Low-phosphorus conditions affect the nitrogen nutrition and associated carbon costs of two legume tree species from a Mediterranean-type ecosystem
Anathi Magadlela A , Aleysia Kleinert A , Léanne L. Dreyer A and Alex 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 62(1) 1-9 https://doi.org/10.1071/BT13264
Submitted: 29 October 2013 Accepted: 11 February 2014 Published: 14 April 2014
Abstract
The role of phosphorus nutrition in two-legume tree species from the Mediterranean-type ecosystem of the Cape Floristic Region (CFR) in South Africa was investigated. There is very little information about the functional adaptations of nitrogen (N) and phosphorus (P) nutrition in these legume trees growing in nutrient-poor soils. Nodulated Virgilia divaricata and V. oroboides tree saplings were grown in sterilised sand and supplied with Long Ashton nutrient solution, which was modified to contain either sufficient-phosphate (500 µM) or low-phosphate (5 µM) nutrient solution for 90 days. During low-P conditions, the growth of V. divaricata was not affected, whereas V. oroboides showed a decrease in growth. The decrease in V. oroboides under low-P conditions was related to the lower P uptake, which resulted in an alteration in belowground biomass allocation, which consequently affected on the N nutrition and carbon (C) cost of growth. In this regard, V. oroboides plants allocated less biomass to roots and nodules, as a proportion of whole plant growth. The impact of this was a decline in N nutrition, growth respiration and photosynthetic costs in V. oroboides. In contrast, V. divaricata maintained its P concentrations, photosynthetic costs and increased its nodule allocation under low-P conditions, to the benefit of N nutrition. The two CFR tree legumes appear to have different adaptations to low-P conditions, which may influence their N and P acquisition in their naturally low-P environment.
Additional keywords: acidic soils, biological nitrogen, fynbos, nutrient deficiencies fixation, Virgilia.
References
Ainsworth EA, Rogers A, Nelson R, Long SP (2004) Testing the ‘source–sink’ hypothesis of down-regulation of hypothesis in elevated [CO2] in the field with single gene substitutions in Glycine max. Agricultural and Forest Meteorology 122, 85–94.| Testing the ‘source–sink’ hypothesis of down-regulation of hypothesis in elevated [CO2] in the field with single gene substitutions in Glycine max.Crossref | GoogleScholarGoogle Scholar |
Al-Niemi TS, Kahn ML, McDermott TR (1998) Phosphorus uptake by bean nodules. Plant and Soil 198, 71–78.
| Phosphorus uptake by bean nodules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhvFKmu7w%3D&md5=1cc871909d700caed192e593412dbb66CAS |
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=f45d28c8aa18527143c9f7b7cd66bb9eCAS |
Bazzaz FA (1997) Allocation of resources in plants: state of science and critical questions. In ‘Plant resource allocation’. (Eds FA Bazzaz, J Grace) pp. 1–37. (Academic Press: San Diego, CA)
Bieleski RL (1973) Phosphate pools, phosphate transport, and phosphate availability. Annual Review of Plant Physiology 24, 225–252.
| Phosphate pools, phosphate transport, and phosphate availability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXltFeitbY%3D&md5=19704fd5a74dea689619444df4652925CAS |
Bordeleau LM, Prevost 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=cb29945e294860beeee12c325d43281eCAS |
Correa OS, Barneix AJ (1997) Cellular mechanisms of pH tolerance in Rhizobium loti. World Journal of Microbiology and Biotechnology 13, 153–157.
| Cellular mechanisms of pH tolerance in Rhizobium loti.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjtVGgtbs%3D&md5=ff236f28d202261a067e5d3bccad045cCAS |
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=4ef7d1deaec3cd2fab8d11e8a08ce0b9CAS |
Dinkelaker B, Hengeler C, Marschner H (1995) Distribution and function of proteoid roots and other root clusters. Botanica Acta 108, 183–200.
| Distribution and function of proteoid roots and other root clusters.Crossref | GoogleScholarGoogle Scholar |
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=f5988251fc8c21da4366d0f7475d4a86CAS |
Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology 40, 503–537.
| Carbon isotope discrimination and photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXktlKmu70%3D&md5=136c49a5bf26dfb3f52abb3d4ecc03e0CAS |
Gilbert GA, Knight JD, Vance CP, Allan DL (1999) Acid phosphatase activity in phosphorus-deficient white lupin roots. Plant, Cell and Environment 22, 801–810.
| Acid phosphatase activity in phosphorus-deficient white lupin roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlsFGnsr8%3D&md5=05169b42c4e9ed233d861dd451292412CAS |
Gilroy S, Jones DL (2000) Through form to function: root hair development and nutrition uptake. Trends in Plant Science 5, 56–60.
| Through form to function: root hair development and nutrition uptake.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M7jt12nsw%3D%3D&md5=5479f5308097a3c6166f4c9d3fe6f41aCAS | 10664614PubMed |
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.)
Gordon AJ, Kessler W, Minchin FR (1990) Defoliation-induced stress in nodules of white clover. I. Changes in physiological parameters and protein synthesis. Journal of Experimental Botany 41, 1245–1253.
| Defoliation-induced stress in nodules of white clover. I. Changes in physiological parameters and protein synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXpvVGmsw%3D%3D&md5=37d37321fc35762f6fd4aac906dbd360CAS |
Gordon AJ, Kessler W, Minchin FR, Skot L, James CL (1997) Stress-induced decline in soybean N2 fixation is related to nodule sucrose synthase activity. Plant Physiology 114, 937–946.
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=a61de08eb1e49af81ac9bc5f42e15916CAS |
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=5c732f51570296b6c63a7fe2d56a8924CAS |
Grigg AM, Veneklass EJ, Lambers H (2008) Water relations and mineral nutrition of closely related woody plant species on desert dunes and interdunes. Australian Journal of Botany 56, 27–43.
| Water relations and mineral nutrition of closely related woody plant species on desert dunes and interdunes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFymtLw%3D&md5=2c0a8b9e4974872b0b6faf050ab8bfc6CAS |
Groves RH (1983) ‘Nutrient cycling in Australian heath and South African fynbos.’ (Springer-Verlag: Berlin)
Harrison MT, Edwards EJ, Farquhar GD, Nicotra AB, Evans JR (2009) Nitrogen in cell walls of sclerophyllous leaves accounts for little of the variation in photosynthetic nitrogen-use-efficiency. Plant, Cell and Environment 32, 259–270.
| Nitrogen in cell walls of sclerophyllous leaves accounts for little of the variation in photosynthetic nitrogen-use-efficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsVKlsLw%3D&md5=83ccd3fda0b34fb22a37551d1a3cbaa9CAS | 19054350PubMed |
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 |
Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant and Soil 237, 173–195.
| Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovVWlsQ%3D%3D&md5=9004d339d2a399d376e3f81cad08732cCAS |
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=c964d613c4589cc8e84e9f4d9cb6e700CAS |
Israel DW (1987) Investigation of the role of phosphorus in symbiotic dinitrogen. Plant Physiology 84, 835–840.
| Investigation of the role of phosphorus in symbiotic dinitrogen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXltFakt7g%3D&md5=ac4f33538158ebe18fe135afe9973454CAS | 16665531PubMed |
Jones DL (1998) Organic acids in the rhizosphere: a critical review. Plant and Soil 205, 25–44.
| Organic acids in the rhizosphere: a critical review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhtlGjs78%3D&md5=2ba08e296cb8f7509773bf165f731cdeCAS |
Jungk A, Seeling B, Gerke J (1993) Mobilisation of different phosphate fractions in the rhizosphere. Plant and Soil 156, 91–94.
| Mobilisation of different phosphate fractions in the rhizosphere.Crossref | GoogleScholarGoogle Scholar |
Juszczuk IM, Rychter AM (2002) Pyruvate accumulation during phosphate deficiency stress of bean roots. Plant Physiology and Biochemistry 40, 783–788.
| Pyruvate accumulation during phosphate deficiency stress of bean roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xnt1Ggtb4%3D&md5=0128286e6328fa925ce229aefe5b71a3CAS |
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 and 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=599dee9ba7bdd7e6c2bd4a066d6a81f5CAS |
Kaschuk G, Kuyper TW, Leffelaar PA, Hungria M, Giller KE (2009) Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biology and Biochemistry 41, 1233–1244.
| Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtVGktbo%3D&md5=3b8d661e5233b5c22f04d81431fa6305CAS |
Kaschuk G, Hungria M, Leffelaar PA, Giller KE, Kuyper TW (2010a) Differences in photosynthetic behaviour and leaf senescence of soybean (Glycine max [L.] Merrill) dependent on N2 fixation or nitrate supply. Plant Biology 12, 60–69.
| Differences in photosynthetic behaviour and leaf senescence of soybean (Glycine max [L.] Merrill) dependent on N2 fixation or nitrate supply.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlslWqtrY%3D&md5=67e6f845c71c3e22cb1bc62060aebae3CAS | 20653888PubMed |
Kaschuk G, Leffelaar PA, Giller KE, Alberton O, Hungria M, Kuyper TW (2010b) Responses of legumes to rhizobia and arbuscular mycorrhizal fungi: a meta-analysis of potential photosynthate limitation of symbioses. Soil Biology and Biochemistry 42, 125–127.
| Responses of legumes to rhizobia and arbuscular mycorrhizal fungi: a meta-analysis of potential photosynthate limitation of symbioses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVGrtLfE&md5=6c36cf4f2f9f90cb97b531426e2f3295CAS |
Koide RT, Goff MD, Dickie IA (2000) Components of growth efficiencies on mycorrhizal and non-mycorrhizal plants. New Phytologist 148, 163–168.
| Components of growth efficiencies on mycorrhizal and non-mycorrhizal plants.Crossref | GoogleScholarGoogle Scholar |
Kruger FJ, Mitchell DT, Jarvis JUM (1983) ‘Mediterranean-type ecosystems. The role of nutrients.’ (Springer-Verlag: Berlin)
Lajtha K, Harrison AF (1995) Strategies of phosphorus acquisition and conservation by plants species and communities. In ‘Phosphorus in the global environment’. (Ed. H Tissen) pp. 140–147. (John Wiley Sons: Chichester, UK)
Lamont BB (2003) Structure, ecology and physiology of root clusters: a review. Plant and Soil 248, 1–9.
| Structure, ecology and physiology of root clusters: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtFCqs7s%3D&md5=324b1c82a25b8a9ff21e780abd7022b7CAS |
Le Roux MR, Kahn S, Valentine AJ (2008) Organic acid accumulation inhibits N2 fixation in P stressed lupin nodules. New Phytologist 177, 956–964.
| Organic acid accumulation inhibits N2 fixation in P stressed lupin nodules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktVSnsLk%3D&md5=070d3ad629e0ce4bb1aeefbd265e3efbCAS | 18069956PubMed |
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=36ec231aff485e82037767996aed37c2CAS |
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)
Lynch JP, Beebe SE (1995) Adaptations of bean (Phaseolus vulgaris L.) to low phosphorus availability. HortScience 30, 1165–1171.
Lynch JP, Brown KM (2001) Topsoil foraging-an architectural adaptations of plants to low phosphorus. Plant and Soil 237, 225–237.
| Topsoil foraging-an architectural adaptations of plants to low phosphorus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovVWltA%3D%3D&md5=9e634f2da28b841af93504bde22d38e5CAS |
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=6c040ce5e9b44d5abec556913341f132CAS |
Marschner H (1995) ‘Mineral nutrition in plants.’ 2nd edn. (Academic: San Diego, CA)
Maseko ST, Dakora FP (2013) Plant Enzymes, root exudates, cluster roots and mycorrhizal symbiosis are the driver of P nutrition in native legumes growing in P deficient soil of the Cape Fynbos in South Africa. Journal of Agricultural Science and Technology 3, 331–340.
Mengel K (1994) Symbiotic dinitrogen fixation-its dependence on plant nutrition and its ecophysiological impact. Zeitschrift für Pflanzenernährung und Bodenkunde 157, 233–241.
Mitchell DT, Brown G, Jongens-Roberts SM (1984) Variation and forms of phosphorus in the sandy soils coastal fynbos, southern-western Cape. Journal of Ecology 72, 575–584.
| Variation and forms of phosphorus in the sandy soils coastal fynbos, southern-western Cape.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXls12rsrg%3D&md5=d520d7019f84b31ae7d26bffc8a24bcbCAS |
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=bc78e864e931d0c584b5365088782ba6CAS | 15883853PubMed |
Mortimer PE, Perez-Fernandez MA, Valentine AJ (2008) The role of arbuscular mycorrhizal colonisation in the carbon and nutrient economy of the tripartite symbiosis with nodulated Phaseolus vulgaris. Soil Biology and Biochemistry 40, 1019–1027.
| The role of arbuscular mycorrhizal colonisation in the carbon and nutrient economy of the tripartite symbiosis with nodulated Phaseolus vulgaris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXksVKru7c%3D&md5=34752c61c7b554ccf3ddb9269fc5f6f1CAS |
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 and 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=ecc6771783a6a288575898ca50353fc1CAS |
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 assessing using 15N natural abundance. Plant and Soil 209, 181–186.
| Nitrogen nutrition in nodulated field plants of the shrub tea legume Aspalathus linearis assessing using 15N natural abundance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlt1emsrw%3D&md5=5ab695e397a06c4f6d71076d2a12050aCAS |
Neumann G, Martinoia E (2002) Cluster root- an underground adaptation for survival in extreme environments. Trends in Plant Science 7, 162–167.
| Cluster root- an underground adaptation for survival in extreme environments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjtVKnsbY%3D&md5=649c1b3cbf74458c659b6069af9a054bCAS | 11950612PubMed |
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=ed2b7781fdd89fc3707f6464a5145f73CAS | 11283178PubMed |
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=1197313fe8a2f0f3f51cac250f2a1a59CAS |
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.
Plaxton WC, Carswell MC (1999) Metabolic aspects of the phosphate starvation response in plants. In ‘Plant responses to environmental stress: from phytohormones to genome reorganisation’. (Ed. HR Lerner) pp. 350–372. (Marcel-Decker: New York)
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=da909e8069c6f07d08ea30251e65f242CAS |
Raghothama KG (1999) Phosphate acquisition. Annual Review of Plant Physiology and Plant Molecular Biology 50, 665–693.
| Phosphate acquisition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkt1yktrs%3D&md5=d7c5df202ff4d3000a97d47a650e0d30CAS | 15012223PubMed |
Richardson AE (1994) Soil microorganisms and phosphorus availability. In ‘Soil biota: management in sustainable farming systems’. (Eds CE Pankhurst, BD Doube, VVSR Gupta, PR Grace) pp. 50–60. (CSIRO: Melbourne)
Ryan PR, Delhaise E, Jones DL (2001) Function and mechanism of organic anion exudation from roots. Annual Review of Plant Physiology and Plant Molecular Biology 52, 527–560.
| Function and mechanism of organic anion exudation from roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkslWgsbg%3D&md5=91e69caed65b0c103adcb7cc7e9acaaeCAS | 11337408PubMed |
Rychter AM, Mikulska M (1990) The relationship between phosphate status and cyanide-resistant respiration in bean roots. Physiologia Plantarum 79, 663–667.
| The relationship between phosphate status and cyanide-resistant respiration in bean roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXlslWjsro%3D&md5=426f9f2f3a34510286ae4cec9914464eCAS | 21087276PubMed |
Sa TM, Israel DW (1991) Energy status and function of phosphorus deficient soybeans nodules. Plant Physiology 97, 928–935.
| Energy status and function of phosphorus deficient soybeans nodules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XktVCjtA%3D%3D&md5=f82904af1edb3c00ef5edad0fa7fc116CAS | 16668533PubMed |
Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiology 116, 447–453.
| Phosphorus uptake by plants: from soil to cell.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXht1ajtbc%3D&md5=e9ced15bcd4b16b542a93014493e6f87CAS | 9490752PubMed |
Shearer G, Kohl DH (1986) N2-fixation in field settings: estimations based on natural 15N abundance. Australian Journal of Plant Physiology 13, 699–756.
Spriggs AC, Dakora FD (2008) Field assessment of symbiotic N2 fixation in wild and cultivated Cyclopia species in the South African fynbos by 15N natural abundance. Tree Physiology 29, 239–247.
| Field assessment of symbiotic N2 fixation in wild and cultivated Cyclopia species in the South African fynbos by 15N natural abundance.Crossref | GoogleScholarGoogle Scholar | 19203949PubMed |
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=afdf358e6bce256868489a53409a0b9aCAS |
Uhde-Stone C, Gilbert G, Johnson JMF, Litjens R, Zinn KE, Temple SJ, Vance CP, Allan DL (2003a) 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=68daab1da024739c1c0f02b42a97de12CAS |
Uhde-Stone C, Zinn KE, Ramerez-Yanez M, Li A, Vance CP, Allan DL (2003b) Nylon filters arrays reveal differential gene expression in proteoid roots of white lupin in response to P deficiency. Plant Physiology 131, 1064–1079.
| Nylon filters arrays reveal differential gene expression in proteoid roots of white lupin in response to P deficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXisFemu74%3D&md5=6bff6b6bf8560e0975d341af0ce2f9cfCAS | 12644659PubMed |
Vadez V, Beck DP, Lasso JH, Drevon JJ (1997) Utilisation of acetylene reduction assay to screen for tolerance of symbiotic N2 fixation to limitation P nutrition in common bean. Physiologia Plantarum 99, 227–232.
| Utilisation 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=b101ea721581b8ee421316e48d7753d4CAS |
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=e0b55789efe26ce5ac76ae505c253c89CAS | 11598215PubMed |
Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a non-renewable resource. New Phytologist 157, 423–447.
| Phosphorus acquisition and use: critical adaptations by plants for securing a non-renewable resource.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXisF2gu70%3D&md5=6475fd5c3e1e1eea82a67eb0e2194ff5CAS |
Von Uexkull HR, Mutert E (1998) Global extent, development and economic impact of acid soils. In ‘Plant–soil interaction at low pH: principles and management’. (Eds RA Date, NJ Grundon NJ, GE Payment, ME Probert) pp. 5–9. (Kluwer Academic Publisher: Dordrecth, The Netherlands)
Williams K, Percival F, Merino J, Mooney HA (1987) Estimation of tissue construction cost from heat of combustion and organic nitrogen content. Plant, Cell and Environment 10, 725–734.
