Skip to main content
Log in

The diageotropica mutation of tomato disrupts a signalling chain using extracellular auxin binding protein 1 as a receptor

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

The diageotropica (dgt) mutant of tomato (Lycopersicon esculentum Mill.) is known to lack a number of typical auxin responses. Here we show that rapid auxin-induced growth of seedling hypocotyls is completely abolished by the mutation over the full range of auxin concentrations tested, and also in early phases of the time course. Protoplasts isolated from wild-type hypocotyls respond to auxin by a rapid increase in cell volume, which we measured by image analysis at a high temporal resolution. A similar swelling could be triggered by antibodies directed against a part of the putative auxin-binding domain (box-a) of the auxin-binding protein 1 (ABP1). Induction of swelling both by auxin and by the antibody was not observed in the protoplasts isolated from the dgt mutant. However, dgt protoplasts are able to respond to the stimulator of the H+-ATPase, fusicoccin, with normal swelling. We propose that dgt is a signal-transduction mutation interfering with an auxin-signalling pathway that uses ABP1 as a receptor.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1a–f.
Fig. 2a, b.
Fig. 3.
Fig. 4. a

Similar content being viewed by others

Abbreviations

ABP:

auxin-binding protein

CCD:

charge-coupled device

2,4-D:

2,4-dichlorophenoxyacetic acid

dgt :

diageotropica

FC:

fusicoccin

References

  • Barbier-Brygoo H, Ephritikhine G, Klämbt D, Maurel C, Palme K, Schell J, Guern J (1991) Perception of the auxin signal at the plasma membrane of tobacco mesophyll protoplasts. Plant J 1:83–93

    CAS  Google Scholar 

  • Chen JG, Ullah H, Young JC, Sussman MR, Jones AM (2001) ABP1 is required for organized cell elongation and division in Arabidopsis embryogenesis. Genes Dev 15:902–911

    CAS  PubMed  Google Scholar 

  • Christian M, Lüthen H (2000) New methods to analyse auxin-induced growth I: Classical auxinology goes Arabidopsis. Plant Growth Regul 32:107–114

    Article  CAS  Google Scholar 

  • Claussen M, Lüthen H, Böttger M (1996) Inside or outside? The localisation of the receptor relevant to auxin induced growth. Physiol Plant 98:861–867

    Article  CAS  Google Scholar 

  • Coenen C, Bierfreund N, Lüthen H, Neuhaus G (2002) Developmental regulation of proton ATPase dependent auxin responses in the diageotropica mutant of tomato (Lycopersicon esculentum). Physiol Plant 114:461–471

    Article  CAS  PubMed  Google Scholar 

  • Daniel SG, Rayle DL, Cleland RE (1989) Auxin physiology of the tomato mutant diageotropica. Plant Physiol 91:804–807

    CAS  PubMed  Google Scholar 

  • Davies PJ (1974) The uptake and elution of indoleacetic acid by pea stem sections in relation to auxin induced growth. In: Plant growth substances 1973. Hirokawa, Tokyo, pp 767–778

  • Fischer C, Lüthen H, Böttger M, Hertel R (1992) Initial transient growth inhibition in maize coleoptiles following auxin application. J Plant Physiol 141:88–92

    Google Scholar 

  • Fujino DW, Nissen SJ, Jones AD, Burger DW, Bradford KJ (1988) Quantification of indole-3-acetic acid in dark-grown seedlings of the diageotropica and epinastic mutants of tomato (Lycopersicon esculentum Mill.). Plant Physiol 88:780–784

    CAS  Google Scholar 

  • Gehring CA, McConchie RM, Venis MA, Parrish RW (1998) Auxin binding protein antibodies and peptides influence stomatal opening and alter cytoplasmic pH. Planta 205:581–586

    Article  CAS  PubMed  Google Scholar 

  • Hertel R (1995) Auxin binding protein 1 is a red herring. J Exp Bot 46:461–462

    CAS  Google Scholar 

  • Jones AM (1994) Auxin binding proteins. Annu Rev Plant Physiol Plant Mol Biol 45:393–420

    Google Scholar 

  • Jones AM, Im KH, Savka MA, Wu MJ, DeWitt G, Shillito R, Binns AN (1998) Auxin dependent cell expansion mediated by overexpressing auxin-binding protein 1. Science 282:1114–1117

    Google Scholar 

  • Kelly MO, Bradford KJ (1986) Insensitivity of the diageotropica mutant to auxin. Plant Physiol 82:713–717

    CAS  Google Scholar 

  • Krautwig B (1993) Etablierung von in vitro-Kultursystemen aus Mikrosporen von Mais (Zea mays L.). Thesis, University of Hamburg, Germany

  • Madlung A, Behringer FJ, Lomax TL (1999) Ethylene plays multiple nonprimary roles in modulating the gravitropic response in tomato. Plant Physiol 120:897–906

    Article  CAS  PubMed  Google Scholar 

  • Marrè E (1979) Fusicoccin: a tool in plant physiology. Annu Rev Plant Physiol 30:273–288

    Article  Google Scholar 

  • Mito N, Bennett AB (1995) The diageotropica mutation and synthetic auxins differentially affect the expression of auxin-regulated genes in tomato. Plant Physiol 109:293–297

    Article  CAS  PubMed  Google Scholar 

  • Muday GK, Lomax TL, Rayle DL (1995) Characterization of the growth and auxin physiology of roots of the tomato mutant, diageotropica. Planta 195:548–553

    CAS  PubMed  Google Scholar 

  • Nebenführ A, White TJ, Lomax TL (2000) The diageotropica mutation alters auxin induction of a subset of the Aux/IAA gene family in tomato. Plant Mol Biol 44:73–84

    Article  PubMed  Google Scholar 

  • Palmgren MG (1991) Regulation of plant plasma membrane H+-ATPase. Plant Physiol 83:314–323

    Article  CAS  Google Scholar 

  • Park WJ (1998) Effect of epibrassinolide on hypocotyl growth of the tomato mutant diageotropica. Planta 207:120–124

    Article  CAS  PubMed  Google Scholar 

  • Parsons A, Firn RD, Digby J (1988) The role of the coleoptile apex in controlling organ elongation. I. The effects of decapitation and apical incisions. J Exp Bot 39:1331–1341

    Google Scholar 

  • Rice MS, Lomax TL (2000) The auxin-resistant diageotropica mutant of tomato responds to gravity via an auxin-mediated pathway. Planta 210:906–913

    Article  CAS  PubMed  Google Scholar 

  • Rück A, Palme K, Venis MA, Napier RM, Felle HH (1993) Patch clamp analysis establishes a role for an auxin binding protein in the auxin stimulation of plasma membrane current in Zea mays protoplasts. Plant J 4:41–46

    Article  Google Scholar 

  • Steffens B, Lüthen H (2000) New methods to analyse auxin-induced growth II: The swelling reaction of protoplasts — a model system for the analysis of auxin signal transduction? Plant Growth Regul 32:115–122

    Article  CAS  Google Scholar 

  • Steffens B, Feckler C, Palme K, Christian M, Böttger M, Lüthen H (2001) The auxin signal for protoplast swelling is perceived by extracellular ABP1. Plant J 27:591–599

    PubMed  Google Scholar 

  • Tietze-Haß E, Dörffling K (1977) Initial phases of indolylacetic acid induced growth in coleoptile segments of Avena sativa L. Planta 135:192–195

    Google Scholar 

  • Venis MA (1995) Auxin binding protein 1 is a red herring ? — Oh no it isn't. J Exp Bot 46:463–465

    CAS  Google Scholar 

  • Venis MA, Napier RM, Barbier-Brygoo H, Maurel C, Perrot-Rechenmann C, Guern J (1992) Antibodies to a peptide from maize auxin-binding protein have auxin agonist activity. Proc Natl Acad Sci USA 89:7208–7212

    CAS  PubMed  Google Scholar 

  • Vesper MJ, Kuss CL (1990) Physiological evidence that the primary site of auxin action in maize coleoptiles is an intracellular site. Planta 182:486–491

    CAS  Google Scholar 

  • Weiler EW, Jourdan PS, Conrad W (1981) Levels of indole-3-acetic acid in intact and decapitated coleoptiles as determined by a specific and highly sensitive solid phase immunoassay. Planta 153:561–571

    CAS  Google Scholar 

  • Zobel RW (1974) Control of morphogenesis in the ethylene-requiring tomato mutant, diageotropica. Can J Bot 52:735–743

    Google Scholar 

Download references

Acknowledgements

We express our thanks to Dr. Catharina Coenen for giving a generous supply of dgt and wild-type seeds. Dr. Christian Feckler and Prof. Klaus Palme (Universität Freiburg) supplied the anti-intern antibodies used in this study. We also thank the Deutsche Forschungsgemeinschaft for funding within the program "molecular analysis of phytohormone action". This work is based in part on the PhD thesis of May Christian at the University of Hamburg.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hartwig Lüthen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Christian, M., Steffens, B., Schenck, D. et al. The diageotropica mutation of tomato disrupts a signalling chain using extracellular auxin binding protein 1 as a receptor. Planta 218, 309–314 (2003). https://doi.org/10.1007/s00425-003-1090-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-003-1090-8

Keywords

Navigation