Phosphorus starvation boosts carboxylate secretion in P-deficient genotypes of Lupinus angustifolius with contrasting root structure
Ying L. Chen A B E , Vanessa M. Dunbabin C , Art J. Diggle D , Kadambot H. M. Siddique B and Zed Rengel A B EA Soil Science and Plant Nutrition, School of Earth and Environment (M087), The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
B The UWA Institute of Agriculture, The University of Western Australia (M082), 35 Stirling Highway, Crawley, WA 6009, Australia.
C Tasmanian Institute of Agriculture, The University of Tasmania, Private Bag 54, Hobart, Tas. 7000, Australia.
D The Department of Agriculture and Food, Western Australia, Locked Bag 4, Bentley, WA 6983, Australia.
E Corresponding authors. Emails: yinglongchen@hotmail.com; zed.rengel@uwa.edu.au
Crop and Pasture Science 64(6) 588-599 https://doi.org/10.1071/CP13012
Submitted: 8 January 2013 Accepted: 8 July 2013 Published: 23 August 2013
Abstract
Lupinus angustifolius L. (narrow-leafed lupin) is an important grain legume crop for the stockfeed industry in Australia. This species does not form cluster roots regardless of phosphorus (P) nutrition. We hypothesise that this species may have adaptive strategies for achieving critical P uptake in low-P environments by altering shoot growth and root architecture and secreting carboxylates from roots. Three wild genotypes of L. angustifolius with contrasting root architecture were selected to investigate the influence of P starvation on root growth and rhizosphere carboxylate exudation and their relationship with P acquisition. Plants were grown in sterilised loamy soil supplied with zero, low (50 μm) or optimal (400 μm) P for 6 weeks. All genotypes showed a significant response in shoot and root development to varying P supply. At P deficit (zero and low P), root systems were smaller and had fewer branches than did roots at optimal P. The amount of total carboxylates in the rhizosphere extracts ranged from 3.4 to 17.3 μmol g–1 dry root. The total carboxylates comprised primarily citrate (61–78% in various P treatments), followed by malate and acetate. Genotype #085 (large root system with deep lateral roots) exuded the greatest amount of total carboxylates to the rhizosphere for each P treatment, followed by #016 (medium root system with good branched lateral roots) and #044 (small root system with short and sparse lateral roots). All genotypes in the low-P treatment significantly enhanced exudation of carboxylates, whereas no significant increase in carboxylate exudation was observed in the zero-P treatment. Small-rooted genotypes had higher P concentration than the medium- and large-rooted genotypes, although larger plants accumulated higher total P content. Large-rooted genotypes increased shoot P utilisation efficiency in response to P starvation. This study showed that narrow-leafed lupin genotypes differing in root architecture differed in carboxylate exudation and P uptake. Our finding suggested that for L. angustifolius there is a minimum plant P concentration below which carboxylate exudation is not enhanced despite severe P deficiency. The outcomes of this study enhance our understanding of P acquisition strategies in L. angustifolius genotypes, which can be used for the selection of P-efficient genotypes for cropping systems.
Additional keywords: intraspecific variation, narrow-leafed lupin, organic acid anions, P-use efficiency, root architecture, root exudation, root–soil interaction.
References
Adams MA, Pate JS (1992) Availability of organic and inorganic forms of phosphorus to lupins (Lupinus spp.). Plant and Soil 145, 107–113.| Availability of organic and inorganic forms of phosphorus to lupins (Lupinus spp.).Crossref | GoogleScholarGoogle Scholar |
Allen DG, Jeffrey RC (1990) ‘Methods of analysis of phosphorus in Western Australian soils.’ (Chemistry Centre of WA: Bentley, W. Aust.)
Ao J, Fu AJ, Tian J, Yan X, Hong L (2010) Genetic variability for root morph-architecture traits and root growth dynamics as related to phosphorus efficiency in soybean. Functional Plant Biology 37, 304–312.
| Genetic variability for root morph-architecture traits and root growth dynamics as related to phosphorus efficiency in soybean.Crossref | GoogleScholarGoogle Scholar |
Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annual Review of Plant Biology 57, 233–266.
| The role of root exudates in rhizosphere interactions with plants and other organisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVKhtr8%3D&md5=46ab069eac082ed231465761d857989dCAS | 16669762PubMed |
Barea JM, Pozo MJ, Azcon R, Azcon-Aguilar C (2005) Microbial co-operation in the rhizosphere. Journal of Experimental Botany 56, 1761–1778.
| Microbial co-operation in the rhizosphere.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpvFKnt7g%3D&md5=3be11e2a83ceab09a60a04defddd4510CAS | 15911555PubMed |
Barrow NJ, Mendoza RE (1990) Equations for describing sigmoid yield responses and their application to some phosphate responses by lupins and by subterranean clover. Fertilizer Research 22, 181–188.
| Equations for describing sigmoid yield responses and their application to some phosphate responses by lupins and by subterranean clover.Crossref | GoogleScholarGoogle Scholar |
Bassett J, Denney RC, Jeffery GH, Mendham J (1978) ‘Vogel’s textbook of quantitative inorganic analysis including elementary instrumental analysis.’ 4th edn (Longman: London & New York)
Blair GJ, Chinoim N, Lefroy RDB, Anderson C, Crocker GJ (1991) A soil sulfur test for pastures and crops. Australian Journal of Soil Research 29, 619–626.
| A soil sulfur test for pastures and crops.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXmsFGjtr4%3D&md5=db131431eba4700fbdc978353aa53e7dCAS |
Bolland MDA, Siddique KHM, Loss SP, Baker MJ (1999) Comparing responses of grain legumes, wheat and canola to applications of superphosphate. Nutrient Cycling in Agroecosystems 53, 157–175.
| Comparing responses of grain legumes, wheat and canola to applications of superphosphate.Crossref | GoogleScholarGoogle Scholar |
Bucher M, Rausch C, Daram P (2001) Molecular and biochemical mechanisms of phosphorus uptake into plants. Journal of Plant Nutrition and Soil Science 164, 209–217.
| Molecular and biochemical mechanisms of phosphorus uptake into plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtlOrtLY%3D&md5=24819afd6161eb67bc5e1b9c3f7bab40CAS |
Buirchell BJ (2008) Narrow-leafed lupin breeding in Australia—Where to from here? In ‘Lupins for health and wealth. Proceedings of the 12th International Lupin Conference’. (Eds JA Palta, JB Berger) pp. 226–230. (International Lupin Association: Canterbury, New Zealand)
Cawthray GR (2003) Improved reversed-phase-liquid chromatography method for the analysis of low-molecular-weight organic acids in plant root exudates. Journal of Chromatography. A 1011, 233–240.
| Improved reversed-phase-liquid chromatography method for the analysis of low-molecular-weight organic acids in plant root exudates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXms1ygur8%3D&md5=f185e8d811bc0d35170bdeb4e64902a3CAS | 14518781PubMed |
Chen YL, Dunbabin VM, Diggle AJ, Siddique KHM, Rengel Z (2011a) Development of a novel semi-hydroponic phenotyping system for studying root architecture. Functional Plant Biology 38, 355–363.
| Development of a novel semi-hydroponic phenotyping system for studying root architecture.Crossref | GoogleScholarGoogle Scholar |
Chen YL, Dunbabin VM, Postma J, Diggle AJ, Palta JA, Lynch JP, Siddique KHM, Rengel Z (2011b) Phenotypic variability and modelling of root structure of wild Lupinus angustifolius genotypes. Plant and Soil 348, 345–364.
| Phenotypic variability and modelling of root structure of wild Lupinus angustifolius genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1Gnt7rE&md5=d7ad816144a2986c6a24b90a8c119826CAS |
Chen YL, Dunbabin VM, Diggle AJ, Siddique KHM, Rengel Z (2012) Assessing variability in root parameters of wild Lupinus angustifolius germplasm: basis for modelling root system structure. Plant and Soil 354, 141–155.
| Assessing variability in root parameters of wild Lupinus angustifolius germplasm: basis for modelling root system structure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlvFWgtb8%3D&md5=937fb94c1cfeb569f57e7fd8922a1bdbCAS |
Chen YL, Dunbabin VM, Postma JA, Diggle AJ, Siddique KHM, Rengel Z (2013) Modelling root plasticity and response of narrow-leafed lupin to heterogeneous phosphorus supply. Plant and Soil
| Modelling root plasticity and response of narrow-leafed lupin to heterogeneous phosphorus supply.Crossref | GoogleScholarGoogle Scholar |
Clements JC, Cowling WA (1991) Catalogue of the Australian lupin collection including field evaluation data for wild, semi-domesticated and fully domesticated accessions. Research Report 3/91. Department of Agriculture Western Australia, South Perth, W. Aust.
Colwell JD (1965) An automatic procedure for the determination of phosphorus in sodium hydrogen carbonate extracts of soils. Chemistry & Industry 21, 893–895.
Coudert Y, Périn C, Courtois B, Khong NG, Gantet P (2010) Genetic control of root development in rice, the model cereal. Trends in Plant Science 15, 219–226.
| Genetic control of root development in rice, the model cereal.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXks1WksLw%3D&md5=e332cc98f2b127981eba7abffa873ab4CAS | 20153971PubMed |
Dunbabin VM (2007) Simulating the role of rooting traits in crop-weed competition. Field Crops Research 104, 44–51.
| Simulating the role of rooting traits in crop-weed competition.Crossref | GoogleScholarGoogle Scholar |
Fitter AH, Stickland TR (1991) Architectural analysis of plant root systems. 2. Influence of nutrient supply on architecture in contrasting plant species. New Phytologist 118, 383–389.
| Architectural analysis of plant root systems. 2. Influence of nutrient supply on architecture in contrasting plant species.Crossref | GoogleScholarGoogle Scholar |
Gahoonia TS, Nielsen NE (1996) Variation in acquisition of soil phosphorus by wheat and barley genotypes. Plant and Soil 178, 223–230.
| Variation in acquisition of soil phosphorus by wheat and barley genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XitVahsLw%3D&md5=176b5926086b4037b21bc13eae29f08fCAS |
Gahoonia TS, Nielsen NE (2004) Root traits as tools for creating phosphorus efficient crop varieties. Plant and Soil 260, 47–57.
| Root traits as tools for creating phosphorus efficient crop varieties.Crossref | GoogleScholarGoogle Scholar |
Gerke J, Römer W, Jungk A (1994) The excretion of citric and malic acid by proteoid roots of Lupinus albus L., effects on soil solution concentrations of phosphate, iron, and aluminum in the proteoid rhizosphere in amples of an oxisol and a luvisol. Zeitschrift für Pflanzenernährung, Düngung Bodenkunde 157, 289–294.
Gerke J, Beissner L, Römer W (2000) The quantitative effect of chemical phosphate mobilization by carboxylate anions on P uptake by a single root. I. The basic concept and determination of soil parameters. Journal of Plant Nutrition and Soil Science 163, 207–212.
| The quantitative effect of chemical phosphate mobilization by carboxylate anions on P uptake by a single root. I. The basic concept and determination of soil parameters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXivVKnsrc%3D&md5=842fc4a279df161fe502ad203f800887CAS |
Gewin V (2010) An underground revolution. Nature 466, 552–553.
| An underground revolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpsFWku74%3D&md5=ba030176d5afc166379f6c02087ea56cCAS | 20671689PubMed |
Gollany HT, Schumacher TE (1993) Combined use of colorimetric and microelectrode methods for evaluating rhizosphere pH. Plant and Soil 154, 151–159.
| Combined use of colorimetric and microelectrode methods for evaluating rhizosphere pH.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXis12kuw%3D%3D&md5=9b65b49372f222b57f9a6a54f2acc9e6CAS |
Greenhill N (1985) ‘Soils 020, available copper and zinc in soil.’ (State Chemistry Laboratory: Werribee, Vic.)
Gregory PJ, Bengough AG, Grinev D, Schmidt S, Thomas WTB, Wojciechowski T, Young M (2009) Root phenomics of crops: opportunities and challenges. Functional Plant Biology 36, 922–929.
| Root phenomics of crops: opportunities and challenges.Crossref | GoogleScholarGoogle Scholar |
Hammond JP, Broadley MR, White PJ, King GJ, Bowen HC, Hayden R, Meacham MC, Mead A, Overs T, Spracklen WP, Greenwood DJ (2009) Shoot yield drives phosphorus use efficiency in Brassica oleracea and correlates with root architecture traits. Journal of Experimental Botany 60, 1953–1968.
| Shoot yield drives phosphorus use efficiency in Brassica oleracea and correlates with root architecture traits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtFSjtbY%3D&md5=034df31fb900a6fe0f991a7a7522543dCAS | 19346243PubMed |
Hedley MJ, Nye PH, White RE (1982) Plant induced changes in the rhizosphere of rape (Brassica napus var. Emerald) seedlings. II. Origin of pH change. New Phytologist 91, 31–44.
| Plant induced changes in the rhizosphere of rape (Brassica napus var. Emerald) seedlings. II. Origin of pH change.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XktVGhtr8%3D&md5=821c672df7e116e5cbacd8d04761e1b0CAS |
Hocking PJ, Jeffery S (2004) Cluster-root production and organic acid exudation in a group of old-world lupins and a new-world lupin. Plant and Soil 258, 135–150.
| Cluster-root production and organic acid exudation in a group of old-world lupins and a new-world lupin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjvF2qsL8%3D&md5=1b3f9a642941b925c06b9a066b04993cCAS |
Holford ICR (1997) Soil phosphorus: its measurement, and its uptake by plants. Australian Journal of Soil Research 35, 227–239.
| Soil phosphorus: its measurement, and its uptake by plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXisVeitrk%3D&md5=984c5df40d9098a80db41acd516e33c8CAS |
Howieson JG, Robson AD, Abbott LK (1992) Acid-tolerant species of medicago produce root exudates at low pH which induce the expression of nodulation genes in Rhizobium meliloti. Australian Journal of Plant Physiology 19, 287–296.
| Acid-tolerant species of medicago produce root exudates at low pH which induce the expression of nodulation genes in Rhizobium meliloti.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xlt1yhsLw%3D&md5=f615e066b2fd19bfa8ce0c2c4ad1d980CAS |
Isbell RF (1996) ‘The Australian Soil Classification.’ (CSIRO Publishing: Melbourne)
Jones D, Farrar J (1999) Phosphorus mobilization by root exudates in the rhizosphere: fact or fiction? Agroforest Forum 9, 20–25.
Koide RT (1991) Nutrient supply, nutrient demand and plant response to mycorrhizal infection. New Phytologist 117, 365–386.
| Nutrient supply, nutrient demand and plant response to mycorrhizal infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXkt1yisbw%3D&md5=4feb105a017324bf6d3ecbde75933db0CAS |
Lambers H, Juniper D, Cawthray GR, Veneklaas EJ, Martínez-Ferri E (2002) The pattern of carboxylate exudation in Banksia grandis (Proteaceae) is affected by the form of phosphate added to the soil. Plant and Soil 238, 111–122.
| The pattern of carboxylate exudation in Banksia grandis (Proteaceae) is affected by the form of phosphate added to the soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xit1Gru7g%3D&md5=ca984057d755778325ef8e2cc4a4c530CAS |
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 |
Loss SP, Robson AD, Ritchie GSP (1994) Nutrient uptake and organic acid anion metabolism in lupins and peas supplied with nitrate. Annals of Botany 74, 69–74.
Lynch JP, Beebe SE (1995) Adaptation of bean (Phaseolus vulgaris L.) to low phosphorus availability. The Journal of Horticultural Science & Biotechnology 30, 1165–1171.
Neumann G (2007) Root exudates and nutrient cycling. In ‘Nutrient cycling in terrestrial ecosystems’. Book Series, Soil Biology. Vol. 10. (Eds Z Rengel, P Marschner) pp. 123–157. (Springer Verlag: Berlin)
Neumann G, Martinoia E (2002) Cluster roots: an underground adaptation for survival in extreme environments. Trends in Plant Science 7, 162–167.
| Cluster roots: an underground adaptation for survival in extreme environments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjtVKnsbY%3D&md5=a286333de4a14d1c134400200fe65bbcCAS | 11950612PubMed |
Nielsen KL, Eshel A, 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=076d47cba8c1d878a9a9b1d4ca54a6a8CAS | 11283178PubMed |
Niu YF, Chai RS, Jin GL, Wang Hm Tang CX, Zhang YS (2012) Responses of root architecture development to low phosphorus availability: a review. Annuals of Botany 112, 391–408.
| Responses of root architecture development to low phosphorus availability: a review.Crossref | GoogleScholarGoogle Scholar |
Noruésis MJ (2011) ‘IBM SPSS Statistics 19 Guide to Data Analysis.’ (Pearson Education, Pearson Schweiz: Zug, Switzerland)
Ochoa IE, Blair MW, Lynch JP (2006) QTL analysis of adventitious root formation in common bean (Phaseolus vulgaris L.) under contrasting phosphorus availability. Crop Science 46, 1609–1621.
| QTL analysis of adventitious root formation in common bean (Phaseolus vulgaris L.) under contrasting phosphorus availability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotV2jurg%3D&md5=e228fa64bc3a7237fc378d65079e58feCAS |
Palta JA, Watt M (2009) Vigorous crop root systems: form and function for improving the capture of water and nutrients. In ‘Applied crop physiology: boundaries between genetic improvement and agronomy’. (Eds VO Sadras, DF Calderini) pp. 309–325. (Academic Press: San Diego, CA)
Pearse SJ, Veneklaas EJ, Cawthray GR, Bolland MDA, Lambers H (2006) 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 |
Postma JA, Lynch JP (2011) Theoretical evidence for the functional benefit of root cortical aerenchyma in soils with low phosphorus availability. Annals of Botany 107, 829–841.
| Theoretical evidence for the functional benefit of root cortical aerenchyma in soils with low phosphorus availability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkvFahs70%3D&md5=147b8b57a86d5b6f857721543670fa83CAS | 20971728PubMed |
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 |
Rayment GE, Higginson FR (1992) ‘Australian laboratory handbook of soil and water chemical methods.’ pp. 15−23. (Inkata Press: Melbourne)
Rengel Z (2002) Genetic control of root exudation. Plant and Soil 245, 59–70.
| Genetic control of root exudation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvVCitrw%3D&md5=9ca3cfddbc3f998efb72123739a668a4CAS |
Roelofs RFR, Rengel Z, Cawthray GR, Dixon KW, Lambers H (2001) Exudation of carboxylates in Australian Proteaceae: chemical composition. Plant, Cell & Environment 24, 891–904.
| Exudation of carboxylates in Australian Proteaceae: chemical composition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXntVKgtr4%3D&md5=724cebc3db58a0dc9fdb5ab863daa081CAS |
Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annual Review of Plant Physiology and Plant Molecular Biology 52, 527–560.
| Function and mechanism of organic anion exudation from plant roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkslWgsbg%3D&md5=5918da9e9112b09be4d9f237e933f74aCAS | 11337408PubMed |
Sánchez-Calderón L, López-Bucio J, Chacón-López A, Gutiérrez-Ortega A, Hernández-Abreu E, Herrera-Estrella L (2005) Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. Plant & Cell Physiology 46, 174–184.
| Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Sánchez-Calderón L, López-Bucio J, Chacón-López A, Gutiérrez-Ortega A, Hernández-Abreu E, Herrera-Estrella L (2006) Characterization of low phosphorus insensitive mutants reveals a crosstalk between low phosphorus-induced determinate root development and the activation of genes involved in the adaptation of Arabidopsis to phosphorus deficiency. Plant Physiology 140, 879–889.
| Characterization of low phosphorus insensitive mutants reveals a crosstalk between low phosphorus-induced determinate root development and the activation of genes involved in the adaptation of Arabidopsis to phosphorus deficiency.Crossref | GoogleScholarGoogle Scholar | 16443695PubMed |
Schefe CR, Watt M, Slattery WJ, Mele PM (2008) Organic anions in the rhizosphere of Al-tolerant and Al-sensitive wheat lines grown in an acid soil in controlled and field environments. Australian Journal of Soil Research 46, 257–264.
| Organic anions in the rhizosphere of Al-tolerant and Al-sensitive wheat lines grown in an acid soil in controlled and field environments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlt1Ogsbg%3D&md5=0411e4ebc3ae9873c7fa7c7ff6c0f1fcCAS |
Schjørring JK (1986) Nitrate and ammonium absorption by plants growing at a sufficient or insufficient level of phosphorus in nutrient solution. Plant and Soil 91, 313–318.
| Nitrate and ammonium absorption by plants growing at a sufficient or insufficient level of phosphorus in nutrient solution.Crossref | GoogleScholarGoogle Scholar |
Searle PL (1984) The bertholet or indophenol reaction and its use in the analytical chemistry of nitrogen. Analyst 109, 549–568.
| The bertholet or indophenol reaction and its use in the analytical chemistry of nitrogen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXlsVartbk%3D&md5=9f35c2051c55191b6078a34e4ee05218CAS |
Shane MW, De Vos M, De Roock S, Lambers H (2003) Shoot P status regulates cluster-root growth and citrate exudation in Lupinus albus grown with a divided root system. Plant, Cell & Environment 26, 265–273.
| Shoot P status regulates cluster-root growth and citrate exudation in Lupinus albus grown with a divided root system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhslOgur8%3D&md5=bc67f0a2b939ba33483cf54db9cabf8cCAS |
Shi S, Condron L, Larsen T, Richardson AE, Jones E, Jiao J, O’Callaghan M, Stewart A (2011) In situ sampling of low molecular weight organic anions from rhizosphere of radiata pine (Pinus radiata) grown in a rhizotron system. Environmental and Experimental Botany 70, 131–142.
| In situ sampling of low molecular weight organic anions from rhizosphere of radiata pine (Pinus radiata) grown in a rhizotron system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVGitbvN&md5=637e3737cc6c755736d8e5c6f85a3e2eCAS |
Shu L, Shen J, Rengel Z, Tang C, Zhang F (2005) Growth medium and phosphorus supply affect cluster root formation and citrate exudation by Lupinus albus grown in a sand/solution split-root system. Plant and Soil 276, 85–94.
| Growth medium and phosphorus supply affect cluster root formation and citrate exudation by Lupinus albus grown in a sand/solution split-root system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1KnsL%2FN&md5=47a951075feb41cc9c7a9e991dfb690dCAS |
Shu L, Shen J, Rengel Z, Tang C, Zhang F, Cawthray GR (2007) Formation of cluster roots and citrate exudation by Lupinus albus in response to localized application of different phosphorus sources. Plant Science 172, 1017–1024.
| Formation of cluster roots and citrate exudation by Lupinus albus in response to localized application of different phosphorus sources.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjvFals7w%3D&md5=698760c8654e9e719e7bfcc7e49ce06eCAS |
Svistoonoff S, Creff A, Reymond M, Sigoillot-Claude C, Ricaud L, Blanchet A, Nussaume L, Desnos T (2007) Root tip contact with low-phosphate media reprograms plant root architecture. Nature Genetics 39, 792–796.
| Root tip contact with low-phosphate media reprograms plant root architecture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlvVSgt7c%3D&md5=f20ea50c583397e5da7dbda4cbb87e65CAS | 17496893PubMed |
Tuberosa R, Salvi S, Giuliani S, Sanguineti MC, Frascaroli E, Conti S, Landi P (2011) Genomics of root architecture and functions in maize. In ‘Root genomics’. (Eds A Costa de Oliveira, RK Varshney) pp. 179–204. (Springer Verlag: Berlin)
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=c6e844486cd562c76c91dde70c27419bCAS |
Veneklaas EJ, Stevens J, Cawthray GR, Turner St, Grigg AM, Lamber H (2003) Chickpea and white lupin rhizosphere carboxylates vary with soil properties and enhance phosphorus uptake. Plant and Soil 248, 187–197.
| Chickpea and white lupin rhizosphere carboxylates vary with soil properties and enhance phosphorus uptake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtFCqs7k%3D&md5=25d3e3fd0219f0f35313adee632f72acCAS |
Vranova V, Rejsek K, Skene KR, Janous D, Formanek P (2013) Methods of collection of plant root exudates in relation to plant metabolism and purpose: a review. Journal of Plant Nutrition and Soil Science 176, 175–199.
| Methods of collection of plant root exudates in relation to plant metabolism and purpose: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXks1Gmurs%3D&md5=d43e72158a98230cb7cef9cc52d7bb6bCAS |
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.
| An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaA2cXitlGmug%3D%3D&md5=957f700a6b66cf2eb603b12d8cbab216CAS |
Wang B, Shen J, Tang C, Rengel Z (2008) Root morphology, proton release, and carboxylate exudation in lupin in response to phosphorus deficiency. Journal of Plant Nutrition and Soil Science 31, 557–570.
Wouterlood M, Cawthray GR, Scanlon TT, Lambers H, Veneklaas EJ (2004a) Carboxylate concentrations in the rhizosphere of lateral roots of chickpea (Cicer arietinum) increase during plant development, but are not correlated with phosphorus status of soil or plants. New Phytologist 162, 745–753.
| Carboxylate concentrations in the rhizosphere of lateral roots of chickpea (Cicer arietinum) increase during plant development, but are not correlated with phosphorus status of soil or plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltlyrsrg%3D&md5=0eadea4f3791472402e9e0c63ade26f7CAS |
Wouterlood M, Cawthray GR, Turner S, Lambers H, Veneklaas EJ (2004b) Rhizosphere carboxylate concentrations of chickpea are affected by genotype and soil type. Plant and Soil 261, 1–10.
| Rhizosphere carboxylate concentrations of chickpea are affected by genotype and soil type.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvVehtL8%3D&md5=d7e847398590ea4e9e4b5fd26b74d203CAS |
Zhu J, Mickelson SM, Kaeppler SM, Lynch JP (2006) Detection of quantitative trait loci for seminal root traits in maize (Zea mays L.) seedlings grown under differential phosphorus levels. Theoretical and Applied Genetics 113, 1–10.
| Detection of quantitative trait loci for seminal root traits in maize (Zea mays L.) seedlings grown under differential phosphorus levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlvVGru74%3D&md5=3eeb0309966ae31069d2fd61fd329af1CAS | 16783587PubMed |