Agronomic and environmental drivers of population size and symbiotic performance of Rhizobium leguminosarum bv. viciae in Mediterranean-type environments

Article

<< Previous

Next >>

Contents Vol 63(5)

doi:10.1071/CP12032

Plant Sciences, Sustainable Farming Systems & Food Quality

	Search




	Advanced Search



	Journal Home

	About the Journal

	New Editor-in-Chief

	Editorial Board

	Contacts



	Content

	Online Early

	Current Issue

	Just Accepted

	All Issues

	Special Issues

	Research Fronts

	Farrer Reviews

	Sample Issue



	For Authors

	General Information

	Notice to Authors

	Submit Article

	Open Access



	For Referees

	Referee Guidelines

	Review Article

	Annual Referee Index



	For Subscribers

	Subscription Prices

	Customer Service

	Print Publication Dates

e-Alerts

Subscribe to our Email Alert or

feeds for the latest journal papers.

Connect with us

Farrer Reviews

Invited Farrer Review Series. More...

PrometheusWiki

Protocols in ecological and environmental plant physiology

Agronomic and environmental drivers of population size and symbiotic performance of Rhizobium leguminosarum bv. viciae in Mediterranean-type environments

E. A. Drew ^A ^D, M. D. Denton ^B ^C, V. O. Sadras ^A ^C and R. A. Ballard ^A

^A South Australian Research and Development Institute, GPO Box 397, Adelaide, SA 5001, Australia.
^B Department of Primary Industries Victoria, Rutherglen, Vic. 3685, Australia.
^C School of Agriculture, Food and Wine, The University of Adelaide, Glen Osmond, SA 5064, Australia.
^D Corresponding author. Email: liz.drew@sa.gov.au

Crop and Pasture Science 63(5) 467-477 http://dx.doi.org/10.1071/CP12032
Submitted: 24 January 2012 Accepted: 18 June 2012 Published: 13 August 2012





	PDF (351 KB) $25



	Export Citation

Print

Abstract

The population size and symbiotic performance (ability to fix N₂) of rhizobia (Rhizobium leguminosarum bv. viciae) capable of nodulating field pea (Pisum sativum) were assessed in 114 soils from Mediterranean-type environments of southern Australia. All soils were collected in autumn, before the growing season, and had a history of crop legumes including field pea, faba bean, lentil, or vetch. The most probable number (MPN) technique, with vetch as a trap plant, was used to estimate the numbers of pea rhizobia in soils. Of the soils tested, 29% had low numbers of pea rhizobia (<100 rhizobia/g), 38% had moderate numbers (100–1000/g), and the remaining 33% had >1000/g. Soil pH, the frequency of a host crop in the rotation, and the number of summer days with a maximum temperature >35°C were strongly correlated with the pea rhizobia population size.

Symbiotic performance (SP) of pea rhizobia in soils was assessed for soils with a MPN >100 rhizobia/g. An extract of the soils was used to inoculate two field pea cultivars growing in a nitrogen-deficient potting media in the greenhouse. Plants were grown for 5 weeks after inoculation and shoot dry matter was expressed as a percentage of the dry matter of plants grown with a commercial strain R. leguminosarum bv. viciae, SU303. Symbiotic performance ranged from 25 to 125%. One-quarter of the soils assessed had suboptimal SP (i.e. <70%). Soil and climatic variables were weakly associated with SP, with pH and average annual rainfall accounting for 17% of the variance.

This research highlights the complexity of factors influencing population size and symbiotic performance of pea rhizobia in soils. Options for the improved management of populations of pea rhizobia in Mediterranean environments are discussed. Specifically, our data indicate that inoculation of pea crops is likely to be beneficial where pH(H₂O) <6.6, particularly when summers have been hot and dry and when a host has been absent for ≥5 years, as numbers of rhizobia are likely to be below the thresholds needed to optimise nodulation and crop growth. New inoculation technologies and plant breeding will be required to overcome large populations of pea rhizobia with suboptimal SP.

Additional keywords: field pea, Mediterranean, nodulation, effectiveness, Pisum sativum, rhizobia.

References

ABARE (1989) Crop Report. Australian Bureau of Agriculture and Resource Economics, Commonwealth of Australia, Canberra.

ABARE (2009) Australian Crop Report. Australian Bureau of Agriculture and Resource Economics, Commonwealth of Australia, Canberra.

Aschmann H (Ed.) (1973) Distribution and peculiarity of Mediterranean ecosystems. In ‘Mediterranean type ecosystems’. (Springer-Verlag: Heildeberg)

Baldock JA (2001) Interactions of organic materials and microorganisms with minerals in the stabilization of soil structure. In ‘Interactions between soil particles and microorganisms: impact on the terrestrial ecosystem.’ (Eds PM Huang, JM Bollag, N Senesi) pp. 85–131. (John Wiley & Sons Ltd: Chichester, UK)

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 |

Ballard RA, Charman N, McInnes A, Davidson JA (2004) Size, symbiotic effectiveness and genetic diversity of field pea rhizobia (Rhizobium leguminosarum bv. viciae) populations in South Australian soils. Soil Biology & Biochemistry 36, 1347–1355.
| CrossRef | CAS |

Blair GJ, Chinoim N, Lefroy RDB, Anderson GC, Crocker GJ (1991) A soil sulfur test for pastures and crops. Australian Journal of Soil Research 29, 619–626.
| CrossRef | CAS |

Bottomley PJ (1992) Ecology of Bradyrhizobium and Rhizobium. In ‘Biological nitrogen fixation’. (Eds G Stacey, R Burris, HJ Evans) pp. 293–348. (Chapman and Hall Inc.: London)

Bowra BJ, Dilworth MJ (1981) Motility and chemotaxis towards sugars in Rhizobium leguminosarum. Journal of General Microbiology 126, 231–235.

Brockwell J (1963) Accuracy of a plant-infection technique for counting populations of Rhizobium trifolii. Applied Microbiology 11, 377–383.

Brockwell J (2004) Abundant, cheap nitrogen for Australian farmers: a history of Australian Nodulation and Nitrogen Fixation Conferences. Soil Biology & Biochemistry 36, 1195–1204.
| CrossRef | CAS |

Brockwell J, Holliday RA, Pilka A (1988) Evaluation of the symbiotic nitrogen-fixing potential of soils by direct microbiological means. Plant and Soil 108, 163–170.
| CrossRef |

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 | CAS |

Chao WL, Alexander M (1982) Influence of soil characteristics on the survival of Rhizobium in soils undergoing drying. Soil Science Society of America Journal 46, 949–952.
| CrossRef |

Chatel DL, Parker CA (1973) Survival of field-grown rhizobia over the dry summer period in Western Australia. Soil Biology & Biochemistry 5, 415–423.
| CrossRef |

Chemining’wa GN, Vessey JK (2006) The abundance and efficacy of Rhizobium leguminosarum bv. viciae in cultivated soils of the eastern Canadian prairie. Soil Biology & Biochemistry 38, 294–302.
| CrossRef | CAS |

Cheng Y, Waktin ELJ, Howieson JG, O’Hara GW (2005) Root and root hair mechanisms that confer symbiotic competence for nodulation in acidic soils within Medicago species: a holistic model. Australian Journal of Experimental Agriculture 45, 231–240.
| CrossRef |

Colwell JD (1965) An automatic procedure for the determination of phosphorus in sodium hydrogen carbonate extracts of soils. Chemistry & Industry (21), 893–895.

Coventry DR, Evans J (1989) Symbiotic nitrogen fixation and soil acidity. In ‘Soil acidity and plant growth’. (Ed. AD Robson) pp. 103–137. (Academic Press: Sydney)

Coventry DR, Hirth JR (1992) Effects of tillage and lime on Rhizobium trifolii populations and survival in wheat-subterranean clover rotation in southeastern Australia. Soil & Tillage Research 25, 67–74.
| CrossRef |

Deaker R, Roughley RJ, Kennedy IR (2004) Legume seed inoculation technology—a review. Soil Biology & Biochemistry 36, 1275–1288.
| CrossRef | CAS |

Denison RF (2009) Darwinian agriculture: real, imaginary and complex trade-offs as constraints and opportunities. In ‘Crop physiology: applications for genetic improvement and agronomy’. (Eds VO Sadras, DF Calderini.) pp. 215–234. (Academic Press: San Diego, CA)

Denton MD, Coventry DR, Bellotti WD, Howieson JG (2000) Distribution, abundance and symbiotic effectiveness of Rhizobium leguminosarum bv. trifolii from alkaline pasture soils in South Australia. Australian Journal of Experimental Agriculture 40, 25–35.
| CrossRef |

Denton MD, Pearce DJ, Ballard RA, Hannah MC, Mutch LA, Norng S, Slattery JF (2009) A multi-site field evaluation of granular inoculants for legume nodulation. Soil Biology & Biochemistry 41, 2508–2516.
| CrossRef | CAS |

Depret G, Laguerre G (2008) Plant phenology and genetic variability in root and nodule development strongly influence genetic structuring of Rhizobium leguminosarum biovar viciae populations nodulating pea. New Phytologist 179, 224–235.
| CrossRef |

Dilworth MJ, Howieson JG, Reeve WG, Tiwari RP, Glenn AR (2001) Acid tolerance in legume root nodule bacteria and selecting for it. Australian Journal of Experimental Agriculture 41, 435–446.
| CrossRef | CAS |

Drew EA, Ballard RA (2010) Improving N₂ fixation from the plant down: compatibility of Trifolium subterraneum L. cultivars with soil rhizobia can influence symbiotic performance. Plant and Soil 327, 261–277.
| CrossRef | CAS |

Drew E, Gupta V, Roget D, Lawrence L (2006) Herbicides and their effects on pulses in Southern Australia. Outlooks on Pest Management 17, 166–167.
| CrossRef |

Etien N, Daux V, Masson-Delmotte V, Mestre O, Stievenard M, Guillemin MT, Boettger T, Breda N, Haupt M, Perraud PP (2009) Summer maximum temperature in northern France over the past century: instrumental data versus multiple proxies (tree-ring isotopes, grape harvest dates and forest fires). Climatic Change 94, 429–456.
| CrossRef | CAS |

Evans J (2005) An evaluation of potential Rhizobium inoculant strains used for pulse production in acidic soils of south-east Australia. Australian Journal of Experimental Agriculture 45, 257–268.
| CrossRef |

Evans J, Wallace C, Dobrowolski N (1993a) Interaction of soil type and temperature on the survival of Rhizobium leguminosarum bv. viciae. Soil Biology & Biochemistry 25, 1153–1160.
| CrossRef |

Evans J, Wallace C, Dobrowolski N, Pritchard I, Sullivan B (1993b) Requirement of field pea for inoculation with Rhizobium and lime pelleting in soils of Western Australia. Australian Journal of Experimental Agriculture 33, 767–773.
| CrossRef |

FAO (2008) FAOSTAT. Food and Agriculture Organization of the United Nations. Available at: http://faostat.fao.org/.

Fettell NA, Evans CM, Carpenter DJ, Brockwell J (2007) Residual effects from lime application on soil pH, rhizobial population and crop productivity in dryland farming systems of central New South Wales. Australian Journal of Experimental Agriculture 47, 608–619.
| CrossRef |

Gemell LG, Hartley EJ, Herridge DF (2005) Point-of-sale evaluation of preinoculated and custom-inoculated pasture legume seed. Australian Journal of Experimental Agriculture 45, 161–169.
| CrossRef |

Gentilli J (1971) The main climatological elements. In ‘Climates of Australia and New Zealand’. (Ed. J Gentilli) pp. 119–188. (Elsevier: New York)

Gonzalez A, Gonzalez-Murua C, Royuela M (1996) Influence of imazethapyr on Rhizobium growth and its symbiosis with pea (Pisum sativum). Weed Science 44, 31–37.

Graham PH (2008) Ecology of root-nodule bacteria of legumes. In ‘Nitrogen-fixing leguminous symbioses’. (Eds MJ Dilworth, EK James, JI Sprent, WE Newton) pp. 23–43. (Springer: Dordrecht)

Groenevelt PH, Grant CD, Murray RS (2004) On water availability in saline soils. Australian Journal of Soil Research 42, 833–840.
| CrossRef |

Gutschick VP, BassiriRad H (2003) Extreme events as shaping physiology, ecology, and evolution of plants: toward a unified definition and evaluation of their consequences. New Phytologist 160, 21–42.
| CrossRef |

Herridge DF (2008) Inoculation technology for legumes. In ‘Nitrogen-fixing leguminous symbioses’. (Eds MJ Dilworth, EK James, JI Sprent, WE Newton) pp. 77–115. (Springer: Dordrecht)

Howieson J, Ballard R (2004) Optimising the legume symbiosis in stressful and competitive environments within southern Australia—some contemporary thoughts. Soil Biology & Biochemistry 36, 1261–1273.
| CrossRef | CAS |

Khaliq MN, St-Hilaire A, Ouarda T, Bobee B (2005) Frequency analysis and temporal pattern of occurrences of southern Quebec heatwaves. International Journal of Climatology 25, 485–504.
| CrossRef |

Khan HR, McDonald GK, Rengel Z (2003) Zn fertilization improves water use efficiency, grain yield and seed Zn content in chickpea. Plant and Soil 249, 389–400.
| CrossRef | CAS |

Kinkle BK, Schmidt EL (1991) Transfer of the pea symbiotic plasmid pJB5JI in nonsterile soil. Applied and Environmental Microbiology 57, 3264–3269.

Kyei-Boahen S, Slinkard AE, Walley FL (2002) Evaluation of rhizobial inoculation methods for chickpea. Agronomy Journal 94, 851–859.
| CrossRef |

Lemerle D, Hinkley RB (1991) Tolerances of canola, field pea, lupin and faba bean cultivars to herbicides. Australian Journal of Experimental Agriculture 31, 379–386.
| CrossRef | CAS |

Loi A, Cocks PS, Howieson JG, Carr SJ (1999) Hardseededness and the pattern of softening in Biserrula pelecinus L., Ornithopus compressus L., and Trifolium subterraneum L. seeds. Australian Journal of Agricultural Research 50, 1073–1081.
| CrossRef |

Marshall KC (1975) Clay mineralogy in relation to survival of soil bacteria. Annual Review of Phytopathology 13, 357–373.
| CrossRef |

Marshall DJ, Bateman JD, Brockwell J (1993) Validation of a serial-dilution, plant-infection test for enumerating Rhizobium leguminosarum bv. viciae and its application for counting rhizobia in acid soils. Soil Biology & Biochemistry 25, 261–268.
| CrossRef |

McKnight T (1949) Efficiency of isolates of Rhizobium in the cowpea (Vigna unguiculata) group, with proposed additions to this group. Queensland Journal of Agricultural Science 6, 61–76.

Mosier AR (1998) Soil processes and global change. Biology and Fertility of Soils 27, 221–229.
| CrossRef | CAS |

Nandasena KG, O’Hara GW, Tiwari RP, Howieson JG (2006) Rapid in situ evolution of nodulating strains for Biserrula pelecinus L. through lateral transfer of a symbiosis island from the original mesorhizobial inoculant. Applied and Environmental Microbiology 72, 7365–7367.
| CrossRef | CAS |

Newton PCD, Lieffering M, Bowatte WMSD, Brock SC, Hunt CL, Theobald PW, Ross DJ (2010) The rate of progression and stability of progressive nitrogen limitation at elevated atmospheric CO₂ in a grazed grassland over 11 years of Free Air CO₂ enrichment. Plant and Soil 336, 433–441.
| CrossRef | CAS |

O’Hara GW (2001) Nutritional constraints on root nodule bacteria affecting symbiotic nitrogen fixation: a review. Australian Journal of Experimental Agriculture 41, 417–433.
| CrossRef | CAS |

Peoples MB, Brockwell J, Herridge DF, Rochester IJ, Alves BJR, Urquiaga S, Boddey RM, Dakora FD, Bhattarai S, Maskey SL, Sampet C, Rerkasem B, Khan DF, Hauggaard-Nielsen H, Jensen ES (2009) The contributions of nitrogen-fixing crop legumes to the productivity of agricultural systems. Symbiosis 48, 1–17.
| CrossRef | CAS |

Rayment GE, Higginson FR (1992) ‘Australian laboratory handbook of soil and chemical methods.’ (Inkata Press: Melbourne)

Richardson AE, Simpson RJ (1988) Enumeration and distribution of Rhizobium trifolii under a subterranean clover-based pasture growing in an acid soil. Soil Biology & Biochemistry 20, 431–438.
| CrossRef |

Richardson AE, Djordjevic MA, Rolfe BG, Simpson RJ (1988) Effects of pH, Ca and Al on the exudation from clover seedlings of compounds that induce the expression of nodulation genes in Rhizobium trifolii. Plant and Soil 109, 37–47.
| CrossRef | CAS |

Rodelas B, Gonzalez-Lopez J, Salmeron V, Martinez-Toledo MV, Pozo C (1998) Symbiotic effectiveness and bacteriocin production by Rhizobium leguminosarum bv viceae isolated from agricultural soils in Spain. Applied Soil Ecology 8, 51–60.
| CrossRef |

Ryan J, Ibrikci H, Sommer R, McNeill A (2009) Nitrogen in rainfed and irrigated cropping systems in the Mediterranean region. Advances in Agronomy 104, 53–136.
| CrossRef | CAS |

Sachs JL, Ehinger MO, Simms EL (2010) Origins of cheating and loss of symbiosis in wild Bradyrhizobium. Journal of Evolutionary Biology 23, 1075–1089.
| CrossRef | CAS |

Sadras V (2002) Interaction between rainfall and nitrogen fertilisation of wheat in environments prone to terminal drought: economic and environmental risk analysis. Field Crops Research 77, 201–215.
| CrossRef |

Sadras VO (2003) Influence of size of rainfall events on water-driven processes. I. Water budget of wheat crops in south-eastern Australia. Australian Journal of Agricultural Research 54, 341–351.
| CrossRef |

Sadras VO, Baldock JA (2003) Influence of size of rainfall events on water-driven processes. II. Soil nitrogen mineralisation in a semi-arid environment. Australian Journal of Agricultural Research 54, 353–361.
| CrossRef |

Sadras V, Roget D, Krause M (2003) Dynamic cropping strategies for risk management in dry-land farming systems. Agricultural Systems 76, 929–948.
| CrossRef |

Škrdleta V, Němcová M, Lisá L, Novák K (1993) Characterization of soil populations of Rhizobium leguminosarum bv. viceae by means of symbiotic traits. Soil Biology & Biochemistry 25, 63–67.
| CrossRef |

Slattery JF, Pearce DJ, Slattery WJ (2004) Effects of resident rhizobial communities and soil type on the effective nodulation of pulse legumes. Soil Biology & Biochemistry 36, 1339–1346.
| CrossRef | CAS |

Spencer MA (2005) Pythium irregulare. ‘Descriptions of fungi and bacteria.’ (CABI: UK)

Srihuttagum M, Sivasithamparam K (1991) The influence of fertilizers on root rot of field peas caused by Fusarium oxysporum, Pythium vexans and Rhizoctonia solani inoculated singly or in combination. Plant and Soil 132, 21–27.
| CrossRef | CAS |

Thies JE, Woomer PL, Singleton PW (1995) Enrichment of Bradyrhizobium spp populations in soil due to cropping of the homologous host legume. Soil Biology & Biochemistry 27, 633–636.
| CrossRef | CAS |

Unkovich MJ, Pate JS, Sanford P (1997) Nitrogen fixation by annual legumes in Australian Mediterranean agriculture. Australian Journal of Agricultural Research 48, 267–293.
| CrossRef |

van Leur JAG, Southwell RJ, Mackie JM (2008) Aphanomyces root rot on faba bean in northern NSW. Australasian Plant Disease Notes 3, 8–9.
| CrossRef |

Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Science 37, 29–38.
| CrossRef | CAS |

Williamson G (2007) Climate and root distribution in Australian perennial grasses; implications for salinity mitigation. PhD Thesis, The University of Adelaide, S. Aust., Australia.

Yates RJ, Howieson JG, Real D, Reeve WG, Vivas-Marfisi A, O’Hara GW (2005) Evidence of selection for effective nodulation in the Trifolium spp. symbiosis with Rhizobium leguminosarum biovar trifolii. Australian Journal of Experimental Agriculture 45, 189–198.
| CrossRef |

Subscriber Login

	Username: Password:

Legal & Privacy | Contact Us | Help