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Spatial and temporal variation in organic acid anion exudation and nutrient anion uptake in the rhizosphere of Lupinus albus L.

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Abstract

We investigated in situ the temporal patterns and spatial extent of organic acid anion exudation into the rhizosphere solution of Lupinus albus, and its relation with the nutrient anions phosphate, nitrate and sulfate by means of a rhizobox micro suction cup method under P sufficient conditions. We compared the soil solution in the rhizosphere of cluster roots with that in the vicinity of normal roots, nodules and bulk soil. Compared to the other rhizosphere and soil compartments, concentrations of organic acid anions were higher in the vicinity of cluster roots during the exudative burst (citrate, oxalate) and nodules (acetate, malate), while concentrations of inorganic nutrient anions were highest in the bulk soil. Both active cluster roots and nodules were most efficient in taking up nitrate and phosphate. The intensity of citrate exudation by cluster roots was highly variable. The overall temporal patterns during the lifetime of cluster roots were overlaid by a diurnal pattern, i.e. in most cases, the exudation burst consisted of one or more peaks occurring in the afternoon. Multiple exudation peaks occurred daily or were separated by 1 or 2 days. Although citrate concentrations decreased with distance from the cluster root apex, they were still significantly higher at a distance of 6 to 10 mm than in the bulk soil. Phosphate concentrations were extremely variable in the proximity of cluster roots. While our results indicate that under P sufficient conditions cluster roots take up phosphate during their entire life time, the influence of citrate exudation on phosphate mobilization from soil could not be assessed conclusively because of the complex interactions between P uptake, organic acid anion exudation and P mobilization. However, we observed indications of P mobilization concurrent with the highest measured citrate concentrations. In conclusion, this study provides semiquantitative in situ data on the reactivity of different root segments of L. albus L. in terms of root exudation and nutrient uptake under nutrient sufficient conditions, in particular on the temporal variability during the lifetime of cluster roots.

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References

  • Arocena JM, Göttlein A, Raidl S (2004) Spatial changes of soil solution and mineral composition in the rhizosphere of Norway-spruce seedlings colonized by Piloderma croceum. J Plant Nutr Soil Sci 67:479–486

    Article  CAS  Google Scholar 

  • Bayon RCL, Weisskopf L, Martinoia E, Jansa J, Frossard E, Keller F, Föllmi KB, Gobat J-M (2006) Soil phosphorus uptake by continuously cropped Lupinus albus: a new microcosm design. Plant Soil 283:309–321

    Article  CAS  Google Scholar 

  • Darrah PR (1991) Measuring the diffusion coefficients of rhizosphere exudates in soil II. The diffusion of sorbing compounds. J Soil Sci 42:421–436

    Article  CAS  Google Scholar 

  • Dessureault-Rompré J, Nowack B, Schulin R, Luster J (2006) Modified micro suction cup/rhizobox approach for the in-situ detection of organic acids in rhizosphere soil solution. Plant Soil 286:99–107

    Article  CAS  Google Scholar 

  • Dieffenbach A, Göttlein A, Matzner E (1997) In-situ soil solution chemistry in an acid forest soil as influenced by growing roots of Norway spruce (Picea abies [L.] Karst.). Plant Soil 192:57–61

    Article  CAS  Google Scholar 

  • 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 Environ 12:285–292

    Article  CAS  Google Scholar 

  • Dinkelaker B, Hengeler C, Marschner H (1995) Distribution and function of proteoid roots and other root clusters. Bot Acta 108:183–200

    Google Scholar 

  • Egle K, Römer W, Keller H (2003) Exudation of low molecular weight organic acids by Lupinus albus L., Lupinus angustifolius L. and Lupinus luteus L. as affected by phosphorus supply. Agronomie 23:511–518

    Article  CAS  Google Scholar 

  • Gardner WK, Boundy KA (1983) The acquisition of phosphorus by Lupinus albus L. IV. The effect of interplanting wheat and white lupin on the growth and mineral composition of the two species. Plant Soil 70:391–402

    Article  CAS  Google Scholar 

  • Gardner WK, Parbery DG (1982a) The acquisition of phosphorus by Lupinus albus L. I. Some characteristics of the soil/root interface. Plant Soil 68:19–32

    Article  CAS  Google Scholar 

  • Gardner WK, Parbery DG (1982b) The acquisition of phosphorus by Lupinus albus L. II. The effect of varying phosphorus supply and soil type on some characteristics of the soil/root interface. Plant Soil 68:33–41

    Article  CAS  Google Scholar 

  • Gardner WK, Barber DA, Parbery DG (1983a) The acquisition of phosphorus by Lupinus albus L. III. The probable mechanism by which phosphorus movement in the soil/root interface is enhanced. Plant Soil 70:107–124

    Article  CAS  Google Scholar 

  • Gardner WK, Parbery DG, Barber DA, Swinden L (1983b) The acquisition of phosphorus by Lupinus albus L. V. The diffusion of exudates away from roots: a computer simulation. Plant Soil 72:13–29

    Article  CAS  Google 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 aluminium in the proteoid rhizosphere in samples of an oxisol and luvisol. J Plant Nutr Soil Sci 157:289–294

    Article  CAS  Google Scholar 

  • 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. J Plant Nutr Soil Sci 163:207–212

    Article  CAS  Google Scholar 

  • Gilbert GA, Knight JD, Vance CP, Allan DL (2000) Proteoid root development of phosphorus deficient Lupin is mimicked by auxin and phosphonate. Ann Bot 85:921–928

    Article  CAS  Google Scholar 

  • Göttlein A, Hell U, Blasek R (1996) A system for microscale tensiometry and lysimetry. Geoderma 69:147–156

    Article  Google Scholar 

  • Göttlein A, Heim A, Matzner E (1999) Mobilization of aluminium in the rhizosphere soil solution of growing tree roots in an acidic soil. Plant Soil 211:41–49

    Article  Google Scholar 

  • Hagström J, James WM, Skene KR (2001) A comparison of structure, development and function in cluster roots of Lupinus albus L. under phosphate and iron stress. Plant Soil 232:81–90

    Article  Google Scholar 

  • Hue NV, Craddock GR, Adams F (1986) Effect of organic acids on aluminium toxicity in subsoils. Soil Sci Soc Am J 50:28–34

    Article  CAS  Google Scholar 

  • Johnson SE, Loeppert RH (2006) Role of organic acids in phosphate mobilization from Iron oxide. Soil Sci Soc Am J 70:222–234

    Article  CAS  Google Scholar 

  • Johnson JF, Allan DL, Vance CP Weiblen G (1996) Root carbon dioxide fixation by phosphorus-deficient Lupinus albus. Plant Physiol 112:19–30

    Article  PubMed  CAS  Google Scholar 

  • Jones DL (1998) Organic acids in the rhizosphere—a critical review. Plant Soil 205:25–44

    Article  CAS  Google Scholar 

  • Jones DL, Darrah PR (1994) Role of root derived organic acids in the mobilization of nutrients from the rhizosphere. Plant Soil 166:247–257

    Article  CAS  Google Scholar 

  • Jones DL, Dennis PG, Owen G, Hees PW (2003) Organic acid behavior in soil-misconceptions and knowledge gaps. Plant Soil 248:31–41

    Article  CAS  Google Scholar 

  • Keerthisinghe G, Hocking P, Ryan PR, Delhaize E (1998) Proteoid roots of lupin (Lupinus albus L.): Effect of phosphorus supply on formation and spatial variation in citrate efflux and enzymes activity. Plant Cell Environ 21:476–478

    Article  Google Scholar 

  • Kuo S (1996) Phosphorus. In Methods of Soil Analysis, Part 3: Chemical Methods. Soil Science Society of America, Ed D L Sparks. pp 869–919, Madison, Wisc.

  • Lambers H, Colmer TD (2005) Root physiology—from gene to function. Plant Soil 274:vii–xv

    Article  CAS  Google Scholar 

  • Li MG, Shinano T, Tadano T (1997) Distribution of exudates of Lupin roots in the rhizosphere under phosphorus deficient conditions. Soil Sci Plant Nutr 43:237–245

    CAS  Google Scholar 

  • Liang R, Li C (2003) Differences in cluster-root formation and carboxylate exudation in Lupinus albus L. under different nutrient deficiencies. Plant Soil 248:221–227

    Article  CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants. Academic, London

    Google Scholar 

  • Neumann G, Martinoia E (2002) Cluster roots—an underground adaptation for survival un extreme environments. Trends Plant Sci 7:162–167

    Article  PubMed  CAS  Google Scholar 

  • Neumann G, Römheld V (2000) The release of root exudates as affected by plant’s physiological status. In The rhizosphere: biochemistry and organic substances in the soil–plant interface. Marcel Deker, New York

    Google Scholar 

  • Neumann G, Massonneau A, Martinoia E, Römheld V (1999) Physiological adaptation to phosphorus deficiency during proteoid root development in white lupin. Planta 208:373–382

    Article  CAS  Google Scholar 

  • Peek CS, Robson AD, Kuo J (2003) The formation morphology and anatomy of cluster root of Lupinus albus L. as dependent on soil type and phosphorus supply. Plant Soil 248:237–246

    Article  CAS  Google Scholar 

  • Penaloza E, Corcuera LJ, Martinez J (2002) Spatial and temporal variation in citrate and malate exudation and tissue concentration as affected by P stress in roots of white lupin. Plant Soil 241:209–221

    Article  CAS  Google Scholar 

  • Raghothama KG, Karthikeyan AS (2005) Phosphate acquisition. Plant Soil 274:37–49

    Article  CAS  Google Scholar 

  • Ryan PR, Delhaize E Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Physiol Plant Mol Biol 52:527–560

    Article  PubMed  CAS  Google Scholar 

  • Shane MW, Lambers H (2005) Cluster roots: a curiosity in context. Plant Soil 274:101–125

    Article  CAS  Google Scholar 

  • Shen J, Tang C, Rengel Z, Zhang F (2004) Root-induced acidification an excess cation uptake by N2-fixing Lupinus albus grown in phosphorus deficient soil. Plant Soil 260:69–77

    Article  CAS  Google Scholar 

  • 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 Soil 276:85–94

    Article  CAS  Google Scholar 

  • Skene KR (2003) The evolution of physiology and development in the cluster root: teaching an old dog new tricks? Plant Soil 248:21–30

    Article  CAS  Google Scholar 

  • Skene KR, Raven JA, Sprent JI (1998) Cluster root development in Grevillea robusta (Proteaceae). I. Xylem, pericycle, cortex, and epidermis development in a determinate root. New Phytol 138:725–732

    Article  Google Scholar 

  • Vetterlein D, Jahn R (2004) Gradients in soil solution composition between bulk soil and rhizosphere: in situ measurement with changing soil water content. Plant Soil 258:307–317

    Article  CAS  Google Scholar 

  • Vetterlein D, Marschner H (1993) Use of a microtensiometer technique to study hydraulic lift in a sandy soil planted with pearl millet (Pennisetum americanum [L.] Leeke). Plant Soil 149:275–282

    Article  Google Scholar 

  • Vetterlein D, Marschner H, Horn R (1993) Microtensiometer technique for in situ measurement of soil matric potential and root water extraction from sandy soil. Plant Soil 149:263–273

    Article  Google Scholar 

  • Wang ZY, Kelly JM, Kovar JL (2004) In situ dynamics of phosphorus in the rhizosphere solution of five species. J Environ Qual 33:1387–1392

    Article  PubMed  CAS  Google Scholar 

  • Watt M, Evans JR (1999a) Linking development and determinacy with organic acid efflux from proteoid roots of white lupin grown with low phosphorus and ambient or elevated atmospheric CO2 concentration. Plant Physiol 120:705–716

    Article  PubMed  CAS  Google Scholar 

  • Watt M, Evans JR (1999b) Proteoid Roots. Physiology and development. Plant Physiol 121:317–323

    Article  PubMed  CAS  Google Scholar 

  • Weisskopf L, Abou-Mansour E, Fromin N, Tomasi N, Santelia D, Edelkott I, Neumann G, Aragno M, Tabacchi R, Martinoia E (2006) White lupin has developed a complex strategy to limit microbial degradation of secreted citrate required for phosphate acquisition. Plant Cell Environ 29:919–927

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This work was supported by project C02.0084, State Secretariat for Research and Education, Switzerland, within COST Action 631 (Understanding and Modelling Plant–Soil Interactions In the Rhizosphere Environment) and the Fond Québécois de la Recherche sur la Nature et les Technologies. The rhizoboxes were designed and produced by Arthur Kölliker, WSL. Lena Püschel helped with the set-up of the rhizoboxes and the intensive sampling of soil solutions.

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Authors and Affiliations

  1. Institute of Terrestrial Ecosystems (ITES), ETH Zurich, Zurich, Switzerland

    J. Dessureault-Rompré, B. Nowack & R. Schulin

  2. Swiss Federal Institute for Forest, Snow, and Landscape Research (WSL), Birmensdorf, Switzerland

    J. Luster

  3. Empa—Materials Science and Technology, Lerchenfeldstrasse 5, CH-9014, St. Gallen, Switzerland

    B. Nowack

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  1. J. Dessureault-Rompré
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  3. R. Schulin
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  4. J. Luster
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Correspondence to B. Nowack.

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Responsible Editor: Philippe Hinsinger.

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Dessureault-Rompré, J., Nowack, B., Schulin, R. et al. Spatial and temporal variation in organic acid anion exudation and nutrient anion uptake in the rhizosphere of Lupinus albus L.. Plant Soil 301, 123–134 (2007). https://doi.org/10.1007/s11104-007-9427-x

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