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Ethylene and polyamine production patterns during in vitro shoot organogenesis of two passion fruit species as affected by polyamines and their inhibitor

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Abstract

Levels of ethylene and polyamines (PAs) were measured during organogenesis of hypocotyl explants of two species of passion fruit (Passiflora cincinnata Masters and Passiflora edulis Sims f. flavicarpa Degener ‘FB-100’) to better understand the relationships of these regulators and their influence on cell differentiation and morphogenesis. Moreover, histological investigation of shoot ontogenesis was conducted to characterize the different events involved in cell redifferentiation and regulation of PA and ethylene levels. A delay was observed in morphogenic responses of P. edulis f. flavicarpa as compared to P. cincinnata, and these changes coincided with production of elevated levels of polyamine and ethylene levels. During differentiation, cells showed high rates of expansion and elongation, and high ethylene levels were associated with high PA levels, suggesting that the two biosynthesis pathways were highly regulated. Moreover, their interaction might be an important factor for determining cell differentiation. The addition of PAs to the culture medium did not promote organogenesis; however, the incorporation of the PA inhibitor methylglyoxal bisguanylhydrazone in the culture medium reduced shoot bud differentiation, suggesting the need to maintaining a minimum level of PAs for morphogenic events to take place.

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References

  • Abeles FB, Morgan PW, Saltveit ME (1992) Ethylene in plant biology, 2nd edn. Academic Press, New York

    Google Scholar 

  • Alvarez I, Tomaro ML, Benavides MP (2003) Changes in polyamines, proline and ethylene in sunflower calluses treated with NaCl. Plant Cell Tiss Organ Cult 74:51–59. doi:10.1023/A:1023302012208

    Article  CAS  Google Scholar 

  • Andersen SE, Bastola DR, Minocha SC (1998) Metabolism of polyamines in transgenic cells of carrot expressing a mouse ornithine decarboxylase cDNA. Plant Physiol 116:299–307

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bajaj S, Rajam MV (1995) Efficient plant regeneration from long term callus culture of rice by spermidine. Plant Cell Rep 14:717–720. doi:10.1007/BF00232654

    Article  CAS  Google Scholar 

  • Baron K, Stasolla C (2008) The role of polyamines during in vivo and in vitro development. In Vitro Cell Dev Biol Plant 44:384–395. doi:10.1007/s11627-008-9176-4

    Article  CAS  Google Scholar 

  • Bezold TN, Loy JB, Minocha SC (2003) Changes in the cellular content of polyamines of seed and fruit of a normal and a hull-less seed variety of pumpkin during development. Plant Sci 164:743–752. doi:10.1016/S0168-9452(03)00035-9

    Article  CAS  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 tobacco thin layers. Protoplasma 202:134–144. doi:10.1007/BF01282541

    Article  CAS  Google Scholar 

  • Buchanan BB, Gruissem W, Jones RL (2000) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville 1367 p

    Google Scholar 

  • Chow B, McCourt P (2004) Hormone signaling from a developmental context. J Exp Bot 55:247–251. doi:10.1093/jxb/erh032

    Article  PubMed  CAS  Google Scholar 

  • Crozier A, Kamiya Y, Bishop G, Yokota T (2000) Biosynthesis of hormones and elicitor molecules. In: Buchanan BB, Gruissem W, Jones RL (eds) Biochemistry & molecular biology of plants, 1st edn. American Society of Plant Physiologists, Rockville, pp 850–929

    Google Scholar 

  • Cunha MAP, Barbosa LV (2002) Aspectos botânicos. In: EMBRAPA. Ministério da Agricultura, Pecuária e Abastecimento (eds) Produção e aspectos técnicos. Série Frutas do Brasil. EMBRAPA, Brasilia, pp 12–15

  • Desai HV, Metha AR (1985) Changes in polyamine levels during shoot formation, root formation, and callus induction in cultured Passiflora leaf discs. J Plant Physiol 119:45–53

    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

    PubMed  CAS  Google Scholar 

  • Falasca G, Capitani F, Rovere FD, Zaghi D, Franchin C, Biondi S, Altamura MM (2008) Oligogalacturonides enhance cytokinin-induced vegetative shoot formation in tobacco explants, inhibit polyamine biosynthetic gene expression, and promote long-term remobilization of cell calcium. Planta 227:835–852. doi:10.1007/s00425-007-0660-6

    Article  PubMed  CAS  Google Scholar 

  • Fernando JA, Vieira ML, Machado SR, Appezzato-da-Glória B (2007) New insight into the in vitro organogenesis process: the case of Passiflora. Plant Cell Tiss Organ Cult 91:37–44. doi:10.1007/s11240-007-9275-7

    Article  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  PubMed  CAS  Google Scholar 

  • Hu WW, Gong HB, Pua EC (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 

  • Hunter DC, Burrit DJ (2005) Light quality influences the polyamine content of lettuce (Lactuca sativa L.) cotyledon explants during shoot production in vitro. Plant Growth Reg 45:53–61. doi:10.1007/s10725-004-5971-z

    Article  CAS  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  PubMed  CAS  Google Scholar 

  • Kakkar RK, Kaur-Sawhney V (2002) Polyamine research in plant—a changing perspective. Physiol Plant 116:281–292. doi:10.1034/j.1399-3054.2002.1160302.x

    Article  CAS  Google Scholar 

  • Kakkar RK, Nagar PK (1997) Distribution and changes in endogenous polyamines during winter dormancy in tea (Camellia sinensis L. Kuntze). J Plant Physiol 151:63–67. doi:10.1034/j.1399-3054.2002.1160302.x

    CAS  Google Scholar 

  • Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228:367–381. doi:10.1007/s00425-008-0772-7

    Article  PubMed  CAS  Google Scholar 

  • Kusanp T, Yamaguchi K, Berberich T, Takahashi Y (2007) Advances in polyamine research in 2007. J Plant Res 120:345–350. doi:10.1007/s10265-007-0074-3

    Article  Google Scholar 

  • Li Z, Burritt DJ (2003) Changes in endogenous polyamines during the formation of somatic embryos from isogenic lines of Dactylis glomerata L. with different regenerative capacities. Plant Growth Reg 40:65–74. doi:10.1023/A:1023028713114

    Article  CAS  Google Scholar 

  • Li C-H, Wang G-X (2004) Interactions between reactive oxygen species, ethylene and polyamines in leaves of Glycyrrhiza inflata seedlings under root osmotic stress. Plant Growth Reg 42:55–60. doi:10.1023/B:GROW.0000014890.97789.fe

    Article  CAS  Google Scholar 

  • Liu JH, Moriguchi T (2007) Changes in free polyamines titers and expression of polyamine biosynthetic genes during growth of peach in vitro callus. Plant Cell Rep 26:125–131. doi:10.1007/s00299-006-0223-5

    Article  PubMed  CAS  Google Scholar 

  • Lombardi SP, Passos IRS, Nogueira MCS, Appezato-da-Glória B (2007) In vitro shoot regeneration from roots and leaf discs of Passiflora cincinnata Mast. Braz Arch Biol Biotech 50:239–247

    Google Scholar 

  • Malmberg RL, Watson MB, Galloway GL, Yu W (1998) Molecular genetic analyses of plant polyamines. Crit Rev Plant Sci 17:199–224

    Article  CAS  Google Scholar 

  • Marino G, Franchin C, Marcolini 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 

  • Matilla AJ (1996) Polyamines and seed germination. Seed Sci Res 6:1–13

    Article  Google Scholar 

  • Metha RA, Cassol T, Li N, Ali N, Handa AK, Mattoo AK (2002) Engineered polyamine accumulation in tomato enhances phytonutrient content, juice quality and vine life. Nature Biotech 20:613–618. doi:10.1038/nbt0602-613

    Article  Google Scholar 

  • Minocha SC, Papa NS, Khan AJ, Samuelsen AI (1991) Polyamines and somatic embryogenesis in carrot III: effects of methyglyoxal bis guanylhydrazone. Plant Cell Physiol 32:395–402

    CAS  Google Scholar 

  • Monteiro M, Kevers C, Dommes J, Gaspar T (2002) A specific role for spermidine in the initiation phase of somatic embryogenesis in Panax ginseng CA Meyer. Plant Cell Tiss Organ Cult 68:225–232. doi:10.1023/A:1013950729576

    Article  CAS  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 

  • Nhut DT, Khiet BLT, Thi NN, Thuy DTT, Duy N, Hai NT, Huyen PX (2007) High frequency shoot formation of yellow passion fruit (Passiflora edulis f. flavicarpa) via thin cell layer (TCL) technology. In: Jain SM, Häggman H (eds) Protocols for micropropagation of woody trees and fruits. Springer, New York, pp 417–426

    Chapter  Google Scholar 

  • O’Brien TP, McCully ME (1981) The study of plant structure principles and select methods. Termacarphi, Melbourne 216 p

    Google Scholar 

  • Park KY, Lee SH (1994) Effects of ethylene and auxin on polyamine levels in suspension-cultured tobacco cells. Physiol Plant 90:382–390. doi:10.1111/j.1399-3054.1994.tb00403.x

    Article  CAS  Google Scholar 

  • Paschadilis KA, Roubelakis-Angelakis KA (2005) Spatial and temporal distribution of polyamines 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  Google Scholar 

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

    Google Scholar 

  • Puga-Hermida MI, Gallardo M, Matilla AJ (2003) The zygotic embryogenesis and ripening of Brassica rapa seeds provokes important alterations in the levels of free and conjugated abscisic acid and polyamines. Physiol Plant 117:279–288. doi:10.1034/j.1399-3054.2003.00033.x

    Article  CAS  Google Scholar 

  • Puga-Hermida MI, Gallardo M, Rodríguez-Gacio MC, Matilla AJ (2007) Polyamines contents, ethylene synthesis, and BrACO2 expression during turnip germination. Biol Plant 50:574–580. doi:10.1007/s10535-006-0090-5

    Article  Google Scholar 

  • Ravanel S, Gakiere B, Job D, Douce R (1998) The specific features of methionine biosynthesis and metabolism in plants. Proc Natl Acad Sci USA 95:7805–7812

    Article  PubMed  CAS  Google Scholar 

  • Reis LB, Silva ML, Lima ABP, Oliveira MLP, Pinto DLP, Lani ERG, Otoni WC (2007) Agrobacterium rhizogenes-mediated transformation of passionfruit species: Passiflora cincinnata and P. edulis f. flavicarpa. Acta Hortic 738:425–431

    Google Scholar 

  • Rey M, Diza-Sala C, Rodriguez R (1994) Comparison of endogenous polyamine content in hazel leaves and buds between the dormancy and flowering annual phases of growth. Physiol Plant 91:45–50. doi:10.1111/j.1399-3054.1994.tb00657.x

    Article  CAS  Google Scholar 

  • Santa-Catarina C (2005) Aspectos fisiológicos, morfológicos e bioquímicos da embriogênese em Ocotea catharinensis Mez. (Lauraceae). Tese [Doutorado]—Instituto de Ciências Biomédicas, Universidade de São Paulo, 117 p

  • 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 

  • Shoeb F, Yadav JS, Bajaj S, Rajam MV (2001) Polyamines as biomarkers for plant regeneration capacity: improvement of regeneration by modulation of polyamine metabolism in different genotypes of indica rice. Plant Sci 160:1229–1235. doi:10.1016/S0168-9452(01)00375-2

    Article  PubMed  CAS  Google Scholar 

  • Silva ML, Paim Pinto DL, Guerra MP, Floh EIS, Bruckner CH, Otoni WC (2009) A novel regeneration system for wild passion fruit species (Passiflora cincinnata Mast.) based on somatic embryogenesis from mature zygotic embryos. Plant Cell Tiss Organ Cult. doi: 10.1007/s11240-009-9574-2

  • 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 Organ Cult 76:53–60. doi:10.1023/A:1025847515435

    Article  CAS  Google Scholar 

  • Taiz L, Zeiger E (2004) Plant physiology, 3rd edn. Artmed, Porto Alegre 719 p

    Google Scholar 

  • Theiss C, Bohley P, Voigt J (2002) Regulation by polyamines of ornithine decarboxylase activity and cell division in the unicellular green alga Chlamydomonas reinhardtii. Plant Physiol 128:1470–1479. doi:10.1104/pp.010896

    Article  PubMed  CAS  Google Scholar 

  • Turano FJ, Kramer GF, Yang CY (1997) The effect of methionine, ethylene and polyamine catabolic intermediates on polyamine accumulation in detached soybean leaves. Physiol Plant 101:510–518. doi:10.1111/j.1399-3054.1997.tb01031.x

    Article  CAS  Google Scholar 

  • Vieira MLC, Carneiro MS (2004) Passiflora spp., passionfruit. In: Litz RE (ed) Biotechnology of fruit and nut crops. CABI, Oxford, pp 435–453

    Google Scholar 

  • Winner L, Apelbaum A (1986) Involvement of polyamines in the development of ripening avocado fruits. J Plant Physiol 26:223–234

    Google Scholar 

  • Zapata PJ, Serrano M, Pretel MT, Amoros A, Botella MA (2004) Polyamines and ethylene changes during germination of different plant species under salinity. Plant Sci 167:781–788. doi:10.1016/j.plantsci.2004.05.014

    Article  CAS  Google Scholar 

  • Zerbini FM, Otoni WC, Vieira MLC (2008) Passionfruit. In: Kole C, Hall TC (eds) A compendium of transgenic crop plants, v.5, tropical and subtropical fruit and nuts, 1st edn. Wiley, Berlin, pp 213–234

    Google Scholar 

  • Zhu C, Chen Z (2005) Role of polyamines in adventitious shoot morphogenesis from cotyledons of cucumber in vitro. Plant Cell Tiss Organ Cult 81:45–53. doi:10.1007/s11240-004-2773-y

    Article  CAS  Google Scholar 

  • Ziosi V, Bregoli AM, Bonghi C, Fossati T, Biondi S, Costa G, Torrigiani P (2006) Transcription of ethylene perception and biosynthesis genes is altered by putrescine, spermidine and aminoethoxyvinilglycine (AVG) during ripening in peach fruit (Prunus persica). New Phytol 172:229–238. doi:10.1111/j.1469-8137.2006.01828.x

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors thank Viveiros Flora Brasil Ltda (Araguari, MG, Brazil) for generously providing ‘FB-100’ Maguary seed population, FAPEMIG (Belo Horizonte, MG, Brazil), CNPq (Brasília, DF, Brazil), and CAPES (Brasília, DF, Brazil), for financial support. The authors are also grateful to the anonymous reviewers and to Dr. Schuyler S. Korban (Editor-in-Chief) for the criticisms and valuable suggestions for the manuscript.

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Correspondence to Wagner C. Otoni.

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Dias, L.L.C., Santa-Catarina, C., Ribeiro, D.M. et al. Ethylene and polyamine production patterns during in vitro shoot organogenesis of two passion fruit species as affected by polyamines and their inhibitor. Plant Cell Tiss Organ Cult 99, 199–208 (2009). https://doi.org/10.1007/s11240-009-9594-y

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