Skip to main content
SpringerLink
Log in

Adventitious rooting adjuvant activity of 1,3-di(benzo[d]oxazol-5-yl)urea and 1,3-di(benzo[d]oxazol-6-yl)urea: new insights and perspectives

  • Original Paper
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

Abstract

Here we report new insights on the adventitious rooting adjuvant activity of 1,3-di(benzo[d]oxazol-5-yl)urea (5-BDPU) and 1,3-di(benzo[d]oxazol-6-yl)urea (6-BDPU), both symmetrically substituted urea derivatives that do not show either auxin- or cytokinin-like activity per se. Our data demonstrate that these synthetic molecules enhance adventitious rooting in distantly-related herbaceous and woody species, in the presence of endogenous or exogenous auxin. For the first time, we report that BDPUs enhance adventitious rooting in the presence of either indole-3-butyric acid (IBA) or 1-naphtalene acetic acid and that their optimal concentration depends on the strength of the exogenous auxin. Trying to understand the mode of action of BDPUs, we also show that their adventitious rooting adjuvant activity correlates with high mRNA levels of auxin-responsive genes related to the adventitious rooting process at the very early stages of adventitious rooting, before the activation of cell divisions in pine hypocotyls cuttings. The high mRNA levels are measured in the presence of low auxin concentrations and BDPUs. The mRNA levels quantified in these conditions are similar to those measured in the presence of high auxin concentrations but in the absence of BDPUs. In addition, the spatial distribution of endogenous auxin is localized in globular-shaped structures of cell divisions located centrifugal to the resin canals, at the positions of adventitious root formation, in the presence of urea derivatives and IBA after 6 days of the root induction process.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Altamura MM (1996) Root histogenesis in herbaceous and woody explants cultured in vitro. A critical review. Agronomie 16:589–602

    Article  Google Scholar 

  • Auderset G, Moncousin C, O’Rourke J, Morré DJ (1996) Stimulation of root formation by thiol compounds. Hortic Sci 31:240–242

    CAS  Google Scholar 

  • Auderset G, Moncousin C, O’Rourke J, Morré DJ (1997) Stimulation of root formation in difficult-to-root woody cuttings by dithiothreitol. Int J Plant Sci 158:132–135

    Article  CAS  Google Scholar 

  • Bai F, DeMason D (2008) Hormone interactions and regulation of PsPK2:GUS compared with DR5:GUS and PID:GUS in Arabidopsis thaliana. Am J Bot 95:133–145

    Article  CAS  PubMed  Google Scholar 

  • Bartel B, LeClere S, Magidin M, Zolman B (2001) Inputs to the active indole-3-acetic acid pool: de novo synthesis, conjugate hydrolysis and indole-3-butyric acid β-oxidation. J Plant Growth Regul 20:198–216

    Article  CAS  Google Scholar 

  • Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients, as a common module for plant organ formation. Cell 115:591–602

    Article  PubMed  Google Scholar 

  • Berlyn GP, Miksche JP (1976) Botanical microtechnique and cytochemistry. Iowa State University Press, Ames

    Google Scholar 

  • Blakesley D (1994) Auxin metabolism and adventitious root initiation. In: Davies TD, Haissig BE (eds) Biology of adventitious root formation. Plenum Press, New York, pp 143–154

    Chapter  Google Scholar 

  • Casimiro I, Marchant A, Bhalerao R, Beeckman T, Dhooge S, Swarup R, Graham N, Inze D, Sandberg G, Casero P, Bennett M (2001) Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell 13:843–852

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cheng B, Peterson CM, Mitchell RJ (1992) The role of sucrose, auxin and explant source on in vitro rooting of seedling explants of Eucalyptus sideroxylon. Plant Sci 87:207–214

    Article  CAS  Google Scholar 

  • Cooper WC (1935) Hormones in relation to root formation on stem cuttings. Plant Physiol 10:789–794

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • De Klerk GJ (1995) Hormone requirements during the successive phases of rooting of Malus microcuttings. In: Terzi M et al (eds) Current issues in plant molecular and cellular biology. Kluwer Academic Publishers, The Netherlands, pp 111–116

    Chapter  Google Scholar 

  • De Klerk GJ, Ter Brugge J, Marinova S (1997) Effectiveness of indoleacetic acid, indolebutyric acid and naphtaleneacetic acid during adventitious root formation in vitro in Malus “Jork 9”. Plant Cell Tissue Organ Cult 49:39–44

    Article  Google Scholar 

  • De Klerk GJ, Van der Krieken W, De Jong JC (1999) The formation of adventitious roots: new concepts, new possibilities. In Vitro Cell Dev Biol Plant 35:189–199

    Article  Google Scholar 

  • Delbarre A, Muller P, Imhoff V, Guern J (1996) Comparison of mechanisms controlling uptake and accumulation of 2,4-dichloro-phenoxy acetic acid, naphthalene-1-acetic acid, and indole-3-acetic acid in suspension-cultured tobacco cells. Planta 198:532–541

    Article  CAS  Google Scholar 

  • Della Rovere F, Fattorini L, D’Angeli S, Veloccia A, Falasca G, Altamura MM (2013) Auxin and cytokinin control formation of the quiescent centre in the adventitious root apex of Arabidopsis. Ann Bot 112:1395–1407

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Diaz-Sala C, Hutchinson KW, Goldfarb B, Greenwood MS (1996) Maturation-related loss in rooting competence in loblolly pine stem cuttings: the role of auxin transport, metabolism and tissue sensitivity. Physiol Plant 97:481–490

    Article  CAS  Google Scholar 

  • Diaz-Sala C, Garrido G, Sabater B (2002) Age-related loss of rooting capability in Arabidopsis thaliana and its reversal by peptides containing the Arg-Gly-Asp (RGD) motif. Physiol Plant 114:601–607

    Article  CAS  PubMed  Google Scholar 

  • Epstein E, Ludwig-Müller J (1993) Indole-3-butyric acid in plants: occurrence, biosynthesis, metabolism, and transport. Physiol Plant 88:382–389

    Article  CAS  Google Scholar 

  • Falasca G, Reverberi M, Lauri P, Caboni E, DeStradis A, Altamura MM (2000) How Agrobacterium rhizogenes triggers de novo root formation in a recalcitrant woody plant: an integrated histological, ultrastructural and molecular analysis. New Phytol 145:77–93

    Article  CAS  Google Scholar 

  • Fogaca CM, Fett-Neto AG (2005) Role of auxin and its modulators in the adventitious rooting of Eucalyptus species differing in recalcitrance. Plant Growth Regul 45:1–10

    Article  CAS  Google Scholar 

  • George EF (1993) Plant propagation by tissue culture. Exegetics Ltd, Edington

    Google Scholar 

  • Haissig BE, Davis TD (1994) A historical evaluation of adventitious rooting research in 1993. In: Davis TD, Haissig BE (eds) Biology of adventitious root formation. Plenum Publishing Corporation, London, pp 275–331

    Chapter  Google Scholar 

  • Hartmann HT, Kester DE, Davies FT, Geneve RL (1997) Plant propagation: principles and practices, 6th edn. Prentice Hall International, New Jersey

    Google Scholar 

  • Hošek P, Kubeš M, Laňková M, Dobrev PI, Klíma P, Kohoutová M, Petrášek J, Hoyerová K, Jiřina M, Zažímalová E (2012) Auxin transport at cellular level: new insights supported by mathematical modelling. J Exp Bot 63:3815–3827

    Article  PubMed Central  PubMed  Google Scholar 

  • James DJ (1983) Adventitious root formation in vitro in apple rootstocks (Malus pumila) I. Factors affecting the length of the auxin-sensitive phase in M9. Physiol Plant 57:149–153

    Article  CAS  Google Scholar 

  • Kevers C, Bringaud C, Hausman JF, Gaspar T (1997) Putrescine involvement in the inductive phase of walnut shoots rooting in vitro. Saussurea 28:47–57

    Google Scholar 

  • Ludwig-Müller J (2000) Indole-3-butyric acid in plant growth and development. Plant Growth Regul 32:219–230

    Article  Google Scholar 

  • Mattsson J, Ckurshumova W, Berleth T (2003) Auxin signaling in Arabidopsis leaf vascular development. Plant Physiol 131:1327–1339

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mugdil Y, Uhrig JF, Zhou J, Temple B, Jiang K, Jones AM (2009) Arabidopsis N-MYC DOWNREGULATED-LIKE1, a positive regulator of auxin transport in a G protein-mediated pathway. Plant Cell 21:3591–3609

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Nick P, Han M-J, An G (2009) Auxin stimulates its own transport by shaping actin filaments. Plant Physiol 151:155–167

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Orlikowska T (1992) Influence of arginine on in vitro rooting of dwarf apple rootstock. Plant Cell Tissue Organ Cult 31:9–14

    CAS  Google Scholar 

  • Pawlicki N, Welander M (1995) Influence of carbohydrate source, auxin concentration and time of exposure on adventitious rooting of the apple rootstock Jork 9. Plant Sci 106:167–176

    Article  CAS  Google Scholar 

  • Pozhvanov GA, Medvedev SS (2008) Auxin quantification based on histochemical staining of GUS under the control of auxin-responsive promoter. Russ J Plant Physiol 55:706–711

    Article  CAS  Google Scholar 

  • Prem D, Solís MT, Bárány I, Rodríguez-Sanz H, Risueño MC, Testillano PS (2012) A new microspore embryogenesis system under low temperature which mimics zygotic embryogenesis initials, expresses auxin and efficiently regenerates doubled-haploid plants in Brassica napus. BMC Plant Biol 12:127

    Article  PubMed Central  PubMed  Google Scholar 

  • Ricci A, Carra A, Torelli A, Maggiali CA, Morini G, Branca C (2001) Cytokinin-like activity of N,N’-diphenylureas. N,N’-bis-(2,3-methylenedioxyphenyl)urea and N,N’-bis-(3,4 methylenedioxyphenyl)urea enhance adventitious root formation in apple rootstock M26 (Malus pumila Mill.). Plant Sci 160:1055–1065

    Article  CAS  PubMed  Google Scholar 

  • Ricci A, Carra A, Rolli E, Bertoletti C, Branca C (2003) N,N’-bis-(2,3-methylenedioxyphenyl)urea and N,N’-bis-(3,4-methylenedioxyphenyl)urea cooperate with auxin in enhancing root formation of M26 apple (Malus pumila Mill.) stem slices. Plant Growth Regul 40:207–212

    Article  CAS  Google Scholar 

  • Ricci A, Incerti M, Rolli E, Vicini P, Morini G, Comini M, Branca C (2006) Diheteroarylurea derivatives as adventitious rooting adjuvants in mung bean shoots and M26 apple rootstock. Plant Growth Regul 50:201–209

    Article  CAS  Google Scholar 

  • Ricci A, Rolli E, Dramis L, Diaz-Sala C (2008) N,N’-bis-(2,3-methylenedioxyphenyl)urea and N,N’-bis-(3,4-methylenedioxyphenyl)urea may enhance adventitious rooting in Pinus radiata and affect expression of genes induced during adventitious rooting in the presence of exogenous auxin. Plant Sci 17:356–363

    Article  Google Scholar 

  • Rugini E, Jacoboni A, Luppino M (1993) Role of basal shoot darkening and exogenous putrescine treatments on in vitro rooting and on endogenous polyamine changes in difficult-to-root woody species. Sci Hortic 53:63–72

    Article  CAS  Google Scholar 

  • Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J, Benfey P, Leyser O, Bechtold N, Weisbeek P, Scheres B (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99:463–472

    Article  CAS  PubMed  Google Scholar 

  • Sanchez C, Vielba JM, Ferro E, Covelo G, Solé A, Abarca D, de Mier BS, Diaz-Sala C (2007) Two SCARECROW-LIKE genes from distantly-related forest species are induced in response to exogenous auxin in rooting-competent cuttings. Tree Physiol 27:1459–1470

    Article  CAS  PubMed  Google Scholar 

  • Schmitz RY, Skoog F (1970) The use of dimethylsulfoxide as a solvent in the tobacco bioassay for cytokinins. Plant Physiol 45:537–538

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Smulders MJM, Van De Ven ETWM, Croes AF, Wullems GJ (1990) Metabolism of 1-naphtaleneacetic acid in explants of tobacco: evidence for release of free hormone from conjugates. J Plant Growth Regul 9:27–34

    Article  CAS  Google Scholar 

  • Solé A, Sanchez C, Vielba JM, Valladares S, Abarca D, Diaz-Sala C (2008) Characterization and expression of a Pinus radiata putative ortholog to the Arabidopsis SHORT-ROOT gene. Tree Physiol 28:1629–1639

    Article  PubMed  Google Scholar 

  • Tamimi SM (2003) Stimulation of adventitious root formation in non-woody stem cuttings by uridine. Plant Growth Regul 40:257–260

    Article  CAS  Google Scholar 

  • Ulmasov T, Murfett U, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Van der Krieken WM, Breteler H, Visser MHM, Mavridou D (1993) The role of the conversion of IBA into IAA on root regeneration in apple: introduction of a test system. Plant Cell Rep 12:203–206

    Article  PubMed  Google Scholar 

  • Welander M, Huntrieser I (1981) The rooting ability of shoots raised in vitro from the apple rootstock A2 in juvenile and in adult growth phase. Physiol Plant 53:301–306

    Article  CAS  Google Scholar 

  • Welander M, Geier T, Zhu L (2009) Improvement of rooting in woody species using the rol genes. In: Niemi K, Scagel C (eds) Adventitious root formation of forest trees and horticultural plants-from genes to applications. Research Signpost, Trivandrum, pp 145–162

    Google Scholar 

  • Zimmerman PW, Wilcoxon F (1935) Several chemical growth substances which cause initiation of roots and other responses in plants. Contrib Boyce Thompson Inst 7:209–229

    CAS  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Dr. Sabrina Sabatini (Università La Sapienza, Rome, Italy) who kindly provided Arabidopsis DR5::GUS seeds. This work has been supported by the Italian Ministry of University and Research (FIL programme 2008, 2009 and Azioni Integrate Italia-Spagna IT0877DD2D to A.R.) and by the Spanish Ministry of Economy and Competitiveness (AGL2011-30462, AGL2008-05105-C02-01 and Acciones Integradas España-Italia HI 2007-0150 to C.D.-S.).

Author information

Authors and Affiliations

  1. Dipartimento di Bioscienze, Università di Parma, Parco Area delle Scienze 11/A, 43124, Parma, Italy

    Federica Brunoni, Enrico Rolli, Lucia Dramis & Ada Ricci

  2. Departamento de Ciencias de la Vida, Universidad de Alcalá, 28871, Alcalá de Henares, Madrid, Spain

    Dolores Abarca, Alberto Pizarro & Carmen Diaz-Sala

  3. Dipartimento di Farmacia, Università di Parma, Parco Area delle Scienze 27/A, 43124, Parma, Italy

    Matteo Incerti

Authors
  1. Federica Brunoni
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Enrico Rolli
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lucia Dramis
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Matteo Incerti
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dolores Abarca
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Alberto Pizarro
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Carmen Diaz-Sala
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ada Ricci
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ada Ricci.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Brunoni, F., Rolli, E., Dramis, L. et al. Adventitious rooting adjuvant activity of 1,3-di(benzo[d]oxazol-5-yl)urea and 1,3-di(benzo[d]oxazol-6-yl)urea: new insights and perspectives. Plant Cell Tiss Organ Cult 118, 111–124 (2014). https://doi.org/10.1007/s11240-014-0466-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-014-0466-8

Keywords

Search

Navigation