Plant and Soil

, Volume 226, Issue 1, pp 87–98 | Cite as

Impact of Agrobacterium tumefaciens-induced stem tumors on NO3− uptake in Ricinus communis

  • Igor Mistrik
  • Jan Pavlovkin
  • Rebecca Wächter
  • Katja S. Pradel
  • Katja Schwalm
  • Wolfram Hartung
  • Ulrike Mathesius
  • Christine Stöhr
  • Cornelia I. Ullrich


Developing tumors induced by Agrobacterium tumefaciens, strain C58, on stems of Ricinus communis L. var. gibsonii cv. Carmencita were shown to be strong metabolic sinks for sucrose and amino acids, thus causing higher nutrient demand in the host plant. However, NO3 uptake and, to a lesser extent, also H2PO4 uptake were strongly inhibited. Correspondingly, NO3 concentration was lower in tumorised than in the control plants. NO3reductase activity was the same in both plant types, but it was completely suppressed in the tumors. The electrical membrane potential difference of root cells was unaffected in tumorised plants when soil-grown, but significantly lowered when grown hydroponically. Consistent with the low NO3 uptake rate, NO3-dependent membrane depolarisation at the onset of NO3/2H+-cotransport was nearly zero. In the phloem sap, sucrose and amino acid concentrations were considerably lower in tumorised than in control plants, and lower below than above the tumor. The qualitative pattern of amino acids of the phloem sap of stems was almost the same in tumorised and control plants. It is concluded that neither the overall amino acid concentration nor special amino acids nor ammonium in the transport phloem suppress NO3 uptake in the roots. Aminocyclopropane-carboxylate, the precursor of ethylene, which is produced in the tumors in high amounts, was low in the stems and the same in both plant types. Thus, ACC and ethylene were ruled out as directly interfering with nutrient uptake in the roots. Root morphology was strongly affected during tumor development. Root fresh weight decreased to 50% of the controls and lateral root development was almost completely prevented. This suggests that the high tumor ethylene production, together with an increasing concentration of phenolic compounds, severely inhibits the basipetal auxin flow to the roots. Auxin accumulation and retention was confirmed by specifically enhanced expression of the auxin-responsive promoter of the soybean gene GH3:GUS in tumors induced in transgenic Trifolium repens L. Hence, root development is poorer and anion uptake inhibited in tumorised plants. This may be aggravated by abscisic acid accumulation in the tumor and its basipetal export into the roots. Moreover, sucrose depletion of the sieve tubes leads to energy shortage at the root level for maintaining energy-dependent anion uptake.

abscisic acid Agrobacterium tumefaciens-induced tumors amino acids ethylene indole-3-acetic acid and GH3:GUS NO3 and H2PO4 uptake 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Aloni R, Pradel K S and Ullrich C I 1995 The three-dimensional structure of vascular tissues in Agrobacterium tumefaciensinduced crown galls and in the host stems of Ricinus communis. Planta 196, 597–605.Google Scholar
  2. Aloni R, Wolf A, Feigenbaum P, Avni A and Klee H J 1998 The Never ripe mutant provides evidence that tumor-induced ethylene controls the morphogenesis of Agrobacterium tumefaciensinduced crown galls on tomato stems. Plant Physiol. 117, 841–849.Google Scholar
  3. Bien E, Lorenz D, Eichhorn K and Plapp R 1990 Isolation and characterization of Agrobacterium tumefaciens from the German vineregion Rheinpfalz. Z. Pflanzenkr. Pflanzenschutz 97, 313–322.Google Scholar
  4. Büttner G, de Fekete M A R and Vieweg G H 1985 Changes in fructan content in developing barley caryopses. Angew. Bot. 59, 171–177.Google Scholar
  5. Davies P J 1995 The plant hormones: their nature, occurrence, and functions. In Plant Hormones: Physiology, Biochemistry and Molecular Biology. Ed. P J Davies, pp 1–12. Kluwer Academic Publishers, Dordrecht.Google Scholar
  6. Else M A and Jackson M B 1998 Transport of 1-aminocyclopropane-1-carboxylic acid (ACC) in the transpiration stream of tomato (Lycopersicon esculentum) in relation to foliar ethylene production and petiole epinasty. Aust. J. Plant Physiol. 25, 453–458.Google Scholar
  7. Goodman R N 1986 Crown gall in grapes. Am. Wine Soc. J. 18, 80–81.Google Scholar
  8. Guilfoyle T J, Hagen G, Li Y, Ulmasov T, Liu Z and Gee M 1993 Auxin-regulated transcription. Aust. J. Plant Physiol. 20, 489–502.Google Scholar
  9. Hagen G, Martin G, Li Y and Guilfoyle T J (1991) Auxin-induced expression of the soybean GH3 promoter in transgenic tobacco plants. Plant Mol. Biol. 17, 567–579.Google Scholar
  10. Jacobs M and Rubery P H 1988 Naturally occurring auxin transport regulators. Science 241, 346–349.Google Scholar
  11. Jefferson R A, Kavanagh T H and Bevan M W 1987 GUS fusion: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. The EMBO J. 6, 3901–3907.Google Scholar
  12. Jeschke W D, Baig A and Hilpert A 1997a Sink-stimulated photosynthesis, increased transpiration and increased demanddependent stimulation of nitrate uptake: Nitrogen and carbon relations in the parasitic association Cuscuta refexa-Coleus blumei. J. Exp. Bot. 48, 915–925.Google Scholar
  13. Jeschke W D, Peuke A D, Pate J S and Hartung W 1997b Transport, synthesis and catabolism of abscisic acid (ABA) in intact plants 98 of castor bean (Ricinus communis L.) under phosphate deficiency and moderate salinity. J. Exp. Bot. 48, 1737–1747.Google Scholar
  14. Kado C I 1984 Phytohormone-mediated tumorigenesis by plant pathogenic bacteria. In Genes Involved in Microbe-Plant Interactions. Eds. D P S Verma and Th Hohn. pp 311–336. Springer-Verlag, Wien.Google Scholar
  15. Lawson M 1991 First to market. Nature 353, 687.Google Scholar
  16. Larkin P J, Gibson J M, Mathesius U, Weinman J J, Gartner E, Hall E, Tanner G J, Rolfe B G and Djordjevic M A 1996 Transgenic white clover. Studies with the auxin-responsive promoter, GH3, in root gravitropism and lateral root development. Transgen. Res. 5, 325–335.Google Scholar
  17. Liu J-H and Reid DM 1992 Auxin and ethylene-stimulated adventitious rooting in relation to tissue sensitivity to auxin and ethylene production in sunflower hypocotyls. J. Exp. Bot. 43, 1191–1198.Google Scholar
  18. Lizada M C C and Yang S F 1979 A simple and sensitive assay for 1-aminocyclopropane-1-carboxylic acid. Analyt. Biochem. 100, 140–145.Google Scholar
  19. Malsy S, van Bel A J E, Kluge M, Hartung W and Ullrich C I 1992 Induction of crown galls by Agrobacterium tumefaciens (strain C 58) reverses assimilate translocation and accumulation in Kalanchoë daigremontiana. Plant Cell Environ. 15, 519–529.Google Scholar
  20. Marx S and Ullrich-Eberius C I 1988 Solute accumulation and electrical membrane potential in Agrobacterium tumefaciensinduced crown galls in Kalanchoë daigremontiana leaves. Plant Sci. 57, 27–36.Google Scholar
  21. Mathesius U, Schlaman H R M, Spaink H P, Sautter C, Rolfe B G and Djordjevic M A 1998 Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. Plant J. 14, 23–34.Google Scholar
  22. Muller B and Touraine B 1992 Inhibition of NO3- uptake by various phloem-translocated amino acids in soybean seedlings. J. Exp. Bot. 43, 617–623.Google Scholar
  23. Pradel K S, Rezmer C, Krausgrill S, Rausch T and Ullrich C I 1996 Evidence for symplastic phloem unloading with a concomitant high level of acid cell-wall invertase in Agrobacterium tumefaciens-induced plant tumors. Bot. Acta 109, 397–404.Google Scholar
  24. Pradel K S, Ullrich C I, Santa Cruz S and Oparka K J 1999 Symplastic continuity in Agrobacterium tumefaciens-induced tumours. J. Exp. Bot. 50, 183–192.Google Scholar
  25. Rapp A and Ziegler A 1973 Bestimmung der Phenolcarbonsäuren in Rebblättern, Weintrauben und Wein mittels Polyamid-Dünnschichtchromatographie. Vitis 12, 226–236.Google Scholar
  26. Roberts LW, Gahan P B and Aloni R 1988 Vascular Differentiation and Plant Growth Regulators. Springer-Verlag, Berlin. 154 p.Google Scholar
  27. Schurr U 1998 Dynamics of nutrient transport from the root to the shoot. Progr. Bot. 60, 234–253.Google Scholar
  28. Schurr U, Schuberth B, Aloni R, Pradel K S, Schmundt D, Jähne B and Ullrich C I 1996 Structural and functional evidence for xylem-mediated water transport and high transpiration in Agrobacterium tumefaciens-induced tumors of Ricinus communis. Bot. Acta 109, 405–411.Google Scholar
  29. Stachel S E, Messens E, van Montagu M and Zambryski P 1985 Identification of the signal molecules produced by wounded plant cells that activate T-DNA transfer in Agrobacterium tumefaciens. Nature 318, 624–629.Google Scholar
  30. Stacewicz-Sapuncakis M, Marsh H V, Vengris J, Jennings P H and Robinson T 1973 Participation of ethylene in common purslane response to Dicamba. Plant Physiol. 52, 466–471.Google Scholar
  31. Stöhr C and Ullrich W R 1997 A succinate-oxidising nitrate reductase is located at the plasma membrane of plant roots. Planta 203, 129–132.Google Scholar
  32. Strickland J D H and Parsons T R 1965 A manual of sea water analysis. Bull. Fish. Res. Board Can. 125, 203.Google Scholar
  33. Suleiman S, Hourmant A and Penot M 1990 Influence de l'acide abscissique sur le transport d'ions inorganiques chez la pomme de terre (Solanum tuberosum cv. Bintje). Etude comparée avec quelques autres phytohormones. Biol. Plant. (Praha) 32, 128–137.Google Scholar
  34. Tillard P, Passama L and Gojon A 1998 Are phloem amino acids involved in the shoot to root control of NO3- uptake in Ricinus communis plants? J. Exp. Bot. 49, 1371–1379.Google Scholar
  35. Wächter R, Fischer K, Gäbler R, Kühnemann F, Urban W, Bögemann G M, Voesenek L A C J, Blom C W P M and Ullrich C I 1999 Ethylene production and ACC-accumulation in Agrobacterium tumefaciens-induced plant tumours and their impact on tumour and host stem structure and function. Plant Cell Environ. 22. (In press).Google Scholar
  36. Yang S F and Hofman N E 1984 Ethylene biosynthesis and its regulation in higher plants. Annu. Rev. Plant Physiol. 35, 155–189.Google Scholar
  37. Zambryski P, Tempé J and Schell J 1989 Transfer and function of T-DNA genes from Agrobacterium Ti and Ri plasmids in plants. Cell 56, 193–201.Google Scholar
  38. Zhuo D, Okamoto M, Vidmar J J and Glass A D M 1999 Regulation of a putative high-affinity nitrate transporter (Nrt2;1At) in roots of Arabidopsis thaliana. Plant J. 17, 563–568.Google Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • Igor Mistrik
  • Jan Pavlovkin
  • Rebecca Wächter
  • Katja S. Pradel
  • Katja Schwalm
  • Wolfram Hartung
  • Ulrike Mathesius
  • Christine Stöhr
  • Cornelia I. Ullrich

There are no affiliations available

Personalised recommendations