Skip to main content
Log in

Association of non-heterocystous cyanobacteria with crop plants

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Cyanobacteria have the ability to form associations with organisms from all domains of life, notably with plants, which they provide with fixed nitrogen, among other substances. This study was aimed at developing artificial associations between non-heterocystous cyanobacteria and selected crop plants. We isolated several non-heterocystous cyanobacteria from various rice fields. The cultures were tested for their capacity to produce the plant hormone indole-3-acetic acid (IAA), and the possible role of IAA in the association of cyanobacteria with seedling roots was evaluated. Axenic cultures were co-inoculated with 10-day-old plant seedlings of Triticum aestivum, Vigna radiata and Pisum sativum and incubated for 1 week. Cyanobacterial association with the roots of these seedlings was quantified by measuring chlorophyll-a. Cyanobacterial association with the roots was observed by light microscopy as well as by confocal laser scanning microscopy (CLSM). Based on sequence analysis of the 16S rRNA gene, the isolates were identified as Synechocystis sp., Chroococcidiopsis sp., Leptolyngbya sp., and Phormidium sp. CLSM observations revealed the intimate association of cyanobacteria with the seedling roots as well as invasion of the roots and root cells. Strains producing IAA were more efficient in the colonization of the roots than those that lacked this ability. IAA-producing cyanobacteria possess a tryptophan-dependent pathway, and these cyanobacteria showed IAA synthesis activity in the presence of roots in media lacking tryptophan. Based on the results of this study, we conclude that non-heterocystous cyanobacteria also have the potential for use in agriculture to improve the growth and yield of crop plants that do not naturally form associations with cyanobacteria.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adams D, Bergman B, Nierzwicki-Bauer S, Rai A, Schüßler A (2006) Cyanobacterial-plant symbioses. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 331–363

  • Ahmad MR, Winter A (1968) Studies on the hormonal relationships of algae in pure culture. Planta 78:277–286

    Article  CAS  Google Scholar 

  • Ali B, Sabri AN, Ljung K, Hasnain S (2009) Quantification of indole-3-acetic acid from plant associated Bacillus spp. and their phytostimulatory effect on Vigna radiata (L.). World J Microbiol Biotechnol 25:519–526

    Article  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389

    Article  CAS  PubMed  Google Scholar 

  • Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266

    Article  CAS  PubMed  Google Scholar 

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

  • Boone DR, Castenholz RW, Garrity GM (2001) Bergey’s manual of systematic bacteriology. Springer, New York

    Google Scholar 

  • Compaoré J, Stal LJ (2009) Oxygen and the light–dark cycle of nitrogenase activity in two unicellular cyanobacteria. Environ Microbiol 12:54–62

    Article  PubMed  Google Scholar 

  • Freiberg E (1999) Influence of microclimate on the occurrence of cyanobacteria in the phyllosphere in a premontane rain forest of Costa Rica. Plant Biol 1:244–252

    Article  Google Scholar 

  • Furey PC (2003) Cosmopolitan cyanobacteria. Am Biol Teach 65:595–598

    Article  Google Scholar 

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

    CAS  Google Scholar 

  • Gantar M, Elhai J (1999) Colonization of wheat para-nodules by the N2-fixing cyanobacterium Nostoc sp. strain 2S9B. New Phytol 141:373–379

    Article  Google Scholar 

  • Gantar M, Kerby NW, Rowell P (1991) Colonization of wheat (Triticum vulgare L.) by N2-fixing cyanobacteria: II. An ultrastructural study. New Phytol 118:485–492

    Article  Google Scholar 

  • Glickmann E, Dessaux Y (1995) A critical examination of the specificity of the salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Appl Environ Microbiol 61:793–796

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Hardy RW, Holsten RD, Jackson EK, Burns RC (1968) The acetylene-ethylene assay for N2 fixation: laboratory and field evaluation. Plant Physiol 43:1185–1207

    Article  CAS  PubMed  Google Scholar 

  • Kamilova F, Kravchenko LV, Shaposhnikov AI, Azarova T, Makarova N, Lugtenberg B (2006) Organic acids, sugars, and l-tryptophane in exudates of vegetables growing on stonewool and their effects on activities of rhizosphere bacteria. Mol Plant-Microb Interact 19:250–256

    Article  CAS  Google Scholar 

  • Mathesius U (2008) Auxin: at the root of nodule development? Funct Plant Biol 35:651–668

    Article  CAS  Google Scholar 

  • McGinnis S, Madden TL (2004) BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Res 32:W20

    Article  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

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Ohki K (2008) Intercellular localization of nitrogenase in a non-heterocystous cyanobacterium (cyanophyte), Trichodesmium sp NIBB1067. J Oceanogr 64:211–216

    Article  CAS  Google Scholar 

  • Prasanna R, Pabby A, Saxena S, Singh PK (2004) Modulation of pigment profiles of Calothrix elenkenii in response to environmental changes. J Plant Physiol 161:1125–1132

    Article  CAS  PubMed  Google Scholar 

  • Prasanna R, Jaiswal P, Nayak S, Sood A, Kaushik BD (2009) Cyanobacterial diversity in the rhizosphere of rice and its ecological significance. Indian J Microbiol 49:89–97

    Article  CAS  Google Scholar 

  • Rai AN, Bergman B (2002) Creation of new nitrogen-fixing cyanobacterial associations. Biol Environ: Proc R Ir Acad 102B:65–68

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Raven J (2002) Evolution of cyanobacterial symbioses. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in symbiosis. Kluwer, Dordrecht, pp 329–346

    Google Scholar 

  • Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61

    Google Scholar 

  • Schenk HE, Bayer MG, Maier TL, Luttke A, Gebhart UB, Stevanovic S (1992) Ferredoxin-NADP + oxidoreductase of C. paradoxa nucleus encoded, but cyanobacterial gene transfer from symbiont to host, an evolutionary mechanism originating new species. Z Naturforsch C 47:387–393

    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

    Article  CAS  PubMed  Google Scholar 

  • Stal LJ, Krumbein WE (1985) Isolation and characterization of cyanobacteria from a marine microbial mat. Bot Mar 28:351–365

    Article  Google Scholar 

  • Svircev Z, Tamas I, Nenin P, Drobac A (1997) Co-cultivation of N2-fixing cyanobacteria and some agriculturally important plants in liquid and sand cultures. Appl Soil Ecol 6:301–308

    Article  Google Scholar 

  • Tandeau de Marsac N, Houmard J (1988) Complementary chromatic adaptation: physiological conditions and action spectra. Methods Enzymol 167:318–328

    Article  CAS  Google Scholar 

  • Tarakhovskaya ER, Maslov YI, Shishova MF (2007) Phytohormones in algae. Russ J Plant Physiol 54:163–170

    Article  CAS  Google Scholar 

  • Theunis M, Kobayashi H, Broughton WJ, Prinsen E (2004) Flavonoids, NodD1, NodD2, and nod-box NB15 modulate expression of the y4wEFG locus that is required for indole-3-acetic acid synthesis in Rhizobium sp strain NGR234. Mol Plant-Microb Interact 17:1153–1161

    Article  CAS  Google Scholar 

  • van Heerden PD, Kiddle G, Pellny TK, Mokwala PW, Jordaan A, Strauss AJ, de Beer M, Schluter U, Kunert KJ, Foyer CH (2008) Regulation of respiration and the oxygen diffusion barrier in soybean protect symbiotic nitrogen fixation from chilling-induced inhibition and shoots from premature senescence. Plant Physiol 148:316–327

    Article  PubMed  Google Scholar 

  • Walsby AE (2007) Cyanobacterial heterocysts: terminal pores proposed as sites of gas exchange. Trends Microbiol 15:340–349

    Article  CAS  PubMed  Google Scholar 

  • Whitton BA (2000) Soils and rice-fields. In: Whitton BA, Potts M (eds) Ecology of cyanobacteria: their diversity in time and space. Kluwer, Dordrecht, pp 233–255

    Google Scholar 

Download references

Acknowledgments

The Higher Education Commission of Pakistan is acknowledged for providing funding to Mehboob Ahmed (IRSIP No.1-8 ⁄HEC⁄HRD⁄ 2007 ⁄ 923) to visit the Netherlands Institute of Ecology (NIOO-KNAW) to perform Confocal Laser Scanning Microscopy. We thank Anita Wijnholds for her help with CLSM and Ms. Veronique Confurius-Guns for her assistance and help with PCR and DNA sequencing.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shahida Hasnain.

Additional information

Responsible Editor: Katharina Pawlowski.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ahmed, M., Stal, L.J. & Hasnain, S. Association of non-heterocystous cyanobacteria with crop plants. Plant Soil 336, 363–375 (2010). https://doi.org/10.1007/s11104-010-0488-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-010-0488-x

Keywords

Navigation