Skip to main content
Log in

Diurnal rhythmicity of endogenous phytohormones and phototropic bending capacity in potato (Solanum tuberosum L.) shoot cultures

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Taking advantage of advanced high performance liquid chromatography–electrospray tandem–mass spectrometry (HPLC–ESI–MS/MS), we screened daily changes in concentrations of endogenous phytohormones of in vitro grown potato (Solanum tuberosum L. cv. Désirée) shoot cultures and checked for possible connections between the rhythmicity of endogenous phytohormones and phototropic bending capacity of the same cultures. Studies done under diurnal 16 h light and 8 h darkness (diurnal) and continuous light (CL) conditions showed prominent daily rhythmicity of endogenous phytohormone levels in both light regimes. Phototropic bending in potato is known to be rhythmic only in the diurnal, whereas in CL conditions the bending response is present but without any daily rhythmicity. For all of the studied phytohormone groups significant differences between the diurnal and CL conditions were found. Changes in the concentration of indole auxins, indole-3-acetic acid (IAA) and its catabolite 2-oxindole-3-acetic acid (OxIAA), were the most prominent. Their levels clearly alternated with level of IAA being high in diurnal and OxIAA in CL conditions. Significant concentration changes were also observed for other phytohormones such as cytokinin ribosides, salicylic acid, abscisic acid and phaseic acid. Observed changes in daily phytohormone levels indicate strong and complex involvement of diverse phytohormone groups in realization of the phototropic bending response of potato shoots.

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

Similar content being viewed by others

References

  • Aksenova NP, Konstatinova TN, Golyanovskaya SA, Sergeeva LI, Romanov GA (2012) Hormonal regulation of tuber formation in potato plants. Russ J Plant Physiol 59:491–508

    Article  CAS  Google Scholar 

  • Alabadi D, Gil J, Blázquez MA, García-Martínez JL (2004) Gibberellins repress photomorphogenesis in darkness. Plant Physiol 134:1050–1057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bruinsma J, Karssen CM, Benschop M, Van Dort JB (1975) Hormonal regulation of phototropism in the light grown sunflower seedling, Helianthus annuus L.: immobility of endogenous indoleacetic acid and inhibition of hypocotyl growth by illuminted cotyledons. J Exp Bot 26:411–418

    Article  CAS  Google Scholar 

  • Collett CE, Harberd NP, Leyser O (2000) Hormonal interactions in the control of Arabidopsis hypocotyl elongation. Plant Physiol 124:553–561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Covington MF, Harmer SL (2007) The circadian clock regulates auxin signaling and responses in Arabidopsis. PLoS Biol 5:e222. https://doi.org/10.1371/journal.pbio.0050222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cowling RJ, Harberd NP (1999) Gibberellins control Arabidopsis hypocotyl growth via regulation of cellular elogation. J Exp Biol 50:1351–1357

    CAS  Google Scholar 

  • Djilianov DL, Dobrev PI, Moyankova DP, Vankova R, Georgieva DT, Gajdosova S, Motyka V (2013) Dynamics of endogenous phytohormones during desiccation and recovery of the resurrection plant species Haberlea rhodopensis. J Plant Growth Regul 32:564–574

    Article  CAS  Google Scholar 

  • Dobrev PI, Vankova R (2012) Quantification of abscisic acid, cytokinin, and auxin content in salt-stressed plant tissues. Methods Mol Biol 913:251–261

    CAS  PubMed  Google Scholar 

  • Dodd AN, Salathia N, Hall A, Kévei E, Tóth R, Nagy F, Hibberd JM, Millar AJ, Webb AAR (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309:630–633

    Article  CAS  PubMed  Google Scholar 

  • Dragićević I, Konjević R, Vinterhalter B, Vinterhalter D, Nešković M (2008) The effects of IAA and tetcyclacis on tuberization in potato (Solanum tuberosum L.) shoot cultures in vitro. Plant Growth Regul 54:189–193

    Article  CAS  Google Scholar 

  • Edwards KD, Takata N, Johansson M et al (2018) Circadian clock components control daily growth activities by modulating cytokinin levels and cell division-associated gene expression in Populus trees. Plant Cell Environ 41:1468–1482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Esmon A, Tinsley AG, Ljung K, Sandberg G, Hearne LB, Liscum E (2006) A gradient of auxin and auxin-dependent transcription precedes tropic growth responses. Proc Nat Acad Sci USA 103:236–241

    Article  CAS  PubMed  Google Scholar 

  • Friedman H, Meir S, Halevy AH, Philosoph-Hadas S (2003) Inhibition of the gravitropic bending response of flowering shoots by salicylic acid. Plant Sci 165:905–911

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Friml J, Wisniewska J, Benkova E, Mendgen K, Palme K (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415:806–809

    Article  PubMed  Google Scholar 

  • Haga K, Sakai T (2012) PIN auxin efflux carriers are necessary for pulse-induced but not continuous light-Induced phototropism in Arabidopsis. Plant Physiol 160:763–776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hall A, Kozma-Bognar L, Tóth R, Nagy F, Millar AJ (2001) Conditional circadian regulation of PHYTOCHROME gene expression. Plant Physiol 127:1808–1818

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hannapel DJ (2007) Signaling the induction of tuber formation. In: Vreugdenhil D (ed) Potato biology and biotechnology: advances and perspectives. Elsevier, Amsterdam

    Google Scholar 

  • Harmer SL, Hogenesch JB, Straume M, Chang et al (2000) Orchestrated transcription of key pathways in Arbidopsis by the circadian clock. Science 290:2110–2113

    Article  CAS  PubMed  Google Scholar 

  • Hussey G, Stacey NJ (1981) In vitro propagation of potato (Solanum tuberosum L.). Ann Bot 48:787–796

    Article  Google Scholar 

  • Hussey G, Stacey NJ (1984) Factors affecting the formation of in vitro tubers of potato (Solanum tuberosum L.). Ann Bot 53:565–578

    Article  CAS  Google Scholar 

  • Jackson SD (1999) Multiple signaling pathways control tuber induction in potato. Plant Physiol 119:1–8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Janoudi A, Poff KL (1990) A common fluence threshold for first positive and second positive phototropism in Arabidopsis. Plant Physiol 94:1605–1608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jouve L, Gaspar T, Kevers C, Greppin H, Degli Agosti R (1999) Involvement of indole-3-acetic acid in the circadian growth of the first internode of Arabidopsis. Planta 209:136–142

    Article  CAS  PubMed  Google Scholar 

  • Kamínek M, Brezinova A, Gaudinova A, Motyka V, Vankova R, Zazimalova E (2000) Purine cytokinins: a proposal of abbreviations. Plant Growth Regul 32:253–256

    Article  Google Scholar 

  • Koda Y, Kikuta Y, Tazaki H, Tsujino Y, Sakamura S, Yoshihara T (1991) Potato tuber-inducing activities of jasmonic acid and related compounds. Phytochemistry 30:1435–1438

    Article  CAS  Google Scholar 

  • Macháčková I, Konstatinova TN, Sergeeva LI, Lozhnikova VN, Golyanovskaya SA, Dudko ND, Eder J, Aksenova NP (1998) Photoperiodic control of growth, development and phytohormone balance in Solanum tuberosum. Physiol Plant 102:272–278

    Article  Google Scholar 

  • Michael TP, Breton G, Hazen SP, Priest H, Mockler TC, Kay SA, Chory J (2008) A morning-specific phytohormone gene expression program underlying rhythmic plant growth. PLoS Biol 6(9):e225. https://doi.org/10.1371/journal.pbio.0060225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Müller D, Leyser O (2011) Auxin, cytokinin and the control of shoot branching. Ann Bot 107:1203–1212

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Nováková M, Motyka V, Dobrev PI, Malbeck J, Gaudinová A, Vanková R (2005) Diurnal variation of cytokinin, auxin and abscisic acid levels in tobacco leaves. J Exp Bot 56:2877–2883

    Article  PubMed  Google Scholar 

  • Östin A, Kowalyczk M, Bhalerao RP, Sandberg G (1998) Metabolism of indole-3-acetic acid in Arabidopsis. Plant Physiol 118:285–296

    Article  PubMed  PubMed Central  Google Scholar 

  • Peer WA, Cheng Y, Murphy AS (2013) Evidence of oxidative attenuation of auxin signaling. J Exp Bot 64:2619–2639

    Article  CAS  Google Scholar 

  • Pelacho AM, Mingo-Castel AM (1991) Jasmonic acid induces tuberization of potato stolons cultured in vitro. Plant Physiol 97:1253–1255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pěnčík A, Simonovik B, Petersson SV, Henyková E et al (2013) Regulation of auxin homeostasis and gradients in Arabidopsis roots through the formation of the indole-3-acetic acid catabolite 2-oxindole-3-acetic acid. Plant Cell 25:3858–3870

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Quinones MA, Zeiger E (1994) Putative roles of the xanthophyll, zeaxanthin in blue light photoreception of corn coleoptiles. Science 264:558–561

    Article  CAS  Google Scholar 

  • Raspor M, Motyka V, Žižková E, Dobrev PI, Trávníčková A et al (2012) Cytokinin profiles of AtCKX2-overexpressing potato plants and the impact of altered cytokinin homeostasis on tuberization in vitro. J Plant Growth Regul 31:460–470

    Article  CAS  Google Scholar 

  • Romanov GA, Aksenova NP, Konstatinova TN, Golyanovskaya SA, Kossmann J, Willmitzer L (2000) Effect of indole-3-acetic acid and kinetin on tuberization parameters of different cultivars and transgenic lines of potato in vitro. Plant Growth Regul 32:245–251

    Article  CAS  Google Scholar 

  • Spalding EP (2013) Diverting the downhill flow of auxin to steer growth during tropisms. Am J Bot 100:203–214

    Article  CAS  PubMed  Google Scholar 

  • Tarkowska D, Novak O, Flokova K, Tarkowski P, Turečkova V, Gruz J, Rolčik Strnad M (2014) Quo vadis plant hormone analysis? Planta 240:55–76

    Article  CAS  PubMed  Google Scholar 

  • Vinterhalter D, Vinterhalter B (2015) Phototropic responses of potato under conditions of continuous light and subsequent darkness. Plant Growth Regul 75:725–732

    Article  CAS  Google Scholar 

  • Vinterhalter D, Vinterhalter B (2016) Interaction with gravitropism, reversibility and lateral movements of phototropically stimulated potato shoots. J Plant Res 129:759–770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vinterhalter D, Vinterhalter B (2017) Phototropic bending of intact and wounded potato shoots. Plant Cell Tiss Org Cult 130:393–404

    Article  CAS  Google Scholar 

  • Vinterhalter D, Dragićević I, Vinterhalter B (2008) Potato in vitro culture techniques and biotechnology. In: Benkeblia N, Tennant P (eds) Potato I. Fruit, vegetable and cereal science and biotechnology 2 (special issue 1). Global Science Books, London, pp 16–45

    Google Scholar 

  • Vinterhalter D, Vinterhalter B, Orbović V (2012) Photo- and gravitropic bending of potato plantlets obtained in vitro from single-node explants. J Plant Growth Regul 31(4):560–569

    Article  CAS  Google Scholar 

  • Vinterhalter D, Vinterhalter B, Miljuš-Đukić J, Jovanović Z, Orbović V (2015) Daily changes in the competence for photo- and gravitropic response by potato plantlets (Correction). J Plant Growth Regul 34:440–450

    Article  CAS  Google Scholar 

  • Voss U, Wilson MH, Kenobi K et al (2015) The circadian clock rephases during lateral root organ initiation in Arabidopsis thaliana. Nature Commun. https://doi.org/10.1038/ncomms8641

    Article  Google Scholar 

  • Vreugdenhil D, Struik PC (1989) An integrated view of the hormonal regulation of tuber formation in potato (Solanum tuberosum). Physiol Plant 75:525–531

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Xu X, van Lammeren AAM, Vermeer E, Vreugdenhil D (1998) The role of gibberellin, abscisic acid, and sucrose in the regulation of potato tuber formation in vitro. Plant Physiol 117:575–584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang T, Davies PJ, Reid JB (1996) Genetic dissection of the relative roles of auxin and gibberellin in the regulation of stem elongation in intact light-grown peas. Plant Physiol 110:1029–1034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zažímalová E, Murphy AS, Yang H, Hoyerová K, Hošek P (2010) Auxin transporters: why so many? Cold Spring Harb Perspect Biol. https://doi.org/10.1101/cshperspect.a001552

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Zhou W, Li H (2005) The role of GA, IAA and BAP in the regulation of in vitro shoot growth and microtuberization in potato. Acta Phys Plant 27:363–369

    Article  CAS  Google Scholar 

  • Zhang J, Lin JE, Harris C, Pereira FCM, Wu F, Blakeslee JJ, Peer WA (2016) DAO1 catalyzes temporal and tissue-specific oxidative inactivation of auxin in Arabidopsis thaliana. Proc Natl Acad Sci USA 113:11010–11015

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Work was supported by the Czech Science Foundation (Grant No. 19-12262S) and the Ministry of Education, Youth and Sports of Czech Republic from European Regional Development Fund-Project “Centre for Experimental Plant Biology” (No. CZ.02.1.01/0.0/0.0/16_019/0000738), Swiss National Science Fondation SCOPES project 152221 headed by Christian Fankhauser and by Serbian Ministry of Education, Science and Technological Development (Project ON 173015). The authors are grateful to Marie Korecka for invaluable technical support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. Vinterhalter.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vinterhalter, D., Savić, J., Stanišić, M. et al. Diurnal rhythmicity of endogenous phytohormones and phototropic bending capacity in potato (Solanum tuberosum L.) shoot cultures. Plant Growth Regul 90, 151–161 (2020). https://doi.org/10.1007/s10725-019-00561-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-019-00561-8

Keywords

Navigation