Plant Cell Reports

, Volume 35, Issue 1, pp 227–238 | Cite as

Cytokinin profiles in ex vitro acclimatized Eucomis autumnalis plants pre-treated with smoke-derived karrikinolide

  • Adeyemi O. Aremu
  • Lenka Plačková
  • Ondřej Novák
  • Wendy A. Stirk
  • Karel Doležal
  • Johannes Van Staden
Original Article
  • 278 Downloads

Abstract

Key message

The current evidence of regulatory effect of smoke–water (SW) and karrikinolide (KAR1) on the concentrations of endogenous cytokinins in plants partly explain the basis for their growth stimulatory activity.

Abstract

Karrikinolide (KAR1) which is derived from smoke–water (SW) is involved in some physiological aspects in the life-cycle of plants. This suggests a potential influence on the endogenous pool (quantity and quality) of phytohormones such as cytokinins (CKs). In the current study, the effect of SW (1:500; 1:1000; 1:1500 v/v dilutions) and KAR1 (10−7; 10−8; 10−9 M) applied during micropropagation of Eucomis autumnalis subspecies autumnalis on the ex vitro growth and CKs after 4 months post-flask duration was evaluated. The interactions of SW and KAR1 with benzyladenine (BA), α-naphthaleneacetic acid (NAA) or BA+NAA were also assessed. Plants treated with SW (1:500) and KAR1 (10−8 M) demonstrated superior growth in terms of the rooting, leaf and bulb sizes and fresh biomass than the control and plants treated with BA and BA+NAA. However, plant growth was generally inhibited with either SW (1:500) or KAR1 (10−8 M) and BA when compared to BA (alone) treatment. Relative to NAA treatment, the presence of KAR1 (10−7 M) with NAA significantly increased the leaf area and fresh biomass. Both SW and KAR1-treated plants accumulated more total CKs, mainly isoprenoid-type than the control and NAA-treated plants. The highest CK content was also accumulated in SW (1:500) with BA+NAA treatments. Similar stimulatory effects were observed with increasing concentrations of KAR1 and BA. The current findings establish that SW and KAR1 exert significant influence on the endogenous CK pools. However, the better growth of plants treated with SW and KAR1 treatments was not exclusively related to the endogenous CKs.

Keywords

Acclimatization Asparagaceae Conservation Medicinal plants Plant growth regulators UHPLC 

Abbreviations

ANOVA

Analysis of variance

BA

N6-Benzyladenine

BA9G

N6-Benzyladenine-9-glucoside

CK

Cytokinin

cZ

cis-Zeatin

cZOG

cis-Zeatin-O-glucoside

cZR

cis-Zeatin riboside

cZR5′MP

cis-Zeatin riboside-5′-monophosphate

cZROG

cis-Zeatin riboside-O-glucoside

DHZOG

Dihydrozeatin-O-glucoside

DHZR

Dihydrozeatin riboside

DHZR5′MP

Dihydrozeatin riboside-5′-monophosphate

DHZROG

Dihydrozeatin riboside-O-glucoside

ESI

Electro-spray interface

iP

N6-Isopentenyladenine

iPR

N6-Isopentenyladenosine

iPR5′MP

N6-Isopentenyladenosine-5′-monophosphate

KAR1

Karrikinolide

MRM

Multiple reaction monitoring

MS

Murashige and Skoog medium

mT

meta-Topolin

mTOG

meta-Topolin O-glucoside

mTR

meta-Topolin riboside

mTR5′MP

meta-Topolin riboside-5′-monophosphate

mTROG

meta-Topolin riboside-O-glucoside

NAA

α-Naphthaleneacetic acid

PGR

Plant growth regulator

PPF

Photosynthetic photon flux density

PTC

Plant tissue culture

SW

Smoke–water

TMB

Trimethylbutenolide

tZ

trans-Zeatin

tZ9G

trans-Zeatin-9-glucoside

tZOG

trans-Zeatin-O-glucoside

tZR

trans-Zeatin riboside

tZR5′MP

trans-Zeatin riboside-5′-monophosphate

tZROG

trans-Zeatin riboside-O-glucoside

UHPLC

Ultra high performance liquid chromatography

Supplementary material

299_2015_1881_MOESM1_ESM.xlsx (42 kb)
Supplementary material 1 (XLSX 42 kb)
299_2015_1881_MOESM2_ESM.xlsx (43 kb)
Supplementary material 2 (XLSX 43 kb)

References

  1. Amoo SO, Aremu AO, Van Staden J (2012) In vitro plant regeneration, secondary metabolite production and antioxidant activity of micropropagated Aloe arborescens Mill. Plant Cell Tissue Organ Cult 111:345–358CrossRefGoogle Scholar
  2. Amoo SO, Aremu AO, Van Staden J (2013) Shoot proliferation and rooting treatments influence secondary metabolite production and antioxidant activity in tissue culture-derived Aloe arborescens grown ex vitro. Plant Growth Regul 70:115–122CrossRefGoogle Scholar
  3. Aremu AO, Bairu MW, Doležal K, Finnie JF, Van Staden J (2012a) Topolins: a panacea to plant tissue culture challenges? Plant Cell Tissue Organ Cult 108:1–16CrossRefGoogle Scholar
  4. Aremu AO, Bairu MW, Finnie JF, Van Staden J (2012b) Stimulatory role of smoke–water and karrikinolide on the photosynthetic pigment and phenolic contents of micropropagated ‘Williams’ bananas. Plant Growth Regul 67:271–279CrossRefGoogle Scholar
  5. Aremu AO, Bairu MW, Szüčová L, Doležal K, Finnie JF, Van Staden J (2012c) Shoot and root proliferation in ‘Williams’ banana: are the topolins better cytokinins? Plant Cell Tissue Organ Cult 111:209–218CrossRefGoogle Scholar
  6. Aremu AO, Plačková L, Bairu MW, Novák O, Szüčová L, Doležal K, Finnie JF, Van Staden J (2014) Endogenous cytokinin profiles of tissue-cultured and acclimatized ‘Williams’ bananas subjected to different aromatic cytokinin treatments. Plant Sci 214:88–98PubMedCrossRefGoogle Scholar
  7. Arnau JA, Tadeo FR, Guerri J, Primo-Millo E (1999) Cytokinins in peach: endogenous levels during early fruit development. Plant Physiol Biochem 37:741–750CrossRefGoogle Scholar
  8. Baldrianová J, Černý M, Novák J, Jedelský PL, Divíšková E, Brzobohatý B (2015) Arabidopsis proteome responses to the smoke-derived growth regulator karrikin. J Proteomics 120:7–20PubMedCrossRefGoogle Scholar
  9. Cheng X, Ruyter-Spira C, Bouwmeester H (2013) The interaction between strigolactones and other plant hormones in the regulation of plant development. Frontiers Plant Sci 4:199. doi:10.3389/fpls.2013.00199 CrossRefGoogle Scholar
  10. Chiwocha SDS, Dixon KW, Flematti GR, Ghisalberti EL, Merritt DJ, Nelson DC, Riseborough J-AM, Smith SM, Stevens JC (2009) Karrikins: a new family of plant growth regulators in smoke. Plant Sci 177:252–256CrossRefGoogle Scholar
  11. Dixon KW, Merritt DJ, Flematti GR, Ghisalberti E (2009) Karrikinolide—a phytoreactive compound derived from smoke with applications in horticulture, ecological restoration and agriculture. Acta Hortic 813:155–170CrossRefGoogle Scholar
  12. Flematti GR, Ghisalberti EL, Dixon KW, Trengove RD (2004) A compound from smoke that promotes seed germination. Science 305:977PubMedCrossRefGoogle Scholar
  13. Flematti GR, Waters MT, Scaffidi A, Merritt DJ, Ghisalberti EL, Dixon KW, Smith SM (2013) Karrikin and cyanohydrin smoke signals provide clues to new endogenous plant signaling compounds. Mol Plant 6:29–37PubMedCrossRefGoogle Scholar
  14. Gaspar T, Kevers C, Penel C, Greppin H, Reid D, Thorpe T (1996) Plant hormones and plant growth regulators in plant tissue culture. In Vitro Cell Dev Biol Plant 32:272–289CrossRefGoogle Scholar
  15. Hazarika BN (2006) Morpho-physiological disorders in in vitro culture of plants. Sci Hortic 108:105–120CrossRefGoogle Scholar
  16. Jain N, Stirk WA, Van Staden J (2008) Cytokinin-and auxin-like activity of a butenolide isolated from plant-derived smoke. S Afr J Bot 74:327–331CrossRefGoogle Scholar
  17. Kulkarni MG, Light ME, Van Staden J (2011) Plant-derived smoke: old technology with possibilities for economic applications in agriculture and horticulture. S Afr J Bot 77:972–979CrossRefGoogle Scholar
  18. Kumari A, Papenfus HB, Kulkarni MG, Pošta M, Van Staden J (2015) Effect of smoke derivatives on in vitro pollen germination and pollen tube elongation of species from different plant families. Plant Biol 17:825–830PubMedCrossRefGoogle Scholar
  19. Light ME, Daws MI, Van Staden J (2009) Smoke-derived butenolide: towards understanding its biological effects. S Afr J Bot 75:1–7CrossRefGoogle Scholar
  20. Light ME, Burger BV, Staerk D, Kohout L, Van Staden J (2010) Butenolides from plant-derived smoke: natural plant-growth regulators with antagonistic actions on seed germination. J Nat Prod 73:267–269PubMedCrossRefGoogle Scholar
  21. Ma G-H, Bunn E, Dixon K, Flematti G (2006) Comparative enhancement of germination and vigor in seed and somatic embryos by the smoke chemical 3-methyl-2H-furo[2,3-C]pyran-2-one in Baloskion tetraphyllum (Restionaceae). In Vitro Cell Dev Biol Plant 42:305–308CrossRefGoogle Scholar
  22. Masondo NA, Aremu AO, Finnie JF, Van Staden J (2015) Growth and phytochemical levels in micropropagated Eucomis autumnalis subspecies autumnalis using different gelling agents, explant source, and plant growth regulators. In Vitro Cell Dev Biol Plant 51:102–110CrossRefGoogle Scholar
  23. Montalbán IA, Novák O, Rolčik J, Strnad M, Moncaleán P (2013) Endogenous cytokinin and auxin profiles during in vitro organogenesis from vegetative buds of Pinus radiata adult trees. Physiol Plant 148:214–231PubMedCrossRefGoogle Scholar
  24. Moyo M, Aremu AO, Van Staden J (2015) Medicinal plants: an invaluable, dwindling resource in sub-Saharan Africa. J Ethnopharmacol: doi: http://dx.doi.org/10.1016/j.jep.2015.1004.1034
  25. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497CrossRefGoogle Scholar
  26. Nair JJ, Pošta M, Papenfus HB, Munro OQ, Beier P, Van Staden J (2014) Synthesis, X-ray structure determination and germination studies on some smoke-derived karrikins. S Afr J Bot 91:53–57CrossRefGoogle Scholar
  27. Nelson DC, Flematti GR, Ghisalberti EL, Dixon KW, Smith SM (2012) Regulation of seed germination and seedling growth by chemical signals from burning vegetation. Ann Rev Plant Biol 63:107–130CrossRefGoogle Scholar
  28. Novák O, Hauserová E, Amakorová P, Doležal K, Strnad M (2008) Cytokinin profiling in plant tissues using ultra-performance liquid chromatography—electrospray tandem mass spectrometry. Phytochemistry 69:2214–2224PubMedCrossRefGoogle Scholar
  29. Papenfus HB, Kumari A, Kulkarni MG, Finnie JF, Van Staden J (2014) Smoke–water enhances in vitro pollen germination and tube elongation of three species of Amaryllidaceae. S Afr J Bot 90:87–92CrossRefGoogle Scholar
  30. Pinheiro C, Chaves MM (2011) Photosynthesis and drought: can we make metabolic connections from available data? J Exp Bot 62:869–882PubMedCrossRefGoogle Scholar
  31. Plačková L, Hrdlička J, Smýkalová I, Cvečková M, Novák O, Griga M, Doležal K (2015) Cytokinin profiling of long-term in vitro pea (Pisum sativum L.) shoot cultures. Plant Growth Regul 77:125–132CrossRefGoogle Scholar
  32. Sakakibara H (2006) Cytokinins: activity, biosynthesis, and translocation. Ann Rev Plant Biol 57:431–449CrossRefGoogle Scholar
  33. Santner A, Calderon-Villalobos LIA, Estelle M (2009) Plant hormones are versatile chemical regulators of plant growth. Nat Chem Biol 5:301–307PubMedCrossRefGoogle Scholar
  34. Scaffidi A, Waters MT, Bond CS, Dixon KW, Smith SM, Ghisalberti EL, Flematti GR (2012) Exploring the molecular mechanism of karrikins and strigolactones. Bioorg Med Chem Lett 22:3743–3746PubMedCrossRefGoogle Scholar
  35. Senaratna T, Dixon K, Bunn E, Touchell D (1999) Smoke-saturated water promotes somatic embryogenesis in geranium. Plant Growth Regul 28:95–99CrossRefGoogle Scholar
  36. Singh S, Kulkarni MG, Van Staden J (2014) Biochemical changes associated with gibberellic acid-like activity of smoke-water, karrikinolide and vermicompost leachate during seedling development of Phaseolus vulgaris L. Seed Sci Res 24:63–70CrossRefGoogle Scholar
  37. Soós V, Sebestyén E, Juhász A, Szalai G, Tandori J, Light ME, Kohout L, Van Staden J, Balázs E (2010) Transcriptome analysis of germinating maize kernels exposed to smoke-water and the active compound KAR1. BMC Plant Biol 10:236. doi:10.1186/1471-2229-1110-1236 PubMedPubMedCentralCrossRefGoogle Scholar
  38. Stirk WA, Van Staden J (2010) Flow of cytokinins through the environment. Plant Growth Regul 62:101–116CrossRefGoogle Scholar
  39. Stirk WA, Van Staden J (2014) Plant growth regulators in seaweeds: Occurrence, regulation and functions. In: Nathalie B (ed) Advances in Botanical Research, Academic Press, Vol 71. pp 125–159Google Scholar
  40. Strnad M (1997) The aromatic cytokinins. Physiol Plant 101:674–688CrossRefGoogle Scholar
  41. Tarkowská D, Novák O, Floková K, Tarkowski P, Turečková V, Grúz J, Rolčík J, Strnad M (2014) Quo vadis plant hormone analysis? Planta 240:55–76PubMedCrossRefGoogle Scholar
  42. Taylor JLS, Van Staden J (2001) In vitro propagation of Eucomis L’Herit species-plants with medicinal and horticultural potential. Plant Growth Regul 34:317–329CrossRefGoogle Scholar
  43. Teixeira da Silva J, Dobránszki J, Ross S (2013) Phloroglucinol in plant tissue culture. In Vitro Cell Dev Biol Plant 49:1–16CrossRefGoogle Scholar
  44. Tréhin C, Planchais S, Glab N, Perennes C, Tregear J, Bergounioux C (1998) Cell cycle regulation by plant growth regulators: involvement of auxin and cytokinin in the re-entry of Petunia protoplasts into the cell cycle. Planta 206:215–224PubMedCrossRefGoogle Scholar
  45. Van Staden J, Brown NAC, Jäger AK, Johnson TA (2000) Smoke as a germination cue. Plant Spec Biol 15:167–178CrossRefGoogle Scholar
  46. Van Staden J, Jäger AK, Light ME, Burger BV (2004) Isolation of the major germination cue from plant-derived smoke. S Afr J Bot 70:654–659CrossRefGoogle Scholar
  47. Vasil I (2008) A history of plant biotechnology: from the cell theory of Schleiden and Schwann to biotech crops. Plant Cell Rep 27:1423–1440PubMedCrossRefGoogle Scholar
  48. Waters MT, Scaffidi A, Flematti GR, Smith SM (2013) The origins and mechanisms of karrikin signalling. Curr Opin Plant Biol 16:667–673PubMedCrossRefGoogle Scholar
  49. Zhao Z, Andersen SU, Ljung K, Dolezal K, Miotk A, Schultheiss SJ, Lohmann JU (2010) Hormonal control of the shoot stem-cell niche. Nature 465:1089–1092PubMedCrossRefGoogle Scholar
  50. Zhou J, Van Staden J, Guo LP, Huang LQ (2011) Smoke-water improves shoot growth and indigo accumulation in shoots of Isatis indigotica seedlings. S Afr J Bot 77:787–789CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Adeyemi O. Aremu
    • 1
  • Lenka Plačková
    • 2
  • Ondřej Novák
    • 2
  • Wendy A. Stirk
    • 1
  • Karel Doležal
    • 2
  • Johannes Van Staden
    • 1
  1. 1.Research Centre for Plant Growth and Development, School of Life SciencesUniversity of KwaZulu-Natal PietermaritzburgScottsvilleSouth Africa
  2. 2.Laboratory of Growth Regulators and Department of Chemical Biology and Genetics, Centre of the Region Haná for Biotechnological and Agricultural Research, Faculty of SciencePalacký University and Institute of Experimental Botany ASCROlomoucCzech Republic

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