Endophytic colonization of plant roots by nitrogen-fixing bacteria
- Edward C. Cocking
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Nitrogen-fixing bacteria are able to enter into roots from the rhizosphere, particularly at the base of emerging lateral roots, between epidermal cells and through root hairs. In the rhizosphere growing root hairs play an important role in symbiotic recognition in legume crops. Nodulated legumes in endosymbiosis with rhizobia are amongst the most prominent nitrogen-fixing systems in agriculture. The inoculation of non-legumes, especially cereals, with various non-rhizobial diazotrophic bacteria has been undertaken with the expectation that they would establish themselves intercellularly within the root system, fixing nitrogen endophytically and providing combined nitrogen for enhanced crop production. However, in most instances bacteria colonize only the surface of the roots and remain vulnerable to competition from other rhizosphere micro-organisms, even when the nitrogen-fixing bacteria are endophytic, benefits to the plant may result from better uptake of soil nutrients rather than from endophytic nitrogen fixation. Azorhizobium caulinodans is known to enter the root system of cereals, other non-legume crops and Arabidopsis, by intercellular invasion between epidermal cells and to internally colonize the plant intercellularly, including the xylem. This raises the possibility that xylem colonization might provide a non-nodular niche for endosymbiotic nitrogen fixation in rice, wheat, maize, sorghum and other non-legume crops. A particularly interesting, naturally occurring, non-nodular xylem colonising endophytic diazotrophic interaction with evidence for endophytic nitrogen fixation is that of Gluconacetobacter diazotrophicus in sugarcane. Could this beneficial endophytic colonization of sugarcane by G. diazotrophicus be extended to other members of the Gramineae, including the major cereals, and to other major non-legume crops of the World?
Al-Mallah M K, Davey M R and Cocking E C 1987 Enzymatic treatment of clover root hairs removes a barrier to Rhizobium-host specificity. Bio/Technology 5, 1319–1322.
Al-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.
Al-Mallah M K, Davey M R and Cocking E C 1990 Nodulation of oilseed rape (Brassica napus) by rhizobia. J. Exp. Bot. 41, 1567–1572.
Bell C R, Dickie G A, Harvey W L G and Chan J W Y F 1995 Endophytic bacteria in grapevine. Can. J. Microbiol. 41, 46–53.
Boddey R M, da Silva L G, Reis V, Alves B J R and Urquiaga S 2000 Assessment of bacterial nitrogen fixation in grass species. In Prokaryotic Nitrogen Fixation: A Model System for Analysis of a Biological Process. Ed. E W Triplett. pp. 705–726. Horizon Scientific Press.
Boddey R M, Urquiaga S, Alves B J R and Reis V 2003 Endophytic nitrogen fixation in sugarcane: present knowledge and future applications. Plant Soil 249, 375–385.
Burdman S, Jurkevitch E and Okon Y 2000 Recent advances in the use of Plant Growth Promoting Rhizobacteria (PGPR) in Agriculture. In Microbial Interactions in Agriculture and Forestry, Vol II. Eds. N Subba Rao and Y R Dommergues. Chapter 10, pp. 29–250. Science Publishers Inc., Plymouth, U.K.
Cocking E C 2000 Helping plants get more nitrogen from the air. European Review 8, 193–200.
Cocking E C, Webster G, Batchelor C A and Davey M R 1994 Nodulation of non-legume crops. A new look. Agro-Food-Industry Hi-Tech. Jan 21–24.
Conway G 1997 The Doubly Green Revolution: Food for All in the Twenty-First Century. Penguin Books Ltd.
Dobbelaere S, Croonenborghs A, Thys A, Vande Broek A, Vanderleyden J 1999 Phytostimulatory effect of Azospirillum brasilense wildtype and mutant strains altered in IAA production on wheat. Plant Soil 212, 155–164.
Döbereiner J, Baldani V L D, Olivares F and Reis V M 1993 Endophytic diazotrophs: The key to BNF in gramineous plants. In Nitrogen Fixation with Non-Legumes. Eds. N A Hegazi, M Fayez and M Monib. pp. 395–408. The American University in Cairo Press.
Gopalaswamy G, Kannaiyan S, O'Callaghan K J, Davey M R and Cocking EC 2000 The xylem of rice (Oryza sativa) is colonized by Azorhizobium caulinodans. Proceedings Royal Society (London) B, 267, 103–107.
Gough C and Dénarié J 2000 Exploring genetic programs for root endosymbioses. In The Quest for Nitrogen Fixation in Rice. Eds. J K Ladha and P M Reddy. pp. 311–326. International Rice Research Institute.
Gough C, Galera C, Vasse J, Webster G, Cocking E C and Dénarié J 1997 Specific flavonoids promote intercellular root colonization of Arabidopsis thaliana by Azorhizobium caulinodans ORS571. Mol. Plant-Microbe Interact. 10, 560–570.PubMed
Gualtieri G and Bisseling T 2000 The evolution of nodulation. Plant Mol. Biol. 42, 181–194.PubMed
James E K, Reis V M, Olivares F L, Baldini J I and Döbereiner J 1994 Infection of sugar cane by the nitrogen-fixing bacterium Acetobacter diazotrophicus. J. Exp. Bot. 45, 757–766.
James E K 2000 Nitrogen fixation in endophytic and associated symbiosis. Field Crops Res. 65, 197–209.
Kennedy I R and Cocking E C 1997 Biological Nitrogen Fixation: The Global Challenge & Future Needs. Position Paper, The Rockefeller Foundation Bellagio Conference Centre, Italy, 8–12 April 1997.
Lambrecht M, Okon Y, Vande Broek A, Vanderleyden J 2000 Indole-3-acetic acid: A reciprocal signalling molecule in bacteria-plant interactions. Trends Microbiol. 8, 298–300.PubMed
Lee S, Sevilla M, Meletzus D, Teixeira K, De Oliveira A, Perlova L, Nawroth R, Baldani I and Kennedy C 1998 Analysis of nitrogen fixation and regulatory genes in the sugar cane endophyte Acetobacter diazotrophicus. In Nitrogen Fixation with Non-Legumes. Eds. K A Malik, M S Mirza and J K Ladha. pp. 11–19. Kluwer Academic Publishers, Dordrecht.
Marschner H 1988 Mineral Nutrition of Higher Plants, Academic Press, New York.
Mateos P F, Baker D L, Perten M, Velàzquez E, Jiménez J I, Martinez-Molina E, Squartini A, Orgambide G, Hubbell D H, Dazzo F B 2001 Erosion of root epidermal cell walls by Rhizobium polysaccharide-degrading enzymes as related to primary host infection in the Rhizobium-legume symbiosis. Can. J. Microbiol. 47, 475–487.PubMed
Nuti M P 1996 Biosafety of Genetically Modified SoilMicrobial Inoculants. Report of Evergreen Laboratory without Walls (Bridge Programme). pp. 1–11.
O'Callaghan K, Davey M R and Cocking E C 1997 Xylem colonization of the legume Sesbania rostrata by Azorhizobium caulinodans. Proc. R. Soc. London: Biol. Sci. 264, 1821–1826.
O'Callaghan K, Dixon R A and Cocking E C 2001 Arabidopsis thaliana: A model for studies of the colonization by nonpathogenic and plant-growth-promoting rhizobacteria. Aust. J. Plant Physiol. 28, 975–982.
Okon Y 1985 Azospirillum as a potential inoculum for agriculture. Trends Biotechnol. 3, 223–228.
Paula M A, Reis V M and Döbereiner J 1991 Interactions of Glomus clarum with Acetobacter diazotrophicus in infection of sweet potato (Ipomoea batatas), sugar cane (Saccharum spp.), and sweet sorghum (Sorghum vulgare). Biol. Fertil. Soils. 11, 111–115.
Perret X, Staehelin C and Broughton W 2000 Molecular basis of symbiotic promiscuity. Microbiol. Mol. Biol. Rev. 64, 180–201.PubMed
Pueppke S G and Broughton W J 1999 Rhizobium sp. NGR234 and R. fredii USDA257 share exceptionally broad, nested host ranges. Mol. Plant-Microbe Interact. 12, 293–318.PubMed
Quispel A 1991 A critical evaluation of the prospects for nitrogen fixation with non-legumes. Plant Soil 137, 1–11.
Quispel A 1998 Evolutionary aspect of symbiotic adaptations. Rhizobium's contribution to evolution by Association. In The Rhizobiaceae. Eds. H P Spaink, A Kondorosi and P J J Hooykaas. pp. 487–507. Kluwer Academic Publishers, Dordrecht.
Reddy P M, Ladha J K, So R B, Hernandez R J, Ramos M C, Angeles O R, Dazzo F B, de Bruijn F J 1997 Rhizobial communication with rice roots: induction of phenotypic changes, mode of invasion and extent of colonization. Plant Soil 194, 81–98.
Reddy P M, Ladha J K, Kouchi H, Stacey G, Hernandez-Oane R J, Ramos M C, So R B, Angeles O R, Sreevidya V S, Day R B, Cohn J, Koh S 2000 Realizing the genetic predisposition of rice for symbiotic nitrogen fixation. In The Quest for Nitrogen Fixation in Rice. Eds. J K Ladha and P M Reddy. pp. 241–261. International Rice Research Institute.
Rolfe B G (and 13 others) 1998 Round Table: Agriculture 2020 8 billion people. In Current Plant Science and Biotechnology in Agriculture: Biological nitrogen fixation for the 21st Centrury. Eds C Elmerich, A Kondorosi and W E Newton. pp. 685–692. Kluwer Academic Publishers, Dordrecht.
Sabry R S, Saleh S A, Batchelor C A, Jones J, Jotham J, Webster G, Kothari S L, Davey M R and Cocking E C 1997 Endophytic establishment of Azorhizobium caulinodans in wheat. Proc. R. Soc. London: Biol. Sci. 264, 341–346.
Sprent J I and de Faria S M 1987 Mechanisms of infection of plants by nitrogen-fixing organisms. In Nitrogen Fixation with Nonlegumes. Eds. FA Skinner, R M Boddey and I Fendrik. pp. 3–11. Kluwer Academic Publishers, Dordrecht.
Stone P J, O'Callaghan K J, Davey M R and Cocking E C 2001 Azorhizobium caulinodans ORS571 colonizes the xylem of Arabidopsis caulinodans. Mol. Plant-Microbe Interact. 14, 93–97.PubMed
Swaminathan M S 1996 Sustainable Agriculture; Towards an Evergreen Revolution. Konark Publishers PVT Ltd, Delhi 10092, India.
Tchan Y T 1993 some aspects of non-rhizobial diazotrophs: their past and their future. In Microbiology in Action. Eds.W G Murrell and I R Kennedy. pp. 193–207. John Wiley and Sons, New York.
Trinick M J 1973 Symbioses between Rhizobium and the nonlegume, Trema aspera. Nature 244, 459–460.
Trinick M J and Hadobas P A 1988 Biology of the Parasponia–Bradyrhizobium symbiosis. Plant Soil 110, 177–185.
Webster G, Davey M R and Cocking E C 1995 Parasponia with rhizobia: a neglected non-legume nitrogen-fixing symbiosis. AgBiotech News Inform. 7, 119N–124N.
Webster G, Gough C, Vasse J, Batchelor C A, O'Callaghan K J, Kothari S L, Davey M R, Dénarié J and Cocking E C 1997 Interactions of rhizobia with rice and wheat. Plant Soil 194, 115–122.
Webster G, Jain V, Davey MR, Gough C, Vasse J, Dénarié J and Cocking EC 1998 The flavonoid naringenin stimulates the intercellular colonization of wheat roots by Azorhizobium caulinodans. Plant Cell Environ. 21, 373–383.
Yanni Y G, Rizk R Y, Abd. El-Fattah F K, Squartini A, Corich V, Giacomini A, de Bruijn F, Rademaker J, Maya-Flores J, Ostrom P, Vega-Hernandez M, Hollingsworth R I, Martinez-Molina E, Mateos P, Velazquez E, Wopereis J, Triplett E, Umali-Garcia M, Anarna J A, Rolfe B G, Ladha J K, Hill J, Mujoo R, Ng P K and Dazzo F B 2001 The beneficial plant growth-promoting association of Rhizobium leguminosarum bv. trifolii with rice roots. Aust. J. Plant Physiol. 28, 845–870.
- Endophytic colonization of plant roots by nitrogen-fixing bacteria
Plant and Soil
Volume 252, Issue 1 , pp 169-175
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- Kluwer Academic Publishers
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- Azorhizobium caulinodans
- biological nitrogen fixation
- endophytic colonization
- Gluconacetobacter diazotrophicus
- Industry Sectors
- Author Affiliations
- 1. Centre for Crop Nitrogen Fixation, University of Nottingham, Nottingham, NG7 2RD, U.K.