Skip to main content
Log in

Cholodny–Went revisited: a role for jasmonate in gravitropism of rice coleoptiles

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

Abstract

Gravitropism is explained by the Cholodny–Went hypothesis: the basipetal flow of auxin is diverted laterally. The resulting lateral auxin gradient triggers asymmetric growth. However, the Cholodny–Went hypothesis has been questioned repeatedly because the internal auxin gradient is too small to account for the observed growth asymmetry. Therefore, an additional gradient in indolyl-3-acetic acid (IAA) sensitivity has been suggested (Brauner and Hager in Planta 51:115–147, 1958). We challenged the Cholodny–Went hypothesis for gravitropism of rice coleoptiles (Oryza sativa L.) and found it to be essentially true. However, we observed, additionally, that the two halves of gravitropically stimulated coleoptiles responded differentially to the same amount of exogenous auxin: the auxin response is reduced in the upper flank but normal in the lower flank. This indicates that the auxin-gradient is amplified by a gradient of auxin responsiveness. Hormone contents were measured across the coleoptile by a GC-MS/MS technique and a gradient of jasmonate was detected opposing the auxin gradient. Furthermore, the total content of jasmonate increased during the gravitropic response. Jasmonate gradient and increase persist even when the lateral IAA gradient is inhibited by 1-N-naphtylphtalamic acid. Flooding with jasmonate delays the onset of gravitropic bending. Moreover, a jasmonate-deficient rice mutant bends more slowly and later than the wild type. We discuss a role of jasmonate as modulator of auxin responsiveness in gravitropism.

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. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

ABA:

Abscicic acid

DMSO:

Di-methyl-sulfoxide

FW:

Fresh weight

GC-MS-MS:

Gas chromatography linked bidimensional mass spectrometry

IAA:

Indole-3-acetic-acid

JA:

Jasmonate

Me-JA:

Methyl jasmonate

2,5-NBD:

2,5-Norbornadien

NPA:

1-N-naphtylphtalamic acid

OPDA:

o-Phytodienoic acid

OPR:

o-Phytodienoic acid reductase

References

  • Blaauw AH (1915) Licht und Wachstum II. Bot Zent 7:465–532

    Google Scholar 

  • Brauner L, Hager A (1958) Beiträge zur Analyse der geotropischen Perzeption. Planta 51:115–147

    Article  CAS  Google Scholar 

  • Briggs WR (1963) The phototropic response of higher plants. Annu Rev Plant Physiol 14:311–352

    Article  CAS  Google Scholar 

  • Bruinsma J, Hasegawa K (1990) A new theory of phototropism—its regulation by a light induced gradient of auxin-inhibiting substances. Physiol Plant 79:700–704

    Article  CAS  Google Scholar 

  • Brummer B, Bertl A, Portykus I, Felle H, Parish RW (1985) Evidence that fusicoccin and indole-3-acetic acid induce acidification of Zea mays cells. FEBS Lett 189:109–114

    Article  CAS  Google Scholar 

  • Cholodny N (1927) Wuchshormone und Tropismen bei den Pflanzen. Biol Zent 47:604–626

    CAS  Google Scholar 

  • Darwin C, Darwin F (1880) Sensitiveness of plants to light: it‘s transmitted effect. The power of movement in plants. John Murray, London, pp 574–592

    Google Scholar 

  • Digby J, Firn RD (1976) A critical assessment of the Cholodny–Went Theory of shoot gravitropism. Curr Adv Plant Sci 8:953–960

    Google Scholar 

  • Dolk HE (1936) Geotropism and the growth substance. Recl Trav Bot Neerl 33:509–585

    Google Scholar 

  • Edelmann H (2001) Lateral redistribution of auxin is not the means for gravitropic differential growth of coleoptiles: a new model. Physiol Plant 112:119–126

    Article  PubMed  CAS  Google Scholar 

  • Evans NH (2003) Modulation of guard cell plasma membrane potassium currents by methyl-jasmonate. Plant Physiol 131:8–11

    Article  PubMed  CAS  Google Scholar 

  • Gillespie B, Briggs WR (1961) Mediation of the geotropic response by lateral transport of auxin. Plant Physiol 36:364–368

    PubMed  CAS  Google Scholar 

  • Godbolé R, Michalke W, Nick P, Hertel R (2000) Cytoskeletal drugs and gravity-induced lateral auxin transport in rice coleoptiles. Plant Biol 2:176–181

    Article  Google Scholar 

  • Goldsmith MHM (1967) Movement of pulses of labeled auxin in corn coleoptiles. Plant Physiol 31:51–82

    Google Scholar 

  • Goldsmith MHM, Wilkins MB (1964) Movement of auxin in coleoptiles of Zea mays L. during geotropic stimulation. Plant Physiol 39:151–162

    PubMed  CAS  Google Scholar 

  • Himmelspach R, Nick P (2001) Gravitropic microtubule orientation can be uncoupled from growth. Planta 212:184–189

    Article  PubMed  CAS  Google Scholar 

  • Iino M (1991) Mediation of tropisms by lateral translocation of endogenous indole-3-acetic acid in maize coleoptiles. Plant Cell Environ 14:279–286

    Article  Google Scholar 

  • Imaseki H, Pjon CJ (1970) The effect of ethylene on auxin-induced growth of excised rice coleoptile segments. Plant Cell Physiol 11:827–829

    CAS  Google Scholar 

  • Irving HR, Dyson G, McConchie R, Parish RW, Gehring CA (1999) Effects of exogenously applied jasmonates on growth and intracellular pH in maize coleoptile segments. J Plant Growth Regul 18:93–100

    Article  PubMed  CAS  Google Scholar 

  • Kögl F, Hagen-Smit J, Erxleben H (1934) Über ein neues Auxin (,,Hetero-Auxin“) aus Harn. Hoppe-Seyler‘s Z Physiol Chem 228:104–112

    Google Scholar 

  • Kramer S, Piotrowski M, Kühnemann F, Edelmann HG (2003) Physiological and biochemical characterization of ethylene-generated gravicompetence in primary shoots of coleoptile-less gravi-incompetent rye seedlings. J Exp Bot 54:2723–2732

    Article  PubMed  CAS  Google Scholar 

  • Kutschera U, Briggs WR (1987) Rapid auxin-induced stimulation of cell wall synthesis in pea internodes. Proc Natl Acad Sci USA 84:2747–2751

    Article  PubMed  CAS  Google Scholar 

  • Lang JM, Eisinger WR, Green PB (1982) Effects of ethylene on the orientation of microtubules and cellulose microfibrils of pea epicotyl cells with polylamellate cell walls. Protoplasma 110:5–14

    Article  CAS  Google Scholar 

  • León J, Sánchez-Serrano JJ (1999) Molecular biology of jasmonate biosynthesis in plants. Plant Physiol Biochem 37:373–380

    Article  Google Scholar 

  • MacDonald IR, Hart JW (1987) New light on the Cholodny-Went theory. Plant Physiol 84:568–570

    PubMed  CAS  Google Scholar 

  • Miyamoto K, Oka M, Ueda J (1997) Update on the possible mode of action of jasmonates: focus on the metabolism of cell wall polysaccharides in relation to growth and development. Physiol Plant 100:631–638

    Article  CAS  Google Scholar 

  • Moseyko N, Zhu T, Chang HS, Wang Z, Feldman LJ (2002) Transcription profiling of the early gravitropic response in Arabidopsis using high-density oligonucleotide probe microarrays. Plant Physiol 130:720–728

    Article  PubMed  CAS  Google Scholar 

  • Müller A, Düchting P, Weiler EW (2002) A multiplex GC-MS/MS technique for the sensitive and quantitative single-run analysis of acidic phytohormones and related compounds, and its application to Arabidopsis thaliana. Planta 216:44–56

    Article  PubMed  CAS  Google Scholar 

  • Nick P, Furuya M (1993) Phytochrome-dependent decrease of gibberellin sensitivity to auxin. J Plant Growth Regul 12:195–206

    Article  CAS  Google Scholar 

  • Parker KE, Briggs WR (1990) Transport of indole-3-acetic acid during gravitopism of intact maize coleoptiles. Plant Physiol 94:1763–1768

    Article  PubMed  CAS  Google Scholar 

  • Philippar K, Fuchs I, Lüthen H, Hoth S, Bauer CS, Haga K, Thiel G, Ljung K, Sandberg G, Böttger M, Becker D, Hedrich R (1999) Auxin-induced K+ channel expression respresents an essential step in coleoptile growth and gravitropism. Proc Natl Acad Sci USA 96:12186–12191

    Article  PubMed  CAS  Google Scholar 

  • Riemann M, Müller A, Korte A, Furuya M, Weiler E, Nick P (2003) Impaired induction of the jasmonate pathway in the rice mutant hebiba. Plant Physiol 133:1820–1830

    Article  PubMed  CAS  Google Scholar 

  • Rorabaugh PA, Salisbury FB (1989) Gravitropism in higher plant shoots VI. Changing sensitivity to auxin in gravistimulated soybean hypocotyls. Plant Physiol 91:1329–1338

    PubMed  CAS  Google Scholar 

  • Salisbury FB, Gillespie L, Rorabaugh P (1988) Gravitropism in higher plant shoots. V. Changing sensitivity to auxin. Plant Physiol 88: 1186–1194

    PubMed  CAS  Google Scholar 

  • Schwechheimer C, Serino G, Callis J, Crosby WL, Lyapina S, Deshaies RJ, Gray WM, Estelle M, Deng XW (2001) Interactions of the COP9 signalosome with the E3 ubiquitin ligase SCFTIR1 in mediating auxin response. Science 292:1379–1382

    Article  PubMed  CAS  Google Scholar 

  • Thimann KV (1935) On the plant growth hormone produced by Rhizopus suinus. J Biol Chem 109:279–291

    CAS  Google Scholar 

  • Thompson KS, Hertel R, Müller S, Tavares JE (1973) 1-N-naphtylphthalamic and 2,3,5-triiodobenzoic acids. In vitro binding to particulate cell fractions and action on auxin transport in corn coleoptiles. Planta 109:337–352

    Article  Google Scholar 

  • Trewavas AJ (1982) Growth substance sensitivity: the limiting factor in plant development. Physiol Plant 55:60–72

    Article  CAS  Google Scholar 

  • Trewavas AJ (1992) Forum: What remains of the Cholodny–Went theory? Plant Cell Environ 15:759–794

    PubMed  Google Scholar 

  • Ueda J, Miyamoto K, Aoki M (1994) Jasmonate inhibits the IAA-induced elongation of oat coleoptile segments: a possible mechanism involving the metabolism of cell wall polysaccharides. Plant Cell Physiol 35:1065–1070

    CAS  Google Scholar 

  • Ueda J, Miyamoto K, Kamisaka S (1995) Inhibition of the synthesis of cell wall polysaccharides in oat coleoptile segments by jasmonate. Relevance to its growth inhibition. J Plant Growth Regul 14:69–76

    Article  CAS  Google Scholar 

  • Waller F (2000) OsARF1, ein Auxin Response Factor aus Reis (Oryza sativa L.), der selbst auxinreguliert ist. PhD Thesis, Albert-Ludwigs-Universität Freiburg

  • Waller F, Furuya M, Nick P (2002) OsARF, an auxin response factor from rice, is auxin-regulated and classifies as primary auxin responsive gene. Plant Mol Biol 50:415–425

    Article  PubMed  CAS  Google Scholar 

  • Wang QY, Nick P (1998) The auxin response of actin is altered in the rice mutant Yin-Yang . Protoplasma 204:22–33

    Article  PubMed  CAS  Google Scholar 

  • Went F (1926) On growth accelerating substances in the coleoptile of Avena sativa. Proc Kon Ned Akad Weten 30:10–19

    Google Scholar 

  • Went FW, Thimann KV (1937) Phytohormones. Macmillan, New York

    Google Scholar 

Download references

Acknowledgements

NPA was synthesized and kindly provided by Dr. Wolfgang Michalke (Albert-Ludwigs-Universität Freiburg). The authors would like to thank Dr. Christina Süßlin for experimental support, Dr. Osamu Yatou (Hokuriku National Agricultural Experiment Station, Niigata, Japan) for providing seed material and Dr. Gerd Leubner (Albert-Ludwigs-Universtiät Freiburg) for a kind gift of 2,5-NBD. The study was supported partially by grants from the Forschungsschwerpunkt “Molekulare Analyse der Phytohormonwirkung” of the DFG to E.W. and P.N, a grant from the Volkswagen-Foundation Nachwuchsgruppen-Programme to P.N., and a partial grant of the Studienstiftung des deutschen Volkes to C.G..

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Peter Nick.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gutjahr, C., Riemann, M., Müller, A. et al. Cholodny–Went revisited: a role for jasmonate in gravitropism of rice coleoptiles. Planta 222, 575–585 (2005). https://doi.org/10.1007/s00425-005-0001-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-005-0001-6

Keywords

Navigation