Competition between plant and bacterial cells at the microscale regulates the dynamics of nitrogen acquisition in wheat (Triticum aestivum)

New Phytologist

Volumn 200, Issue 3, 2013, Pages 796-807

  Jones, David L ^a   Clode, Peta L ^b   Kilburn, Matt R ^b   Stockdale, Elizabeth A ^c   Murphy, Daniel V ^b  

^a BANGOR UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Amino acids; Dissolved organic nitrogen; NanoSIMS; Nitrogen cycling; Nutrient uptake; Rhizobacteria; Rhizosphere architecture

Indexed keywords

DISSOLVED ORGANIC NITROGEN; INTERSPECIFIC COMPETITION; ION; MASS SPECTROMETRY; NITROGEN; NUTRIENT UPTAKE; NUTRITION; PLANT; RHIZOBACTERIUM; RHIZOSPHERE; SURVIVAL; TRANSFORMATION; WHEAT;

BACTERIA (MICROORGANISMS); RHIZOBIALES; TRITICUM AESTIVUM;

AMINO ACID; AMMONIUM DERIVATIVE; DISSOLVED ORGANIC NITROGEN; GLUTAMIC ACID; NITROGEN;

ARTICLE; BACTERIUM; CHEMISTRY; METABOLISM; MICROBIOLOGY; NANOSIMS; NITROGEN CYCLING; NUTRIENT UPTAKE; PLANT ROOT; RHIZOBACTERIA; RHIZOSPHERE; RHIZOSPHERE ARCHITECTURE; SOIL; WHEAT;

AMINO ACIDS; DISSOLVED ORGANIC NITROGEN; NANOSIMS; NITROGEN CYCLING; NUTRIENT UPTAKE; RHIZOBACTERIA; RHIZOSPHERE ARCHITECTURE;

AMMONIUM COMPOUNDS; BACTERIA; GLUTAMIC ACID; NITROGEN; NITROGEN ISOTOPES; PLANT ROOTS; RHIZOSPHERE; SOIL; SOIL MICROBIOLOGY; TRITICUM;

EID: 84885427024     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12405     Document Type: Article

References (58)

1. Abaas E, Hill PW, Roberts P, Murphy DV, Jones DL. 2012. Microbial activity differentially regulates the vertical mobility of nitrogen compounds in soil. Soil Biology & Biochemistry 53: 120-123.
2. Anraku Y. 1980. Transport and utilization of amino acids by bacteria. In: Payne JW, ed. Microorganisms and nitrogen sources. New York, NY, USA: Wiley, 9-33.
3. Ayers WA, Thornton RH. 1968. Exudation of amino-acids by intact and damaged roots of wheat and peas. Plant and Soil 18: 193-207.
4. Boddy E, Roberts P, Hill PW, Farrar J, Jones DL. 2008. Turnover of low molecular weight dissolved organic C (DOC) and microbial C exhibit different temperature sensitivities in Arctic tundra soils. Soil Biology & Biochemistry 40: 1557-1566.
5. 15N analysis. Soil Science Society of America Journal 53: 1707-1711.
6. Clode PL, Kilburn MR, Jones DL, Stockdale EA, Cliff JB, Herrmann AM, Murphy DV. 2009. In situ mapping of nutrient uptake in the rhizosphere using nanoscale secondary ion mass spectrometry. Plant Physiology 151: 1751-1757.
7. Cobelli C, Foster D, Toffolo G. 2001. Tracer kinetics in biomedical research: from data to model. New York, NY, USA: Springer.
8. Dempster DN, Jones DL, Murphy DV. 2012. Organic nitrogen mineralisation in two contrasting agro-ecosystems is unchanged by biochar addition. Soil Biology & Biochemistry 48: 47-50.
9. Denison RF, Bledsoe C, Kahn M, O'Gara F, Simms EL, Thomashow LS. 2003. Cooperation in the rhizosphere and the "free rider" problem. Ecology 84: 838-845.
10. Forde BG, Walch-Liu P. 2009. Nitrate and glutamate as environmental cues for behavioural responses in plant roots. Plant, Cell & Environment 32: 682-693.
11. Forgeard F, Frenot Y. 1996. Effects of burning on heathland soil chemical properties: an experimental study on the effect of heating and ash deposits. Journal of Applied Ecology 33: 803-811.
12. Forsum O, Svennerstam H, Ganeteg U, Näsholm T. 2008. Capacities and constraints of amino acid utilization in Arabidopsis. New Phytologist 179: 1058-1069.
13. Frensch J, Hsiao TC, Steudle E. 1996. Water and solute transport along developing maize roots. Planta 198: 348-355.
14. Friedel JK, Scheller E. 2002. Composition of hydrolysable amino acids in soil organic matter and soil microbial biomass. Soil Biology & Biochemistry 34: 315-325.
15. Gattolin S, Newbury HJ, Bale JS, Tseng HM, Barrett DA, Pritchard J. 2008. A diurnal component to the variation in sieve tube amino acid content in wheat. Plant Physiology 147: 912-921.
16. Glass ADM, Britto DT, Kaiser BN, Kinghorn JR, Kronzucker HJ, Kumar A, Okamoto M, Rawat S, Siddiqi MY, Unkles SE et al. 2002. The regulation of nitrate and ammonium transport systems in plants. Journal of Experimental Botany 53: 855-864.
17. Hawkins HJ, Johansen A, George E. 2000. Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi. Plant and Soil 226: 275-285.
18. Herrmann AM, Clode PL, Fletcher IR, Nunan N, Stockdale EA, O'Donnel AG, Murphy DV. 2007. A novel method for the study of the biophysical interface in soils using nano-scale secondary ion mass spectrometry. Rapid Communications in Mass Spectrometry 21: 29-34.
19. Hill PW, Farrell M, Jones DL. 2012. Bigger may be better in soil N cycling: does rapid acquisition of small L-peptides by soil microbes dominate fluxes of protein-derived N in soil? Soil Biology & Biochemistry 48: 106-112.
20. Hill PW, Quilliam RS, DeLuca TH, Farrar J, Farrell M, Roberts P, Newsham KK, Hopkins DW, Bardgett RD, Jones DL. 2011. Acquisition and assimilation of nitrogen as peptide-bound and D-enantiomers of amino acids by wheat. PLoS ONE 6: e19220.
21. Inselsbacher E, Näsholm T. 2012. The below-ground perspective of forest plants: soil provides mainly organic nitrogen for plants and mycorrhizal fungi. New Phytologist 195: 329-334.
22. Jones DL, Darrah PR. 1994. Amino-acid influx at the soil-root interface of Zea mays L. and its implications in the rhizosphere. Plant and Soil 163: 1-12.
23. Jones DL, Healey JR, Willett VB, Farrar JF, Hodge A. 2005a. Dissolved organic nitrogen uptake by plants - an important N uptake pathway? Soil Biology & Biochemistry 37: 413-423.
24. Jones DL, Hodge A. 1999. Biodegradation kinetics and sorption reactions of three differently charged amino acids in soil and their effects on plant organic nitrogen availability. Soil Biology & Biochemistry 31: 1331-1342.
25. Jones DL, Nguyen C, Finlay RD. 2009. Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant and Soil 321: 5-33.
26. Jones DL, Owen AG, Farrar JF. 2002. Simple method to enable the high resolution determination of total free amino acids in soil solutions and soil extracts. Soil Biology & Biochemistry 34: 1893-1902.
27. Jones DL, Shannon D, Junvee-Fortune T, Farrar JF. 2005b. Plant capture of free amino acids is maximized under high soil amino acid concentrations. Soil Biology & Biochemistry 37: 179-181.
28. Jörgensen RG. 1996. Quantification of the microbial biomass by determining ninhydrin-reactive N. Soil Biology and Biochemistry 28: 301-306.
29. 4 soil extracts. Soil Biology & Biochemistry 22: 1023-1027.
30. Kuzyakov Y, Jones DL. 2006. Glucose uptake by maize roots and its transformation in the rhizosphere. Soil Biology & Biochemistry 38: 851-860.
31. Loomis RS, Connor DJ. 1992. Crop ecology. Cambridge, UK: Cambridge University Press.
32. Manzoni S, Porporato A, Schimel JP. 2008. Soil heterogeneity in lumped mineralization-immobilization models. Soil Biology & Biochemistry 40: 1137-1148.
33. Marschner P, Crowley D, Rengel Z. 2011. Rhizosphere interactions between microorganisms and plants govern iron and phosphorus acquisition along the root axis - model and research methods. Soil Biology & Biochemistry 43: 883-894.
34. Mays ET, Feldhoff RC, Nettleton GS. 1984. Determination of protein loss during aqueous and phase partition fixation using formalin and glutaraldehyde. Journal of Histochemistry & Cytochemistry 32: 1107-1112.
35. McKee HS. 1962. Nitrogen metabolism in plants. Oxford, UK: Clarendon Press.
36. Miller AJ, Cookson SJ, Smith SJ, Wells DM. 2001. The use of microelectrodes to investigate compartmentation and the transport of metabolized inorganic ions in plants. Journal of Experimental Botany 52: 541-549.
37. Mosier AR, Syers JK, Freney JR. 2004. Agriculture and the nitrogen cycle: assessing the impacts of fertilizer use on food production and the environment. Washington, DC, USA: Island Press.
38. Mulvaney RL. 1996. Nitrogen - inorganic forms. In: Sparks DL, ed. Methods of soil analysis. Madison, WI, USA: Soil Science Society of America, American Society of Agronomy Inc, 1123-1184.
39. 15N pool dilution techniques. Advances in Agronomy 79: 69-118.
40. Näsholm T, Huss-Danell K, Hogberg P. 2001. Uptake of glycine by field grown wheat. New Phytologist 150: 59-63.
41. Näsholm T, Kielland K, Ganeteg U. 2009. Uptake of organic nitrogen by plants. New Phytologist 182: 31-48.
42. Owen AG, Jones DL. 2001. Competition for amino acids between wheat roots and rhizosphere microorganisms and the role of amino acids in plant N acquisition. Soil Biology & Biochemistry 33: 651-657.
43. Pernice M, Meibom A, Van Den Heuvel A, Kopp C, Domart-Coulon I, Hoegh-Guldberg O, Dove S. 2012. A single-cell view of ammonium assimilation in coral-dinoflagellate symbiosis. ISME Journal 6: 1314-1324.
44. Persson J, Näsholm T. 2001. A GC-MS method for determination of amino acid uptake by plants. Physiologia Plantarum 113: 352-358.
45. Peteranderl R, Lechene C. 2004. Measure of carbon and nitrogen stable isotope ratios in cultured cells. Journal of the American Society for Mass Spectrometry 15: 478-485.
46. Phillips DA, Fox TC, King MD, Bhuvaneswari TV, Teuber LR. 2004. Microbial products trigger amino acid exudation from plant roots. Plant Physiology 136: 2887-2894.
47. Rasmussen J, Sauheitl L, Eriksen J, Kuzyakov Y. 2010. Plant uptake of dual-labeled organic N biased by inorganic C uptake: results of a triple labeling study. Soil Biology & Biochemistry 42: 524-527.
48. Reeve JR, Smith JL, Carpenter-Boggs L, Reganold JP. 2009. Glycine, nitrate, and ammonium uptake by classic and modern wheat varieties in a short-term microcosm study. Biology and Fertility of Soils 45: 723-732.
49. Roberts P, Stockdale R, Khalid M, Iqbal Z, Jones DL. 2009. Carbon-to-nitrogen ratio is a poor predictor of low molecular weight organic nitrogen mineralization in soil. Soil Biology & Biochemistry 41: 1750-1752.
50. 4 soil extracts. Soil Biology & Biochemistry 42: 2331-2335.
51. Sadras VO, Lawson C. 2013. Nitrogen and water-use efficiency of Australian wheat varieties released between 1958 and 2007. European Journal of Agronomy 46: 34-41.
52. Sauheitl L, Glaser B, Weigelt A. 2009. Advantages of compound-specific stable isotope measurements over bulk measurements in studies on plant uptake of intact amino acids. Rapid Communications in Mass Spectrometry 23: 3333-3342.
53. Schreiber L. 2010. Transport barriers made of cutin, suberin and associated waxes. Trends in Plant Science 15: 546-553.
54. Sivaguru M, Pike S, Gassmann W, Baskin TI. 2003. Aluminum rapidly depolymerizes cortical microtubules and depolarizes the plasma membrane: evidence that these responses are mediated by a glutamate receptor. Plant and Cell Physiology 44: 667-675.
55. Soper FM, Paungfoo-Lonhienne C, Brackin R, Rentsch D, Schmidt S, Robinson N. 2011. Arabidopsis and Lobelia anceps access small peptides as a nitrogen source for growth. Functional Plant Biology 38: 788-796.
56. Thornton B. 2001. Uptake of glycine by non-mycorrhizal Lolium perenne. Journal of Experimental Botany 52: 1315-1322.
57. Warren CR. 2012. Post-uptake metabolism affects quantification of amino acid uptake. New Phytologist 193: 522-531.
58. Yuan L, Loque D, Kojima S, Rauch S, Ishiyama K, Inoue E, Takahashi H, von Wiren N. 2007. The organization of high-affinity ammonium uptake in Arabidopsis roots depends on the spatial arrangement and biochemical properties of AMT1-type transporters. Plant Cell 19: 2636-2652.