Increased lucerne nodulation in acid soils with Sinorhizobium meliloti and lucerne tolerant to low pH and high aluminium
Kathryn Wigley
A D , Hayley J. Ridgway B , Alan W. Humphries C , Ross A. Ballard C and Derrick J. Moot A
+ Author Affiliations
- Author Affiliations
A Faculty of Agriculture and Life Sciences, Lincoln University, PO Box 85084, Lincoln 7647, Canterbury, New Zealand.
B Plant & Food Research, Canterbury Agriculture & Science Centre, Gerald Street, Lincoln 7608, Canterbury, New Zealand.
C South Australian Research and Development Institute, Box 397, Adelaide, SA 5001, Australia.
D Corresponding author. Email: kathryn.wigley@gmail.com
Crop and Pasture Science 69(10) 1031-1040 https://doi.org/10.1071/CP18124
Submitted: 29 March 2018 Accepted: 17 August 2018 Published: 19 September 2018
Abstract
Acidic conditions with damaging levels of available aluminium (Al3+) currently limit lucerne (Medicago sativa) production on soils in the New Zealand high country and in large areas of Australia. Increased lucerne nodulation could be achieved by using an Al3+-tolerant strain of Sinorhizobium meliloti to inoculate an Al3+-tolerant lucerne line. The Al3+ tolerance of the current commercial Australasian inoculant strain for lucerne, S. meliloti RRI128, was compared with strain SRDI736, selected in Australia for tolerance to low pH. Four Al3+ levels (0, 2, 4 and 8 µm) were created at pH 5.1 in a hydroponic system. The rhizobial strains were evaluated on SARDI AT7, a lucerne line selected for improved growth and nodulation in acidic solution culture with Al3+, and on Stamina 5, a commercial cultivar commonly grown in Australasia. SARDI AT7 when inoculated with strain SRDI736 produced more nodules per plant (3.6 vs 2.4) and had higher nodulation percentage (>80% vs <50%) at all Al3+ levels than when inoculated with RRI128. The percentage of nodulated Stamina 5 plants after inoculation with the commercial strain was lower than after inoculation with strain SRDI736 (10–16% vs 25–70%) at all Al3+ levels.
The potential of S. meliloti strains SRDI736, SRDI672 and RRI128 and rates of lime to increase lucerne nodulation and dry matter production in soils of low pH (<5.5, in water) and high Al3+ (>3 mg kg–1 soil) was also investigated in a pot trial. Lime had a more consistent effect than inoculant strain for increasing nodulation. At 0.5 and 2 t lime ha–1, plants inoculated with strains SRDI672 and SRDI736 had more nodules per plant than plants inoculated with the commercial strain. At 4 t lime ha–1, the number of nodules per plant was highest for all three inoculants, and there were no differences among them. This confirms the importance of lime to increase lucerne nodulation in low-pH, high-Al3+ soils. However, where liming is uneconomic or impractical, the results show that it was possible to select rhizobial strains to increase lucerne nodulation in acidic soils with damaging levels of available Al3+.
Additional keywords: alfalfa, Rhizobia.
References
Ballard RA, Slattery JF, Charman N (2005) Host range and saprophytic competence of Sinorhizobium meliloti—a comparison of strains for the inoculation of lucerne, strand and disc medics. Australian Journal of Experimental Agriculture 45, 209–216.| Host range and saprophytic competence of Sinorhizobium meliloti—a comparison of strains for the inoculation of lucerne, strand and disc medics.Crossref | GoogleScholarGoogle Scholar |
Berenji S (2015) Constraints and opportunities for lucerne (Medicago sativa L.), Caucasian clover (Trifolium ambiguum M. Bieb), and Russell lupin (Lupinus polyphyllus L.) in the high country of New Zealand. PhD Thesis, Lincoln University, New Zealand.
Berenji S, Moot DJ, Moir JL, Ridgway HJ (2015) Lucerne dry matter and N-fixation, when sown with or without lime and inoculant. Journal of New Zealand Grasslands 77, 109–116.
Berenji S, Moot DJ, Moir JL, Ridgway HJ, Rafat A (2017) Dry matter yield, root traits, and nodule occupancy of lucerne and Caucasian clover when grown in acidic soil with high aluminium concentrations. Plant and Soil 416, 227–241.
| Dry matter yield, root traits, and nodule occupancy of lucerne and Caucasian clover when grown in acidic soil with high aluminium concentrations.Crossref | GoogleScholarGoogle Scholar |
Bouton JH (1996) Screening the alfalfa core collection for acid soil tolerance. Crop Science 36, 198–200.
| Screening the alfalfa core collection for acid soil tolerance.Crossref | GoogleScholarGoogle Scholar |
Bouton JH (2001) ‘Alfalfa.’ (FEALQ: Piracicaba, São Pedro, SP, Brazil)
Bouton JH, Sumner ME (1983) Alfalfa, Medicago sativa L., in highly weathered, acid soils. V. Field performance of alfalfa selected for acid tolerance. Plant and Soil 74, 431–436.
| Alfalfa, Medicago sativa L., in highly weathered, acid soils. V. Field performance of alfalfa selected for acid tolerance.Crossref | GoogleScholarGoogle Scholar |
Brockwell J, Pilka A, Holliday RA (1991) Soil pH is a major determinant of the numbers of naturally occurring Rhizobium meliloti in non-cultivated soils in central New South Wales. Australian Journal of Experimental Agriculture 31, 211–219.
| Soil pH is a major determinant of the numbers of naturally occurring Rhizobium meliloti in non-cultivated soils in central New South Wales.Crossref | GoogleScholarGoogle Scholar |
Brooks CO, Bouton JH, Sumner ME (1982) Alfalfa, Medicago sativa L., in highly weathered, acid soils. III. The effects of seedling selection in an acid soil on alfalfa growth at varying levels of phosphorus and lime. Plant and Soil 65, 27–33.
| Alfalfa, Medicago sativa L., in highly weathered, acid soils. III. The effects of seedling selection in an acid soil on alfalfa growth at varying levels of phosphorus and lime.Crossref | GoogleScholarGoogle Scholar |
Bullard GK, Roughley RJ, Pulsford DJ (2005) The legume inoculant industry and inoculant quality control in Australia: 1953–2003. Australian Journal of Experimental Agriculture 45, 127–140.
| The legume inoculant industry and inoculant quality control in Australia: 1953–2003.Crossref | GoogleScholarGoogle Scholar |
Campbell TA, Elgin J, Foy CD, McMurtrey J (1988) Selection in alfalfa for tolerance to toxic levels of aluminum. Canadian Journal of Plant Science 68, 743–753.
| Selection in alfalfa for tolerance to toxic levels of aluminum.Crossref | GoogleScholarGoogle Scholar |
Casida LE (1982) Ensifer adhaerens gen. nov., sp. nov.: a bacterial predator of bacteria in soil. International Journal of Systematic and Evolutionary Microbiology 32, 339–345.
Charman N, Ballard RA, Humphries AW, Auricht GC (2008) Improving lucerne nodulation at low pH: contribution of rhizobial and plant genotype to the nodulation of lucerne seedlings growing in solution culture at pH 5. Australian Journal of Experimental Agriculture 48, 512–517.
| Improving lucerne nodulation at low pH: contribution of rhizobial and plant genotype to the nodulation of lucerne seedlings growing in solution culture at pH 5.Crossref | GoogleScholarGoogle Scholar |
Chen WX, Yan GH, Li JL (1988) Numerical taxonomic study of fast-growing soybean rhizobia and a proposal that Rhizobium fredii be assigned to Sinorhizobium gen. nov. International Journal of Systematic and Evolutionary Microbiology 38, 392–397.
Dall’Agnol M, Bouton JH, Parrott WA (1996) Screening methods to develop alfalfa germplasms tolerant of acid, aluminum toxic soils. Crop Science 36, 64–70.
| Screening methods to develop alfalfa germplasms tolerant of acid, aluminum toxic soils.Crossref | GoogleScholarGoogle Scholar |
Dear BS, Moore GA, Hughes SJ (2003) Adaptation and potential contribution of temperate perennial legumes to the southern Australian wheatbelt: a review. Australian Journal of Experimental Agriculture 43, 1–18.
| Adaptation and potential contribution of temperate perennial legumes to the southern Australian wheatbelt: a review.Crossref | GoogleScholarGoogle Scholar |
Delhaize E, Ryan PR (1995) Aluminum toxicity and tolerance in plants. Plant Physiology 107, 315–321.
| Aluminum toxicity and tolerance in plants.Crossref | GoogleScholarGoogle Scholar |
Devine TE, Foy CD, Fleming AL, Hanson CH, Campbell TA, McMurtrey JE, Schwartz JW (1976) Development of alfalfa strains with differential tolerance to aluminum toxicity. Plant and Soil 44, 73–79.
| Development of alfalfa strains with differential tolerance to aluminum toxicity.Crossref | GoogleScholarGoogle Scholar |
Edmeades DC, Blamey FPC, Asher CJ, Edwards DG (1991) Effects of pH and aluminium on the growth of temperate pasture species. II. Growth and nodulation of legumes. Australian Journal of Agricultural Research 42, 893–900.
| Effects of pH and aluminium on the growth of temperate pasture species. II. Growth and nodulation of legumes.Crossref | GoogleScholarGoogle Scholar |
Ghahramani A, Moore AD (2013) Climate change and broadacre livestock production across southern Australia. 2. Adaptation options via grassland management. Crop & Pasture Science 64, 615–630.
| Climate change and broadacre livestock production across southern Australia. 2. Adaptation options via grassland management.Crossref | GoogleScholarGoogle Scholar |
Hartel PG, Bouton JH (1991) Rhizobium meliloti inoculation of alfalfa selected for tolerance to acid, aluminium-rich soils. In ‘Plant–soil interactions at low pH’. (Eds RJ Wright, VC Baligar, RP Murrmann) pp. 597–601. (Springer: Netherlands)
Hayes RC, Scott BJ, Dear BS, Li GD, Auricht GCl (2011) Seedling validation of acid soil tolerance of lucerne populations selected in solution culture high in aluminium. Crop & Pasture Science 62, 803–811.
| Seedling validation of acid soil tolerance of lucerne populations selected in solution culture high in aluminium.Crossref | GoogleScholarGoogle Scholar |
Hayes RC, Li GD, Conyers MK, Virgona JM, Dear BS (2016) Lime increases productivity and the capacity of lucerne (Medicago sativa L.) and phalaris (Phalaris aquatica L.) to utilise stored soil water on an acidic soil in south-eastern Australia. Plant and Soil 400, 29–43.
| Lime increases productivity and the capacity of lucerne (Medicago sativa L.) and phalaris (Phalaris aquatica L.) to utilise stored soil water on an acidic soil in south-eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Horsnell LJ (1985) The growth of improved pastures on acid soils. 2. The effect of soil incorporation of lime and phosphorus on the growth of subterranean clover and lucerne pastures and on their response to topdressing. Australian Journal of Experimental Agriculture 25, 157–163.
| The growth of improved pastures on acid soils. 2. The effect of soil incorporation of lime and phosphorus on the growth of subterranean clover and lucerne pastures and on their response to topdressing.Crossref | GoogleScholarGoogle Scholar |
Howieson JG, Ewing MA (1986) Acid tolerance in the Rhizobium meliloti–medicago symbiosis. Australian Journal of Agricultural Research 37, 55–64.
| Acid tolerance in the Rhizobium meliloti–medicago symbiosis.Crossref | GoogleScholarGoogle Scholar |
Howieson JG, Ewing MA (1989) Annual species of Medicago differ greatly in their ability to nodulate on acid soils. Australian Journal of Agricultural Research 40, 843–850.
| Annual species of Medicago differ greatly in their ability to nodulate on acid soils.Crossref | GoogleScholarGoogle Scholar |
Howieson JG, Robson AD, Ewing MA (1993) External phosphate and calcium concentrations, and pH, but not the products of rhizobial nodulation genes, affect the attachment of Rhizobium meliloti to roots of annual medics. Soil Biology & Biochemistry 25, 567–573.
| External phosphate and calcium concentrations, and pH, but not the products of rhizobial nodulation genes, affect the attachment of Rhizobium meliloti to roots of annual medics.Crossref | GoogleScholarGoogle Scholar |
Humphries AW (2015) SARDI acid tolerant lucerne, AT7. Plant Varieties Journal 28, 63
Humphries AW, Ballard RA, Charman N, Venkatanagappa S, Denton MD, Marshall E, Hayes RC, Auricht GC (2009) Developing lucerne and rhizobia with improved tolerance to acidic soils: A novel approach. In ‘Proceedings 14th Australasian Plant Breeding Conference and 11th Society for the Advancement of Plant Breeding in Asia and Oceania (SABRAO) Congress’. Cairns, Qld. (Horticulture Australia: Sydney)
JCICSP (2008) The genus name Sinorhizobium Chen et al. 1988 is a later synonym of Ensifer Casida 1982 and is not conserved over the latter genus name, and the species name ‘Sinorhizobium adhaerens’ is not validly published. Opinion 84. International Journal of Systematic and Evolutionary Microbiology 58, 1973
| The genus name Sinorhizobium Chen et al. 1988 is a later synonym of Ensifer Casida 1982 and is not conserved over the latter genus name, and the species name ‘Sinorhizobium adhaerens’ is not validly published. Opinion 84.Crossref | GoogleScholarGoogle Scholar |
Keyser HH, Munns DN (1979) Tolerance of rhizobia to acidity, aluminum, and phosphate. Soil Science Society of America Journal 43, 519–523.
| Tolerance of rhizobia to acidity, aluminum, and phosphate.Crossref | GoogleScholarGoogle Scholar |
Khu DM, Reyno R, Brummer EC, Monteros MJ (2012) Screening methods for aluminum tolerance in alfalfa. Crop Science 52, 161–167.
| Screening methods for aluminum tolerance in alfalfa.Crossref | GoogleScholarGoogle Scholar |
Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annual Review of Plant Biology 46, 237–260.
| Cellular mechanisms of aluminum toxicity and resistance in plants.Crossref | GoogleScholarGoogle Scholar |
Latta RA, Cocks PS, Matthews C (2002) Lucerne pastures to sustain agricultural production in southwestern Australia. Agricultural Water Management 53, 99–109.
| Lucerne pastures to sustain agricultural production in southwestern Australia.Crossref | GoogleScholarGoogle Scholar |
Maxwell TMR, Moir JL, Edwards GR (2012) Sulphur and lime response of four adventive annual clovers grown in a New Zealand high country soil under glasshouse conditions. New Zealand Journal of Agricultural Research 55, 47–62.
| Sulphur and lime response of four adventive annual clovers grown in a New Zealand high country soil under glasshouse conditions.Crossref | GoogleScholarGoogle Scholar |
McLaren RG, Cameron KC (1996) ‘Soil science: sustainable production and environmental protection.’ (Oxford University Press: Melbourne)
Moir JL, Jordan P, Moot DJ, Lucas D (2016) Phosphorus response and optimum pH ranges of twelve pasture legumes grown in an acid upland New Zealand soil under glasshouse conditions. Journal of Soil Science and Plant Nutrition 16, 438–460.
Moot DJ, Brown HE, Pollock K, Mills A (2008) Yield and water use of temperate pastures in summer dry environments. Proceedings of the New Zealand Grassland Association 70, 51–57.
Mugwira LM, Haque I (1993) Screening forage and browse legumes germplasm to nutrient stress I: tolerance of Medicago sativa L. to aluminum and low phosphorus in soils and nutrient solutions. Journal of Plant Nutrition 16, 17–35.
| Screening forage and browse legumes germplasm to nutrient stress I: tolerance of Medicago sativa L. to aluminum and low phosphorus in soils and nutrient solutions.Crossref | GoogleScholarGoogle Scholar |
Mullen CL, Scott BJ, Evans CM, Conyers MK (2006) Effect of soil acidity and liming on lucerne and following crops in central-western New South Wales. Australian Journal of Experimental Agriculture 46, 1291–1300.
| Effect of soil acidity and liming on lucerne and following crops in central-western New South Wales.Crossref | GoogleScholarGoogle Scholar |
Munns DN (1965) Soil acidity and growth of a legume. 1. Interactions of lime with nitrogen and phosphate on growth of Medicago sativa L. and Trifolium subterraneum L. Australian Journal of Agricultural Research 16, 733–741.
| Soil acidity and growth of a legume. 1. Interactions of lime with nitrogen and phosphate on growth of Medicago sativa L. and Trifolium subterraneum L.Crossref | GoogleScholarGoogle Scholar |
Narasimhamoorthy B, Blancaflor EB, Bouton JH, Payton ME, Sledge MK (2007) A comparison of hydroponics, soil, and root staining methods for evaluation of aluminum tolerance in Medicago truncatula (barrel medic) germplasm. Crop Science 47, 321–328.
| A comparison of hydroponics, soil, and root staining methods for evaluation of aluminum tolerance in Medicago truncatula (barrel medic) germplasm.Crossref | GoogleScholarGoogle Scholar |
O’Hara GW, Goss TJ, Dilworth MJ, Glenn AR (1989) Maintenance of intracellular pH and acid tolerance in Rhizobium meliloti. Applied and Environmental Microbiology 55, 1870–1876.
Pinkerton A, Simpson JR (1986) Responses of some crop plants to correction of subsoil acidity. Australian Journal of Experimental Agriculture 26, 107–113.
| Responses of some crop plants to correction of subsoil acidity.Crossref | GoogleScholarGoogle Scholar |
Rice WA, Clayton GW, Olsen PE, Lupwayi NZ (2000) Rhizobial inoculant formulations and soil pH influence field pea nodulation and nitrogen fixation. Canadian Journal of Soil Science 80, 395–400.
| Rhizobial inoculant formulations and soil pH influence field pea nodulation and nitrogen fixation.Crossref | GoogleScholarGoogle Scholar |
Robertson MJ (2006) ‘Lucerne prospects: drivers for widespread adoption of lucerne for profit and salinity management.’ (Cooperative Research Centre for Plant-Based Management of Dryland Salinity: Perth, W. Aust.)
Scott BJ, Ewing MA, Williams R, Humphries AW, Coombes NE (2008) Tolerance of aluminium toxicity in annual Medicago species and lucerne. Australian Journal of Experimental Agriculture 48, 499–511.
| Tolerance of aluminium toxicity in annual Medicago species and lucerne.Crossref | GoogleScholarGoogle Scholar |
Soto MJ, van Dillewijn P, Martínez-Abarca F, Jiménez-Zurdo JI, Toro N (2004) Attachment to plant roots and nod gene expression are not affected by pH or calcium in the acid-tolerant alfalfa-nodulating bacteria Rhizobium sp. LPU83. FEMS Microbiology Ecology 48, 71–77.
| Attachment to plant roots and nod gene expression are not affected by pH or calcium in the acid-tolerant alfalfa-nodulating bacteria Rhizobium sp. LPU83.Crossref | GoogleScholarGoogle Scholar |
von Uexküll HR, Mutert E (1995) Global extent, development and economic impact of acid soils. Plant and Soil 171, 1–15.
| Global extent, development and economic impact of acid soils.Crossref | GoogleScholarGoogle Scholar |
Wheeler DM, O’Connor MB (1998) Why do pastures respond to lime? Proceedings of the New Zealand Grasslands Association 60, 57–62.
White JGH (1967) Establishment of lucerne on acid soils. In ‘The lucerne crop’. (Ed. R Langer) pp. 105–113. (Reed Publishing: Wellington, New Zealand)
Willems A, Fernandez-Lopez M, Munoz-Adelantado E, Goris J, de Vos P, Martínez-Romero E, Toro N, Gillis M (2003) Description of new Ensifer strains from nodules and proposal to transfer Ensifer adhaerens Casida 1982 to Sinorhizobium as Sinorhizobium adhaerens comb. nov. Request for an opinion. International Journal of Systematic and Evolutionary Microbiology 53, 1207–1217.
| Description of new Ensifer strains from nodules and proposal to transfer Ensifer adhaerens Casida 1982 to Sinorhizobium as Sinorhizobium adhaerens comb. nov. Request for an opinion.Crossref | GoogleScholarGoogle Scholar |
Wood M (1995) A mechanism of aluminium toxicity of soil bacteria and possible ecological implications. Plant and Soil 171, 63–69.
| A mechanism of aluminium toxicity of soil bacteria and possible ecological implications.Crossref | GoogleScholarGoogle Scholar |
Wood M, Cooper JE (1984) Aluminium toxicity and multiplication of Rhizobium trifolii in a defined growth medium. Soil Biology & Biochemistry 16, 571–576.
| Aluminium toxicity and multiplication of Rhizobium trifolii in a defined growth medium.Crossref | GoogleScholarGoogle Scholar |
Young J (2003) The genus name Ensifer Casida 1982 takes priority over Sinorhizobium Chen et al. 1988, and Sinorhizobium morelense Wang et al. 2002 is a later synonym of Ensifer adhaerens Casida 1982. Is the combination ‘Sinorhizobium adhaerens’ (Casida 1982) Willems et al. 2003 legitimate? Request for an opinion. International Journal of Systematic and Evolutionary Microbiology 53, 2107–2110.
| The genus name Ensifer Casida 1982 takes priority over Sinorhizobium Chen et al. 1988, and Sinorhizobium morelense Wang et al. 2002 is a later synonym of Ensifer adhaerens Casida 1982. Is the combination ‘Sinorhizobium adhaerens’ (Casida 1982) Willems et al. 2003 legitimate? Request for an opinion.Crossref | GoogleScholarGoogle Scholar |
