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.
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
Alabadi D, Gil J, Blázquez MA, García-Martínez JL (2004) Gibberellins repress photomorphogenesis in darkness. Plant Physiol 134:1050–1057
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
Collett CE, Harberd NP, Leyser O (2000) Hormonal interactions in the control of Arabidopsis hypocotyl elongation. Plant Physiol 124:553–561
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
Cowling RJ, Harberd NP (1999) Gibberellins control Arabidopsis hypocotyl growth via regulation of cellular elogation. J Exp Biol 50:1351–1357
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
Dobrev PI, Vankova R (2012) Quantification of abscisic acid, cytokinin, and auxin content in salt-stressed plant tissues. Methods Mol Biol 913:251–261
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
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
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
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
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
Friml J (2003) Auxin transport—shaping the plant. Curr Opin Plant Biol 6:7–12
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
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
Hall A, Kozma-Bognar L, Tóth R, Nagy F, Millar AJ (2001) Conditional circadian regulation of PHYTOCHROME gene expression. Plant Physiol 127:1808–1818
Hannapel DJ (2007) Signaling the induction of tuber formation. In: Vreugdenhil D (ed) Potato biology and biotechnology: advances and perspectives. Elsevier, Amsterdam
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
Hussey G, Stacey NJ (1981) In vitro propagation of potato (Solanum tuberosum L.). Ann Bot 48:787–796
Hussey G, Stacey NJ (1984) Factors affecting the formation of in vitro tubers of potato (Solanum tuberosum L.). Ann Bot 53:565–578
Jackson SD (1999) Multiple signaling pathways control tuber induction in potato. Plant Physiol 119:1–8
Janoudi A, Poff KL (1990) A common fluence threshold for first positive and second positive phototropism in Arabidopsis. Plant Physiol 94:1605–1608
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
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
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
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
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
Müller D, Leyser O (2011) Auxin, cytokinin and the control of shoot branching. Ann Bot 107:1203–1212
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497
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
Östin A, Kowalyczk M, Bhalerao RP, Sandberg G (1998) Metabolism of indole-3-acetic acid in Arabidopsis. Plant Physiol 118:285–296
Peer WA, Cheng Y, Murphy AS (2013) Evidence of oxidative attenuation of auxin signaling. J Exp Bot 64:2619–2639
Pelacho AM, Mingo-Castel AM (1991) Jasmonic acid induces tuberization of potato stolons cultured in vitro. Plant Physiol 97:1253–1255
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
Quinones MA, Zeiger E (1994) Putative roles of the xanthophyll, zeaxanthin in blue light photoreception of corn coleoptiles. Science 264:558–561
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
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
Spalding EP (2013) Diverting the downhill flow of auxin to steer growth during tropisms. Am J Bot 100:203–214
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
Vinterhalter D, Vinterhalter B (2015) Phototropic responses of potato under conditions of continuous light and subsequent darkness. Plant Growth Regul 75:725–732
Vinterhalter D, Vinterhalter B (2016) Interaction with gravitropism, reversibility and lateral movements of phototropically stimulated potato shoots. J Plant Res 129:759–770
Vinterhalter D, Vinterhalter B (2017) Phototropic bending of intact and wounded potato shoots. Plant Cell Tiss Org Cult 130:393–404
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
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
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
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
Vreugdenhil D, Struik PC (1989) An integrated view of the hormonal regulation of tuber formation in potato (Solanum tuberosum). Physiol Plant 75:525–531
Went FW, Thimann KV (1937) Phytohormones. The Macmillan Company, New York
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
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
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
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
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
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
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-019-00561-8