Skip to main content
SpringerLink
Log in

Ethylene and polyamine interactions in morphogenesis of Passiflora cincinnata: effects of ethylene biosynthesis and action modulators, as well as ethylene scavengers

  • Original Research
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Ethylene is a plant hormone that is of fundamental importance to in vitro morphogenesis, but in many species, it has not been thoroughly studied. Its relationship with polyamines has been studied mainly because the two classes of hormones share a common biosynthetic precursor, S-adenosylmethionine (SAM). In order to clarify whether competition between polyamines and ethylene influences in vitro morphogenetic responses of Passiflora cincinnata Mast., a climacteric species, different compounds were used that act on ethylene biosynthesis and action, or as ethylene scavengers. Treatment with the ethylene inhibitor, aminoethoxyvinylglycine (AVG) caused a greater regeneration frequency in P. cincinnata, whereas treatment with the ethylene precursor, 1-aminocyclopropane-1-carboxylic-acid (ACC) lessened regeneration frequencies. The data suggested that levels of polyamines and ethylene are not correlated with morphogenic responses in P. cincinnata. It was ascertained that neither the absolute ethylene and polyamine levels, nor competition between the compounds, correlated to the obtained morphogenic responses. However, sensitivity to, and signaling by, ethylene appears to play an important role in differentiation. This study reinforces previous reports regarding the requirement of critical concentrations and temporal regulation of ethylene levels for morphogenic responses. Temporal regulation also appeared to be a key factor in competition between the two biosynthetic pathways, without having any effects on morphogenesis. Further studies investigating the silencing or overexpression of genes related to ethylene perception, under the influence of polyamines in cell differentiation are extremely important for the complete understanding of this 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

  • Arigita L, Tamés R, González A (2003) 1-Methycyclopropene and ethylene as regulators of in vitro organogenesis in kiwi explants. Plant Growth Reg 40:59–64. doi:10.1023/A:1023070131422

    Article  CAS  Google Scholar 

  • Arigita L, Majada JP, Gonzalez A, Sanchez-Tames R (2005) Controle ambiental en cultivo in vitro: CO2 y etileno. In: Sanchez-Olate ME, Leal DGR (eds) Biotecnologia vegetal en especies leñosas de interés forestal. Universidad de Concepcion, Concepcion-Chile, pp 105–117

    Google Scholar 

  • Aziz A, Martin-Tunguy J, Larher F (1997) Plasticity of polyamine metabolism associated with high osmotic stress in leaf discs and with ethylene treatment. Plant Growth Reg 21:153–163. doi:10.1023/A:1005730509433

    Article  CAS  Google Scholar 

  • Bais HP, Sudha G, Ravishankar GA (2001) Influence of putrescine, silver nitrate and polyamine inhibitors on the morphogenetic response in untransformed and transformed tissues of Cichorium intybus and their regenerants. Plant Cell Rep 20:547–555. doi:10.1007/s002990100367

    Article  CAS  Google Scholar 

  • Barbosa WM, Otoni WC, Carnellossi M, Silva E, Azevedo AA, Vieira G (2001) Rhizogenesis in vitro shoot cultures of passion fruit (Passiflora edulis f. flavicarpa Deg.) is affected by ethylene precursor and by inhibitors. Int J Hortic Sci 7:47–51

    Google Scholar 

  • Biddington NL (1992) The influence of ethylene in plant tissue culture. Plant Growth Reg 11:173–187. doi:10.1007/BF00024072

    Article  CAS  Google Scholar 

  • Biondi S, Scaramagli S, Capitani F, Marino G, Altamura MM, Torrigiani P (1998) Ethylene involvement in the vegetative bud formation in tabacco thin layers. Protoplasma 202:134–144. doi:10.1007/BF01282541

    Article  CAS  Google Scholar 

  • Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Ann Rev Cell Dev Biol 16:1–18. doi:10.1146/annurev.cellbio.16.1.1

    Article  CAS  Google Scholar 

  • Bregoli AM, Ziosi V, Biondi S, Claudio B, Costa G, Torrigiani P (2006) A comparison between intact fruit and fruit explants to study the effect of polyamines and aminoethoxyvinylglycine (AVG) on fruit ripening in peach and nectarine (Prunus persica L. Batch). Postharvest Biol Technol 42:31–40. doi:10.1016/j.postharvbio.2006.05.009

    Article  CAS  Google Scholar 

  • Carvalho MHC, Le BV, Zuily-Fodil Y, Thi ATP, Van KTT (2000) Efficient whole plant regeneration of common bean (Phaseolus vulgaris L.) using thin-cell-layer culture and silver nitrate. Plant Sci 159:223–232 10.1016/S0168-9452(00)00346-0

    Article  Google Scholar 

  • Chatfield SP, Raizada MN (2008) Ethylene and shoot regeneration: hookless1 modulates de novo shoot organogenesis in Arabidopsis thaliana. Plant Cell Rep 27:655–666. doi:10.1007/s00299-007-0496-3

    Article  CAS  PubMed  Google Scholar 

  • Chi GL, Pua EC, Goh CJ (1991) Role of ethylene on de novo shoot regeneration from cotyledonary explants of Brassica campestris ssp. Pekinensis (Lour) Olsson in vitro. Plant Physiol 96:178–183

    Article  CAS  PubMed  Google Scholar 

  • Dias LLC, Santa-Catarina C, Ribeiro DM, Barros RS, Floh EIS, Otoni WC (2009) Ethylene and polyamines production patterns during in vitro shoot organogenesis of two passion fruit as affected by polyamines and their inhibitor. Plant Cell Tiss Org Cult 99:199–208. doi:10;1007/s11240-009-9594-y

    Article  CAS  Google Scholar 

  • El Meskaoui A, Tremblay FM (2001) Involvement of ethylene in the maturation of black spruce embryogenic cell lines with different maturation capacities. J Exp Bot 52:761–769. doi:10.1093/jexbot/52.357.761

    CAS  PubMed  Google Scholar 

  • Faria JLC, Segura J (1997) In vitro control of adventitious bud differentiation by inorganic medium components and silver thiosulfate in explants of Passiflora edulis f. flavicarpa. In Vitro Cell Dev Biol Plant 33:209–212. doi:10.1007/s11627-997-0024-8

    Article  CAS  Google Scholar 

  • Franchin C, Fossati T, Pasquini E, Lingua G, Castiglione S, Torrigiani P, Biondi S (2007) High concentrations of zinc and copper induce differential polyamine responses in micropropagated white poplar (Populus alba). Physiol Plant 130:77–90. doi:10.1111/j.1399-3054.2007.00886.x

    Article  CAS  Google Scholar 

  • Fukuda H (1996) Xylogenesis: initiation, progression, and cell death. Ann Rev Plant Physiol Plant Mol Biol 47:299–325

    Article  CAS  Google Scholar 

  • Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50:151–158. doi:10.1016/0014-4827(68)90403-5

    Article  CAS  PubMed  Google Scholar 

  • Gaspar T, Kevers C, Faivre-Rampant O, Crêvecoler M, Pennel GL, Greppin H, Dommes J (2003) Changing concepts in plant hormone action. In Vitro Cell Dev Biol Plant 39:85–106. doi:10.1079/IVP2002393

    Article  CAS  Google Scholar 

  • George EF (1993) Plant propagation by tissue culture. Part 1: the technology, 2nd edn. Exegetics Limited, Edington

    Google Scholar 

  • González A, Arigita L, Majada J, Sánchez-Tamés R (1997) Ethylene in in vitro organogenesis and plant growth of Populus tremula L. Plant Growth Reg 22:1–6. doi:10.1023/A:1005751017498

    Article  Google Scholar 

  • Hatanaka T, Sawabeb E, Azuma T, Uchidab N, Yasudab T (1995) The role of ethylene in somatic embryogenesis from leaf discs of Coffea canephora. Plant Sci 107:199–204. doi:10.1016/0168-9452(95)04103-2

    Article  CAS  Google Scholar 

  • Hu W-W, Gong H, Pua E-C (2006) Modulation of SAMDC expression in Arabidopsis thaliana alters in vitro shoot organogenesis. Physiol Plant 128:740–750. doi:10.1111/j.1399-3054.2006.00799.x

    Article  CAS  Google Scholar 

  • Huai Q, Xia Y, Chen Y, Callahan B, Li N, Ke H (2001) Crystal structures of 1-aminocyclopropane-1-carboxylate (ACC) synthase in complex with aminoethoxyvinylglycine and pyridoxal-5-phosphate provide new insight into catalytic mechanism. J Biol Chem 276:38210–38216

    Article  CAS  PubMed  Google Scholar 

  • Jha AK, Dahleen LS, Suttle JC (2007) Ethylene influences green plant regeneration from barley callus. Plant Cell Rep 26:285–290. doi:10.1007/s00299-006-0252-0

    Article  CAS  PubMed  Google Scholar 

  • Jona R, Cattro A, Travaglio D (2002) The climacteric feature of fruits is reflected in the sensitivity to ethylene of plantlets in vitro. Sci Hort 94:273–284. doi:10.1016/S0304-4238(01)00380-6

    Article  Google Scholar 

  • Joshi A, Kothari SL (2007) High copper levels in the medium improves shoot bud differentiation and elongation from the cultured cotyledons of Capsicum annuum L. Plant Cell Tiss Org Cult 88:127–133. doi:10.1007/s11240-006-9171-6

    Article  CAS  Google Scholar 

  • Li C, Jiao J, Wang G (2004) The important roles of reactive oxygen species in the relationship between ethylene and polyamines in leaves of spring wheat seedlings under root osmotic stress. Plant Sci 166:303–315. doi:10.1016/j.plantsci.2003.09.019

    Article  CAS  Google Scholar 

  • Ma JH, Yao JL, Cohen D, Morris B (1998) Ethylene inhibitors enhance in vitro root formation from apple shoot cultures. Plant Cell Rep 17:211–214. doi:10.1007/s002990050380

    Article  CAS  Google Scholar 

  • Magdalita PM, Godwin ID, Drew RA, Adkins SW (1997) Effects of ethylene and culture environment on development of papaya nodal cultures. Plant Cell Tiss Org Cult 49:93–100. doi:10.1023/A:1005869211684

    Article  CAS  Google Scholar 

  • Marino G, Franchim C, Marcolino G, Biondi S (2008) Adventitious shoot formation in cultured leaf explants of quince and pear is accompanied by different patterns of ethylene and polyamine production, and responses to aminoethoxyvinylglycine. J Hort Sci Biotech 83:260–266

    CAS  Google Scholar 

  • Martin-Tunguy J (2001) Metabolism and function of polyamines in plant: recent development (new approaches). Plant Growth Reg 34:135–148. doi:10.1023/A:1013343106574

    Article  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497. doi:10.1111/j.1399-3054.1962.tb08052.x

    Article  CAS  Google Scholar 

  • Naik SK, Chand PK (2003) Silver nitrate and aminoethoxyvinilglycine promote in vitro adventitious shoot regeneration of pomegranate (Punica granatum L.). J Plant Physiol 160:423–430

    Article  CAS  PubMed  Google Scholar 

  • Ortega-Martínez O, Pernas M, Carol RJ, Dolan L (2007) Ethylene modulates stem cell division in the Arabidopsis thaliana root. Science 317:507–510. doi:10.1126/science.1143409

    Article  PubMed  Google Scholar 

  • Ozudogru EA, Ozden-Tokatli Y, Akcin A (2005) Effect of silver nitrate on multiple shoot formation of Virginia-type peanut through shoot tip culture. In Vitro Cell Dev Biol Plant 41:151–156. doi:10.1079/IVP2004591

    Article  CAS  Google Scholar 

  • Paiva Neto VB, Reis LB, Finger FL, Barros RS, Carvalho CR, Otoni WC (2009) Involvement of ethylene in the rooting of seedling shoot cultures of Bixa orellana L. In Vitro Cell Dev Biol Plant 45:693–700. doi: 10.1007/s11627-009-9236-4

    Article  CAS  Google Scholar 

  • Paschalidis KA, Roubelakis-Angelakis KA (2005) Spatial and temporal distribution of polyamine levels and polyamine anabolism in different organs/tissues of the tobacco plant: correlations with age, cell division/expansion, and differentiation. Plant Physiol 138:142–152. doi:10.1104/pp.104.055483

    Article  CAS  PubMed  Google Scholar 

  • Pua E-C (1999) Morphogenesis in cell and tissue cultures: role of ethylene and polyamines. In: Soh WY, Bhojwani SS (eds) Morphogenesis in plant tissue culture. Kluwer Academic Publishers, Dordrecht, pp 255–303

    Google Scholar 

  • Reid MS, Paul JL, Farhoomand MB, Kofranek AM, Staby GL (1980) Pulse treatments with the silver thiosulfate complex extend the vase life of cut carnations. J Amer Soc Hortic Sci 105:25–27

    CAS  Google Scholar 

  • Reis LB (2001) In vitro morphogenesis of the yellow passion fruit (Passiflora edulis f. flavicarpa Degener) associated to ethylene and jellifying agents. Dissertation, University of Viçosa (In Portuguese)

  • Reis LB, Paiva Neto VB, Picoli EAT, Costa MGC, Rêgo MM, Carvalho CR, Finger FL, Otoni WC (2003) Axillary bud development of passion fruit as affected by ethylene precursor and inhibitors. In Vitro Cell Dev Biol Plant 39:618–622. doi:10.1079/IVP2003455

    Article  CAS  Google Scholar 

  • Roustan JP, Latche A, Fallot J (1990) Control of carrot somatic embryogenesis by AgNO3 an inhibitor of ethylene action effect on arginine descarboxylase activity. Plant Sci 67:89–95. doi:10.1016/0168-9452(90)90054-R

    Article  CAS  Google Scholar 

  • Santana-Buzzy N, Canto-Flick R, Iglesias-Andreu LG, Montalvo-Peniche MD, Lopez-Puc G, Barahona-Perez F (2006) Improvement of in vitro culturing of Habanero pepper by inhibition of ethylene effects. HortScience 41:405–409

    CAS  Google Scholar 

  • Scaramagli S, Biondi S, Capitani F, Gerola P, Altamura MM, Torrigiani P (1999) Polyamine conjugate levels and ethylene biosynthesis: inverse relationship with vegetative bud formation in tobacco thin layers. Physiol Plant 105:367–376. doi:10.1034/j.1399-3054.1999.105223.x

    Article  CAS  Google Scholar 

  • Schaller GE, Kieber JJ (2002) Ethylene. The Arabidopsis book. American Society of Plant Biologists, Rockville

    Google Scholar 

  • Silveira V, Floh EIS, Handro W, Guerra MP (2004) Effect of plant growth regulators on the cellular growth and levels of intracellular protein, starch and polyamines in embryogenic suspension cultures of Pinus taeda. Plant Cell Tiss Org Cult 76:53–60. doi:10.1023/A:1025847515435

    Article  CAS  Google Scholar 

  • Torrigiani P, Altamura MM, Pasqua G, Monacelli B, Serafini-Fracassini D, Bagni N (1987) Free and conjugated polyamines during de novo floral and vegetative bud formation in thin cell layers of tobacco. Physiol Plant 70:453–460. doi:10.1111/j.1399-3054.1987.tb02842.x

    Article  CAS  Google Scholar 

  • Tsuchisaka A, Theologis A (2004) Unique and overlapping expression patterns among the Arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family members. Plant Physiol 136:2982–3000. doi:10.1104/pp.104.049999

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thanks the Brazilian sponsoring agencies, CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico, Brasil) and CAPES (Coordenação de Aperfeiçoamento de Pessoal de Ensino Superior), FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo), and FAPEMIG (Fundação de Amparo à Pesquisa do Estado de Minas Gerais), for financial support.

Author information

Authors and Affiliations

  1. Plant Cell Biology Laboratory, Department of Botany, IB-University of São Paulo, São Paulo, SP, CP 11461, Brazil

    Leonardo Lucas Carnevalli Dias, Claudete Santa Catarina & Eny Iochevet Segal Floh

  2. Department of Plant Biology, Plant Growth and Development Laboratory, Federal University of Viçosa, University Campus, Peter Henry Rolfs Avenue, Viçosa, MG, 36570-000, Brazil

    Dimas Mendes Ribeiro & Raimundo Santos Barros

  3. Plant Biology Department, Plant Tissue Culture Laboratory, BIOAGRO, Federal University of Viçosa, University Campus, Peter Henry Rolfs Avenue, Viçosa, MG, 36570-000, Brazil

    Wagner Campos Otoni

Authors
  1. Leonardo Lucas Carnevalli Dias
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dimas Mendes Ribeiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Claudete Santa Catarina
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Raimundo Santos Barros
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Eny Iochevet Segal Floh
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wagner Campos Otoni
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wagner Campos Otoni.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dias, L.L.C., Ribeiro, D.M., Catarina, C.S. et al. Ethylene and polyamine interactions in morphogenesis of Passiflora cincinnata: effects of ethylene biosynthesis and action modulators, as well as ethylene scavengers. Plant Growth Regul 62, 9–19 (2010). https://doi.org/10.1007/s10725-010-9478-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-010-9478-5

Keywords

Search

Navigation