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Stimulatory role of smoke–water and karrikinolide on the photosynthetic pigment and phenolic contents of micropropagated ‘Williams’ bananas

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Abstract

At low concentrations, smoke–water (SW) and smoke-derived karrikinolide (KAR1) are compounds with potential cytokinin and auxin-like activity. Their roles on the growth, photosynthetic pigment and phenolic contents of micropropagated ‘Williams’ bananas were investigated in comparison with meta-topolin (mT). Explants were cultured on modified Murashige and Skoog basal media supplemented with either SW (1:125; 1:250; 1:500; 1:1,000; 1:2,000 dilutions) or KAR1 at four concentrations ranging from 4.8 × 10−22 to 3.3 × 10−12 M. After 42 days, growth parameters were measured while the photosynthetic pigments and phenolic contents were quantified using spectrophotometric methods. Chlorophyll a, b and total carotenoid contents were significantly enhanced by KAR1 (4.8 × 10−22 M) and SW (1:125 and 1:1,000 dilutions). The pigments in KAR1-treated plantlets were approximately two-fold to three-fold higher than those in the control and mT-treated plants, respectively. Total phenolic content was highest with KAR1 at 1.0 × 10−19 M in the leaves and 7.8 × 10−17 M in the roots. Furthermore, KAR1-treated plants at 1.0 × 10−19 M yielded the highest level of total phenolics (leaves) and proanthocyanidins (roots). At 1:500 dilutions, SW stimulated the highest total flavonoid content in the leaves across all the treatments. Combining mT with either SW (1:500) or KAR1 (4.8 × 10−22 M) significantly increased the quantity of secondary metabolites. However, the growth parameters and pigment contents were not improved. Based on the significant role of photosynthetic pigments and phenolic compounds on the defense and survival strategies of plants, current findings will have practical significance for important processes such as acclimatization and survival of micropropagated plants. These results are also demonstrating the potential of SW and KAR1 as an eliciting agent for secondary metabolite production.

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Abbreviations

ANOVA:

Analysis of variance

BA:

N6 Benzyladenine

CCE:

Cyanidin chloride equivalents

CE:

Catechin equivalents

CK:

Cytokinin

DMRT:

Duncan’s multiple range test

DW:

Dry weight

Folin-C:

Folin-Ciocalteu

FW:

Fresh weight

GAE:

Gallic acid equivalents

KAR1 :

Karrikinolide

MS:

Murashige and Skoog basal medium

mT:

meta-Topolin

PGR:

Plant growth regulator

PPF:

Photosynthetic photon flux density

PTC:

Plant tissue culture

SW:

Smoke-water

References

  • Abdullahil Baque M, Lee E-J, Paek K-Y (2010) Medium salt strength induced changes in growth, physiology and secondary metabolite content in adventitious roots of Morinda citrifolia: the role of antioxidant enzymes and phenylalanine ammonia lyase. Plant Cell Rep 29:685–694

    Article  PubMed  CAS  Google Scholar 

  • Alain-Michel B (2007) Evolution and current status of research in phenolic compounds. Phytochemistry 68:2722–2735

    Article  Google Scholar 

  • Aremu AO, Kulkarni MG, Bairu MW, Finnie JF, Van Staden J (2012) Growth stimulation effects of smoke-water and vermicompost leachate on greenhouse grown-tissue-cultured ‘Williams’ bananas. Plant Growth Regul 66:111–118

    Article  CAS  Google Scholar 

  • Bairu MW, Stirk WA, Doležal K, Van Staden J (2008) The role of topolins in micropropagation and somaclonal variation of banana cultivars ‘Williams’ and ‘Grand Naine’ (Musa spp. AAA). Plant Cell Tiss Org Cult 95:373–379

    Article  CAS  Google Scholar 

  • Baxter BJM, Van Staden J, Granger JE, Brown NAC (1994) Plant-derived smoke and smoke extracts stimulate seed germination of the fire-climax grass Themeda triandra. Environ Exp Bot 34:217–223

    Article  Google Scholar 

  • Bennett RN, Wallsgrove RM (1994) Secondary metabolites in plant defence mechanisms. New Phytol 127:617–633

    Article  CAS  Google Scholar 

  • Bieza K, Lois R (2001) An Arabidopsis mutant tolerant to lethal ultraviolet-B levels shows constitutively elevated accumulation of flavonoids and other phenolics. Plant Physiol 126:1105–1115

    Article  PubMed  CAS  Google Scholar 

  • Brown NAC, Van Staden J (1997) Smoke as a germination cue: a review. Plant Growth Regul 22:115–124

    Article  CAS  Google Scholar 

  • Brown DE, Rashotte AM, Murphy AS, Normanly J, Tague BW, Peer WA, Taiz L, Muday GK (2001) Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiol 126:524–535

    Article  PubMed  CAS  Google Scholar 

  • Buer CS, Imin N, Djordjevic MA (2010) Flavonoids: new roles for old molecules. J Integrat Plant Biol 52:98–111

    Article  CAS  Google Scholar 

  • 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 177:252–256

    Article  CAS  Google Scholar 

  • Chow WS, Anderson JM, Melis A (1990) The photosystem stoichiometry in thylakoids of some Australian shade-adapted plant species. Aust J Plant Physiol 17:665–674

    Article  CAS  Google Scholar 

  • Curir P, VanSumere CF, Termini A, Barthe P, Marchesini A, Dolci M (1990) Flavonoid accumulation is correlated with adventitious roots formation in Eucalyptus gunnii Hook micropropagated through axillary bud stimulation. Plant Physiol 92:1148–1153

    Article  PubMed  CAS  Google Scholar 

  • De Klerk G-J, Guan H, Huisman P, Marinova S (2011) Effects of phenolic compounds on adventitious root formation and oxidative decarboxylation of applied indoleacetic acid in Malus ‘Jork 9’. Plant Growth Regul 63:175–185

    Article  CAS  Google Scholar 

  • 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 Hort 813:155–170

    CAS  Google Scholar 

  • Flematti GR, Ghisalberti EL, Dixon KW, Trengove RD (2004) A compound from smoke that promotes seed germination. Science 305:977

    Article  PubMed  CAS  Google Scholar 

  • Fletcher RA, McCullagh D (1971) Benzyladenine as a regulator of chlorophyll synthesis in cucumber cotyledons. Can J Bot 49:2197–2201

    Article  CAS  Google Scholar 

  • Goltsev V, Genkov T, Lexa M, Ivanova I (2001) Effect of benzyladenine, 4-PU-30 and thidiazuron on millisecond delayed and prompt chlorophyll fluorescence of Dianthus caryophyllus L. axillary buds cultured in vitro. Sci Hortic 89:41–55

    Article  CAS  Google Scholar 

  • Jacobs M, Rubery PH (1988) Naturally occurring auxin transport regulators. Science 241:346–349

    Article  PubMed  CAS  Google Scholar 

  • 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 74:327–331

    Article  CAS  Google Scholar 

  • Kaufman PB, Cseke LJ, Warber S, Duke JA, Brielmann HL (1999) Natural products from plants. CRC Press, Florida

    Google Scholar 

  • Kulkarni MG, Ascough GD, Van Staden J (2008) Smoke-water and a smoke-isolated butenolide improve growth and yield of tomatoes under greenhouse conditions. Hort Technol 18:449–454

    CAS  Google Scholar 

  • Kulkarni MG, Ascough GD, Verschaeve L, Baeten K, Arruda MP, Van Staden J (2010) Effect of smoke-water and a smoke-isolated butenolide on the growth and genotoxicity of commercial onion. Sci Hortic 124:434–439

    Article  CAS  Google Scholar 

  • 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 77:972–979

    Article  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. In: Douce R, Packer L (eds) Methods in enzymology. Academic Press, New York, pp 350–382

    Google Scholar 

  • Light ME, Daws MI, Van Staden J (2009) Smoke-derived butenolide: towards understanding its biological effects. S Afr J Bot 75:1–7

    Article  CAS  Google Scholar 

  • 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 73:267–269

    Article  PubMed  CAS  Google Scholar 

  • Liu X-N, Zhang X-Q, Sun J-S (2007) Effects of cytokinins and elicitors on the production of hypericins and hyperforin metabolites in Hypericum sampsonii and Hypericum perforatum. Plant Growth Regul 53:207–214

    Article  CAS  Google Scholar 

  • Makkar HPS, Sidhuraju P, Becker K (2007) Plant secondary metabolites. Humana Press Inc, New Jersey

    Book  Google Scholar 

  • Marinova D, Ribarova F, Atanassova M (2005) Total phenolics and total flavonoids in Bulgarian fruits and vegetables. J Univ Chem Technol Metal 40:255–260

    CAS  Google Scholar 

  • Matsuo K, Shindo M (2011) Efficient synthesis of karrikinolide via Cu(II)-catalyzed lactonization. Tetrahedron 67:971–975

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Mutui TM, Mibus H, Serek M (2012) Effect of meta-topolin on leaf senescence and rooting in Pelargonium × hortorum cuttings. Postharvest Biol Technol 63:107–110

    Article  CAS  Google Scholar 

  • Peer WA, Murphy AS (2007) Flavonoids and auxin transport: modulators or regulators? Trends Plant Sci 12:556–563

    Article  PubMed  CAS  Google Scholar 

  • Peer WA, Brown DE, Tague BW, Muday GK, Taiz L, Murphy AS (2001) Flavonoid accumulation patterns of transparent testa mutants of Arabidopsis. Plant Physiol 126:536–548

    Article  PubMed  CAS  Google Scholar 

  • Porter LJ, Hrstich LN, Chan BG (1985) The conversion of proanthocyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25:223–230

    Article  Google Scholar 

  • Rokich DP, Dixon KW (2007) Recent advances in restoration ecology, with a focus on the Banksia woodland and the smoke germination tool. Aust J Bot 55:375–389

    Article  Google Scholar 

  • Savio LE, Astarita LV, Santarém ER (2012) Secondary metabolism in micropropagated Hypericum perforatum L. grown in non-aerated liquid medium. Plant Cell Tiss Org Cult 108:465–472

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Stevens J, Merritt D, Flematti G, Ghisalberti E, Dixon K (2007) Seed germination of agricultural weeds is promoted by the butenolide 3-methyl-2H-furo[2,3-c]pyran-2-one under laboratory and field conditions. Plant Soil 298:113–124

    Article  CAS  Google Scholar 

  • Van Staden J, Jäger AK, Light ME, Burger BV (2004) Isolation of the major germination cue from plant-derived smoke. S Afr J Bot 70:654–659

    Google Scholar 

  • Verschaeve L, Maes J, Light ME, Van Staden J (2006) Genetic toxicity testing of 3-methyl-2H-furo[2,3-c]pyran-2-one, an important biologically active compound from plant-derived smoke. Mutat Res Genet Toxicol Environ Mutagen 611:89–95

    Article  CAS  Google Scholar 

  • Vlčková A, Špundová M, Kotabová E, Novotný R, Doležal K, Nauš J (2006) Protective cytokinin action switches to damaging during senescence of detached wheat leaves in continuous light. Physiol Plant 126:257–267

    Article  Google Scholar 

  • Vuylseke DR (1998) Shoot-tip culture for the propagation, conservation, and distribution of Musa germplasm. International Institute of Tropical Agriculture, Ibadan, Nigeria

    Google Scholar 

  • Zhang J, Gao W-Y, Wang J, Li X-L (2011) Effects of explant types and media salt strength on growth and secondary metabolite accumulation in adventitious roots of Periploca sepium Bunge. Acta Physiol Plant 33:2447–2452

    Article  CAS  Google Scholar 

  • Zhishen J, Mengcheng T, Jianming W (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64:555–559

    Article  CAS  Google Scholar 

  • 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 77:787–789

    Article  Google Scholar 

Download references

Acknowledgments

We thank the team at the Laboratory of Growth Regulators, Czech Republic for the generous gift of meta-topolin. We appreciate the help of Dr Manoj Kulkarni (University of KwaZulu-Natal), in the preparation of the smoke solutions. Financial support from the University of KwaZulu-Natal Pietermaritzburg, South Africa is appreciated.

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Authors and Affiliations

  1. Research Centre for Plant Growth and Development, School of Life Sciences, University of KwaZulu-Natal, Pietermaritzburg, Private Bag X01, Scottsville, 3209, South Africa

    Adeyemi O. Aremu, Michael W. Bairu, Jeffrey F. Finnie & Johannes Van Staden

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  1. Adeyemi O. Aremu
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  2. Michael W. Bairu
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  3. Jeffrey F. Finnie
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  4. Johannes Van Staden
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Correspondence to Johannes Van Staden.

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Aremu, A.O., Bairu, M.W., Finnie, J.F. et al. Stimulatory role of smoke–water and karrikinolide on the photosynthetic pigment and phenolic contents of micropropagated ‘Williams’ bananas. Plant Growth Regul 67, 271–279 (2012). https://doi.org/10.1007/s10725-012-9685-3

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  • DOI: https://doi.org/10.1007/s10725-012-9685-3

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