Evidence of selection for effective nodulation in the Trifolium spp. symbiosis with Rhizobium leguminosarum biovar trifolii
R. J. Yates A B D , J. G. Howieson A B , D. Real A C , W. G. Reeve A , A. Vivas-Marfisi A B and G. W. O’Hara AA Centre for Rhizobium Studies, Murdoch University, South Street, WA 6150, Australia.
B Department of Agriculture Western Australia, 3 Baron-Hay Court, South Perth, WA 6151, Australia.
C National Agricultural Research Institute, INIA, Ruta 5 km 386, Tacuarembó, Uruguay.
D Corresponding author. Email: ryates@agric.wa.gov.au
Australian Journal of Experimental Agriculture 45(3) 189-198 https://doi.org/10.1071/EA03168
Submitted: 8 August 2003 Accepted: 17 June 2004 Published: 14 April 2005
Abstract
The pasture-breeding program to improve production in the natural grasslands in Uruguay has acknowledged that indigenous Rhizobium strains are incompatible with introduced Mediterranean clovers. In an attempt to understand and overcome this problem, a cross-row experiment was set up in 1999 in a basaltic, acid soil in Glencoe, Uruguay, to follow the survival and performance of 9 exotic strains of Rhizobium leguminosarum bv. trifolii. This paper reports on the ability of the introduced strains to compete for nodule occupancy of Mediterranean clover hosts and impacts of the introduced strains on the productivity of the indigenous Uruguayan clover Trifolium polymorphum. Strain WSM1325 was a superior inoculant and remained highly persistent and competitive for the effective symbiosis with the Mediterranean hosts, T. purpureum and T. repens, in the Uruguayan environment in the third year of the experiment. The Mediterranean hosts (T. purpureum and T. repens) nodulated with the introduced strains but did not nodulate with any indigenous R. leguminosarum bv. trifolii typed from nodules of T. polymorphum. Conversely, there were no nodules on the Uruguayan host T. polymorphum that contained introduced R. leguminosarum bv. trifolii. These results reveal the establishment of effective symbioses between strains of R. leguminosarum bv. trifolii and clover even though the soil contained ineffective R. leguminosarum bv. trifolii for all hosts. We believe our results are the first reported example of ‘selective’ nodulation for an effective symbiosis in situ with annual and perennial clovers in acid soils.
Acknowledgments
The authors gratefully acknowledge the support from the Grains Research and Development Corporation (GRDC) and Instituto Nacional de Investigación Agropecuaria (INIA) Uruguay. We also thank Regina Carr and Julie Ardley for technical assistance.
Ballard RA, Charman N
(2000) Nodulation and growth of pasture legumes with naturalised soil rhizobia. 1. Annual Medicago spp. Australian Journal of Experimental Agriculture 40, 939–948.
| Crossref | GoogleScholarGoogle Scholar |
Brockwell J
(2001) Sinorhizobium meliloti in Australian soils: population studies of the root-nodule bacteria for species of Medicago in soils of the Eyre Peninsula, South Australia. Australian Journal of Experimental Agriculture 41, 753–762.
| Crossref | GoogleScholarGoogle Scholar |
Brockwell J, Bottomley PJ
(1995) Recent advances in inoculant technology and prospects for the future. Soil Biology and Biochemistry 27, 683–697.
| Crossref | GoogleScholarGoogle Scholar |
Brockwell J,
Bottomley PJ, Thies JE
(1995) Manipulation of rhizobia microflora for improving legume productivity and soil fertility: a critical assessment. Plant and Soil 174, 143–180.
| Crossref | GoogleScholarGoogle Scholar |
Charman N, Ballard RA
(2004) Burr medic (Medicago polymorpha L.) selections for improved N2 fixation with naturalised soil rhizobia. Soil Biology and Biochemistry 36, 1331–1337.
| Crossref |
Cocks PS
(2001) Ecology of herbaceous perennial legumes: a review of characteristics that may provide management options for the control of salinity and waterlogging in dryland cropping systems. Australian Journal of Agricultural Research 52, 137–151.
| Crossref | GoogleScholarGoogle Scholar |
Cransberg L, MacFarlane DJ
(1994) Can perennial pastures provide the basis for a sustainable farming system in southern Australia? New Zealand Journal of Agricultural Research 37, 287–294.
Crawford MC, MacFarlane MR
(1995) Lucerne reduces soil moisture and increases livestock production in an area of high ground water recharge potential. Australian Journal of Experimental Agriculture 35, 171–180.
| Crossref |
Dakora FD
(2003) Defining new roles for plant and rhizobial molecules in sole and mixed plant cultures involving symbiotic legumes. The New Phytologist 158, 39–49.
| Crossref |
Denton MD,
Coventry DR,
Bellotti WD, Howieson JG
(2000) Distribution, abundance and effectiveness of Rhizobium leguminosarum bv. trifolii from alkaline pasture soils in South Australia. Australian Journal of Experimental Agriculture 40, 25–35.
| Crossref | GoogleScholarGoogle Scholar |
Denton MD,
Coventry DR,
Howieson JG,
Murphy PJ, Bellotti WD
(2002) Competition between inoculated and naturalized R. leguminosarum bv. trifolii for nodulation of annual clovers in alkaline soils. Australian Journal of Agricultural Research 53, 1019–1026.
| Crossref | GoogleScholarGoogle Scholar |
Dowling DN, Broughton WJ
(1986) Competition for nodulation of legumes. Annual Review of Microbiology 40, 131–157.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Graham PH, Vance CP
(2000) Nitrogen fixation in perspective: an overview of research and extension needs. Field Crops Research 65, 93–106.
| Crossref | GoogleScholarGoogle Scholar |
Hebb DM,
Richardson AE,
Reid R, Brockwell J
(1998) PCR as an ecological tool to determine the establishment and persistence of Rhizobium strains introduced into the field as seed inoculant. Australian Journal of Agricultural Research 49, 923–934.
| Crossref | GoogleScholarGoogle Scholar |
Hogg B,
Davies AE,
Wilson KE,
Bisseling T, Downie JA
(2002) Competitive nodulation blocking of cv. Afghanistan pea is related to high levels of nodulation factors made by some strains of Rhizobium leguminosarum bv. viciae. Molecular Plant–Microbe Interactions 15, 60–68.
| PubMed |
Howieson JG, Ballard RA
(2004) Optimising the legume symbiosis in stressful and competitive environments within southern Australia — some contemporary thoughts. Soil Biology and Biochemistry 36, 1261–1273.
| Crossref |
Howieson JG, Ewing MA
(1986) Acid tolerance in the Rhizobium meliloti–Medicago symbiosis. Australian Journal of Agricultural Research 36, 55–64.
| Crossref | GoogleScholarGoogle Scholar |
Howieson JG,
Ewing MA, D’Antuono MF
(1988) Selection for acid tolerance in Rhizobium meliloti. Plant and Soil 105, 179–188.
Howieson JG,
Malden J,
Yates RJ, O’Hara GW
(2000b) Techniques for the selection and development of elite inoculant rhizobial strains in southern Australia. Symbiosis 28, 33–48.
Howieson JG,
Loi A, Carr SJ
(1995) Biserrula pelecinus L. — a legume pasture species with potential for acid, duplex soils which is nodulated by a unique root-nodule bacteria. Australian Journal of Agricultural Research 46, 997–1009.
| Crossref | GoogleScholarGoogle Scholar |
Howieson JG,
O’Hara GW, Carr SJ
(2000a) Changing roles for legumes in Mediterranean agriculture: developments from an Australian perspective. Field Crops Research 65, 107–122.
| Crossref | GoogleScholarGoogle Scholar |
Howieson JG,
Yates RJ,
O’Hara GW,
Ryder M, Real D
(2005) The interactions of Rhizobium leguminosarum biovar trifolii in nodulation of annual and perennial Trifolium spp. from diverse centres of origin. Australian Journal of Experimental Agriculture 45, 199–207.
Jones DG, Hardarson G
(1979) Variation within and between white clover varieties in their preference for strains of Rhizobium trifolii. Annals of Applied Biology 92, 221–228.
Labandera CA, Vincent JM
(1975) Competition between an introduced strain and native Uruguayan strains of Rhizobium trifolii. Plant and Soil 42, 327–347.
Laguerre G,
Mavingui P,
Allard MR,
Charnay M,
Louvrier P,
Mazurier S,
Rigottter-Gois L, Amarger N
(1996) Typing of rhizobia by PCR DNA fingerprinting and PCR-restriction fragment length polymorphism analysis of chromosomal and symbiotic gene regions: application to Rhizobium leguminosarum and its different biovars. Applied and Environmental Microbiology 62, 2029–2036.
| PubMed |
Latta RA,
Blacklow LJ, Cocks PS
(2001) Comparative soil water, pasture production, and crop yields in phase farming systems with lucerne and annual pasture in western Australia. Australian Journal of Agricultural Research 52, 295–303.
| Crossref | GoogleScholarGoogle Scholar |
Lefroy EC,
Pate JS, Stirzaker RJ
(2001) Growth, water use efficiency, and adaptive features of the tree legume tagasaste (Chamaecytisus proliferus Link.) on deep sands in south-western Australia. Australian Journal of Agricultural Research 52, 221–234.
| Crossref | GoogleScholarGoogle Scholar |
Lewis-Henderson WR, Djordjevic MA
(1991) A cultivar-specific interaction between Rhizobium leguminosarum bv. trifolii and subterranean clover is controlled by nodM, other bacterial cultivar specificity genes, and a single recessive host gene. Journal of Bacteriology 173, 2791–2799.
| PubMed |
Loi A,
Howieson JG,
Nutt BJ, Carr SJ
(2005) A second generation of annual pasture legumes and their potential for inclusion in Mediterranean-type farming systems. Australian Journal of Experimental Agriculture 45, 289–299.
Mpepereki S,
Javaheri F,
Davis P, Giller KE
(2000) Soyabeans and sustainable agriculture. Promiscuous soybeans in southern Africa. Field Crops Research 65, 137–149.
| Crossref | GoogleScholarGoogle Scholar |
Phillips DA,
Joseph CM,
Yang GP,
Martinez-Romero E,
Sanborn JR, Volpin H
(1999) Identification of lumichrome as a Sinorhizobium enhancer of alfalfa root respiration and shoot growth. Proceedings of the National Academy of Sciences of the United States of America 96, 12275–12280.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pryor HN,
Lowther WL,
McIntyre HJ, Ronson CW
(1998) An inoculant Rhizobium strain for improved establishment and growth of hexaploid Caucasian clover (Trifolium ambiguum). New Zealand Journal of Agricultural Research 41, 179–189.
Real D,
Labandera CA, Howieson JG
(2005) Performance of temperate and subtropical forage legumes for over-seeding native pastures in the basaltic region of Uruguay. Australian Journal of Experimental Agriculture 45, 279–287.
Richardson AE,
Viccars LA,
Watson JM, Gibson AH
(1995) Differentiation of Rhizobium strains using the polymerase chain reaction with random and directed primers. Soil Biology and Biochemistry 27, 515–524.
| Crossref | GoogleScholarGoogle Scholar |
Robinson AC
(1969a) Competition between effective and ineffective strains of Rhizobium trifolii in the nodulation of Trifolium subterraneum. Australian Journal of Agricultural Research 20, 827–841.
| Crossref | GoogleScholarGoogle Scholar |
Robinson AC
(1969b) Host selection for effective Rhizobium trifolii by red clover and subterranean clover in the field. Australian Journal of Agricultural Research 20, 1053–1060.
| Crossref | GoogleScholarGoogle Scholar |
Roughley RJ,
Blowes WM, Herridge DF
(1976) Nodulation of Trifolium subterraneum by introduced rhizobia in competition with naturalized strains. Soil Biology and Biochemistry 8, 403–407.
| Crossref | GoogleScholarGoogle Scholar |
Sessitsch A,
Howieson JG,
Perret X,
Antoun H, Martínez-Romero E
(2002) Advances in Rhizobium research. Critical Reviews in Plant Sciences 21, 323–378.
Slattery JF, Coventry DR
(1999) Persistence of introduced strains of Rhizobium leguminosarum bv. trifolii in acidic soils of north-eastern Victoria. Australian Journal of Experimental Agriculture 39, 829–837.
| Crossref | GoogleScholarGoogle Scholar |
Slattery JF,
Coventry DR, Slattery WJ
(2001) Rhizobial ecology as affected by the soil environment. Australian Journal of Experimental Agriculture 41, 289–298.
| Crossref | GoogleScholarGoogle Scholar |
Streeter JG
(1994) Failure of inoculant rhizobia to overcome the dominance of indigenous strains for nodule formation. Canadian Journal of Microbiology 40, 513–522.
Thies JE,
Singleton PW, Bohlool BB
(1991) Modeling symbiotic performance of introduced rhizobia in the field by use of indices of indigenous population size and nitrogen status of the soil. Applied and Environmental Microbiology 57, 29–37.
Triplett EW, Sadowsky MJ
(1992) Genetics of competition for nodulation of legumes. Annual Review of Microbiology 46, 399–428.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Versalovic J,
Koeuth T, Lupski JR
(1991) Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Research 19, 6823–6831.
| PubMed |
Versalovic J,
Schneider M,
de Bruijn FJ, Lupski JR
(1994) Genomic fingerprinting of bacteria using repetitive sequence/based polymerase chain reaction. Methods in Molecular and Cellular Biology 5, 25–40.
Vlassak KM, Vanderleyden J
(1997) Factors influencing nodule occupancy by inoculant rhizobia. Critical Reviews in Plant Sciences 16, 163–229.
Yates RJ,
Nandasena KG,
O’Hara GW, Howieson JG
(2004) Root-nodule bacteria from indigenous legumes in the north-west of Western Australia and their interaction with exotic legumes. Soil Biology and Biochemistry 36, 1319–1329.
| Crossref |
Zahran IH
(1999) Rhizobium–legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiology and Molecular Biology Reviews 63, 968–989.
| PubMed |
