Skip to main content
Log in

Potential and pitfalls of trying to extend symbiotic interactions of nitrogen-fixing organisms to presently non-nodulated plants, such as rice

  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

It has been a long-standing goal in the field of biological nitrogen fixation to extend nitrogen-fixing symbioses to presently non-nodulated cereal plants, such as rice. A number of researchers have recently described the induction of “nodule-like” structures on the roots of cereals primarily by rhizobia, in either the presence or absence of plant cell-wall-degrading enzymes or plant hormones. We briefly review this research and discuss the potential problems associated with the introduction of nitrogen-fixing microbes in novel physiological environments, such as rice roots. The results of experiments carried out in China on the induction of “nodule-like” structures on rice roots by rhizobia are highlighted. In addition, we present preliminary results of a series of experiments designed to repeat and evaluate these results using a variety of microscopic techniques and molecular genetic approaches.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • AI-Mallah M K, Davey M R and Cocking E C 1989 formation of nodular structures on rice seedlings by rhizobia. J. Exp. Bot. 40, 473–478.

    Google Scholar 

  • Appleby C A 1984 Leghemoglobin and Rhizobium respiration. Annu. Rev. Plant Physiol. 35, 443–478.

    Google Scholar 

  • Bender G L, Preston L, Barnard D and Rolfe B G 1990 Formation of nodule-like structures on the roots of the non-legumes rice and wheat. In Nitrogen Fixation: Achievements and Objectives. Eds. P M Gresshoff, L E Roth, G Stacey and W E Newton. p 825. Chapman and Hall, New York.

    Google Scholar 

  • Boddey R M, de Oliveira O C, Urquiaga S, Resi V M, de Olivares F L, Baldani V L D and Döbereiner J 1995 Biological nitrogen fixation associated with sugar cane and rice: contributions and prospects for improvement. Plant and soil 174.

  • Bogusz D, Appleby C A, Landsmann J, Dennis E S, Trinick N J and Peacock W J 1988 Functioning hemoglobin genes in non-nodulating plants. Nature 331, 178–180.

    Google Scholar 

  • Chen T-W 1993 Nitrogen fixation of Azorhizobium in artificially induced root para-nodules in wheat. Sci. China 35, 1463–1469.

    Google Scholar 

  • Chen T-W, Scherer S and Böger 1993 Nitrogen fixation of Azorhizobium in artificially induced root para-nodules in wheat. In Advances in Molecular Genetics of Plant-Microbe Interactions. Eds. E W Nester and D P S Verma. pp 593–606. Kluwer Academic Publishers, Dordrecht.

    Google Scholar 

  • Christansen-Weniger C and Vanderleyden J 1994 Ammonium-excreting Azospirillum sp. become intracellulariy established in maize (Zea mays) para nodules. Biol. Fertil. Soils 17, 1–8.

    Google Scholar 

  • Cocking E C and Davey M R 1991 Nitrogen from the air for non-legume crops. Chem., London 18 Nov, 831–835.

  • Cocking E C, AI-Mallah M K, Benson E and Davey M R 1990 Nodulation of non-legumes by rhizobia. In Nitrogen Fixation: Achievements and Objectives. Eds. P M Gresshoff, L E Roth, G Stacey and W E Newton. pp 813–823. Chapman and Hall, New York.

    Google Scholar 

  • Cocking E, Srivastava J, Kothari S and Davey M 1992 Invasion of nonlegume plants by diazotrophic bacteria. In Nodulation and Nitrogen Fixation in Rice: Potentials and Prospects. Eds. G Khush and J Bennett. pp 119–121. IRRI, Manila.

    Google Scholar 

  • David M, Daveran M-L, Batut J, Dedieu A, Domergue O, Ghai J, Hertig C, Boistard P and Kahn D 1988 Cascade regulation of nif gene expression in Rhizobium meliloti. Cell 54, 671–683.

    Google Scholar 

  • Dazzo F 1982 Leguminous root nodules. In Experimental Microbial Ecology. Eds. R Burns and J Slater. pp 431–466. Blackwell Scientic Publications, Oxford, UK.

    Google Scholar 

  • Dazzo F, Mateos P, Orgambide G, Philip-Hollingsworth S, Squartini A, Subba-Rao N, Pankratz H S, Baker D, Hollingsworth R and Whallon J 1993 The infection process in the Rhizobium-legume symbiosis and visualization of rhizoplane microorganisms by laser scanning confocal microscopy. In Trends in Microbial Ecology. Eds. R Guerrero and C Pedros-Alio. pp 259–262. Spanish Society for Microbiology, Barcelona.

    Google Scholar 

  • De Bruijn F J 1992 Use of repetitive (repetitive extragenic palindromic and enterobacterial repetitive intergenic consensus) sequences and the polymerase chain reaction to fingerprint the genomes of Rhizobium meliloti isolates and other soil bacteria. Appl. Environ. Microbiol. 58, 2180–2187.

    Google Scholar 

  • De Bruijn F J, Chen R, Dehio C, Goel A, Reiser S and Szczyglowski K 1992 Hormones and nodule formation: cytokinin induction of the Sesbania rostrata early nodulin gene Enod2. In Nodulation and Nitrogen Fixation in Rice: Potential and Prospects. Eds. G S Khush and J Bennett. pp 33–40. IRRI, Manila.

    Google Scholar 

  • De Bruijn F J, Chen R, Fujimoto S Y, Pinaev A, Silver D and Szczyglowski K 1994 Regulation of nodulin gene expression. Plant and Soil 161, 59–68.

    Google Scholar 

  • De Bruijn F J and Downie J A 1991 Biochemical and molecular studies of symbiotic nitrogen fixation. Curr. Op. Biotech. 2, 184–192.

    Google Scholar 

  • De Bruijn F J and Schell J 1992 Regulation of plant genes specifically induced in developing and mature nitrogen-fixing nodules: Cis-acting elements and Trans-acting factors. In Control of Plant Gene Expression. Ed. D P S Verma. pp 241–258. CRC Press, Boca Raton, Florida.

    Google Scholar 

  • Dehio C and de Bruijn F J 1992 The early nodulin gene SrEnod2 from Sesbania rostrata is inducible by cytokinin. Plant J. 2, 117–128.

    Google Scholar 

  • Dénarié J and Cullimore J 1993 Lipo-oligosaccharide nodulation. factors: a new class of signaling molecules mediating recognition and morphogenesis. Cell 74, 951–954.

    Google Scholar 

  • Döbereiner J, Reis V M, Paula M A and Olivares F 1993 Endophytic diazotrophs in sugar cane, cereals and tuber plants. In New Horizons in Nitrogen Fixation. Eds. R Palacios, J Mora and W E Newton. pp 671–676. Kluwer Acad. Publ., Dordrecht, Netherlands.

    Google Scholar 

  • Earl C D and Ausubel F M 1983 The genetic engineering of nitrogen fixation. Nutr. Rev. 41, 1–6.

    Google Scholar 

  • Elmerich C, Dreyfus B, Reysset G and Aubert J P 1982 Genetic analysis of nitrogen fixation in a tropical fast-growing Rhizobium. EMBO J. 1, 499–503.

    Google Scholar 

  • Fischer H-M 1994 Genetic regulation of nitrogen fxation in rhizobia. Microbiol. Rev. 58, 352–386.

    Google Scholar 

  • Fisher R F and Long S R 1992 Rhizobium-plant signal exchange. Nature 357, 655–660.

    Google Scholar 

  • Gilles-Gonzalez M A, Ditta G S and Helinski D R 1991 A haemoprotein with kinase activity encoded by the oxygen sensor of Rhizobium meliloti. Nature 350, 170–172.

    Google Scholar 

  • Hirsch A M 1992 Tansley review no. 40: Developmental biology of legume nodulation. New Phytol. 122, 211–237.

    Google Scholar 

  • Hollingsworth R, Squartini A, Philip-Hollingsworth S and Dazzo F 1989 Root hair deforming and nodule initiating factors from Rhizobium trifolii. In Signal Molecules in Plants and Plant-Microbe Interactions. Ed. B Lugtenberg. pp 387–393. Springer-Verlag, Berlin.

    Google Scholar 

  • Horvath B, Heidstra R, Lados M, Moerman M, Spaink H P, Promé J-C, van Kammen A and Bisseling T 1993 Lipo-oligosaccharides of Rhizobium induce infection-related early nodulin gene expression in pea root hairs. Plant J. 4, 727–733.

    Google Scholar 

  • Hurek T, Reinhold-Hurek B, van Montagu M and Kellenberger E 1994 Root colonization and systemic spreading of Azoarcus sp. strain BH72 in grasses. J. Bacteriol. 176, 1913–1923.

    Google Scholar 

  • Jing Y, Li G, Jin G, Shan X, Zhang B, Guan C and Li J 1990a Rice root nodules with acetylene reduction activity. In Nitrogen Fixation: Achievements and Objectives. Eds. P M Gresshoff, L E Roth, G Stacey and W E Newton. p 829. Chapman and Hall, New York.

    Google Scholar 

  • Jing Y, Li G and Shan X 1992 Development of nodulelike structure on rice roots. In Nodulation and Nitrogen Fixation in Rice: Potentials and prospects Eds. G Khush and J Bennett pp 123–126. IRRI, Manila, Phillippines.

    Google Scholar 

  • Jing Y, Zhang B T and Shan X Q 1990b Pseudonodules formation on barley roots induced by Rhizobium astragali. FEMS Microbiol. Lett. 69, 123–128.

    Google Scholar 

  • Kennedy I R and Tchan Y-T 1992 Biological nitrogen fixation in non-leguminous field crops: Recent advances. Plant and Soil 141, 93–118.

    Google Scholar 

  • Khush G S and Bennett J (Eds.) 1992 Nodulation and Nitrogen Fixation in Rice: Potential and Prospects. IRRI Press, Manila.

    Google Scholar 

  • Ladha J K, Trol-Padre A, Reddy K and Ventura W 1993 Prospects and problems of biological nitrogen fixation in rice production: A critical assessment. In New Horizons in Nitrogen Fixation. Eds. R Palacios et al. pp.677–682. Kluwer Academic Publishers, Dordrecht.

    Google Scholar 

  • Lauridsen P, Franssen H, Stougaard J, Bisseling T and Marcker K A 1993 Conserved regulation of the soybean early nodulin Enod2 gene promoter in determinate and indeterminate transgenic root nodules. Plant J. 3, 483–492.

    Google Scholar 

  • Li G, Jing Y, Shan X, Wang H and Guan C 1991 Identification of rice nodules that contain Rhizobium bacteria. Chin. J. Bot. 3, 8–17.

    Google Scholar 

  • Orgambide G G, Hollingsworth R I and Dazzo F B 1992 Structural characterization of a novel diglycosyl diacylglyceride glycolipid from Rhizobium trifolii ANU 843. Carbohydr. Res. 233, 151–159.

    Google Scholar 

  • Orgambide G G, Philip-Hollingsworth S, Hollingsworth R I and Dazzo F B 1994 Flavone-enhanced accumulation and symbiosis-related biological activity of a diglycosyl diacylglycerol membrane glycolipid from Rhizobium leguminosarum biovar trifolii. J. Bacteriol. 176, 4338–4347.

    Google Scholar 

  • Pawlowski K, Ratet R, Schell J and de Bruijn F J 1987 Cloning and characterization of nifA and ntrC genes of the stem nodulating bacterium ORS571, the nitrogen fixing symbiont of Sesbania rostrata: Regulation of nitrogen fixation (nif) genes in the free living versus symbiotic state. Mol. Gen. Genet. 206, 207–219.

    Google Scholar 

  • Peoples M B, Herridge D F and Ladha J K 1995 Biological nitrogen fixation: an efficient source of nitrogen for sustainable agriculture? Plant and Soil 174.

  • Peters N K and Verma D P S 1990 Phenolic compounds as regulators of gene expression in plant-microbe interactions. Mol. Plant-Micr. Interact. 3, 4–8.

    Google Scholar 

  • Phillips D A 1992 Flavonoids: Plant signals to soil microbes. In Phenolic Metabolism in Plants. Ed. H A Stafford. pp 201–231. Plenum Press, New York, USA.

    Google Scholar 

  • Phillips D A, Dakora F D, Sande E, Joseph C M and Zon J 1994 Synthesis, release, and transmission of alfalfa signals to rhizobial symbionts. Plant and Soil 161, 69–80.

    Google Scholar 

  • Quispel A 1992 A search for signals in endophytic microorganisms. In Molecular Signals in Plant-Microbe Communications. Ed. D P S Verma. pp 475–491. CRC Press, Boca Raton, FL.

    Google Scholar 

  • Ridge R W, Bender G L and Rolfe B G 1992 Nodule-like structures induced on the roots of wheat seedlings by the addition of the synthetic auxin 2,4-dichlorophenoxyacetic acid and the effects of microorganisms. Aust. J. Plant Physiol. 19, 481–492.

    Google Scholar 

  • Rolfe B G and Bender G L 1990 Evolving a Rhizobium for non-legume nodulation. In Nitrogen Fixation: Achievements and Objectives. Eds. P M Gresshoff, L E Roth, G Stacey and Vlr E Newton. pp 829. Chapman and Hall, New York.

    Google Scholar 

  • Rolfe B, Ride K and Ridge R 1992 Rhizobium nodulation of non-legumes. In Nodulution and Nitrogen Fixation in Rice: Potentials and Prospects. Eds. G Khush and J Bennett. pp 83–86. IRRI, Manila.

    Google Scholar 

  • Schubert K R 1986 Products of biological nitrogen fixation in higher plants: synthesis, transport, and metabolism. Ann. Rev. Plant Physiol. 37, 539–574.

    Google Scholar 

  • Simon Moffatt A 1990 Nitrogen-fixing bacteria find new partners. Science 250, 910–912.

    Google Scholar 

  • Szczyglowski K, Szabados L, Fujimoto S Y, Silver D and de Bruijn F J 1994 Site-specific mutagenesis of the nodule-infected-cell expression (NICE) element and the AT-rich element (ATRE-BS2*) of the Sesbania rostrata leghemoglobin glb3 promoter. Plant Cell 6, 317–332.

    Google Scholar 

  • Tchan Y T, Zeman A M M and Kennedy I R 1991 Nitrogen Fixation in para-nodules of wheat roots by introduced free-living diazotrophs. Plant and Soil 137, 43–47.

    Google Scholar 

  • Truchet G, Camut S, DeBill F, Ororico R and Vasse J 1989 The Rhizobium-legume symbiosis: two methods to discriminate between nodules and other root derived structures. Protoplasma 149, 82–88.

    Google Scholar 

  • Umali-Garcia M, Hubbell D Gaskins M and Dazzo F 1980 Association of Azospirillum with grass roots. Appl. Environ. Microbiol. 39, 219–226.

    Google Scholar 

  • Van Kammen A 1984 Suggested nomenclature for plant genes involved in nodulation and symbiosis. Plant Mol. Biol. Rep. 2, 43–45.

    Google Scholar 

  • Vijn L, das Neves L, van Kammen A, Franssen H and Bisseling T 1993 Nod factors and nodulation in plants. Science 260, 1764–1765.

    Google Scholar 

  • Welters P, Metz B, Felix G, Palme K, Szczyglowski K and de Bruijn F J 1993 Interaction of a rhizobiai DNA-binding protein with the promoter region of a plant leghemoglobin gene. Plant Physiol. 102, 1095–1107.

    Google Scholar 

  • Yu D, Kennedy I R and Tchan Y T 1993 Verification of nitrogenase activity (C2H2 reduction) in Azospirillum populated, 2,4-dichlorophenoxyacetic acid induced root structures of wheat. Aust. J. Plant Physiol. 29, 187–195.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

de Bruijn, F.J., Jing, Y. & Dazzo, F.B. Potential and pitfalls of trying to extend symbiotic interactions of nitrogen-fixing organisms to presently non-nodulated plants, such as rice. Plant Soil 174, 225–240 (1995). https://doi.org/10.1007/BF00032249

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00032249

Key words

Navigation