Plant and Soil

, Volume 406, Issue 1–2, pp 359–374 | Cite as

Simultaneous efflux and uptake of metabolites by roots of wheat

  • Charles R. Warren
Regular Article


Background & aims

Some metabolites (e.g. amino acids) present in root exudates can be taken up by roots, but we do not know if this ability extends to the broader suite of metabolites found in exudates. The aim of this study was to examine the ability of wheat (Triticum aestivum L.) to efflux and take up a broad suite of small metabolites.


Four-week-old plants were placed into an uptake solution that contained a broad suite of 13C-labelled metabolites. Uptake was estimated from the decrease in concentration of the 13C isotopologue in the solution; and from the appearance of 13C isotopologues within roots. Efflux was estimated from appearance of 12C isotopologues in solution.


When wheat plants were placed in 13C-metabolite solutions the concentration of U-13C isotopologues of 37 metabolites decreased – as would be expected if plants were taking up the U-13C metabolites. After 4 h immersion in 13C metabolite solution, roots contained detectable amounts of U-13C isotopologues of 55 metabolites. U-13C isotopologues of organic acids were not detected within roots.


These findings indicate that wheat can take up a broad suite of N-containing metabolites and some sugars, but there was no evidence for uptake of organic acids.


Efflux Uptake Root Mass spectrometry Stable isotope Metabolite 



Charles Warren was supported by a Future Fellowship from the Australian Research Council. The University of Sydney is thanked for financial support via the major equipment scheme.

Supplementary material

11104_2016_2892_MOESM1_ESM.xlsx (16 kb)
Table S1 (XLSX 15 kb)
11104_2016_2892_MOESM2_ESM.xlsx (18 kb)
Table S2 (XLSX 17 kb)
11104_2016_2892_MOESM3_ESM.docx (27 kb)
Note S1 Details of how metabolites were identified. (DOCX 27 kb)


  1. Albrecht G, Mustroph A, Fox TC (2004) Sugar and fructan accumulation during metabolic adjustment between respiration and fermentation under low oxygen conditions in wheat roots. Physiol Plant 120:93–105CrossRefPubMedGoogle Scholar
  2. Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681CrossRefPubMedGoogle Scholar
  3. Bais HP, Loyola-Vargas VM, Flores HE, Vivanco JM (2001) Invited review: root-specific metabolism: the biology and biochemistry of underground organs. In Vitro Cell Dev Biol Plant 37:730–741CrossRefGoogle Scholar
  4. Bais HP, Park SW, Weir TL, Callaway RM, Vivanco JM (2004) How plants communicate using the underground information superhighway. Trends Plant Sci 9:26–32CrossRefPubMedGoogle Scholar
  5. Bajad SU, Lua W, Kimball EH, Yuan J, Peterson C, Rabinowitz JD (2006) Separation and quantitation of water soluble cellular metabolites by hydrophilic interaction chromatography-tandem mass spectrometry. J Chromatogr A 1125:76–88CrossRefPubMedGoogle Scholar
  6. Bardgett RD, Streeter TC, Bol R (2003) Soil microbes compete effectively with plants for organic-nitrogen inputs to temperate grasslands. Ecology 84:1277–1287CrossRefGoogle Scholar
  7. Boddy E, Hill PW, Farrar J, Jones DL (2007) Fast turnover of low molecular weight components of the dissolved organic carbon pool of temperate grassland field soils. Soil Biol Biochem 39:827–835CrossRefGoogle Scholar
  8. Chang CW, Bandurski RS (1964) Exocellular enzymes of corn roots. Plant Physiol 39:60–64CrossRefPubMedPubMedCentralGoogle Scholar
  9. Chaparro JM, Badri DV, Bakker MG, Sugiyama A, Manter DK, Vivanco JM (2013) Root exudation of phytochemicals in Arabidopsis follows specific patterns that are developmentally programmed and correlate with soil microbial functions. Plos One 8Google Scholar
  10. Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245:35–47CrossRefGoogle Scholar
  11. Fan TWM, Lane AN, Shenker M, Bartley JP, Crowley D, Higashi RM (2001) Comprehensive chemical profiling of gramineous plant root exudates using high-resolution NMR and MS. Phytochemistry 57:209–221CrossRefPubMedGoogle Scholar
  12. Farrar J, Hawes M, Jones D, Lindow S (2003) How roots control the flux of carbon to the rhizosphere. Ecol 84:827–837Google Scholar
  13. Flores HE, Vivanco JM, Loyola-Vargas VM (1999) ‘Radicle’ biochemistry: the biology of root-specific metabolism. Trends Plant Sci 4:220–226CrossRefPubMedGoogle Scholar
  14. Grayston SJ, Campbell CD, Vaughan D, Jones D (1995) Influence of root exudate heterogeneity on microbial diversity in the rhizosphere. J Exp Bot 46:27–27CrossRefGoogle Scholar
  15. Grierson PF (1992) Organic-acids in the rhizosphere of Banksia integrifolia LF. Plant Soil 144:259–265CrossRefGoogle Scholar
  16. Hodge A, Robinson D, Fitter A (2000) Are microorganisms more effective than plants at competing for nitrogen? Trends Plant Sci 5:304–308CrossRefPubMedGoogle Scholar
  17. Hutsch BW, Augustin J, MerbachW (2002) Plant rhizodeposition - an important source for carbon turnover in soils. J Plant Nutr Soil Sci-Z Pflanzenernahr Bodenkd 165:397–407Google Scholar
  18. Ivanisevic J, Zhu ZJ, Plate L, Tautenhahn R, Chen S, O'Brien PJ, Johnson CH, Marletta MA, Patti GJ, Siuzdak G (2013) Toward ‘Omic scale metabolite profiling: a dual separation-mass spectrometry approach for coverage of lipid and central carbon metabolism. Anal Chem 85:6876–6884CrossRefPubMedPubMedCentralGoogle Scholar
  19. Jones DL (1998) Organic acids in the rhizosphere—a critical review. Plant Soil 205:25–44Google Scholar
  20. Jones DL, Darrah PR (1993) Influx and efflux of amino-acids from Zea mays L roots and their implications for N-nutrition and the rhizosphere. Plant Soil 156:87–90CrossRefGoogle Scholar
  21. Jones DL, Darrah PR (1994) Amino-acid influx at the soil-root Interface of Zea mays L and its implications in the rhizosphere. Plant Soil 163:1–12Google Scholar
  22. Jones DL, Darrah PR (1995) Influx and efflux of organic-acids across the soil-root Interface of Zea mays L. And its implications in rhizosphere C flow. Plant Soil 173:103–109CrossRefGoogle Scholar
  23. Jones DL, Darrah PR (1996) Re-sorption of organic compounds by roots of Zea mays L and its consequences in the rhizosphere .3. Characteristics of sugar influx and efflux. Plant Soil 178:153–160CrossRefGoogle Scholar
  24. Jones DL, Farrar J, Giller KE (2003) Associative nitrogen fixation and root exudation - what is theoretically possible in the rhizosphere? Symbiosis 35:19–38Google Scholar
  25. Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phytol 163:459–480CrossRefGoogle Scholar
  26. Jones DL, Healey JR, Willett VB, Farrar JF, Hodge A (2005) Dissolved organic nitrogen uptake by plants - an important N uptake pathway? Soil Biol Biochem 37:413–423CrossRefGoogle Scholar
  27. Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant Soil 321:5–33CrossRefGoogle Scholar
  28. Kraffczyk I, Trolldenier G, Beringer H (1984) Soluble root exudates of maize - influence of potassium supply and rhizosphere microorganisms. Soil Biol Biochem 16:315–322CrossRefGoogle Scholar
  29. Kuijken RCP, Snel JFH, Heddes MM, Bouwmeester HJ, Marcelis LFM (2015) The importance of a sterile rhizosphere when phenotyping for root exudation. Plant Soil 387:131–142CrossRefGoogle Scholar
  30. Kuzyakov Y, Domanski G (2000) Carbon input by plants into the soil. Review. Journal of Plant Nutrition and Soil Science-Zeitschrift Fur Pflanzenernahrung Und Bodenkunde 163:421–431CrossRefGoogle Scholar
  31. Marschner H (1986) Mineral nutrition of higher plants. Academic Press, LondonGoogle Scholar
  32. Neumann G, Romheld V (1999) Root excretion of carboxylic acids and protons in phosphorus-deficient plants. Plant Soil 211:121–130CrossRefGoogle Scholar
  33. Nguyen C (2003) Rhizodeposition of organic C by plants: mechanisms and controls. Agronomie 23:375–396CrossRefGoogle Scholar
  34. Perry LG, Thelen GC, Ridenour WM, Weir TL, Callaway RM, Paschke MW, Vivanco JM (2005) Dual role for an allelochemical: (+/−)-catechin from Centaurea maculosa root exudates regulates conspecific seedling establishment. J Ecol 93:1126–1135CrossRefGoogle Scholar
  35. Persson J, Nasholm T (2001) A GC-MS method for determination of amino acid uptake by plants. Physiol Plant 113:352–358CrossRefPubMedGoogle Scholar
  36. Phillips DA, Fox TC, King MD, Bhuvaneswari TV, Teuber LR (2004) Microbial products trigger amino acid exudation from plant roots. Plant Physiol 136:2887–2894CrossRefPubMedPubMedCentralGoogle Scholar
  37. Phillips DA, Fox TC, Six J (2006) Root exudation (net efflux of amino acids) may increase rhizodeposition under elevated CO2. Glob Chang Biol 12:561–567CrossRefGoogle Scholar
  38. Read DB, Bengough AG, Gregory PJ, Crawford JW, Robinson D, Scrimgeour CM, Young IM, Zhang K, Zhang X (2003) Plant roots release phospholipid surfactants that modify the physical and chemical properties of soil. New Phytol 157:315–326CrossRefGoogle Scholar
  39. Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Physiol Plant Mol Biol 52:527–560CrossRefPubMedGoogle Scholar
  40. Sacchi G, Abruzzese A, Lucchini G, Fiorani F, Cocucci S (2000) Efflux and active re-absorption of glucose in roots of cotton plants grown under saline conditions. Plant Soil 220:1–11CrossRefGoogle Scholar
  41. 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 Commun Mass Spectrom 23:3333–3342CrossRefPubMedGoogle Scholar
  42. Shi SJ, Richardson AE, O'Callaghan M, DeAngelis KM, Jones EE, Stewart A, Firestone MK, Condron LM (2011) Effects of selected root exudate components on soil bacterial communities. FEMS Microbiol Ecol 77:600–610CrossRefPubMedGoogle Scholar
  43. Strehmel N, Bottcher C, Schmidt S, Scheel D (2014) Profiling of secondary metabolites in root exudates of Arabidopsis thaliana. Phytochemistry 108:35–46CrossRefPubMedGoogle Scholar
  44. Stubbs VEC, Standing D, Knox OGG, Killham K, Bengough AG, Griffiths B (2004) Root border cells take up and release glucose-C. Ann Bot 93:221–224CrossRefPubMedPubMedCentralGoogle Scholar
  45. van Hees PAW, Johansson E, Jones DL (2008) Dynamics of simple carbon compounds in two forest soils as revealed by soil solution concentrations and biodegradation kinetics. Plant Soil 310:11–23CrossRefGoogle Scholar
  46. Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51CrossRefPubMedPubMedCentralGoogle Scholar
  47. Warren CR (2012) Post-uptake metabolism affects quantification of amino acid uptake. New Phytol 193:522–531CrossRefPubMedGoogle Scholar
  48. Warren CR (2013) High diversity of small organic N observed in soil water. Soil Biol Biochem 57:444–450CrossRefGoogle Scholar
  49. Warren CR (2014) Response of osmolytes in soil to drying and rewetting. Soil Biol Biochem 70:22–32CrossRefGoogle Scholar
  50. Warren CR (2015) Wheat roots efflux a diverse array of organic N compounds and are highly proficient at their recapture. Plant Soil:1–16Google Scholar
  51. Yuan M, Breitkopf SB, Yang X, Asara JM (2012) A positive/negative ion-switching, targeted mass spectrometry-based metabolomics platform for bodily fluids, cells, and fresh and fixed tissue. Nat Protoc 7:872–881CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.School of Life and Environmental SciencesThe University of SydneySydneyAustralia

Personalised recommendations