Skip to main content
SpringerLink
Log in

Dose- and tissue-specific interaction of monoterpenes with the gibberellin-mediated release of potato tuber bud dormancy, sprout growth and induction of α-amylases and β-amylases

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

Abstract

Gibberellins (GA) are involved in bud dormancy release in several species. We show here that GA-treatment released bud dormancy, initiated bud sprouting and promoted sprout growth of excised potato tuber bud discs (‘eyes’). Monoterpenes from peppermint oil (PMO) and S-(+)-carvone (CAR) interact with the GA-mediated bud dormancy release in a hormesis-type response: low monoterpene concentrations enhance dormancy release and the initiation of bud sprouting, whereas high concentrations inhibit it. PMO and CAR did, however, not affect sprout growth rate after its onset. We further show that GA-induced dormancy release is associated with tissue-specific regulation of α- and β-amylases. Molecular phylogenetic analysis shows that potato α-amylases cluster into two distinct groups: α-AMY1 and α-AMY2. GA-treatment induced transcript accumulation of members of both α-amylase groups, as well as α- and β-amylase enzyme activity in sprout and ‘sub-eye’ tissues. In sprouts, CAR interacts with the GA-mediated accumulation of α-amylase transcripts in an α-AMY2-specific and dose-dependent manner. Low CAR concentrations enhance the accumulation of α-AMY2-type α-amylase transcripts, but do not affect the α-AMY1-type transcripts. Low CAR concentrations also enhance the accumulation of α- and β-amylase enzyme activity in sprouts, but not in ‘sub-eye’ tissues. In contrast, high CAR concentrations have no appreciable effect in sprouts on the enzyme activities and the α-amylase transcript abundances of either group. The dose-dependent effects on the enzyme activities and the α-AMY2-type α-amylase transcripts in sprouts are specific for CAR but not for PMO. Different monoterpenes therefore may have specific targets for their interaction with hormone signalling pathways.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

GA:

Gibberellin

CIPC:

Isopropyl N-(3-chlorophenyl)carbamate

CAR:

S-(+)-Carvone

PMO:

Peppermint oil

CON:

Control

References

  • An M (2005) Mathematical modelling of dose–response relationship (hormesis) in allelopathy and its application. Nonlinearity Biol Toxicol Med 3:153–172

    Article  PubMed  CAS  Google Scholar 

  • Barrero JM, Talbot MJ, White RG, Jacobsen JV, Gubler F (2009) Anatomical and transcriptomic studies of the coleorhiza reveal the importance of this tissue in regulating dormancy in barley. Plant Physiol 150:1006–1021

    Article  PubMed  CAS  Google Scholar 

  • Bassel GW, Lan H, Glaab E, Gibbs DJ, Gerjets T, Krasnogor N, Bonner AJ, Holdsworth MJ, Provart NJ (2011) Genome-wide network model capturing seed germination reveals coordinated regulation of plant cellular phase transitions. Proc Natl Acad Sci USA 108:9709–9714

    Article  PubMed  CAS  Google Scholar 

  • Baydar H, Karadoğan T (2003) The effects of volatile oils on in vitro potato sprout growth. Potato Res 46:1–8

    Article  Google Scholar 

  • Biemelt S, Hajirezaei M, Hentschel E, Sonnewald U (2000) Comparative analysis of abscisic acid content and starch degradation during storage of tubers harvested from different potato varieties. Potato Res 43:371–382

    Article  CAS  Google Scholar 

  • Bozonnet S, Jensen MT, Nielsen MM, Aghajari N, Jensen MH, Kramhøft B, Willemoës M, Tranier S, Haser R, Svensson B (2007) The ‘pair of sugar tongs’ site on the non-catalytic domain C of barley α-amylase participates in substrate binding and activity. FEBS J 274:5055–5067

    Article  PubMed  CAS  Google Scholar 

  • Bradford KJ, Trewavas J (1994) Sensitivity thresholds and variable time scales in plant hormone action. Plant Physiol 105:1029–1036

    PubMed  CAS  Google Scholar 

  • Calabrese EJ, Blain RB (2009) Hormesis and plant biology. Environ Pollut 157:42–48

    Article  PubMed  CAS  Google Scholar 

  • Calabrese EJ, Bachmann KA, Bailer AJ, Bolger PM, Borak J, Cai L, Cedergreen N, Cherian MG, Chiueh CC, Clarkson TW et al (2007) Biological stress response terminology: Integrating the concepts of adaptive response and preconditioning stress within a hormetic dose–response framework. Toxicol Appl Pharmacol 222:122–128

    Article  PubMed  CAS  Google Scholar 

  • Campbell MA, Gleichsner A, Alsbury R, Horvath D, Suttle J (2010) The sprout inhibitors chlorpropham and 1,4-dimethylnaphthalene elicit different transcriptional profiles and do not suppress growth through a prolongation of the dormant state. Plant Mol Biol 73:181–189

    Article  PubMed  CAS  Google Scholar 

  • Clegg MD, Rappaport L (1970) Regulation of bud rest in tubers of potato, Solanum tuberosum L: VI. Biochemical changes induced in excised potato buds by gibberellic acid. Plant Physiol 45:8–13

    Article  PubMed  CAS  Google Scholar 

  • Cuttler EG (1978) Structure and development of the potato plant. In: Harris PM (ed) The potato crop. Chapman Hall, London, pp 70–152

    Google Scholar 

  • Davies HV, Viola R (1988) The effect of gibberellic acid on starch breakdown in sprouting tubers of Solanum tuberosum L. Ann Bot 61:689–693

    CAS  Google Scholar 

  • Delaplace P, Fauconnier ML, Sergeant K, Dierick JF, Oufir M, van der Wal F, America AH, Renaut J, Hausman JF, du Jardin P (2009) Potato (Solanum tuberosum L.) tuber ageing induces changes in the proteome and antioxidants associated with the sprouting pattern. J Exp Bot 60:1273–1288

    Article  PubMed  CAS  Google Scholar 

  • Destefano-Beltran L, Knauber D, Huckle L, Suttle J (2006a) Chemically forced dormancy termination mimics natural dormancy progression in potato tuber meristems by reducing ABA content and modifying expression of genes involved in regulating ABA synthesis and metabolism. J Exp Bot 57:2879–2886

    Article  PubMed  CAS  Google Scholar 

  • Destefano-Beltran L, Knauber D, Huckle L, Suttle JC (2006b) Effects of postharvest storage and dormancy status on ABA content, metabolism, and expression of genes involved in ABA biosynthesis and metabolism in potato tuber tissues. Plant Mol Biol 61:687–697

    Article  PubMed  CAS  Google Scholar 

  • Dimandja J-MD, Stanfill SB, Grainger J, Patterson DG (2000) Application of comprehensive two-dimensional gas chromatography (GC × GC) to the qualitative analysis of essential oils. J High Resol Chromat 23:208–214

    Article  CAS  Google Scholar 

  • Duke SO, Cedergreen N, Velini ED, Belz RG (2006) Hormesis: is it an important factor in herbicide use and allelopathy? Outlooks Pest Manag: 29–33. doi:10.1564/16feb10

  • Eshel D, Orenstein J, Tsror L, Hazanovsky M (2009) Environmentally friendly method for the control of sprouting and tuber-borne diseases in stored potato. Acta Horticult 830:363–368

    Google Scholar 

  • Fernie AR, Willmitzer L (2001) Molecular and biochemical triggers of potato tuber development. Plant Physiol 127:1459–1465

    Article  PubMed  CAS  Google Scholar 

  • Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171:501–523

    Article  PubMed  CAS  Google Scholar 

  • Gerjets T, Scholefield D, Foulkes MJ, Lenton JR, Holdsworth MJ (2010) An analysis of dormancy, ABA responsiveness: after-ripening and pre-harvest sprouting in hexaploid wheat (Triticum aestivum L.) caryopses. J Exp Bot 61:597–607

    Article  PubMed  CAS  Google Scholar 

  • Godard KA, White R, Bohlmann J (2008) Monoterpene-induced molecular responses in Arabidopsis thaliana. Phytochemistry 69:1838–1849

    Article  PubMed  CAS  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Hartmann A, Senning M, Hedden P, Sonnewald U, Sonnewald S (2011) Reactivation of meristem activity and sprout growth in potato tubers require both cytokinin and gibberellin. Plant Physiol 155:776–796

    Article  PubMed  CAS  Google Scholar 

  • Hermann K, Meinhard J, Dobrev P, Linkies A, Pesek B, Heß B, Machackova I, Fischer U, Leubner-Metzger G (2007) 1-Aminocyclopropane-1-carboxylic acid and abscisic acid during the germination of sugar beet (Beta vulgaris L.): a comparative study of fruits and seeds. J Exp Bot 58:3047–3060

    Article  PubMed  CAS  Google Scholar 

  • Holdsworth MJ, Bentsink L, Soppe WJJ (2008) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol 179:33–54

    Article  PubMed  CAS  Google Scholar 

  • Horvath DP, Anderson JV, Chao WS, Foley ME (2003) Knowing when to grow: signals regulating bud dormancy. Trends Plant Sci 8:534–540

    Article  PubMed  CAS  Google Scholar 

  • Inderjit, Duke SO (2003) Ecophysiological aspects of allelopathy. Planta 217:529–539

    Article  PubMed  CAS  Google Scholar 

  • Kaplan F, Sung DY, Guy CL (2006) Roles of ß-amylase and starch breakdown during temperature stress. Physiol Plant 126:120–128

    Article  CAS  Google Scholar 

  • Kendig EL, Le HH, Belcher SM (2010) Defining hormesis: evaluation of a complex concentration response phenomenon. Int J Toxicol 29:235–246

    Article  PubMed  CAS  Google Scholar 

  • Kleinkopf GE, Oberg NA, Olsen NL (2003) Sprout inhibition in storage: current status, new chemistries and natural products. Am J Potato Res 80:317–327

    Article  CAS  Google Scholar 

  • Kriegs B, Jansen M, Hahn K, Peisker H, Samajova O, Beck M, Braun S, Ulbrich A, Baluska F, Schulz M (2010) Cyclic monoterpene mediated modulations of Arabidopsis thaliana phenotype: effects on the cytoskeleton and on the expression of selected genes. Plant Signal Behav 5:832–838

    Article  PubMed  CAS  Google Scholar 

  • Leubner-Metzger G (2002) Seed after-ripening and over-expression of class I ß-1,3-glucanase confer maternal effects on tobacco testa rupture and dormancy release. Planta 215:959–968

    Article  PubMed  CAS  Google Scholar 

  • Leubner-Metzger G (2003) Functions and regulation of ß-1,3-glucanase during seed germination, dormancy release and after-ripening. Seed Sci Res 13:17–34

    Article  CAS  Google Scholar 

  • Leubner-Metzger G (2007) Samendormanz und Keimungskontrolle: Gene, Umweltfaktoren und Klimawandel. Vorträge für Pflanzenzüchtung 72:87–104

    Google Scholar 

  • Leubner-Metzger G, Amrhein N (1993) The distribution of hydroxycinnamoylputrescines in different organs of Solanum tuberosum and other Solanaceous species. Phytochemistry 32:551–555

    Article  CAS  Google Scholar 

  • Linkies A, Müller K, Morris K, Turečkovác V, Cadman CSC, Corbineau F, Strnad M, Lynn JR, Finch-Savage WE, Leubner-Metzger G (2009) Ethylene interacts with abscisic acid to regulate endosperm rupture during germination: a comparative approach using Lepidium sativum and Arabidopsis thaliana. Plant Cell 21:3803–3822

    Article  PubMed  CAS  Google Scholar 

  • Lovegrove A, Hooley R (2000) Gibberellin and abscisic acid signalling in aleurone. Trends Plant Sci 5:102–110

    Article  PubMed  CAS  Google Scholar 

  • Lovett JV, Ryuntyu MY, Liu DL (1989) Allelopathy, chemical communication, and plant defense. J Chem Ecol 15:1193–1202

    Article  Google Scholar 

  • Maffei M, Camusso W, Sacco S (2001) Effect of Mentha × piperita essential oil and monoterpenes on cucumber root membrane potential. Phytochemistry 58:703–707

    Article  PubMed  CAS  Google Scholar 

  • Mitsui T, Itoh K (1997) The α-amylase multigene family. Trends Plant Sci 2:255–261

    Article  Google Scholar 

  • Nielsen TH, Deiting U, Stitt M (1997) A β-amylase in potato tubers is induced by storage at low temperature. Plant Physiol 113:503–510

    Article  PubMed  CAS  Google Scholar 

  • Oosterhaven K, Hartmans K, Scheffer J (1995a) Inhibition of potato sprout growth by carvone enantiomers and their bioconversion in sprouts. Potato Res 38:219–230

    Article  CAS  Google Scholar 

  • Oosterhaven K, Poolman B, Smid EJ (1995b) S-carvone as a natural potato sprout inhibiting, fungistatic and bacteristatic compound. Ind Crop Prod 4:23–31

    Article  CAS  Google Scholar 

  • Owolabi MS, Lajide L, Oladimeji MO, Setzer WN (2010) The effect of essential oil formulations for potato sprout suppression. Nat Prod Commun 5:645–648

    PubMed  CAS  Google Scholar 

  • Pierik R, Tholen D, Poorter H, Visser EJ, Voesenek LA (2006) The Janus face of ethylene: growth inhibition and stimulation. Trends Plant Sci 11:176–183

    Article  PubMed  CAS  Google Scholar 

  • Pujadas G, Palau J (2001) Evolution of α-amylases: architectural features and key residues in the stabilization of the (β/α)8 scaffold. Mol Biol Evol 18:38–54

    PubMed  CAS  Google Scholar 

  • Rinne PLH, Kaikuranta PM, van der Schoot C (2001) The shoot apical meristem restores its symplastic organization during chilling-induced release from dormancy. Plant J 26:249–264

    Article  PubMed  CAS  Google Scholar 

  • Rinne PL, Welling A, Vahala J, Ripel L, Ruonala R, Kangasjarvi J, van der Schoot C (2011) Chilling of dormant buds hyperinduces FLOWERING LOCUS T and recruits GA-inducible 1,3-β-glucanases to reopen signal conduits and release dormancy in Populus. Plant Cell 23:130–146

    Article  PubMed  CAS  Google Scholar 

  • Rohde A, Ruttink T, Hostyn V, Sterck L, Van Driessche K, Boerjan W (2007) Gene expression during the induction, maintenance, and release of dormancy in apical buds of poplar. J Exp Bot 58:4047–4060

    Article  PubMed  CAS  Google Scholar 

  • Rohloff J (1999) Monoterpene composition of essential oil from peppermint (Mentha × piperita L.) with regard to leaf position using solid-phase microextraction and gas chromatography/mass spectrometry analysis. J Agric Food Chem 47:3782–3786

    Article  PubMed  CAS  Google Scholar 

  • Smith AM, Zeeman SC, Smith SM (2005) Starch degradation. Annu Rev Plant Biol 56:73–98

    Article  PubMed  CAS  Google Scholar 

  • Stebbing AR (1982) Hormesis - the stimulation of growth by low levels of inhibitors. Sci Total Environ 22:213–234

    Article  PubMed  CAS  Google Scholar 

  • Stensballe A, Hald S, Bauw G, Blennow A, Welinder KG (2008) The amyloplast proteome of potato tuber. FEBS J 275:1723–1741

    Article  PubMed  CAS  Google Scholar 

  • Suttle JC (2004) Involvement of endogenous gibberellins in potato tuber dormancy and early sprout growth: a critical assessment. J Plant Physiol 161:157–164

    Article  PubMed  CAS  Google Scholar 

  • Taylor MA, George LA, Ross HA, Davies HV (1998) cDNA cloning and characterisation of an α-glucosidase gene from potato (Solanum tuberosum L.). Plant J 13:419–425

    Article  PubMed  CAS  Google Scholar 

  • Teper-Bamnolker P, Dudai N, Fischer R, Belausov E, Zemach H, Shoseyov O, Eshel D (2010) Mint essential oil can induce or inhibit potato sprouting by differential alteration of apical meristem. Planta 232:179–186

    Article  PubMed  CAS  Google Scholar 

  • Vaughn S, Spencer G (1991) Volatile monoterpenes inhibit potato tuber sprouting. Am J Potato Res 68:821–831

    Article  CAS  Google Scholar 

  • Velini ED, Alves E, Godoy MC, Meschede DK, Souza RT, Duke SO (2008) Glyphosate applied at low doses can stimulate plant growth. Pest Manag Sci 64:489–496

    Article  PubMed  CAS  Google Scholar 

  • Viola R, Pelloux J, van der Ploeg A, Gillespie T, Marquis N, Roberts AG, Hancock RD (2007) Symplastic connection is required for bud outgrowth following dormancy in potato (Solanum tuberosum L.) tubers. Plant Cell Environ 30:973–983

    Article  PubMed  CAS  Google Scholar 

  • Voegele A, Linkies A, Müller K, Leubner-Metzger G (2011) Members of the gibberellin receptor gene family GID1 (GIBBERELLIN INSENSITIVE DWARF1) play distinct roles during Lepidium sativum and Arabidopsis thaliana seed germination. J Exp Bot. doi:10.1093/jxb/err214

  • Xiong ZT, Peng YH (2001) Response of pollen germination and tube growth to cadmium with special reference to low concentration exposure. Ecotoxicol Environ Saf 48:51–55

    Article  PubMed  CAS  Google Scholar 

  • Zeeman SC, Kossmann J, Smith AM (2010) Starch: its metabolism, evolution, and biotechnological modification in plants. Annu Rev Plant Biol 61:209–234

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Our work was funded by grants from the Deutsche Forschungsgemeinschaft (Grant DFG LE720/6 and MU3114/1-1) to G.L.-M. and K.M., respectively, and the Wissenschaftliche Gesellschaft Freiburg to A.L., A.V. and Kai Graeber (licences for Geneious bioinformatics software) which are gratefully acknowledged. We also acknowledge awards related to this work to S.R. by the Faculty of Biology in Freiburg, and to M.I. in the national competition ‘Schweizer Jugend forscht’ in Switzerland. For further information see: ‘The Seed Biology Place’ - http://www.seedbiology.de.

Author information

Authors and Affiliations

  1. Faculty of Biology, Institute for Biology II, Botany/Plant Physiology, Albert-Ludwigs-University, Schänzlestr.1, 79104, Freiburg, Germany

    Sonja Rentzsch, Dagmara Podzimska, Antje Voegele, Madeleine Imbeck, Ada Linkies & Gerhard Leubner-Metzger

  2. Department of Biological Sciences, Simon Fraser University, 8888, University Drive, Burnaby, BC, V5A 1S6, Canada

    Kerstin Müller

Authors
  1. Sonja Rentzsch
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dagmara Podzimska
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Antje Voegele
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Madeleine Imbeck
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kerstin Müller
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ada Linkies
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gerhard Leubner-Metzger
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Ada Linkies or Gerhard Leubner-Metzger.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rentzsch, S., Podzimska, D., Voegele, A. et al. Dose- and tissue-specific interaction of monoterpenes with the gibberellin-mediated release of potato tuber bud dormancy, sprout growth and induction of α-amylases and β-amylases. Planta 235, 137–151 (2012). https://doi.org/10.1007/s00425-011-1501-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-011-1501-1

Keywords

Search

Navigation