Advertisement

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

  • D. VinterhalterEmail author
  • J. Savić
  • M. Stanišić
  • B. Vinterhalter
  • P. I. Dobrev
  • V. Motyka
Original paper
  • 54 Downloads

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.

Keywords

Potato In vitro Phototropism Endogenous phytohormones Diurnal rhythmicity Circadian regulation 

Notes

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.

References

  1. Aksenova NP, Konstatinova TN, Golyanovskaya SA, Sergeeva LI, Romanov GA (2012) Hormonal regulation of tuber formation in potato plants. Russ J Plant Physiol 59:491–508CrossRefGoogle Scholar
  2. Alabadi D, Gil J, Blázquez MA, García-Martínez JL (2004) Gibberellins repress photomorphogenesis in darkness. Plant Physiol 134:1050–1057PubMedPubMedCentralCrossRefGoogle Scholar
  3. 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 26:411–418CrossRefGoogle Scholar
  4. Collett CE, Harberd NP, Leyser O (2000) Hormonal interactions in the control of Arabidopsis hypocotyl elongation. Plant Physiol 124:553–561PubMedPubMedCentralCrossRefGoogle Scholar
  5. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Cowling RJ, Harberd NP (1999) Gibberellins control Arabidopsis hypocotyl growth via regulation of cellular elogation. J Exp Biol 50:1351–1357Google Scholar
  7. 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 32:564–574CrossRefGoogle Scholar
  8. Dobrev PI, Vankova R (2012) Quantification of abscisic acid, cytokinin, and auxin content in salt-stressed plant tissues. Methods Mol Biol 913:251–261PubMedPubMedCentralGoogle Scholar
  9. 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 309:630–633PubMedCrossRefPubMedCentralGoogle Scholar
  10. 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 54:189–193CrossRefGoogle Scholar
  11. 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 41:1468–1482PubMedPubMedCentralCrossRefGoogle Scholar
  12. 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 103:236–241PubMedCrossRefPubMedCentralGoogle Scholar
  13. Friedman H, Meir S, Halevy AH, Philosoph-Hadas S (2003) Inhibition of the gravitropic bending response of flowering shoots by salicylic acid. Plant Sci 165:905–911PubMedCrossRefPubMedCentralGoogle Scholar
  14. Friml J (2003) Auxin transport—shaping the plant. Curr Opin Plant Biol 6:7–12PubMedCrossRefPubMedCentralGoogle Scholar
  15. Friml J, Wisniewska J, Benkova E, Mendgen K, Palme K (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415:806–809PubMedCrossRefPubMedCentralGoogle Scholar
  16. Haga K, Sakai T (2012) PIN auxin efflux carriers are necessary for pulse-induced but not continuous light-Induced phototropism in Arabidopsis. Plant Physiol 160:763–776PubMedPubMedCentralCrossRefGoogle Scholar
  17. Hall A, Kozma-Bognar L, Tóth R, Nagy F, Millar AJ (2001) Conditional circadian regulation of PHYTOCHROME gene expression. Plant Physiol 127:1808–1818PubMedPubMedCentralCrossRefGoogle Scholar
  18. Hannapel DJ (2007) Signaling the induction of tuber formation. In: Vreugdenhil D (ed) Potato biology and biotechnology: advances and perspectives. Elsevier, AmsterdamGoogle Scholar
  19. Harmer SL, Hogenesch JB, Straume M, Chang et al (2000) Orchestrated transcription of key pathways in Arbidopsis by the circadian clock. Science 290:2110–2113PubMedCrossRefPubMedCentralGoogle Scholar
  20. Hussey G, Stacey NJ (1981) In vitro propagation of potato (Solanum tuberosum L.). Ann Bot 48:787–796CrossRefGoogle Scholar
  21. Hussey G, Stacey NJ (1984) Factors affecting the formation of in vitro tubers of potato (Solanum tuberosum L.). Ann Bot 53:565–578CrossRefGoogle Scholar
  22. Jackson SD (1999) Multiple signaling pathways control tuber induction in potato. Plant Physiol 119:1–8PubMedPubMedCentralCrossRefGoogle Scholar
  23. Janoudi A, Poff KL (1990) A common fluence threshold for first positive and second positive phototropism in Arabidopsis. Plant Physiol 94:1605–1608PubMedPubMedCentralCrossRefGoogle Scholar
  24. 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 209:136–142PubMedCrossRefPubMedCentralGoogle Scholar
  25. Kamínek M, Brezinova A, Gaudinova A, Motyka V, Vankova R, Zazimalova E (2000) Purine cytokinins: a proposal of abbreviations. Plant Growth Regul 32:253–256CrossRefGoogle Scholar
  26. Koda Y, Kikuta Y, Tazaki H, Tsujino Y, Sakamura S, Yoshihara T (1991) Potato tuber-inducing activities of jasmonic acid and related compounds. Phytochemistry 30:1435–1438CrossRefGoogle Scholar
  27. 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 102:272–278CrossRefGoogle Scholar
  28. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Müller D, Leyser O (2011) Auxin, cytokinin and the control of shoot branching. Ann Bot 107:1203–1212PubMedPubMedCentralCrossRefGoogle Scholar
  30. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497CrossRefGoogle Scholar
  31. 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 56:2877–2883PubMedCrossRefPubMedCentralGoogle Scholar
  32. Östin A, Kowalyczk M, Bhalerao RP, Sandberg G (1998) Metabolism of indole-3-acetic acid in Arabidopsis. Plant Physiol 118:285–296PubMedPubMedCentralCrossRefGoogle Scholar
  33. Peer WA, Cheng Y, Murphy AS (2013) Evidence of oxidative attenuation of auxin signaling. J Exp Bot 64:2619–2639CrossRefGoogle Scholar
  34. Pelacho AM, Mingo-Castel AM (1991) Jasmonic acid induces tuberization of potato stolons cultured in vitro. Plant Physiol 97:1253–1255PubMedPubMedCentralCrossRefGoogle Scholar
  35. 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 25:3858–3870PubMedPubMedCentralCrossRefGoogle Scholar
  36. Quinones MA, Zeiger E (1994) Putative roles of the xanthophyll, zeaxanthin in blue light photoreception of corn coleoptiles. Science 264:558–561CrossRefGoogle Scholar
  37. 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 31:460–470CrossRefGoogle Scholar
  38. 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 32:245–251CrossRefGoogle Scholar
  39. Spalding EP (2013) Diverting the downhill flow of auxin to steer growth during tropisms. Am J Bot 100:203–214PubMedCrossRefGoogle Scholar
  40. Tarkowska D, Novak O, Flokova K, Tarkowski P, Turečkova V, Gruz J, Rolčik Strnad M (2014) Quo vadis plant hormone analysis? Planta 240:55–76PubMedCrossRefPubMedCentralGoogle Scholar
  41. Vinterhalter D, Vinterhalter B (2015) Phototropic responses of potato under conditions of continuous light and subsequent darkness. Plant Growth Regul 75:725–732CrossRefGoogle Scholar
  42. Vinterhalter D, Vinterhalter B (2016) Interaction with gravitropism, reversibility and lateral movements of phototropically stimulated potato shoots. J Plant Res 129:759–770PubMedPubMedCentralCrossRefGoogle Scholar
  43. Vinterhalter D, Vinterhalter B (2017) Phototropic bending of intact and wounded potato shoots. Plant Cell Tiss Org Cult 130:393–404CrossRefGoogle Scholar
  44. 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 16–45Google Scholar
  45. 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):560–569CrossRefGoogle Scholar
  46. 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 34:440–450CrossRefGoogle Scholar
  47. 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 CrossRefGoogle Scholar
  48. Vreugdenhil D, Struik PC (1989) An integrated view of the hormonal regulation of tuber formation in potato (Solanum tuberosum). Physiol Plant 75:525–531CrossRefGoogle Scholar
  49. Went FW, Thimann KV (1937) Phytohormones. The Macmillan Company, New YorkGoogle Scholar
  50. 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 117:575–584PubMedPubMedCentralCrossRefGoogle Scholar
  51. 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 110:1029–1034PubMedPubMedCentralCrossRefGoogle Scholar
  52. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  53. 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 27:363–369CrossRefGoogle Scholar
  54. 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 113:11010–11015PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Institute for Biological Research “Siniša Stanković”, National Institute of Republic of SerbiaUniversity of BelgradeBelgradeSerbia
  2. 2.Institute of Experimental Botany of the Czech Academy of SciencesPrague 6Czech Republic

Personalised recommendations