Skip to main content
SpringerLink
Log in

Signalling in Cyanobacteria–Plant Symbioses

  • Chapter
  • First Online:
Signaling and Communication in Plant Symbiosis

Part of the book series: Signaling and Communication in Plants ((SIGCOMM,volume 11))

Abstract

Cyanobacteria are a morphologically diverse and widespread group of phototrophic bacteria, many of which are capable of nitrogen fixation. They form symbioses with a wide range of eukaryotic hosts including fungi (lichens and Geosiphon pyriformis), diatoms, dinoflagellates, sponges, ascidians (sea squirts), corals and plants. The best understood are the plant symbioses, which are the subject of this chapter. In the cyanobacteria–plant associations, the cyanobacteria provide the host with fixed nitrogen and usually adopt a heterotrophic form of nutrition, using fixed carbon supplied by the plant, enabling them to occupy regions of the host, such as the roots, that receive little or no light. Most cyanobacterial symbionts of plants belong to the genus Nostoc, members of which fix nitrogen in specialised cells known as heterocysts, which provide the necessary microoxic environment for the functioning of the oxygen-sensitive enzyme nitrogenase. These cyanobacteria, which are immotile for most of their life cycles, produce specialised motile filaments known as hormogonia, as a means of dispersal and as the infective agents in plant symbioses. Host plants improve their chances of infection by releasing external chemical signals that both stimulate hormogonia formation and serve as chemoattractants. However, within the symbiotic tissue the plant releases hormogonia-repressing factors to ensure the conversion of hormogonia into heterocyst-containing, nitrogen-fixing filaments.

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

Access this chapter

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 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
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

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 (2011) Cyanobacterial symbioses. In: Whitton B (ed.) Ecology of cyanobacteria II. Springer, Heidelberg

    Google Scholar 

  • Adams DG, Duggan PS (1999) Heterocyst and akinete differentiation in cyanobacteria. New Phytol 144:3–33

    Google Scholar 

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

    CAS  PubMed  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 

  • 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. Biol Environ Proc R Ir Acad 102B:35–39

    Google Scholar 

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

    Google Scholar 

  • Bergman B, Rasmussen U, Rai AN (2007a) 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, Zheng W, Ekman M, Ran L (2007b) The cyanobacterium-Azolla symbiosis: interactions and cell differentiation. Comp Biochem Physiol A Mol Integr Physiol 146A:S218

    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, Norfolk, pp 447–473

    Google Scholar 

  • Berry AM, Rasmussen U, Bateman K, Huss-Danell K, Lindwall S, Bergman B (2002) Arabinogalactan proteins are expressed at the symbiotic interface in root nodules of Alnus spp. New Phytol 155:469–479

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Black K, Osborne B (2004) An assessment of photosynthetic downregulation in cyanobacteria from the Gunnera-Nostoc symbiosis. New Phytol 162:125–132

    CAS  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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  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

    CAS  PubMed  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

    CAS  PubMed Central  PubMed  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Carrapico F (2002) The Azolla-Anabaena-bacteria system as a natural microcosm. In: Hoover RB, Levin GV, Paepe RR, Rozanov AY (eds) Instruments, methods, and missions for astrobiology IV, Proceedings of SPIE vol 4495, pp 261–265

    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

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Choudhury A, Kennedy IR (2004) Prospects and potentials for systems of biological nitrogen fixation in sustainable rice production. Biol Fertil Soils 39:219–227

    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

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  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

    CAS  PubMed  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

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Diaz E-M, Sacristan M, Legaz M-E, Vicente C (2009) Isolation and characterization of a cyanobacterium-binding protein and its cell wall receptor in the lichen Peltigera canina. Plant Signal Behav 4:598–603

    CAS  PubMed Central  PubMed  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ekman M, Tollback 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

    CAS  PubMed  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 

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

    CAS  PubMed  Google Scholar 

  • Flores E, Herrero A (2010) Compartmentalised function through cell differentiation in filamentous cyanobacteria. Nat Rev Microbiol 8:39–50

    CAS  PubMed  Google Scholar 

  • Gantar M (2000a) Mechanical damage of roots provides enhanced colonization of the wheat endorhizosphere by the dinitrogen-fixing cyanobacterium Nostoc sp. strain 2S9B. Biol Fertil Soils 32:250–255

    Google Scholar 

  • Gantar M (2000b) Co-cultivation of N2-fixing cyanobacterium Nostoc sp strain 2S9B and wheat callus. Symbiosis 29:1–18

    CAS  Google Scholar 

  • Gaspar Y, Johnson KL, McKenna JA, Bacic A, Schultz CJ (2001) The complex structures of arabinogalactan proteins and the journey towards understanding function. Plant Mol Biol 47:161–176

    CAS  PubMed  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

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Gorelova OA (2001) Surface ultrastructure of the heteromorphic cells of Nostoc muscorum CALU 304 in a mixed culture with the Rauwolfia callus tissue. Microbiology 70:285–294

    CAS  Google Scholar 

  • Gorelova OA (2006) Communication of cyanobacteria with plant partners during association formation. Microbiology 75:465–469

    CAS  Google Scholar 

  • Gorelova OA, Baulina OI (2009) Ultrastructure of cyanobacterium Nostoc sp f. Blasia cell forms in persisting populations. Microbiology 78:609–617

    CAS  Google Scholar 

  • Gorelova OA, Kleimenov SY (2003) The accumulation and degradation dynamics of cyanophycin in cyanobacterial cells grown in symbiotic associations with plant tissues and cells. Microbiol 72:318–326

    Google Scholar 

  • Gorelova OA, Korzhenevskaya TG (2002) Formation of giant and ultramicroscopic forms of Nostoc muscorum CALU 304 during cocultivation with Rauwolfia tissues. Microbiol 71:563–569

    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

    CAS  PubMed  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 

  • 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

    CAS  PubMed  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 

  • Karthikeyan N, Prasanna R, Nain L, Kaushik BD (2007) Evaluating the potential of plant growth promoting cyanobacteria as inoculants for wheat. Eur J Soil Biol 43:23–30

    CAS  Google Scholar 

  • Karthikeyan N, Prasanna R, Sood A, Jaiswal P, Nayak S, Kaushik BD (2009) Physiological characterization and electron microscopic investigation of cyanobacteria associated with wheat rhizosphere. Folia Microbiol 54:43–51

    CAS  Google Scholar 

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

    CAS  PubMed Central  PubMed  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 (2002) A fungus eats a cyanobacterium: the story of the Geosiphon pyriformis endocyanosis. Biol Environ Proc R Ir Acad 102B:11–14

    Google Scholar 

  • Kluge M, Mollenhauer D, Wolf E, Shussler A (2002) The Nostoc-Geosiphon endocytobiosis. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in symbiosis. Kluwer, Dordrecht, pp 19–30

    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 

  • 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 

  • 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

    CAS  PubMed  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 

  • Liaimer A, Bergman B (2004) Phytohormones in cyanobacteria: occurrence and perspectives. In: Tikhonovich I, Lugtenberg B, Provorov N (eds) Biology of plant-microbe interactions. International Society for Molecular Plant Microbe Interactions, St Paul, MN, pp 394–397

    Google Scholar 

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

    CAS  Google Scholar 

  • Lindblad P (2009) Cyanobacteria in symbiosis with cycads. Microbiol Monogr 8:225–233

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Lobakova ES, Dol’nikova GA, Korzhenevshaya TG (2001a) Cyanobacterial-bacterial complexes in plant syncyanoses. Microbiology 70:111–116

    CAS  Google Scholar 

  • Lobakova ES, Shchelmanova AG, Korzhenevskaya TG, Gusev MV (2001b) Infection of plants and plant tissue cultures with cyanobacteria-bacteria complexes. Microbiology 70:299–305

    CAS  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 

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

    CAS  PubMed  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 (2006) Molecular mechanisms in the nitrogen-fixing Nostoc-bryophyte symbiosis. Prog Molec Subcell Biol 41:165–196

    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 monographs. 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

    CAS  PubMed Central  PubMed  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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Muro-Pastor MI, Reyes JC, Florencio FJ (2001) Cyanobacteria perceive nitrogen status by sensing intracellular 2-oxoglutarate levels. J Biol Chem 276:38320–38328

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Nilsson MC, Wardle DA (2005) Understory vegetation as a forest ecosystem driver: evidence from the northern Swedish boreal forest. Eur J Phycol 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

    CAS  PubMed  Google Scholar 

  • Nilsson M, Bhattacharya J, Rai AN, Bergman B (2002) Colonization of roots of rice (Oryza sativa) by symbiotic Nostoc strains. New Phytol 156:517–525

    Google Scholar 

  • Nilsson M, Rasmussen U, Bergman B (2005) Competition among symbiotic cyanobacterial Nostoc strains forming artificial associations with rice (Oryza sativa). FEMS Microbiol Lett 245:139–144

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Osborne B, Sprent JI (2002) Ecology of the Nostoc-Gunnera symbiosis. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in symbiosis. Kluwer, Dordrecht, pp 233–251

    Google Scholar 

  • Pabby A, Prasanna BM, Nayak S, Singh AK (2003) Physiological characterization of the cultured and freshly isolated endosymbionts from different species of Azolla. Mar Biotechnol 41:73–79

    CAS  Google Scholar 

  • Pabby A, Prasanna BM, Singh AK (2004a) Biological significance of Azolla and its utilization in agriculture. Proc Indian Natl Sci Acad B 3:299–333

    Google Scholar 

  • Pabby A, Prasanna R, Singh PK (2004b) Morphological characterization of cultured and freshly separated cyanobionts (Nostocales, Cyanophyta) from Azolla species. Acta Bot Hung 46:211–223

    Google Scholar 

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

    PubMed  Google Scholar 

  • Papaefthimiou D, Van Hove C, Lejeune A, Rasmussen U, Wilmotte A (2008b) Diversity and host specificity of Azolla cyanobionts. J Phycol 44:60–70

    CAS  Google Scholar 

  • Paulsrud P, Lindblad P (2002) Fasciclin domain proteins are present in Nostoc symbionts of lichens. Appl Environ Microbiol 68:2036–2039

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rai AN, Soderback E, Bergman B (2000) Cyanobacterium-plant symbioses. New Phytol 147:449–481

    CAS  Google Scholar 

  • Ran LA, Larsson J, Vigil-Stenman T, Nylander JAA, Ininbergs K, Zheng WW, 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 Central  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 MM (2001) Characterization by genotypic methods of symbiotic Nostoc strains isolated from five species of Gunnera. Arch Microbiol 176:204–210

    CAS  PubMed  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 

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

    CAS  PubMed  Google Scholar 

  • Renzaglia KS, Schuette S, Duff RJ, Ligrone R, Shaw AJ, Mishler BD, Duckett JG (2007) Bryophyte phylogeny: advancing the molecular and morphological frontiers. Bryologist 110:179–213

    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, Virtanen V (2008) Genetic diversity in cyanobacterial symbionts of thalloid bryophytes. J Exp Bot 59:1013–1021

    CAS  PubMed  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 Central  PubMed  Google Scholar 

  • Seifert GJ, Roberts K (2007) The biology of arabinogalactan proteins. Annu Rev Plant Biol 58:137–161

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Showalter AM (2001) Arabinogalactan proteins: structure, expression and function. Cell Mol Life Sci 58:1399–1417

    CAS  PubMed  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 (2008a) Genetic diversity among and within cultured cyanobionts of diverse species of Azolla. Folia Microbiol 53:35–43

    CAS  Google Scholar 

  • Sood A, Prasanna R, Singh PK (2008b) Fingerprinting of freshly separated and cultured cyanobionts from different Azolla species using morphological and molecular markers. Aquat Bot 88:142–147

    CAS  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

    CAS  PubMed  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

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Ungerer JL, Pratte BS, Thiel T (2008) Regulation of fructose transport and its effect on fructose toxicity in Anabaena spp. J Bacteriol 190:8115–8125

    CAS  PubMed Central  PubMed  Google Scholar 

  • Usher KM (2008) The ecology and phylogeny of cyanobacterial symbionts in sponges. Mar Ecol Evol Perspect 29:178–192

    Google Scholar 

  • Vaishampayan A, Sinha RP, Hader D-P, Dey T, Gupta AK, Bhan U, Rao AL (2001) Cyanobacterial biofertilizers in rice agriculture. Bot Rev 67:453–516

    Google Scholar 

  • van Hove C, Lejeune A (2002a) The Azolla-Anabaena symbiosis. Biol Environ Proc R Ir Acad 102B:23–26

    Google Scholar 

  • van Hove C, Lejeune A (2002b) Applied aspects of Azolla-Anabaena symbiosis. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in symbiosis. Kluwer, Dordrecht, pp 179–193

    Google Scholar 

  • Vazquez-Bermudez MF, Herrero A, Flores E (2002) 2-oxoglutarate increases the binding affinity of the NtcA (nitrogen control) transcription factor for the Synechococcus glnA promoter. FEBS Lett 512:71–74

    CAS  PubMed  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 

  • 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 

  • Vivas M, Sacristan M, Legaz M-E, Vicente C (2010) The cell recognition model in chlorolichens involving a fungal lectin binding to an algal ligand can be extended to cyanolichens. Plant Biol 12:615–621

    CAS  PubMed  Google Scholar 

  • Wang CM, 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 17:436–443

    CAS  PubMed  Google Scholar 

  • Watts SD (2000) Signalling in the Nostoc-plant symbiosis. PhD thesis, University of Leeds, UK, pp 185

    Google Scholar 

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

    CAS  PubMed Central  PubMed  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

    CAS  PubMed Central  PubMed  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

    CAS  PubMed  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 

  • 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

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Zheng WW, Ran L, Bergman B (2009a) Structural characteristics of the cyanobacterium-Azolla symbiosis. In: Pawlowski K (ed) Prokaryotic symbionts in plants, vol 8, Microbiol monographs. Springer, Heidelberg, pp 235–263

    Google Scholar 

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

    CAS  PubMed  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. Arct 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. Arct Antarct Alpine Res 37:372–378

    Google Scholar 

Download references

Acknowledgements

Our thanks go to the authors who gave permission for us to use the images reproduced in this chapter.

Author information

Authors and Affiliations

  1. Faculty of Biological Sciences, Institute of Integrative and Comparative Biology, University of Leeds, Leeds, LS2 9JT, UK

    David G. Adams & Paula S. Duggan

Authors
  1. David G. Adams
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paula S. Duggan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David G. Adams .

Editor information

Editors and Affiliations

  1. Dipto. Biologia Vegetale, Universita Torino Dipto. Biologia Vegetale, Torino, Italy

    Silvia Perotto

  2. Botanik (IZMB), Universität Bonn Inst. Zelluläre und Molekulare, Bonn, Germany

    František Baluška

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Adams, D.G., Duggan, P.S. (2012). Signalling in Cyanobacteria–Plant Symbioses. In: Perotto, S., Baluška, F. (eds) Signaling and Communication in Plant Symbiosis. Signaling and Communication in Plants, vol 11. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-20966-6_5

Download citation

Publish with us

Policies and ethics

Search

Navigation