman R, Hawkey PM (1999) Pyrolysis mass spectrometry analysis of free-living and symbiotic cyanobacteria. Antonie Van Leeuwenhoek 75:201–206

    PubMed  CAS  Google Scholar 

  • Wolf E, Schüßler A (2005) Phycobiliprotein fluorescence of Nostoc punctiforme changes during the life cycle and chromatic adaptation: characterization by spectral confocal laser scanning microscopy and spectral unmixing. Plant Cell Environ 28:480–491

    CAS  Google Scholar 

  • Wolk CP (2000) Heterocyst formation in Anabaena. In: Brun YV, Shimkets LJ (eds) Prokaryotic development. ASM Press, Washington, DC, pp 83–104

    Google Scholar 

  • Wong FCY, Meeks JC (2001) The hetF gene product is essential to heterocyst differentiation and affects HetR function in the cyanobacterium Nostoc punctiforme. J Bacteriol 183:2654–2661

    PubMed  CAS  Google Scholar 

  • Wong FCY, Meeks JC (2002) Establishment of a functional symbiosis between the cyanobacterium Nostoc punctiforme and the bryophyte Anthoceros punctatus requires genes involved in nitrogen control and initiation of heterocyst differentiation. Microbiology 148:315–323

    PubMed  CAS  Google Scholar 

  • Wouters J, Janson S, Bergman B (2000) The effect of exogenous carbohydrates on nitrogen fixation and hetR expression in Nostoc PCC 9229 forming symbiosis with Gunnera. Symbiosis 28:63–76

    CAS  Google Scholar 

  • Yoshimura I, Yamamoto Y (1991) Development of Peltigera praetextata lichen thalli in culture. Symbiosis 11:109–117

    Google Scholar 

  • Zhang C-C, Laurent S, Sakr S, Peng L, Bedu S (2006) Heterocyst differentiation and pattern formation in cyanobacteria: a chorus of signals. Mol Microbiol 59:367–375

    PubMed  CAS  Google Scholar 

  • Zheng WW, Nilsson M, Bergman B, Rasmussen U (1999) Genetic diversity and classification of cyanobacteria in different Azolla species by the use of PCR fingerprinting. Theor Appl Genet 99:1187–1193

    CAS  Google Scholar 

  • Zheng WW, Song TY, Bao XD, Bergman B, Rasmussen U (2002) High cyanobacterial diversity in coralloid roots of cycads revealed by PCR fingerprinting. FEMS Microbiol Ecol 40:215–222

    PubMed  CAS  Google Scholar 

  • Zheng S-P, Chen B, Guan X, Zheng W (2008) Diversity analysis of endophytic bacteria within Azolla microphylla using PCR-DGGE and electron microscopy. Chin J Agric Biotechnol 16:508–514

    CAS  Google Scholar 

  • Zheng W, Bergman B, Chen B, Zheng S, Xiang G, Rasmussen U (2009) Cellular responses in the cyanobacterial symbiont during its vertical transfer between plant generations in the Azolla microphylla symbiosis. New Phytol 181:53–61

    PubMed  CAS  Google Scholar 

  • Zielke M, Ekker AS, Olsen RA, Spjelkavik S, Solheim B (2002) The influence of abiotic factors on biological nitrogen fixation in different types of vegetation in the High Arctic, Svalbard Arctic. Arctic Antarct Alpine Res 34:293–299

    Google Scholar 

  • Zielke M, Solheim B, Spjelkavik S, Olsen RA (2005) Nitrogen fixation in the high arctic: role of vegetation and environmental conditions. Arctic Antarct Alpine Res 37:372–378

    Google Scholar 

  • Zimmerman WJ, Watanabe I, Lumpkin TA (1991) The Anabaena-Azolla symbiosis: diversity and relatedness of neotropical host taxa. Plant Soil 137:167–170

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Faculty of Biological Sciences, University of Leeds, Leeds, UK

    Dr. David G. Adams & Dr. Paula S. Duggan

  2. Department of Botany, Stockholm University, 106 91, Stockholm, Sweden

    Birgitta Bergman (Professor)

  3. Department of Biology, Rensselaer Polytechnic Institute, 110 Eighth Street, 12180-3590, Troy, NY, USA

    Sandra A. Nierzwicki-Bauer (Professor)

  4. Department of Biochemistry, North-Eastern Hill University, 793022, Shillong, Meghalaya, India

    Dr. Amar N. Rai

  5. Genetics Biocenter, University of Munich, Grosshaderner Str. 2-4, 82152, Munich, Germany

    Dr. Arthur Schüßler

Authors
  1. Dr. David G. Adams
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Birgitta Bergman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sandra A. Nierzwicki-Bauer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dr. Paula S. Duggan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dr. Amar N. Rai
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dr. Arthur Schüßler
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Molecular Microbiology and Biotechnology, Tel Aviv University, Tel Aviv, Israel

    Eugene Rosenberg

  2. Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA

    Edward F. DeLong

  3. Department of Microbiology and Immunology, Harvard Medical School, Boston, MA, USA

    Stephen Lory

  4. Leibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures, Braunschweig, Germany

    Erko Stackebrandt

  5. Laboratory of Microbiology, Institute of Biology, Center for Health Sciences, Federal University of Rio de Janeiro (UFRJ), Ilha do Fundão, Rio de Janeiro, Brazil

    Fabiano Thompson

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer-Verlag Berlin Heidelberg

About this entry

Cite this entry

Adams, D.G., Bergman, B., Nierzwicki-Bauer, S.A., Duggan, P.S., Rai, A.N., Schüßler, A. (2013). Cyanobacterial-Plant Symbioses. In: Rosenberg, E., DeLong, E.F., Lory, S., Stackebrandt, E., Thompson, F. (eds) The Prokaryotes. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-30194-0_17

Download citation

Publish with us

Policies and ethics

Search

Navigation