Abstract
Diversity in both legumes and rhizobia is discussed, in the light of evolution of nodulation. An hypothesis is developed that two separate nodulation events occurred in the humid tropics during the evolution of legumes in the late Cretaceous. One of these involved an ancestor of Rhizobium and a root infection. This was initially parasitic and provided little benefit until bacteria were released from infection threads as in modern crop species. The other involved a photosynthetic ancestor of Bradyrhizobium with a wound infection on stems, and has never involved infection threads. As continents moved and climates changed to a seasonal type, involving either rainfall or temperature extremes, further constraints were imposed. The argument is pursued for the case of acacias and their rhizobia in arid regions. Here selection pressures on rhizobia led to the evolution of stress tolerant forms, not all of which are capable of symbiosis, and where symbiotic genes may be an expensive encumbrance. Lateral transfer of material on megaplasmids led to a wide range of symbiotic and non-symbiotic forms in response to local pressures. When environmental constraints are superimposed on initial evolutionary developments, the result is an apparently chaotic situation where there is no obvious pattern of co-evolution between hosts and rhizobia. Evidence of such coevolution may still be buried in this chaos and may be amenable to molecular analysis.
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References
Allen O N and Allen E K 1981 The Leguminosae. University of Wisconsin Press, Madison. Macmillan Publishing Company, London. 812 p.
Anon 1980 Firewood crops. National Academy of Sciences, Washington D.C. 236 p.
Barnet Y and Catt P C 1991 Distribution and characteristics of root nodule bacteria isolated from Australian Acacia spp. Plant and Soil 135, 109–120.
Barnet Y, Catt P C, Jenzaniontham R and Mann K 1993 Fast growing root-nodule bacteria from Australian Acacia spp. In New Horizons in Nitrogen Fixation. Eds. R Palacios, J Mora and W E Newton. p 594. Kluwer Academic Publishers, Dordrecht.
Faria S M de, Hay G T and Sprent J I 1988 Entry of rhizobia into roots of Mimosa scabrella. Bentham occurs between epidermal cells. J. Gen. Microbiol. 134, 2291–2296.
Faria S M de, Lewis G P, Sprent J I and Sutherland J M 1989 Occurrence of nodulation in the Leguminosae. New Phytol. 111,607-619.
Faria S M de, McInroy S G and Sprent J I 1987 The occurrence of infected cells, with persistent infection threads, in legume root nodules. Can. J. Bot. 65, 553–558.
Faria S M de and Sprent J I 1994 Legume nodule development, an evolutionary hypothesis. In Advances in Legume Systematics 5. The Nitrogen Factor. Eds. J I Sprent and D McKey. Royal Botanic Gardens, Kew. (In press).
Goi S R, Sprent J I, James E K and Jacob-Neto J 1992 Influence of nitrogen form and concentration on the nitrogen fixation of Acacia auriculiformis. Symbiosis 14, 115–122.
Goi S R, 1993 Nitrogen nutrition of woody legumes. PhD thesis, University of Dundee. 199 p.
Graham P H 1992 Stress tolerance in Rhizobium and Bradyrhizobium and nodulation under adverse conditions. Can. J. Microbiol. 38, 475–484.
Herendeen P S and Dilcher D L (Eds.) 1992 Advances in Legume Systematics, part 4. The Fossil Record. Royal Botanic Gardens, Kew. 326 p.
Hungria M, Franco A A and Sprent J I 1993 New sources of high-temperature tolerant rhizobia for Phaseolus vulgaris. Plant and Soil 149, 103–109.
Irwin H S and Barneby R C 1982 The American Cassiinae: a synoptical revision of leguminosae tribe Cassiiae subtribe Cassiinae in the New World. Memoirs of the New York Botanic Garden 35, 1–454.
James E K, Shaw J E, Catellan A J, Faria S M de and Sprent J I 1993 The infection of aquatic and terrestrial Neptunia species by Rhizobium In New Horizons in Nitrogen Fixation. Eds R Palacios, J Mora and W E Newton. p 351. Kluwer Academic Publishers, Dordrecht.
James E K, Sprent J I, Sutherland J M, McInroy S G and Minchin F R 1992 The stucture of nitrogen fixing roote nodules on the aquatic mimisoid legume Neptunia plena. Ann. Bot. 69, 173–180.
Kuykendall L D 1989 Influence of Glycine max nodulation on the persistence in soil of a genetically marked Bradyrhi zobium japonicum strain. Plant and Soil 116, 275–277.
Kuykendall L D, Devine T E and Cregan P B 1982 Positive role of nodulation in the establishment of Rhizobium japonicum in subsequent crops of soybean. Current Microbiol. 7, 79–91.
Lewis G P 1987 Legumes of Bahia. Royal Botanic Gardens, Kew. 369 p.
Moreira F M de Souza, de Silva M F and Faria S M de 1992 Occurrence of nodulation in legume species in the Amazon region of Brazil. New Phytol. 121, 563–570.
Moreira F and Franco A A 1993 Rhizobia-host interactions in tropical ecosystems in Brazil. In Advances in Legume Systematics 5, the Nitrogen Factor. Eds. J I Sprent and D McKey. Royal Botanic Gardens, Kew. (In press).
Naisbitt T, James E K and Sprent J I 1992 The evolutionary significance of the legume genus Chamaecrista ,as determined by nodule structure. New Phytol, 122, 487–492.
Norris D P 1965 Rhizobium relationships in legumes. Proc. 9th Int. Grassl. Congr. Sao Paulo 2, 1087–1092.
Odee D W 1993 The ecology of nitrogen-fixing symbioses under arid conditions of Kenya. PhD thesis, University of Dundee. 145 p.
Odee D W and Sprent J I 1992 Acacia brevispica: a nonnodulated mimosoid legume? Soil Biol. Biochem. 24, 717–719.
Oram R N 1990 Register of Australian Herbage Plant Cultivars, CSIRO Publications, Parchment Press, Melbourne.
Owens S J and Lewis G P 1989 Taxonomic and functional implications of stigma morphology in species of Cassia, Chamaecrista and Senna (Leguminosae: Caesalpinioideae). Pl. Syst. Evol. 163, 93–105.
Parker C A 1957 Evolution of nitrogen-fixing symbiosis in higher plants. Nature 179, 593–4.
Parsons R, Raven J A and Sprent J I 1992 A simple open flow system used to measure acetylene reduction activity of Sesbania rostrata stem and root nodules. J. Exp. Bot. 43, 595–604.
Parsons R, Sprent JI and Raven J A 1993 Humidity and light affect the growth, development and nitrogenase activity of stem nodule of Sesbania rostrata Brem. New Phytol. 125, 749–755.
Peters N K, Frost J W and Long S R 1986 A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233, 977–980.
Polhill R M 1981 Dalbergieae. In Advances in Legume Systematics. Eds. R M Polhill and P H Raven. pp 233–242. Royal Botanic Gardens, Kew.
Polhill R M and Raven P H (Eds.) 1981 Advances in Legume Systematics, Part 1. Royal Botanic Gardens, Kew. 425 p.
Postgate J 1992 Bacterial evolution and the nitrogen-fixing plant. Phil. Trans. Roy. Soc. London B, 338, 409–416.
Raven J A and Sprent J I 1989 Phototrophy, diazotrophy and palaeoatmospheres: biological catalysts and the H, C, N and O cycles. J. Geol. Soc. 146, 161–170.
Richardson A E, Simpson R J, Djordjevic M A and Rolfe B G 1988 Expression of nodulation genes in Rhizobium leguminosarum bv trifolii is affected by low pH, Ca and Al. Appl. Environ. Microbiol. 54, 2541–2548.
Smith L T, Allaith A A and Smith G M 1994 Mechanism of osmotically regulated N-acetylglutaminylglutamine amide production in Rhizobium meliloti. Plant and Soil 161, 103–108.
Sprent J I 1989 Which steps are essential for the formation of functional legume nodules? New Phytol. 111, 129–153.
Sprent J I, Minchin F R and Parsons R 1993 Evolution since Knoxville: were rhizobia wise to inhabit land plants? In New Horizons in Nitrogen Fixation. Eds. R. Palacios, J Mora and W E Newton. pp 65–76. Kluwer Academic Publishers, Dordrecht.
Sprent J I and Raven J A 1992 Evolution of nitrogen fixing symbioses. In Biological Nitrogen Fixation. Eds. G Stacey, R H Burns and H J Evans. pp 461–496. Chapman and Hall, NY.
Sprent J I and Sprent P 1990 Nitrogen Fixing Organisms: pure and applied aspects, 256 p. Chapman and Hall, London.
Sprent J I, Sutherland J M and Faria S M de 1989 Structure and function of root nodules from woody legumes. In Advances in Legume Biology. Ed. C H Stirton and J L Zarucchi. Monogr. Syst. Bot. Missouri Bot. Gard. 29, 559–578.
Stewart I 1989 Does God Play Dice? Penguin Books, London. 317 p.
Stouthamer A H 1992 Metabolic pathways in Paracoccus denitrificans and closely related bacteria in relation to the phylogeny of prokaryotes. Antonie van Leeuwenhoek 61, 1–33.
Stouthamer A H and Kooijman S A L M 1993 Why it pays for bacteria to delete disused DNA and to maintain megaplasmids. Antonie van Leeuwenhoek 63, 39–43.
Sun J S, Sands R and Simpson R J 1992 Genotypic variaton in growth and nodulation by seedlings of Acacia species. For. Ecol. Manage. 55, 209–223.
Trinick M J 1982 Biology. In Nitrogen Fixation. Eds. W J Broughton. pp 76–146. Oxford, Clarendon Press.
Young J P W 1985 Rhizobium population genetics: enzyme polymorphism in isolates from peas, clover, beans and lucerne grown at the same site. J. Gen. Microbiol. 1331, 2399–2408.
Young J P W 1993 Molecular phylogeny of rhizobia and their relatives. In New Horizons in Nitrogen Fixation. Eds. R Palacios, J Mora and W E Newton. pp 587–592. Kluwer Academic Publishers, Dordrecht.
Young J P W and Johnston A W B 1989 The evolution of specificity in the legume-rhizobium symbiosis. Trends Ecol. Evol. 4, 341–349.
Zhang X, Harper R, Karsish M and Lindström K 1991 Diversity of Rhizobium bacteria isolated from root nodules of Leguminous trees. Inter. J. Syst. Bacteriol. 41, 104–113.
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Sprent, J.I. (1994). Evolution and diversity in the legume-rhizobium symbiosis: chaos theory?. In: Graham, P.H., Sadowsky, M.J., Vance, C.P. (eds) Symbiotic Nitrogen Fixation. Developments in Plant and Soil Sciences, vol 57. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-1088-4_1
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DOI: https://doi.org/10.1007/978-94-011-1088-4_1
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