Rhizosphere properties in monocropping and intercropping systems between faba bean (Vicia faba L.) and maize (Zea mays L.) grown in a calcareous soil
Haigang Li A C , Fusuo Zhang A , Zed Rengel B and Jianbo Shen A
+ Author Affiliations
- Author Affiliations
A Center for Resources, Environment and Food Security, China Agricultural University, Beijing 100193, China.
B Soil Science and Plant Nutrition, School of Earth and Environment, The UWA Institute of Agriculture, The University of Western Australia, Crawley, WA 6009, Australia.
C Corresponding author. Email: haigangli@cau.edu.cn
Crop and Pasture Science 64(10) 976-984 https://doi.org/10.1071/CP13268
Submitted: 31 July 2013 Accepted: 5 November 2013 Published: 13 December 2013
Abstract
The processes involving pH modification, carboxylate exudation and phosphorus (P) dynamics in the rhizosphere of crops grown in intercropping are poorly understood. Two groups of maize (Zea mays L.) or faba bean (Vicia faba L.) plants (monocropping) or one group of plant of each species (intercropping) were grown between three 1-mm-thick soil layers; the central soil layer is referred to as inter-rhizosphere, and the two outer soil layers are designated sole-rhizosphere. Faba bean intercropped with maize had an 11% increase in shoot biomass and a 15% increase in P uptake compared with monocropped faba bean. The cropping pattern did not significantly influence maize growth. After 4 weeks of growth, faba bean significantly decreased soil pH in both the sole- and inter-rhizosphere in monocropping, but no effects were apparent for the intercropping rhizosphere. The major carboxylates in the rhizosphere of faba bean were malate (18–45 nmol g–1 soil) and maleate (1.2–2.4 nmol g–1 soil). Only trace amounts of carboxylates were measured in the rhizosphere of monocropped maize. However, intercropped maize had a high concentration of malate (~11 nmol g–1 soil) in both sole- and inter-rhizosphere; the malate was likely exuded by faba bean and was then diffused to the sole-rhizosphere of intercropped maize. The amount of malate exuded by intercropped faba bean was 19% higher than with monocropped plants. The results indicate that diffusion of protons and carboxylates extended the interaction zone between maize and faba bean, and may have contributed to enhancements of P uptake in the intercropping system.
Additional keywords: carboxylates, malate, mini-rhizobox, phosphorus, rhizosphere pH, root exudation.
References
Ae N, Arihara J, Okada K (1990) Phosphorus uptake by pigeon pea and its role in cropping systems of the Indian subcontinent. Science 248, 477–480.| Phosphorus uptake by pigeon pea and its role in cropping systems of the Indian subcontinent.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXkslOitbw%3D&md5=127a5a716dcbf3e31b5942364d1f9e83CAS | 17815599PubMed |
Bai Z, Li H, Yang X, Zhou B, Shi X, Wang B, Li D, Shen J, Chen Q, Qin W, Oenema O, Zhang F (2013) The critical soil P levels for crop yield, soil fertility and environmental safety in different soil types. Plant and Soil 372, 27–37.
| The critical soil P levels for crop yield, soil fertility and environmental safety in different soil types.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXltl2ku78%3D&md5=fe9aceb52e87574e3872a8c8bf9d5284CAS |
Bao S (1999) ‘Soil chemical analysis.’ (China Agriculture Press: Beijing)[in Chinese]
Bertrand I, Hinsinger P, Jaillard B, Arvieu JC (1999) Dynamics of phosphorus in the rhizosphere of maize and rape grown on synthetic, phosphated calcite and goethite. Plant and Soil 211, 111–119.
| Dynamics of phosphorus in the rhizosphere of maize and rape grown on synthetic, phosphated calcite and goethite.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXnt1Kru7c%3D&md5=27de4270b06757164c1b629318807c0eCAS |
Betencourt E, Duputel M, Colomb B, Desclaux D, Hinsinger P (2012) Intercropping promotes the ability of durum wheat and chickpea to increase rhizosphere phosphorus availability in a low P soil. Soil Biology & Biochemistry 46, 181–190.
| Intercropping promotes the ability of durum wheat and chickpea to increase rhizosphere phosphorus availability in a low P soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XosFCmtA%3D%3D&md5=410c049457f062b5c21bd38f0b76a6b7CAS |
Casarin V, Plassard C, Hinsinger P, Arvieu JC (2004) Quantification of ectomycorrhizal fungal effects on the bioavailability and mobilisation of soil P in the rhizosphere of Pinus pinaster. New Phytologist 163, 177–185.
| Quantification of ectomycorrhizal fungal effects on the bioavailability and mobilisation of soil P in the rhizosphere of Pinus pinaster.Crossref | GoogleScholarGoogle Scholar |
Cu STT, Hutson J, Schuller KA (2005) Mixed culture of wheat (Triticum aestivum L.) with white lupin (Lupinus albus L.) improves the growth and phosphorus nutrition of the wheat. Plant and Soil 272, 143–151.
| Mixed culture of wheat (Triticum aestivum L.) with white lupin (Lupinus albus L.) improves the growth and phosphorus nutrition of the wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXks1ekurY%3D&md5=f1f38fa0cb3d880ceae248dacd2538efCAS |
Desnos T (2008) Root branching responses to phosphate and nitrate. Current Opinion in Plant Biology 11, 82–87.
| Root branching responses to phosphate and nitrate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVeqtb8%3D&md5=3c49af938774d06e4131bbfe85231d99CAS | 18024148PubMed |
Dinkelaker B, Römheld V, Marschner H (1989) Citric acid excretion and precipitation of calcium in the rhizosphere of white lupin (Lupinus albus L.). Plant, Cell & Environment 12, 285–292.
| Citric acid excretion and precipitation of calcium in the rhizosphere of white lupin (Lupinus albus L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXmtFertrY%3D&md5=599383aaf0a7c3dcd058d6e638fb00bfCAS |
Fan X, Tang C, Rengel Z (2002) Nitrate uptake, nitrate reductase distribution and their relation to proton release in five nodulated grain legumes. Annals of Botany 90, 315–323.
| Nitrate uptake, nitrate reductase distribution and their relation to proton release in five nodulated grain legumes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvVOgsrc%3D&md5=97511813ec54f948d44a3b632a391bc7CAS | 12234143PubMed |
Gahoonia TS, Nielsen NE, Joshi PA, Jahoor A (2001) A root hairless barley mutant for elucidating genetic of root hairs and phosphorus uptake. Plant and Soil 235, 211–219.
| A root hairless barley mutant for elucidating genetic of root hairs and phosphorus uptake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXotFahurg%3D&md5=3997855f259e81d66ebd1a0d63abf9e6CAS |
Ge Z, Rubio G, Lynch JP (2000) The importance of root gravitropism for inter-root competition and phosphorus acquisition efficiency: results from a geometric simulation model. Plant and Soil 218, 159–171.
| The importance of root gravitropism for inter-root competition and phosphorus acquisition efficiency: results from a geometric simulation model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhvVGrtLc%3D&md5=b6c62299f2635dd1bcaaa1782ca6b770CAS | 11543364PubMed |
George TS, Richardson AE, Hadobas PA, Simpson RJ (2004) Characterization of transgenic Trifolium subterraneum L. which expresses phyA and releases extracellular phytase: growth and P nutrition in laboratory media and soil. Plant, Cell & Environment 27, 1351–1361.
| Characterization of transgenic Trifolium subterraneum L. which expresses phyA and releases extracellular phytase: growth and P nutrition in laboratory media and soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhs1OqsA%3D%3D&md5=4c233132d431156556a12c1c2e57828bCAS |
Gong Z (1999) ‘Chinese Soil Taxonomy.’ (Science Press: Beijing, China)[in Chinese]
Hinsinger P (1998) How do plant roots acquire mineral nutrients? Chemical processes involved in the rhizosphere. Advances in Agronomy 64, 225–265.
| How do plant roots acquire mineral nutrients? Chemical processes involved in the rhizosphere.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmsVOq&md5=6002d5a7c05a1aefb6c3130324f9ed17CAS |
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=8991bca6a5f81d192cc3ee94d2ed0671CAS |
Hinsinger P, Gilkes RJ (1997) Dissolution of phosphate rock in the rhizosphere of five plant species grown in an acid, P fixing mineral substrate. Geoderma 75, 231–249.
| Dissolution of phosphate rock in the rhizosphere of five plant species grown in an acid, P fixing mineral substrate.Crossref | GoogleScholarGoogle Scholar |
Hinsinger P, Plassard C, Tang C, Jaillard B (2003) Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: A review. Plant and Soil 248, 43–59.
| Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: A review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtFCqsr8%3D&md5=9f468364f5cd8a1aae1c7b03c9e0f94eCAS |
Hinsinger P, Gobran GR, Gregory PJ, Wenzel WW (2005) Rhizosphere geometry and heterogeneity arising from root-mediated physical and chemical processes. New Phytologist 168, 293–303.
| Rhizosphere geometry and heterogeneity arising from root-mediated physical and chemical processes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Smu7bJ&md5=0e818659dc1089b2cee33e49c0b9e66dCAS | 16219069PubMed |
Hinsinger P, Betencourt E, Bernard L, Brauman A, Plassard C, Shen J, Tang X, Zhang F (2011) P for two, sharing a scarce resource: soil phosphorus acquisition in the rhizosphere of intercropped species. Plant Physiology 156, 1078–1086.
| P for two, sharing a scarce resource: soil phosphorus acquisition in the rhizosphere of intercropped species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptFWlu7w%3D&md5=fceda93717f13408aca6a9fff2f5a1faCAS | 21508183PubMed |
Horst BG, Waschkies C (1987) Phosphorus nutrition of spring wheat in mixed culture with white lupin (Lupinus albus L.). Zeitschrift für Pflanzenernährung und Bodenkunde 150, 1–8.
| Phosphorus nutrition of spring wheat in mixed culture with white lupin (Lupinus albus L.).Crossref | GoogleScholarGoogle Scholar |
Jones CA (1983) A survey of the variability in tissue nitrogen and phosphorus concentrations in maize and grain sorghum. Field Crops Research 6, 133–147.
| A survey of the variability in tissue nitrogen and phosphorus concentrations in maize and grain sorghum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXlt1Omu7o%3D&md5=a38a8c6b4e932abc4a21a908eb2a2cfdCAS |
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=44b734cb4650291068518c390ff5d53bCAS |
Jones DL, Dennis PG, Owen AG, Van Hees PAW (2003) Organic acid behavior in soils—misconceptions and knowledge gaps. Plant and Soil 248, 31–41.
| Organic acid behavior in soils—misconceptions and knowledge gaps.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtFCqsro%3D&md5=643549423e8d2ce693d2e0deb4ccbc74CAS |
Kamh M, Horst WJ, Am F, Mostafa H, Maier P (1999) Mobilization of soil and fertilizer phosphate by cover crops. Plant and Soil 211, 19–27.
| Mobilization of soil and fertilizer phosphate by cover crops.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXnt1Krt7c%3D&md5=6db182a9ad801a1e0606242239ff1136CAS |
Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Annals of Botany 98, 693–713.
| Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits.Crossref | GoogleScholarGoogle Scholar | 16769731PubMed |
Li M, Osaki M, Rao IM, Tadano T (1997) Secretion of phytase from the roots of several plant species under phosphorus deficient conditions. Plant and Soil 195, 161–169.
| Secretion of phytase from the roots of several plant species under phosphorus deficient conditions.Crossref | GoogleScholarGoogle Scholar |
Li L, Yang S, Li X, Zhang F, Christie P (1999) Interspecific complementary and competitive interactions between intercropped maize and faba bean. Plant and Soil 212, 105–114.
| Interspecific complementary and competitive interactions between intercropped maize and faba bean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXns1Glu7k%3D&md5=600f24cb66a2b303a96bc9ace9e8016bCAS |
Li L, Zhang F, Li X, Christie P, Sun J, Yang S, Tang C (2003) Interspecific facilitation of nutrient uptake by intercropped maize and faba bean. Nutrient Cycling in Agroecosystems 65, 61–71.
| Interspecific facilitation of nutrient uptake by intercropped maize and faba bean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmvFQ%3D&md5=696f73d8c1ba75f0ef42a54b593d471cCAS |
Li S, Li L, Zhang F, Tang C (2004) Acid phosphatase role in chickpea/maize intercropping. Annals of Botany 94, 297–303.
| Acid phosphatase role in chickpea/maize intercropping.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnsV2ktbo%3D&md5=90695e4c10fcae7b207cf1fd4558df6fCAS | 15238349PubMed |
Li L, Sun J, Zhang F, Guo T (2006) Root distribution and interactions between intercropped species. Oecologia 147, 280–290.
| Root distribution and interactions between intercropped species.Crossref | GoogleScholarGoogle Scholar | 16211394PubMed |
Li L, Li S, Sun J, Zhou L, Bao X, Zhang H, Zhang F (2007) Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus-deficient soils. Proceedings of the National Academy of Sciences of the United States of America 104, 11 192–11 196.
| Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus-deficient soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnvFGgtLc%3D&md5=29d55c1671641c34e3ed14d4f203bda8CAS |
Li H, Shen J, Zhang F, Clairotte M, Drevon JJ, Le Cadre E, Hinsinger P (2008a) Dynamics of phosphorus fractions in the rhizosphere of common bean (Phaseolus vulgaris L.) and durum wheat (Triticum turgidum durum L.) grown in monocropping and intercropping systems. Plant and Soil 312, 139–150.
| Dynamics of phosphorus fractions in the rhizosphere of common bean (Phaseolus vulgaris L.) and durum wheat (Triticum turgidum durum L.) grown in monocropping and intercropping systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1aju7nF&md5=09e7eb592a648ae920936060cc49f143CAS |
Li H, Shen J, Zhang F, Tang C, Lambers H (2008b) Is there a critical level of shoot phosphorus concentration for cluster-root formation in Lupinus albus? Functional Plant Biology 35, 328–336.
| Is there a critical level of shoot phosphorus concentration for cluster-root formation in Lupinus albus? Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmsFOitr4%3D&md5=c8a5067d87621424cdf21850201429bdCAS |
Li H, Shen J, Zhang F, Marschner P, Cawthray G, Rengel Z (2010) Phosphorus uptake and rhizosphere properties of intercropped and monocropped maize, faba bean, and white lupin in acidic soil. Biology and Fertility of Soils 46, 79–91.
| Phosphorus uptake and rhizosphere properties of intercropped and monocropped maize, faba bean, and white lupin in acidic soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktl2lsg%3D%3D&md5=4293279fb770018c84b3a45cb361b506CAS |
Li H, Huang G, Meng Q, Ma L, Yuan L, Wang F, Zhang W, Cui Z, Shen J, Chen X, Jiang R, Zhang F (2011) Integrated soil and plant phosphorus management for crop and environment in China. A review. Plant and Soil 349, 157–167.
| Integrated soil and plant phosphorus management for crop and environment in China. A review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFKntbzK&md5=e697a5b35ecb6c2b8d1ca9718115cd4cCAS |
Lindsay WL (1979) ‘Chemical equilibria in soils.’ (Wiley: New York)
Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta 27, 31–36.
| A modified single solution method for the determination of phosphate in natural waters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF38XksVyntr8%3D&md5=7f2eef87180712cf3b97da6109d6e9ebCAS |
Neumann G, Römheld V (1999) Root excretion of carboxylic acids and protons in phosphorus-deficient plants. Plant and Soil 211, 121–130.
| Root excretion of carboxylic acids and protons in phosphorus-deficient plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXnt1Kqsr4%3D&md5=ee0028f0679ca65a415f0be801eb1dd8CAS |
Neumann G, Massonneau A, Langlade N, Dinkelaker B, Hengeler CH, Römheld V, Martinoia E (2000) Physiological aspects of cluster root function and development in phosphorus-deficient white lupin (Lupinus albus L.). Annals of Botany 85, 909–919.
| Physiological aspects of cluster root function and development in phosphorus-deficient white lupin (Lupinus albus L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjs12hu7o%3D&md5=0cf9fa918676d3a299a495fb83c9722aCAS |
Nuruzzaman M, Lambers H, Bolland MDA, Veneklaas EJ (2006) Distribution of carboxylates and acid phosphatase and depletion of different phosphorus fractions in the rhizosphere of a cereal and three grain legumes. Plant and Soil 281, 109–120.
| Distribution of carboxylates and acid phosphatase and depletion of different phosphorus fractions in the rhizosphere of a cereal and three grain legumes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xktlyhsbw%3D&md5=f67e6d07a55abac304f11e391c070fadCAS |
Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) ‘Estimation of available phosphorus in soils by extraction with sodium bicarbonate.’ Circular No. 939. (United States Department of Agriculture: Washington, DC)
Pearse SJ, Veneklaas EJ, Cawthray GR, Bolland MDA, Lambers H (2006a) Carboxylate release of wheat, canola and 11 grain legume species as affected by phosphorus status. Plant and Soil 288, 127–139.
| Carboxylate release of wheat, canola and 11 grain legume species as affected by phosphorus status.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFaksL7F&md5=5d36e8e5910ea3ec15d2488a3f11d454CAS |
Pearse SJ, Veneklaas EJ, Cawthray G, Bolland MDA, Lambers H (2006b) Triticum aestivum shows a greater biomass response to a supply of aluminium phosphate than Lupinus albus despite releasing fewer carboxylates into the rhizosphere. New Phytologist 169, 515–524.
| Triticum aestivum shows a greater biomass response to a supply of aluminium phosphate than Lupinus albus despite releasing fewer carboxylates into the rhizosphere.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhvV2ju7o%3D&md5=cacd2d5739e1c8499befb8805ac404dcCAS | 16411954PubMed |
Phiri S, Barrios E, Rao LM, Singh BR (2001) Change in soil organic matter and phosphorus fractions under planted fallows and a crop rotation system on a Colombian volcanic-ash soil. Plant and Soil 231, 211–223.
| Change in soil organic matter and phosphorus fractions under planted fallows and a crop rotation system on a Colombian volcanic-ash soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXltVemu7c%3D&md5=573cce497cbd5e18ffd0c30b1790242aCAS |
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=2996c5f4c46878339fe74dbc98ae8ad7CAS | 15012223PubMed |
Raghothama KG, Karthikeyan AS (2005) Phosphate acquisition. Plant and Soil 274, 37–49.
| Phosphate acquisition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVWiurfJ&md5=1507bb662ad79c214d07a3c517d2cde8CAS |
Richardson AE, Hadobas PA, Hayes JE (2000) Acid phosphomonoesterase and phytase activities of wheat (Triticum aestivum L.) roots and utilization of organic phosphorus substrates by seedlings grown in sterile culture. Plant, Cell & Environment 23, 397–405.
| Acid phosphomonoesterase and phytase activities of wheat (Triticum aestivum L.) roots and utilization of organic phosphorus substrates by seedlings grown in sterile culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjsFCktLg%3D&md5=7401ae236bc2fa470ddee8819b4e4b93CAS |
Rose TJ, Damon P, Rengel Z (2010) Phosphorus-efficient faba bean (Vicia faba L.) genotypes enhance subsequent wheat crop growth in an acid and an alkaline soil. Crop & Pasture Science 61, 1009–1016.
| Phosphorus-efficient faba bean (Vicia faba L.) genotypes enhance subsequent wheat crop growth in an acid and an alkaline soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFamtrzI&md5=4ffceb975b0952e7090a8cb831bdc369CAS |
Schubert S, Schubert E, Mengel K (1990) Effect of low pH of the root medium on proton release, growth, and nutrient uptake of field beans (Vicia faba). Plant and Soil 124, 239–244.
| Effect of low pH of the root medium on proton release, growth, and nutrient uptake of field beans (Vicia faba).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXltlWisLw%3D&md5=6186bfbf1a116cc3baca16c96427355bCAS |
Shen J, Rengel Z, Tang C, Zhang F (2003) Role of phosphorus nutrition in development of cluster roots and release of carboxylates in soil-grown Lupinus albus. Plant and Soil 248, 199–206.
| Role of phosphorus nutrition in development of cluster roots and release of carboxylates in soil-grown Lupinus albus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtFCqsr0%3D&md5=cb66536efb88c6215ed9f1a16bf9a57eCAS |
Shen J, Tang C, Rengel Z, Zhang F (2004) Root-induced acidification and excess cation uptake by N2-fixing Lupinus albus grown in phosphorus-deficient soil. Plant and Soil 260, 69–77.
| Root-induced acidification and excess cation uptake by N2-fixing Lupinus albus grown in phosphorus-deficient soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXksFGlt7c%3D&md5=123db4dc97b4e0f59f6ab1b2c370e932CAS |
Shen J, Li H, Neumann G, Zhang F (2005) Nutrient uptake, cluster root formation and exudation of protons and citrate in Lupinus albus as affected by localized supply of phosphorus in a split-root system. Plant Science 168, 837–845.
| Nutrient uptake, cluster root formation and exudation of protons and citrate in Lupinus albus as affected by localized supply of phosphorus in a split-root system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXosVGgsQ%3D%3D&md5=17876bebdc7e97837ada1d10ab311a8eCAS |
Shen J, Yuan L, Zhang J, Li H, Bai Z, Chen X, Zhang W, Zhang F (2011) Phosphorus dynamics: From soil to plant. Plant Physiology 156, 997–1005.
| Phosphorus dynamics: From soil to plant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptFWlur0%3D&md5=f425b6431222e5aabd80e470a73eabd4CAS | 21571668PubMed |
Smith SE, Read DJ (2000) ‘Mycorrhizal symbiosis.’ 3rd edn (Elsevier and Academic Press: New York)
Ström L, Owen AG, Godbold DL, Jones DL (2002) Organic acid mediated P mobilization in the rhizosphere and uptake by maize roots. Soil Biology & Biochemistry 34, 703–710.
| Organic acid mediated P mobilization in the rhizosphere and uptake by maize roots.Crossref | GoogleScholarGoogle Scholar |
Tang C (1998) Factors affecting soil acidification under legumes I. Effect of potassium supply. Plant and Soil 199, 275–282.
| Factors affecting soil acidification under legumes I. Effect of potassium supply.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjslOns7g%3D&md5=92da3371a4adf6a5c79deadb476fdde4CAS |
Tang C, Hinsinger P, Jaillard B, Rengel Z, Drevon JJ (2001) Effect of phosphorus deficiency on the growth, symbiotic N2 fixation and proton release by two bean (Phaseolus vulgaris) genotypes. Agronomie 21, 683–689.
| Effect of phosphorus deficiency on the growth, symbiotic N2 fixation and proton release by two bean (Phaseolus vulgaris) genotypes.Crossref | GoogleScholarGoogle Scholar |
Tang C, Drevon JJ, Jaillard B, Souche G, Hinsinger P (2004) Proton release of two genotypes of bean (Phaseolus vulgaris L.) as affected by N nutrition and P deficiency. Plant and Soil 260, 59–68.
| Proton release of two genotypes of bean (Phaseolus vulgaris L.) as affected by N nutrition and P deficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXksFGlt7s%3D&md5=d614654dbe1f73b7bf32a7611aadbbd9CAS |
Turner BL (2008) Resource partitioning for soil phosphorus: a hypothesis. Journal of Ecology 96, 698–702.
| Resource partitioning for soil phosphorus: a hypothesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXptFygs70%3D&md5=d47eecca44930fbe578014264f29d8f1CAS |
Vance CP (2008) Plants without arbuscular mycorrhizae. In ‘The ecophysiology of plant–phosphorus interactions’. (Eds PJ White, JP Hammond) pp. 117–142. (Springer: Dordrecht, The Netherlands)
Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytologist 157, 423–447.
| Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXisF2gu70%3D&md5=c6e844486cd562c76c91dde70c27419bCAS |
Wang B, Shen J, Zhang W, Zhang F, Neumann G (2007) Citrate exudation from white lupin induced by phosphorus deficiency differs from that induced by aluminum. New Phytologist 169, 515–524.
Wang J, Liu W, Mu H, Dang T (2010) Inorganic phosphorus fractions and phosphorus availability in a calcareous soil receiving 21-year superphosphate application. Pedosphere 20, 304–310.
| Inorganic phosphorus fractions and phosphorus availability in a calcareous soil receiving 21-year superphosphate application.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpslOru78%3D&md5=b9fd0c2d15b2373ba30c82cf4f309b61CAS |
Westerman RL (1990) ‘Soil testing and plant analysis.’ 3rd edn (American Society of Agronomy and Soil Science Society of America: Madison, WI)
Zhou L, Cao J, Zhang F, Li L (2009) Rhizosphere acidification of faba bean, soybean and maize. The Science of the Total Environment 407, 4356–4362.
| Rhizosphere acidification of faba bean, soybean and maize.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlaltLo%3D&md5=619d7439026602649f72a6e3e6862409CAS | 19249080PubMed |
