Advertisement

Acta Physiologiae Plantarum

, Volume 35, Issue 7, pp 2251–2258 | Cite as

Identification of dehydrocostus lactone and 4-hydroxy-β-thujone as auxin polar transport inhibitors

  • Junichi Ueda
  • Yuta Toda
  • Kiyotaka Kato
  • Yuichi Kuroda
  • Tsukasa Arai
  • Tsuyoshi Hasegawa
  • Hideyuki Shigemori
  • Koji Hasegawa
  • Jinichiro Kitagawa
  • Kensuke Miyamoto
  • Eiji Uheda
Original Paper

Abstract

The survey of naturally occurring of auxin polar transport regulators in Asteraceae was investigated using the radish (Raphanus sativus L.) hypocotyl bioassay established in this study. Significant auxin polar transport was observed when radiolabeled indole-3-acetic acid (IAA) was applied at the apical side of radish hypocotyl segments, but not when it was applied at the basal side of the segments. Almost no auxin polar transport was observed in radish hypocotyl segments treated with synthetic auxin polar transport inhibitors of N-(1-naphthyl)phthalamic acid (NPA) and 9-hydroxyfluorene-9-carboxylic acid (HFCA) at 0.5 μg/plant. 2,3,5-Triiodobenzoic acid (TIBA) at 0.5 μg/plant was less effective than NPA and HFCA, and p-chlorophenoxyisobutyric acid (PCIB) at 0.5 μg/plant had almost no effect on auxin polar transport in the radish hypocotyl bioassay. These results strongly suggest that the radish hypocotyl bioassay is suitable for the detection of bioassay-derived auxin polar transport regulators. Using the radish hypocotyl bioassay and physicochemical analyses, dehydrocostus lactone (decahydro-3,6,9-tris-methylene-azulenol(4,5-b)furan-2(3H)-one) and 4-hydroxy-β-thujone (4-hydroxy-4-methyl-1-(1-methylethyl)-bicyclo[3.1.0]hexan-3-one) were successfully identified as auxin polar transport inhibitors from Saussurea costus and Arctium lappa, and Artemisia absinthium, respectively. About 50 and 40 % inhibitions of auxin polar transport in radish hypocotyl segments were observed at 2.5 μg/plant pre-treatment (see “Materials and methods”) of dehydrocostus lactone and 4-hydroxy-β-thujone, respectively. Although the mode of action of these compounds in inhibiting auxin polar transport has not been clear yet, their possible mechanisms are discussed.

Keywords

Auxin polar transport Dehydrocostus lactone 4-Hydroxy-β-thujone Inhibitor Asteraceae 

Abbreviations

GC-MS

Combined gas–liquid chromatography–mass spectrometry

HFCA

9-Hydroxyfluorene-9-carboxylic acid

1H-NMR

Proton nuclear magnetic resonance

IAA

Indole-3-acetic acid

NPA

N-(1-Naphthyl)phthalamic acid

PCIB

p-Chlorophynoxyisobutyric acid

TIBA

2,3,5-Triiodobenzoic acid

TLC

Thin-layer chromatography

Notes

Acknowledgments

This work was partially supported by JSPS KAKENHI Grant Number 23510260.

References

  1. Bernasconi P, Patel BC, Reagan JD, Subramanian MV (1996) The N-1-naphthylphthalamic acid-binding protein is an integral membrane protein. Plant Physiol 111:427–432PubMedGoogle Scholar
  2. Brown DE, Rashotte AM, Murphy AS, Normanly J, Tague BW, Peer WA, Taiz L, Muday GK (2001) Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiol 126:524–535PubMedCrossRefGoogle Scholar
  3. Burton JD, Pedersen MK, Coble HD (2008) Effect of cyclanilide on auxin activity. J Plant Growth Regul 27:342–352CrossRefGoogle Scholar
  4. Butturini E, Cavalieri E, Carcereri de Prati A, Darra E, Rigo A, Shoji K, Murayama N, Yamazaki H, Watanabe Y, Suzuki H, Mariotto S (2011) Two naturally occurring terpenes, dehydrocostuslactone and costunolide, decrease intracellular GSH content and inhibit STAT3 activation. PLoS ONE 6:e20174. doi: 10.1371/journal.pone.0020174 PubMedCrossRefGoogle Scholar
  5. Chen R, Masson PH (2005) Auxin transport and recycling of PIN proteins in plants. In: Šamaja J, Balška F, Menzel D (eds) Plant endocytosis. Springer, Berlin, pp 139–157CrossRefGoogle Scholar
  6. Gälweiler L, Guan C, Müller A, Wisman E, Mendgen K, Yephremov A, Palme K (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282:2226–2230PubMedCrossRefGoogle Scholar
  7. Geldner N, Friml J, Stierhof Y-D, Jürgens G, Palme K (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413:425–428PubMedCrossRefGoogle Scholar
  8. He X, Ortiz de Montellano PR (2004) Radical rebound mechanism in cytochrome P-450-catalyzed hydroxylation of the multifaceted radical clocks α- and β-thujone. J Biol Chem 279:39479–39484PubMedCrossRefGoogle Scholar
  9. Höld KM, Sirisoma NS, Ikeda T, Narahashi T, Casida JE (2000) α-Thujone (the active component of absinthe): γ-aminobutyric acid type A receptor modulation and metabolic detoxification. PNAS 97:3826–3831PubMedCrossRefGoogle Scholar
  10. Höld KM, Sirisoma NS, Casida JE (2001) Detoxification of α- and β-thujones (the active ingredients of absinthe): site specificity and species differences in cytochrome P450 oxidation in vitro and in vivo. Chem Res Toxicol 14:589–595PubMedCrossRefGoogle Scholar
  11. Hoshino T, Miyamoto K, Ueda J (2006) Requirement of the gravity-controlled transport of auxin for a negative gravitropic response in early growth stage of etiolated pea epicotyls. Plant Cell Physiol 47:1496–1508PubMedCrossRefGoogle Scholar
  12. Hoshino T, Miyamoto K, Ueda J (2007) Gravity-controlled asymmetrical transport of auxin regulates a gravitropic response in the early growth stage of etiolated pea (Pisum sativum) epicotyls: studies using simulated microgravity conditions on a three-dimensional clinostat and using an agravitropic mutant, ageotropum. J Plant Res 120:619–628PubMedCrossRefGoogle Scholar
  13. Hussain S, Tripathi D, Sharma M (2011) Synthesis and biological study of some new derivatives of sesquiterpene lactones isolated from medicinal plants. J Phys Sci 22:57–75Google Scholar
  14. Joel DM, Chaudhuri SK, Plakhine D, Ziadna H, Steffens JC (2011) Dehydrocostus lactone is exuded from sunflower roots and stimulates germination of the root parasite Orobanche cumana. Phytochemistry 72:624–634PubMedCrossRefGoogle Scholar
  15. Judþentienë A, Mockutë D (2004) Chemical composition of essential oils of Artemisia absinthium L. (wormwood) growing wild in Vilnius. Chemija 15:64–68Google Scholar
  16. Kim J-Y, Henrichs S, Bailly A, Vincenzetti V, Sovero V, Mancuso S, Pollmann S, Kim D, Geisler M, Nam H-G (2010) Identification of an ABCB/P-glycoprotein-specific inhibitor of auxin transport by chemical genomics. J Biol Chem 285:23309–23317PubMedCrossRefGoogle Scholar
  17. Konaklieva MI, Plotkin BJ (2005) Lactones: generic inhibitors of enzymes? Mini Rev Med Chem 5:73–95PubMedCrossRefGoogle Scholar
  18. Krecek P, Skupa P, Libus J, Naramoto S, Tejos R, Friml J, Zazímalová E (2009) The PIN-FORMED (PIN) protein family of auxin transporters. Genome Biol 10:249. doi: 10.1186/gb-2009-10-12-249 PubMedCrossRefGoogle Scholar
  19. Lomax TL, Muday GK, Rubery H (1995) Auxin transport. In: Davis PJ (ed) Plant hormones. Kluwer Academic Publishers, Dordrecht, pp 509–530Google Scholar
  20. 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 18:2066–2073PubMedCrossRefGoogle Scholar
  21. Matsuda H, Kagerura T, Toguchida I, Ueda H, Morikawa T, Yoshikawa M (2000) Inhibitory effects of sesquiterpenes from bay leaf on nitric oxide production in lipopolysaccharide-activated macrophages: structure requirement and role of heat shock protein induction. Life Sci 66:2151–2157PubMedCrossRefGoogle Scholar
  22. Maya DJ, Cassels BK, Iturriaga-Vásquez P, Ferreira J, Faúndez M, Galanti N, Ferreira A, Morello A (2007) Mode of action of natural and synthetic drugs against Trypanosoma cruzi and their interaction with the mammalian host. Comp Biochem Physiol Part A 146:601–620CrossRefGoogle Scholar
  23. Michalke W, Katekar GF, Geissler AE (1992) Phytotropin-binding sites and auxin transport in Cucurbita pepo: evidence for two recognition sites. Planta 181:254–260Google Scholar
  24. Muday GK, Brunn SA, Haworth P, Subramanian M (1993) Evidence for a single naphthylphthalamic acid binding site on the zucchini plasma membrane. Plant Physiol 103:449–456PubMedGoogle Scholar
  25. Nishimura T, Matano N, Morishima T, Kakinuma C, Hayashi K, Komano T, Kubo M, Hasebe M, Kasahara H, Kamiya Y, Koshiba T (2012) Identification of IAA transport inhibitors including compounds affecting cellular PIN trafficking by two chemical screening approaches using maize coleoptile systems. Plant Cell Physiol 53:1671–1682PubMedCrossRefGoogle Scholar
  26. Noh B, Murphy AS, Spalding EP (2001) Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development. Plant Cell 13:2441–2454PubMedGoogle Scholar
  27. Noh B, Bandyopadhyay A, Peer WA, Spalding EP, Murphy AS (2003) Enhanced gravi- and phototropism in plant mdr mutants mislocalizing the auxin efflux protein PIN1. Nature 423:999–1002PubMedCrossRefGoogle Scholar
  28. Oka M, Ueda J, Miyamoto K, Yamamoto R, Hoson T, Kamisaka S (1995) Effect of simulated microgravity on auxin polar transport in inflorescence axis of Arabidopsis thaliana. Biol Sci Space 9:331–336PubMedCrossRefGoogle Scholar
  29. Oka M, Miyamoto K, Okada K, Ueda J (1999) Auxin polar transport and flower formation in Arabidopsis thaliana transformed with indoleacetamide hydrolase (iaaH) gene. Plant Cell Physiol 40:231–237PubMedCrossRefGoogle Scholar
  30. Okada K, Ueda J, Komaki MK, Bell CJ, Shimura Y (1991) Requirement of auxin polar transport system in early stage of Arabidopsis floral bud formation. Plant Cell 3:677–684PubMedGoogle Scholar
  31. 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 transport and diverse morphological defects. Plant Cell 9:745–757PubMedGoogle Scholar
  32. Santelia D, Vincenzetti V, Azzarello E, Bovet L, Fukao Y, Duchtig P, Mancuso S, Martinoia E, Geisler M (2005) MDR-like ABC transporter AtPGP4 is involved in auxin-mediated lateral root and root hair development. FEBS Lett 579:5399–5406PubMedCrossRefGoogle Scholar
  33. Santelia D, Henrichs S, Vincenzetti V, Sauer M, Bigler L, Klein M, Bailly A, Lee Y, Friml J, Geisler M, Martinoia E (2008) Flavonoids redirect PIN-mediated polar auxin fluxes during root gravitropic responses. J Biol Chem 283:31218–31226PubMedCrossRefGoogle Scholar
  34. Singh IP, Talwar KK, Arora JK, Chhabra BR, Kalsi PS (1992) A biologically active guaianolide from Saussurea lappa. Phytochemistry 31:2529–2531CrossRefGoogle Scholar
  35. Sun CM, Syu W Jr, Don MJ, Lu JJ, Lee GH (2003) Cytotoxic sesquiterpene lactones from the root of Saussurea lappa. J Nat Prod 66:1175–1180PubMedCrossRefGoogle Scholar
  36. Sussman MR, Goldsmith MHM (1981) The action of specific inhibitors of auxin transport on uptake of auxin and binding of N-naphthylphthalamic acid to a membrane site in maize coleoptiles. Planta 152:13–18CrossRefGoogle Scholar
  37. Swarup R, Friml J, Marchant A, Ljung K, Sandberg G, Palme K, Bennett M (2001) Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes Dev 15:2648–2653PubMedCrossRefGoogle Scholar
  38. Tetley RM, Thimann KV (1975) The metabolism of oat leaves during senescence. IV. The effects of α,α′-dipyridyl and other metal chelators on senescence. Plant Physiol 56:140–142PubMedCrossRefGoogle Scholar
  39. Thimann KV (1977) Polarity and the transport of auxin. In: Hormon action in the whole life of plants. The University of Massachusetts Press, Amherst, pp 71–92Google Scholar
  40. Thomson KS, Leopold AC (1974) In vitro binding of morphactins and 1-N-naphthylphthalamic acid in corn coleoptiles and their effect on auxin transport. Planta 115:259–270CrossRefGoogle Scholar
  41. Thomson KS, Hertel R, Muller S, Tavares JE (1973) 1-N-Naphthylphthalamic acid and 2,3,5-triiodobenzoic acid. In-vitro binding to particulate cell fractions and action on auxin transport in corn coleoptiles. Planta 109:337–352CrossRefGoogle Scholar
  42. Ueda J, Miyamoto K, Uheda E, Oka M (2011) Auxin transport and a graviresponse in plants: relevance to ABC proteins. Biol Sci Space 25:69–75CrossRefGoogle Scholar
  43. Wendy AP, Murphy AS (2007) Flavonoids and auxin transport: modulators or regulators? Trends Plant Sci 12:556–563CrossRefGoogle Scholar
  44. Yokota T, Murofushi N, Takahashi N (1980) Extraction, purification, and identification. In: MacMillan J (ed) Hormonal regulation of development I. Encyclopedia of Plant Physiology, vol 9. Springer, Berlin, pp 113–201 Google Scholar
  45. Yoshikawa M, Shimoda H, Uemura T, Morikawa T, Kawahara Y, Matsuda H (2000) Alcohol absorption inhibitors from bay leaf (Laurus nobilis): structure-requirements of sesquiterpenes for the activity. Bioorg Med Chem 8:2071–2077PubMedCrossRefGoogle Scholar
  46. Yuuya S, Hagiwara H, Suzuki T, Ando M, Yamada A, Suda K, Kataoka T, Nagai K (1999) Guaianolides as immunomodulators. Synthesis and biological activities of dehydrocostus lactone, mokkolactone, eremanthin, and their derivatives. J Nat Prod 62:22–30PubMedCrossRefGoogle Scholar
  47. Zheng X, Miller ND, Lewis DR, Christians MJ, Lee K-H, Muday GK, Spalding EP, Vierstra RD (2011) AUXIN UP-REGULATED F-BOX PROTEIN1 regulates the cross Talk between auxin transport and cytokinin signaling during plant root growth. Plant Physiol 156:1878–1893PubMedCrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2013

Authors and Affiliations

  • Junichi Ueda
    • 1
  • Yuta Toda
    • 1
  • Kiyotaka Kato
    • 1
  • Yuichi Kuroda
    • 1
  • Tsukasa Arai
    • 2
  • Tsuyoshi Hasegawa
    • 2
  • Hideyuki Shigemori
    • 2
  • Koji Hasegawa
    • 2
  • Jinichiro Kitagawa
    • 3
  • Kensuke Miyamoto
    • 4
  • Eiji Uheda
    • 1
  1. 1.Graduate School of Science, Osaka Prefecture UniversitySakaiJapan
  2. 2.Graduate School of Life and Environmental Sciences, University of TsukubaTsukubaJapan
  3. 3.Koshiro Co. Ltd.KameokaJapan
  4. 4.Faculty of Liberal Arts and Sciences, Osaka Prefecture UniversitySakaiJapan

Personalised recommendations