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Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

The role of phosphorus deficiency in nodule microbial composition, and carbon and nitrogen nutrition of a native legume tree in the Cape fynbos ecosystem

Anathi Magadlela A , Waafeka Vardien A , Aleysia Kleinert A , Léanne L. Dreyer A and Alexander J. Valentine A B
+ Author Affiliations
- Author Affiliations

A Botany and Zoology Department, University of Stellenbosch, Private Bag X1, Matieland, 7602, South Africa.

B Corresponding author. Email: alexvalentine@mac.com

Australian Journal of Botany 63(5) 379-386 https://doi.org/10.1071/BT14216
Submitted: 1 September 2014  Accepted: 26 March 2015   Published: 6 May 2015

Abstract

In phosphorus (P)-poor ecosystems, microbial communities can play a major role in the nitrogen (N) mineral nutrition during N2 fixation in legumes. This study investigated the role of P nutrition on the composition of N2-fixing bacterial community in Virgilia divaricata root nodules, grown under glasshouse conditions. V. divaricata seeds were germinated in Fynbos soil as a natural inoculum, and, thereafter, transferred into sterile quartz-sand cultures and supplied with 500 µM P and 5 µM P, respectively. The N2-fixing bacterial communities in the rhizosphere and root nodules were examined on the basis of the polymerase chain reaction–denaturing gradient gel electrophoresis (PCR–DGGE) banding patterns of 16S rDNA and sequencing methods. The GenBank blast results showed that V. divaricata was nodulated by a wide range of root-nodule bacterial strains also found in the rhizosphere. These included Burkholderia phytofirmans, Burkholderia sp. and Bradyrhizobium sp., during both high and low P supply. The 15N natural-abundance data also confirmed that 40–50% of the N nutrition was from symbiotic N2 fixation. This is not only evidence of nodulation, but an indication of the adaptation of a range of N2-fixing bacterial strain species to the nutrient-poor, sandy, acidic soil of the Mediterranean-type ecosystems of the fynbos vegetation in the Cape Floristic Region (CFR). Legume species V. divaricata is highly adapted to the low-nutrient soils of its native range by its association with the symbiotic N2-fixing bacteria.

Additional keywords: acidic, P nutrient-poor soils, rhizobia strains, symbiotic nitrogen fixation, Virgilia divaricata.


References

Al-Niemi ST, Kahn LM, McDermott TR (1997) P Metabolism in the bean–Rhizobium tropici symbiosis. Plant Physiology 113, 1233–1242.

Almeida JPF, Hartwig UA, Frehner M, Nösberger J, Lüscher A (2000) Evidence that P deficiency induced N feedback regulation of symbiotic N2 fixation in white clover (Trifolium repens L.). Journal of Experimental Botany 51, 1289–1297.
Evidence that P deficiency induced N feedback regulation of symbiotic N2 fixation in white clover (Trifolium repens L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsVyjtbs%3D&md5=af34ca17f12c5b39ce74d6e9e80640d2CAS |

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.
Basic local alignment search tool.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXitVGmsA%3D%3D&md5=469c425d75ce11f6ce2d3b749e575236CAS | 2231712PubMed |

Beukes CW, Venter SN, Law IJ, Phalane FL, Steenkamp ET (2013) South Africa papilionoid legumes are nodulated the diverse Burkholderia with unique nodulation and nitrogen-fixation Loci. PLoS One 8,
South Africa papilionoid legumes are nodulated the diverse Burkholderia with unique nodulation and nitrogen-fixation Loci.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFymtrbP&md5=4c647dd8882936a6031e9dea25f81bacCAS | 23874611PubMed |

Bordeleau LM, Prévost D (1994) Nodulation and nitrogen fixation in extreme environments. Plant and Soil 161, 115–125.
Nodulation and nitrogen fixation in extreme environments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlt12rt7Y%3D&md5=a4c3440f6028035bd810c0f5084536e5CAS |

Brown G, Mitchell DT (1986) Influence of fire on the soil phosphorus status in sandplain lowland fynbos, south western Cape. South African Journal of Botany 52, 67–72.

Cocks MP, Stock WD (2001) Field patterns of nodulation in fifteen Aspalathus species and their ecological role in the fynbos vegetation of southern Africa. Basic and Applied Ecology 2, 115–125.
Field patterns of nodulation in fifteen Aspalathus species and their ecological role in the fynbos vegetation of southern Africa.Crossref | GoogleScholarGoogle Scholar |

Coetsee C, Wigley BJ (2013) Virgilia divaricata may facilitate forest expansion in the afrotemperate forests of the southern Cape, South Africa. Koedoe 55, 1–8.
Virgilia divaricata may facilitate forest expansion in the afrotemperate forests of the southern Cape, South Africa.Crossref | GoogleScholarGoogle Scholar |

Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant and Soil 245, 35–47.
Root exudates as mediators of mineral acquisition in low-nutrient environments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvVCit70%3D&md5=0ba533616e389a0ab8b8b5c8de91df47CAS |

Di Castri F (1981) Mediterranean-type shrublands of the world. In ‘Mediterranean-type shrublands’. (Eds F Di Castri, DW Goodall, RL Specht) pp. 1–52. (Elsevier Science Publishing Company: Amsterdam)

Drevon JJ, Hartwig UA (1997) Phosphorus deficiency increases the argon-induced decline of nodule nitrogenase activity in soybean and alfalfa. Planta 201, 463–469.
Phosphorus deficiency increases the argon-induced decline of nodule nitrogenase activity in soybean and alfalfa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjtVehsro%3D&md5=3c23e5fa615e1218286e6500437ddc92CAS |

Elliott GN, Chen W-M, Bontemps C, Chou J-H, Young JPW, Sprent JI, James EK (2007) Nodulation of Cyclopia spp. (Leguminosae, Papilionoideae) by Burkholderia tuberum. Annals of Botany 100, 1403–1411.
Nodulation of Cyclopia spp. (Leguminosae, Papilionoideae) by Burkholderia tuberum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFKis70%3D&md5=ef066ab790d8dbba176ff30bcfb0e297CAS | 17881339PubMed |

Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40, 503–537.
Carbon isotope discrimination and photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXktlKmu70%3D&md5=0429e9c7a94b57061eb46db3b068cb93CAS |

Fjellbirkeland A, Torsvik V, Øvreås L (2001) Methanotrophic diversity in an agricultural soil as evaluated by denaturing gradient gel electrophoresis profiles of pmoA, mxaF and 16S rDNA sequences. Antonie van Leeuwenhoek 79, 209–217.
Methanotrophic diversity in an agricultural soil as evaluated by denaturing gradient gel electrophoresis profiles of pmoA, mxaF and 16S rDNA sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmslWktL8%3D&md5=e3d4d6f4b42e518999358a21373bb52bCAS | 11520007PubMed |

Gentili F, Huss-Danell K (2002) Phosphorus modifies the effects of nitrogen on nodulation in split-root systems of Hippophaë rhamnoides. New Phytologist 153, 53–61.
Phosphorus modifies the effects of nitrogen on nodulation in split-root systems of Hippophaë rhamnoides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xns1ykuw%3D%3D&md5=00a7d6e28c94f26f2d0e953876e0dbe0CAS |

Gill AM, Groves RH (1981) Fire regimes in heathlands and their plant ecological effects. In ‘Heathlands and related shrublands of the world: analytical studies’. (Ed. RL Specht) pp. 61–84. (Elsevier: Amsterdam)

Goldblatt P, Manning J (2000) ‘Cape plants: a conspectus of the Cape flora of South Africa. Strelitzia, vol. 9.’ (National Botanical Institute: Pretoria, South Africa)

Graham PH (1992) Stress tolerance in Rhizobium and Bradyrhizobium and nodulation under adverse soil conditions. Canadian Journal of Microbiology 38, 475–484.
Stress tolerance in Rhizobium and Bradyrhizobium and nodulation under adverse soil conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xlt1Ort7Y%3D&md5=cf21ae0a4e5dca6d3fa0709765caaccaCAS |

Graham PH, Draeger KJ, Ferrey ML, Conroy MJ, Hammer BE, Martinez E, Aarons SR, Quinto C (1994) Acid pH tolerance in strains of Rhizobium and Bradyrhizobium, and initial studies on the basis for acid tolerance of Rhizobium tropici UMR1899. Canadian Journal of Microbiology 40, 198–207.
Acid pH tolerance in strains of Rhizobium and Bradyrhizobium, and initial studies on the basis for acid tolerance of Rhizobium tropici UMR1899.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXktlWjs7s%3D&md5=65082be1c0c8e3de5cce587e5b50a7feCAS |

Greinwald R, Veen G, Van Wyk BE, Witte L, Czygan FC (1989) Distribution and taxonomic significance of major alkaloids in the genus Virgilia. Biochemical Systematics and Ecology 17, 231–238.
Distribution and taxonomic significance of major alkaloids in the genus Virgilia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXlt1WksA%3D%3D&md5=d8443202773e95b442cecab7bbf23ab2CAS |

Groves RH (1983). ‘Nutrient cycling in Australian heath and South African fynbos.’ (Springer-Verlag: Berlin)

Hernández G, Ramírez M, Valdés-López O, Tesfaye M, Graham MA, Czechowski T, Schlereth A, Wandrey M, Erban A, Chueng F, Wu HC, Lara M, Town CD, Kopka J, Udvardi MK, Vance CP (2007) Phosphorus stress in common bean: root transcript and metabolic response. Plant Physiology 144, 752–767.
Phosphorus stress in common bean: root transcript and metabolic response.Crossref | GoogleScholarGoogle Scholar | 17449651PubMed |

Herppich M, Herppich WB, Willert DJ (2002) Leaf nitrogen content and photosynthesis activity in relation to soil nutrient availability in coastal and mountain fynbos plants (South Africa). Basic and Applied Ecology 3, 329–337.
Leaf nitrogen content and photosynthesis activity in relation to soil nutrient availability in coastal and mountain fynbos plants (South Africa).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XpsV2ntLs%3D&md5=509f98ba47717b75d4f9ff64d68afb2eCAS |

Hewitt EJ (1966) ‘Sand and water culture methods used in the study of plant nutrition. 2nd edn.’ (Commonwealth Agricultural Bureau: London)

Høgh-Jensen H, Schjoererring JK, Soussana JF (2002) The influence of phosphorus deficiency on growth and nitrogen fixation of white clover plants. Annals of Botany 90, 745–753.
The influence of phosphorus deficiency on growth and nitrogen fixation of white clover plants.Crossref | GoogleScholarGoogle Scholar | 12451030PubMed |

Horst WJ, Kamh M, Jibrin JM, Chude VA (2001) Agronomic measures for increasing P availability to crops. Plant and Soil 237, 211–223.
Agronomic measures for increasing P availability to crops.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovVWltw%3D%3D&md5=7cd71e2feed21c2d413d0115d86d755bCAS |

Jia Y, Gray VM, Straker CJ (2004) The influence of Rhizobium and arbuscular mycorrhizal fungi on nitrogen and phosphorus accumulation by Vicia faba. Annals of Botany 94, 251–258.
The influence of Rhizobium and arbuscular mycorrhizal fungi on nitrogen and phosphorus accumulation by Vicia faba.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnsV2ktLY%3D&md5=d945b77f6275d1023efd216f19f22aa6CAS | 15205177PubMed |

Kanu SA, Dakora FD (2012) Symbiotic nitrogen contribution and biodiversity of root-nodule bacteria nodulating Psoralea species in the Cape Fynbos, South Africa. Soil Biology & Biochemistry 54, 68–76.
Symbiotic nitrogen contribution and biodiversity of root-nodule bacteria nodulating Psoralea species in the Cape Fynbos, South Africa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVSlsb7P&md5=1d2941fc912d99a2b486a26de7597ff3CAS |

Kochian LV (1995) Cellular mechanisms of aluminium toxicity and resistance in plants. Annual Review of Plant Physiology 46, 237–260.
Cellular mechanisms of aluminium toxicity and resistance in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmsVCqtb0%3D&md5=a021288c37dbc3f11de4a3d6eac0fd68CAS |

Kruger FJ, Mitchell DT, Jarvis JUM (1983) ‘Mediterranean-type ecosystems. The role of nutrients.’ (Springer-Verlag: Berlin)

Lazarevic V, Gaia N, Girard M, Francois P, Schrenzel J (2013) Comparison of DNA extraction methods in analysis of salivary bacterial communities. PLoS One 8, e67699
Comparison of DNA extraction methods in analysis of salivary bacterial communities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFKktrrO&md5=17021f08654791348bab3f05a98bb588CAS | 23844068PubMed |

Le Maitre DC, Midgley JJ (1992) Plant reproductive ecology. In ‘The ecology of fynbos: nutrients, fire, and diversity’. (Ed. RM Cowling) pp. 135–174. (Oxford University Press: Cape Town, South Africa)

Le Roux MR, Khan S, Valentine AJ (2009) Nitrogen and carbon costs of soybean and lupin root systems during phosphate starvation. Symbiosis 48, 102–109.
Nitrogen and carbon costs of soybean and lupin root systems during phosphate starvation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpsFenurY%3D&md5=a33d439db4ec4c4263e59fbbafad48d9CAS |

Leung K, Bottomley PJ (1987) Influence of phosphate on the growth and nodulation characteristics of Rhizobium trifolii. Applied and Environmental Microbiology 53, 2098–2105.

Lie TA (1981) Environmental physiology of legume–Rhizobium symbiosis. In ‘Nitrogen fixation. Vol. 1: ecology’. (Ed. WJ Broughton) pp. 104–134. (Clarendon Press: Oxford, UK)

Lodwig E, Poole P (2003) Metabolism of Rhizobium bacteroids. Critical Reviews in Plant Sciences 22, 37–78.
Metabolism of Rhizobium bacteroids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjs1ahsbg%3D&md5=50dc6958b038696cb6d1cc701fb526c2CAS |

Lowendorf HS (1980) Factors affecting survival of Rhizobium in soil. Advances in Microbial Ecology 4, 87–124.
Factors affecting survival of Rhizobium in soil.Crossref | GoogleScholarGoogle Scholar |

Lynch JP, Beebe SE (1995) Adaptations of bean (Phaseolus vulgaris L.) to low phosphorus availability. HortScience 30, 1165–1171.

Lynch JP, Ho MD (2005) Rhizoeconomics: carbon costs of phosphorus acquisition. Plant and Soil 269, 45–56.
Rhizoeconomics: carbon costs of phosphorus acquisition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXks1Oisrw%3D&md5=3eb318769e3d0eb56a7d0ab4cd23a7baCAS |

Magadlela A, Kleinert A, Dreyer LL, Valentine A (2014) Low-phosphorus conditions affect the nitrogen nutrition and associated carbon costs of two legume tree species from a Mediterranean-type ecosystem. Australian Journal of Botany 62, 1–9.
Low-phosphorus conditions affect the nitrogen nutrition and associated carbon costs of two legume tree species from a Mediterranean-type ecosystem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXnsFWisbo%3D&md5=bbcfc82c364fc3e56bf49b06b16c858aCAS |

Manders PT, Richardson DM, Masson PH (1992) Is fynbos a stage in succession to forest? Analysis of the perceived ecological distinction between two communities. In ‘Fire in South African mountain fynbos: ecosystem, community and species response at Swartboskloof. (Ecological Studies vol. 93.) (Eds BW van Wilgen, DM Richardson, FJ Kruger, HJ van Hensbergen) pp. 81–107. (Springer Verlag: Berlin)

Maseko ST, Dakora FD (2013) Plant enzymes, root exudates, cluster roots and mycorrhizal symbiosis are the drivers of P nutrition in native legumes growing in P deficient soils of the Cape Fynbos in South Africa. Journal of Agricultural Science and Technology A 3, 331–340.

Mortimer PE, Archer E, Valentine AJ (2005) Mycorrhizal C costs and nutritional benefits in developing grapevines. Mycorrhiza 15, 159–165.
Mycorrhizal C costs and nutritional benefits in developing grapevines.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2M3ksFWisw%3D%3D&md5=11c86af5be849c370dfeec08be698d42CAS | 15883853PubMed |

Mortimer PE, Perez-Fernandez MA, Valentine AJ (2008) The role of arbuscular mycorrhizal colonization in the carbon and nutrient economy of the tripartite symbiosis with nodulated Phaseolus vulgaris. Soil Biology & Biochemistry 40, 1019–1027.
The role of arbuscular mycorrhizal colonization in the carbon and nutrient economy of the tripartite symbiosis with nodulated Phaseolus vulgaris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXksVKru7c%3D&md5=52b7918ebc80bbb021637bba5a418c7fCAS |

Mortimer PE, Perez-Fernandez MA, Valentine AJ (2009) Arbuscular mycorrhizae affects the N and C economy of nodulated Phaseolus vulgaris (L.) during NH4+ nutrition. Soil Biology & Biochemistry 41, 2115–2121.
Arbuscular mycorrhizae affects the N and C economy of nodulated Phaseolus vulgaris (L.) during NH4+ nutrition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFKnsrjF&md5=ec67204c79a7d15ac1ffd5ad26cc4002CAS |

Munns DN (1986) Acid soil tolerance in legume and rhizobia. Advances in Plant Nutrition 2, 63–91.

Muofhe ML, Dakora FD (1999) Nitrogen nutrition in nodulated field plants of the shrub tea legume Aspalathus linearis assessed using 15N natural abundance. Plant and Soil 209, 181–186.
Nitrogen nutrition in nodulated field plants of the shrub tea legume Aspalathus linearis assessed using 15N natural abundance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlt1emsrw%3D&md5=1846340f35835e5f63069f454e2b5b10CAS |

Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling of complex microbial communities by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Applied and Environmental Microbiology 59, 695–700.

Nielsen KL, Bouma TJ, Lynch J, Eissenstat DM (1998) Effects of phosphorus availability and vesicular-arbuscular mycorrhizas on the carbon budget of common bean (Phaseolus vulgaris). New Phytologist 139, 647–656.
Effects of phosphorus availability and vesicular-arbuscular mycorrhizas on the carbon budget of common bean (Phaseolus vulgaris).Crossref | GoogleScholarGoogle Scholar |

Nielsen KL, Amram E, Lynch JP (2001) The effect of phosphorus availability on the carbon economy of contrasting common bean (Phaseolus vulgaris L.) genotypes. Journal of Experimental Botany 52, 329–339.
The effect of phosphorus availability on the carbon economy of contrasting common bean (Phaseolus vulgaris L.) genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtVaju7w%3D&md5=acf45c30afd97cf0952289c8aa6d2263CAS | 11283178PubMed |

Norland S (2004) ‘Gel2K gel analysis software.’ (University of Bergen: Bergen, Norway). Available at http://www.im.uib.no/~nimsn/program/ [Verified 22 April 2015]

O’Hara GW (2001) Nutritional constraints on root nodule bacteria affecting symbiotic nitrogen fixation: a review. Australian Journal of Experimental Agriculture 41, 417–433.
Nutritional constraints on root nodule bacteria affecting symbiotic nitrogen fixation: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkt1Crtrk%3D&md5=e154ec9f166c752829d6f7c3878b3163CAS |

Olivera M, Tejera N, Iribarne C, Ocana A, Lluch C (2004) Growth, nitrogen fixation and ammonium assimilation in common bean (Phaseolus vulgaris): effect of phosphorus. Physiologia Plantarum 121, 498–505.
Growth, nitrogen fixation and ammonium assimilation in common bean (Phaseolus vulgaris): effect of phosphorus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvFOiur8%3D&md5=2140ec2f66c56515841db6a31eddf21aCAS |

Peng S, Eissenstat DM, Graham JH, Williams K, Hodge NC (1993) Growth depression in mycorrhizal citrus at high-phosphorus supply. Plant Physiology 101, 1063–1070.

Power SC, Cramer MD, Verboom GA, Chimphango SBM (2010) Does phosphate acquisition constraint legume persistence in the fynbos of the Cape Floristic Region? Plant and Soil 334, 33–46.
Does phosphate acquisition constraint legume persistence in the fynbos of the Cape Floristic Region?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVaqur7F&md5=3f091f972882f6a76bd81f2df395219fCAS |

Shearer GB, Kohl DM (1986) N2-fixation in the field settings: estimations based on natural 15N abundance. Australian Journal of Plant Physiology 13, 699–756.

Siciliano SD, Germida JJ, Banks K, Greer CW (2003) Changes in microbial community composition and function during a polyaromatic hydrocarbon phytoremediation field trial. Applied and Environmental Microbiology 69, 483–489.
Changes in microbial community composition and function during a polyaromatic hydrocarbon phytoremediation field trial.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkvVarsw%3D%3D&md5=302116b5d385549880ebf443b8786c70CAS | 12514031PubMed |

Sprent JI (2009) ‘Legume nodulation: a global perspective.’ (John Wiley and Sons: Chichester, UK)

Straker CJ (1996) Ericoid mycorrhizal: ecological and host specificity. Mycorrhiza 6, 215–225.
Ericoid mycorrhizal: ecological and host specificity.Crossref | GoogleScholarGoogle Scholar |

Sulieman S, Van Ha C, Schulze J, Tran L-SP (2013) Growth and nodulation of symbiotic Medicago truncatula at different levels of phosphorus availability. Journal of Experimental Botany 64, 2701–2712.
Growth and nodulation of symbiotic Medicago truncatula at different levels of phosphorus availability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVaks7%2FP&md5=faa82fd929205fd371aa6e7c4ef75fcaCAS | 23682114PubMed |

Tang C, Hensinger P, Drevon J-J, Jaillard B (2001) Phosphorus deficiency impairs early nodule functioning and enhances proton release in roots of Medicago truncatula L. Annals of Botany 88, 131–138.
Phosphorus deficiency impairs early nodule functioning and enhances proton release in roots of Medicago truncatula L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkvVOltL4%3D&md5=5eb5810bd466ad3e6f7f8af948b9f56cCAS |

Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.
The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntFyntQ%3D%3D&md5=995692a7f2d605c7167ceefda8306a3aCAS | 9396791PubMed |

Uhde-Stone C, Gilbert G, Johnson JMF, Litjens R, Zinn KE, Temple SJ, Vance CP, Allan DL (2003) Acclimation of white lupin to phosphorus deficiency involves enhanced expression of genes related to organic acid metabolism. Plant and Soil 248, 99–116.
Acclimation of white lupin to phosphorus deficiency involves enhanced expression of genes related to organic acid metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtFCru7g%3D&md5=bd8597e0c6406c0d082e5cb0e8a96a3dCAS |

Vadez V, Beck DP, Lasso JH, Drevon JJ (1997) Utilization of acetylene reduction assay to screen for tolerance of symbiotic N2 fixation to limitation P nutrition in common bean. Physiologia Plantarum 99, 227–232.
Utilization of acetylene reduction assay to screen for tolerance of symbiotic N2 fixation to limitation P nutrition in common bean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjtFWjsLc%3D&md5=25e50bd9502b897c72640e1f98307ecbCAS |

Valentine AJ, Benedito VA, Kang Y (2010) Abiotic stress in legume N2 fixation: from physiology to genomics and beyond. In ‘Annual Plant Reviews Volume 42: Nitrogen Metabolism in Plants in the Post-genomic Era’. (Eds C Foyer, M Zhao) pp. 207–248. (Wiley-Blackwell: Oxford)

Vance CP (2001) Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources. Plant Physiology 127, 390–397.
Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnslGltbw%3D&md5=3f07c1b47a5acc0810af089225e93c16CAS | 11598215PubMed |

Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition in low-nutrient environments. Plant and Soil 245, 35–47.
Phosphorus acquisition in low-nutrient environments.Crossref | GoogleScholarGoogle Scholar |

Vargas AAT, Graham PH (1988) Phaseolus vulgaris cultivar and Rhizobium strain variation in acid-pH tolerance and nodulation under acid conditions. Field Crops Research 19, 91–101.
Phaseolus vulgaris cultivar and Rhizobium strain variation in acid-pH tolerance and nodulation under acid conditions.Crossref | GoogleScholarGoogle Scholar |

Williams K, Percival F, Merino J, Mooney HA (1987) Estimation of tissue construction cost from heat of combustion and organic nitrogen content. Plant, Cell & Environment 10, 725–734.

Wisheu IC, Rosenzweig ML, Olsvig-Whittaker L, Shmida A (2000) What makes nutrient-poor soils Mediterranean heathlands so rich in plant diversity? Evolutionary Ecology Research 2, 935–955.

Zahran HZ (1999) Rhizobium–legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiology and Molecular Biology Reviews 63, 986–989.