Skip to main content
Log in

Effect of Cyclanilide on Auxin Activity

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Cyclanilide is a plant growth regulator that is registered for use in cotton at different stages of growth, to either suppress vegetative growth (in combination with mepiquat chloride) or accelerate senescence (enhance defoliation and boll opening, used in combination with ethephon). This research was conducted to study the mechanism of action of cyclanilide: its potential interaction with auxin (IAA) transport and signaling in plants. The activity of cyclanilide was compared with the activity of the auxin transport inhibitors NPA and TIBA. Movement of [3H]IAA was inhibited in etiolated corn coleoptiles by 10 μM cyclanilide, NPA, and TIBA, which demonstrated that cyclanilide affected polar auxin transport. Although NPA inhibited [3H]IAA efflux from cells in etiolated zucchini hypocotyls, cyclanilide had no effect. NPA did not inhibit the influx of IAA into cells in etiolated zucchini hypocotyls, whereas cyclanilide inhibited uptake 25 and 31% at 10 and 100 μM, respectively. Also, NPA inhibited the gravitropic response in tomato roots (85% at 1 μM) more than cyclanilide (30% at 1 μM). Although NPA inhibited tomato root growth (30% at 1 μM), cyclanilide stimulated root growth (165% of control at 5 μM). To further characterize cyclanilide action, plasma membrane fractions from etiolated zucchini hypocotyls were obtained and the binding of NPA, IAA, and cyclanilide studied. Cyclanilide inhibited the binding of [3H]NPA and [3H]IAA with an IC50 of 50 μM for both. NPA did not affect the binding of IAA, nor did IAA affect the binding of NPA. Kinetic analysis indicated that cyclanilide is a noncompetitive inhibitor of both NPA and IAA binding, with inhibition constants (K i) of 40 and 2.3 μM, respectively. These data demonstrated that cyclanilide interacts with auxin-regulated processes via a mechanism that is distinct from other auxin transport inhibitors. This research identifies a possible mechanism of action for cyclanilide when used as a plant growth regulator.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Abas L, Benjamins R, Malenica N, Paciorek T, Wisniewska J, Moulinier-Anzola JC, Sieberer T, Friml J, Lusching C (2006) Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat Cell Biol 8:249–256

    Article  PubMed  CAS  Google Scholar 

  • Bernasconi P (1996) Effect of synthetic and natural protein tyrosine kinase inhibitors on auxin efflux in zucchini (Curcurbita pepo) hypocotyls. Physiol Plant 96:205–210

    Article  CAS  Google Scholar 

  • Bernasconi P, Patel BC, Reagan JD, Subramania M (1996) The N-1-Naphthylphthalamic acid-binding protein is an integral membrane protein. Plant Physiol 111:427–432

    PubMed  CAS  Google Scholar 

  • Blakeslee JJ, Peer WA, Murphy AS (2005) Auxin transport. Curr Opin Plant Biol 8:494–500

    Article  PubMed  CAS  Google Scholar 

  • Blakeslee JJ, Bandyopadhyay A, Lee OR, Mravec J, Titapiwatanakun B, Sauer M, Makam SN, Cheng Y, Bouchard R, Adamec J, Geisler M, Nagashima A, Sakai T, Martinoia E, Friml J, Peer WA, Murphy AS (2007) Interactions among PIN-FORMED and P-glycoprotein auxin transporters in Arabidopsis. Plant Cell 19:131–147

    Article  PubMed  CAS  Google Scholar 

  • Boonshirichai K, Sedbrook JC, Chen R, Gilroy S, Masson PH (2003) ALTERED RESPONSE TO GRAVITY is a peripheral membrane protein that modulates gravity-induced cytoplasmic alkalinization and lateral auxin transport in plant statocytes. Plant Cell 15:2612–2625

    Article  CAS  Google Scholar 

  • Brown DE, Rashotte AM, Murphy AS, Tague BW, Peer WA, Taiz L, Muday GK (2001) Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiol 126(2):524–535

    Article  PubMed  CAS  Google Scholar 

  • Brunn SA, Muday GK, Haworth P (1992) Auxin transport and the interaction of phytotropins Probing the properties of a phytotropin binding protein. Plant Physiol 98:101–107

    PubMed  CAS  Google Scholar 

  • Buer CS, Muday GK (2004) The transparent testa4 mutation prevents flavonoid synthesis and alters auxin transport and the response of Arabidopsis roots to gravity and light. Plant Cell 16:1191–1205

    Article  PubMed  CAS  Google Scholar 

  • Campillo E, Lewis LN (1992) Identification and kinetics of accumulation of proteins induced by ethylene in bean abscission zones. Plant Physiol 98:955–961

    PubMed  Google Scholar 

  • Casimiro I, Merchant A, Bhalerao RP, Beeckman T, Dhooge S, Swarup R, Graham N, Inzé D, Sandberg G, Casero PJ, Bennett M (2001) Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell 13:843–852

    Article  PubMed  CAS  Google Scholar 

  • Christian M, Steffens B, Schenck D, Burmester S, Bottger M, Luthen H (2006) How does auxin enhance cell elongation? Roles of auxin binding proteins and potassium channels in growth control. Plant Biol 8:346–352

    Article  PubMed  CAS  Google Scholar 

  • Cooper WC, Rasmussen GK, Rogers BJ, Reece PC, Henry WH (1968) Control of abscission in agricultural crops and its physiological basis. Plant Physiol 43:1560–1576

    PubMed  CAS  Google Scholar 

  • Dhonukshea P, Grigorievd I, Fischere R, Tominaga M, Robinsonh DG, Hasek J, Pacioreka T, Petrasek J, Seifertova D, Tejos R, Meiselm LA, Zazımalova E, ThWJ Gadella Jr, Stierhofa YD, Uedan T, Oiwaf K, Akhmanova A, Brock R, Spang A, Friml J (2008) Auxin transport inhibitors impair vesicle motility and actin cytoskeleton dynamics in diverse eukaryotes. Proc Natl Acad Sci USA 105:4489–4494

    Article  CAS  Google Scholar 

  • Elfving DC, Visser DB (2005) Cyclanilide induces lateral branching in apple trees. HortScience 40:119–122

    CAS  Google Scholar 

  • Frigerio M, Alabadí D, Pérez-Gómez J, García-Cárcel L, Phillips AL, Hedden P, Blázquez MA (2006) Transcriptional regulation of gibberellin metabolism genes by auxin signaling in Arabidopsis. Plant Physiol 142:553–563

    Article  PubMed  CAS  Google Scholar 

  • Friml J (2003) Auxin transport–shaping the plant. Curr Opin Plant Biol 6:7–12

    Article  PubMed  CAS  Google Scholar 

  • Gallagher SR, Leonard RT (1982) Effect of vanadate, molybdate, and azide on membrane-associated ATPase and soluble phosphatase activities of corn roots. Plant Physiol 70:1335–1340

    PubMed  CAS  Google Scholar 

  • Geisler M, Murphy AS (2006) The ABC of auxin transport: the role of p-glycoproteins in plant development. FEBS Lett 580:1094–1102

    Article  PubMed  CAS  Google Scholar 

  • Hertel R (1987) Auxin transport: binding of auxins and phytotropins to the carriers Accumulation into and efflux from membrane vesicles. NATO ASI Ser 10:81–92

    CAS  Google Scholar 

  • Hertel R, Thomson KS, Russo VEA (1972) In-vitro auxin binding to particulate cell fractions from corn coleoptiles. Planta 107:325–340

    Article  CAS  Google Scholar 

  • Hodges TK, Leonard RT (1974) Purification of a plasma membrane-bound adenosine triphosphate from plant roots. Methods Enzymol 32:392–406

    Article  PubMed  CAS  Google Scholar 

  • Hodges TK, Mills D (1986) Isolation of the plasma membrane. Methods Enzymol 118:41–54

    Article  CAS  Google Scholar 

  • Hulme EC, Birdsall JM (1992) Strategy and tactics in receptor-binding studies. In: Hulme EC (ed) Receptor-ligand interactions, a practical approach. Oxford University Press, New York, pp 63–176

    Google Scholar 

  • Jacobs M, Rubery PH (1988) Naturally occurring auxin transport regulators. Science 241:346–349

    Article  PubMed  CAS  Google Scholar 

  • Jones AM (1990) Location of transported auxin in etiolated maize shoots using 5-azidoindole-3-acetic acid. Plant Physiol 93:1154–1161

    PubMed  CAS  Google Scholar 

  • Katekar GF, Geissler AE (1977) Auxin transport inhibitors III. Chemical requirements of a class of auxin transport inhibitors. Plant Physiol 60:826–829

    CAS  Google Scholar 

  • Kerr ID, Bennett MJ (2007) New insight into the biochemical mechanisms regulating auxin transport in plants. Biochem J 401:613–622

    Article  PubMed  CAS  Google Scholar 

  • Kramer EM, Bennett MJ (2006) Auxin transport: a field in flux. Trends Plant Sci 11:382–386

    Article  PubMed  CAS  Google Scholar 

  • Leopold AC, Lam SL (1962) The auxin transport gradient. Physiol Plant 15:631–638

    Article  CAS  Google Scholar 

  • Leyser O (2006) Dynamic integration of auxin transport and signalling. Current Biol 16:R424–R433

    Article  CAS  Google Scholar 

  • Lomax TL, Muday GK, Rubery PH (1995) Auxin transport. In: Davies PJ (ed) Plant Hormones. Kluwer Academic Publishers, Dordrecht, pp 509–530

    Google Scholar 

  • Marchant A, Kargul J, May ST, Muller P, Delbarre A, Perrot-Rechenmann C, Bennett MJ (1999) AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. EMBO J 18:2066–2073

    Article  PubMed  CAS  Google Scholar 

  • Morgan PW (1985) Chemical manipulation of abscission and desiccation. Beltsville Symp Agric Res 8:61–67

    CAS  Google Scholar 

  • Muday GK, Haworth P (1994) Tomato root growth, gravitropism, and lateral development: correlation with auxin transport. Plant Physiol Biochem 32(2):193–203

    PubMed  CAS  Google Scholar 

  • Muday GK, Brunn SA, Haworth P, Subramanian M (1993) Evidence for a single naphthylphthalamic acid binding site on the zucchini plasma membrane. Plant Physiol 103:449–456

    PubMed  CAS  Google Scholar 

  • Murphy A, Peer WA, Taiz L (2000) Regulation of auxin transport by aminopeptidases and endogenous flavonoids. Planta 211(3):315–324

    Article  PubMed  CAS  Google Scholar 

  • Murphy AS, Hoogner KR, Peer WA, Taiz L (2002) Identification, purification, and molecular cloning of N-1-naphthylphthalmic acid- binding plasma membrane-associated aminopeptidases from Arabidopsis. Plant Physiol 128:935–950

    Article  PubMed  CAS  Google Scholar 

  • Noh B, Murphy AS, Spalding EP (2001) Multi-drug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development. Plant Cell 13:2441–2454

    Article  PubMed  CAS  Google Scholar 

  • Osborne DJ (1989) Abscission. Crit Rev Plant Sci 8(2):103–129

    Article  CAS  Google Scholar 

  • Parry G, Delbarre A, Marchant A, Swarup R, Napier R, Perrot-Rechenmann C, Bennett MJ (2001) Novel auxin transport inhibitors phenocopy the auxin influx carrier mutation aux1. Plant J 25:399–406

    Article  PubMed  CAS  Google Scholar 

  • Peer WA, Bandyopadhyay A, Blakeslee JJ, Makam SN, Chen RJ, Masson PH, Murphy AS (2004) Variation in expression and protein localization of the PIN family of auxin efflux facilitator proteins in flavonoid mutants with altered auxin transport in Arabidopsis thaliana. Plant Cell 16:1898–1911

    Article  PubMed  CAS  Google Scholar 

  • Petrasek J, Mravec J, Bouchard R, Blakeslee JJ, Abas M, Seifertova D, Wisniewska J, Tadele Z, Kubes M, Covanova M, Dhonukshe P, Skupa P, Benkova E, Perry L, Krecek P, Lee OR, Fink GR, Geisler M, Murphy AS, Luschnig C, Zazímalová E, Friml J (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312:914–918

    Article  PubMed  CAS  Google Scholar 

  • Pedersen MK, Burton JD, Coble HD (2006) Effect of cyclanilide, ethephon, auxin transport inhibitors, and temperature on whole plant defoliation. Crop Sci 46:1666–1672

    Article  CAS  Google Scholar 

  • Peterson GL (1978) A simplified method for analysis of inorganic phosphate in the presence of interfering substances. Anal Biochem 84:164–172

    Article  PubMed  CAS  Google Scholar 

  • Rahman A, Bannigan A, Sulaman W, Pechter P, Blancaflor EB, Baskin TI (2007) Auxin, actin and growth of the Arabidopsis thaliana primary root. Plant J 50:514–528

    Article  PubMed  CAS  Google Scholar 

  • Reddy VR, Trent A, Acock B (1992) Mepiquat chloride and irrigation versus cotton growth and development. Agron J 84:930–933

    CAS  Google Scholar 

  • Roberts JA, Elliott KA, Gonzalez-Carranza AH (2002) Abscission, dehiscence, and other cell separation processes. Annu Rev Plant Biol 53:131–158

    Article  PubMed  CAS  Google Scholar 

  • Ross JJ, O’Neill DP, Rathbone DA (2003) Auxin-gibberellin interactions in pea: integrating the old with the new. J Plant Growth Regul 22:99–108

    Article  CAS  Google Scholar 

  • Rubery PH (1990) Phytotropins: receptors and endogenous ligands. Symp Soc Exp Biol 44:119–146

    PubMed  CAS  Google Scholar 

  • Ruegger M, Dewey E, Hobbie L, Brown D, Bernasconi P, Turner J, Muday G, Estelle M (1997) Reduced naphthylphthalamic acid binding in the tir3 mutant of Arabidopsis is associated with a reduction in polar auxin transport and diverse morphological defects. Plant Cell 9:745–757

    Article  PubMed  CAS  Google Scholar 

  • Schlicht M, Strnad M, Scanlon MJ, Mancuso S, Hochholdinger F, Palme K, Volkmann D, Menzel D, Baluska F (2006) Auxin immunolocalization implicates vesicular neurotransmitter-like mode of polar auxin transport in root apices. Plant Signal Behav 1:122–133

    PubMed  Google Scholar 

  • Segel IH (1976) Biochemical Calculations, 2nd edn. John Wiley & Sons, New York, pp 246–266

    Google Scholar 

  • Sexton R, Roberts JA (1982) Cell biology of abscission. Ann Rev Plant Physiol 33:133–162

    Article  CAS  Google Scholar 

  • Sieberer T, Leyser O (2006) Auxin transport, but in which direction? Science 312:58–60

    Article  Google Scholar 

  • Swarup R, Bennett M (2003) Auxin transport: the fountain of life in plants? Dev Cell 5:824–826

    Article  PubMed  CAS  Google Scholar 

  • Taylor JE, Whitelaw CA (2001) Signals in abscission. New Phytol 151:323–339

    Article  CAS  Google Scholar 

  • Teale WD, Paponov IA, Plame K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7:847–859

    Article  PubMed  CAS  Google Scholar 

  • Thomas WE, Weverman WJ, Collins JR, Koger CH, Wilcut JW (2007) Rain-free requirement and physiological properties of cotton plant growth regulators. Pest Biochem Physiol 88:247–251

    Article  CAS  Google Scholar 

  • Wilson WJ, Walker ES, Wilson WPM (1988) The role of basipetal auxin transport in the positional control of abscission sites induced in Impatiens sultani stem explants. Ann Bot 62:487–495

    CAS  Google Scholar 

  • Yang Y, Hammes UZ, Taylor CG, Schachtman DP, Nielsen E (2006) High-affinity auxin transport by the AUX1 influx carrier protein. Curr Biol 16:1123–1127

    Article  PubMed  CAS  Google Scholar 

  • Zazímalová E, Krecek P, Skůpa P, Hoyerová K, Petrásek J (2007) Polar transport of the plant hormone auxin—the role of PIN-FORMED (PIN) proteins. Cell Mol Life Sci 64:1621–1637

    Article  PubMed  CAS  Google Scholar 

  • Zhao D, Oosterhuis DM (2000) Pix plus and mepiquat chloride effects on physiology, growth, and yield of field-grown cotton. J Plant Growth Regul 19:415–422

    CAS  Google Scholar 

Download references

Acknowledgment

The authors thank Bayer Crop Science (formerly Rhone Poulenc Ag. Co) for partial funding of this research.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to James D. Burton.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Burton, J.D., Pedersen, M.K. & Coble, H.D. Effect of Cyclanilide on Auxin Activity. J Plant Growth Regul 27, 342–352 (2008). https://doi.org/10.1007/s00344-008-9062-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-008-9062-7

Keywords

Navigation