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Plant Growth Regulation

, Volume 67, Issue 1, pp 1–8 | Cite as

Establishment of suspension culture in Theobroma cacao and polyamines associated with cacao embryogenesis

  • Nicolas Niemenak
  • Tita Margaret Awah
  • Reinhard Lieberei
Original paper

Abstract

The effect of the position of excised hypocotyl discs on somatic embryo induction in liquid culture was studied. Shaking culture seems to be a rapid way of cacao somatic embryo regeneration since more than 40 embryos can be produced within 6 weeks directly from 5 mm hypocotyl discs cut near the apex. The importance of the position of transverse section cell layer explants and their biochemical characteristics on the establishment of cacao embryogenic suspension culture was scrutinized and discussed. In order to further improve cacao in vitro culture change in endogenous polyamines during zygotic versus somatic embryogenesis in Theobroma cacao L was analysed. Spermidine was the main polyamine in cacao tissues. In their early stages of embryogenesis, zygotic embryos contained more polyamine than in later stages. At the early stages, the zygotic embryos also contained more polyamine than the endosperm. Similar results were observed during somatic embryogenesis. The potential of using spermidine for cacao in vitro culture medium improvement is discussed.

Keywords

Zygotic and somatic embryogenesis Cacao Liquid culture Cell layer Polyamines 

Notes

Acknowledgments

The study was supported by the Alexander von Humboldt Stiftung (www.humboldt-stiftung.de) via grant to Nicolas Niemenak (Grant No KAM/1115305). The authors express gratitude to Thomas Tumforde and Detlef Böhm for their assistance during experiments.

References

  1. Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249PubMedCrossRefGoogle Scholar
  2. Alemanno L, Berthouly M, Michaux-Ferrière N (1997) A comparison between Theobroma cacao L. zygotic embryogenesis and somatic embryogenesis from floral explants. In Vitro Cell Dev Biol Plant 33:163–172CrossRefGoogle Scholar
  3. Alemanno L, Devic M, Niemenak N, Sanier C, Guilleminot J, Rio M, Verdeil J-L, Montoro P (2008) Characterization of leafy cotyledon1-like during embryogenesis in Theobroma cacao L. Planta 227:853–866PubMedCrossRefGoogle Scholar
  4. Argout X, Fouet O, Wincker P, Gramacho K, Legavre T et al (2008) Towards the understanding of the cocoa transcriptome: Production and analysis of an exhaustive dataset of ESTs of Theobroma cacao L. generated from various tissues and under various conditions. BMC Genomics 9:512PubMedCrossRefGoogle Scholar
  5. Argout X, Salse J, Aury JM, Guiltinan MJ, Droc G, Gouzy J et al (2011) The genome of Theobroma cacao. Nat Genet 43:101–109PubMedCrossRefGoogle Scholar
  6. Bagni N, Tassoni A (2001) Biosynthesis, oxidation and conjugation of aliphatic polyamines in higher plants. Amino Acids 20:301–317PubMedCrossRefGoogle Scholar
  7. Baron K, Stasolla C (2008) The role of polyamines during in vivo and in vitro development. In Vitro Cell Dev Biol Plant 44:384–395CrossRefGoogle Scholar
  8. Bashan Y, Okon Y, Henis Y (1985) Peroxidase, polyphenol oxidase, and phenols in relation to resistance against Pseudomonas syringae pv. tomato in tomato plant. Can J Bot 65:366–372CrossRefGoogle Scholar
  9. Becher T, Haberland G, Koop H-U (1992) Callus formation and plant regeneration in standard and microexplants from seedlings of barley (Hordeum vulgare L.). Plant Cell Rep 11:39–43CrossRefGoogle Scholar
  10. Bennett AB (2003) Out of the Amazon: Theobroma cacao enters the genomic era. Trends Plant Sci 8:561–563PubMedCrossRefGoogle Scholar
  11. Carlberg I, Söderhäll K, Eriksson T (1985) Phenoloxidase activity in Daucus carota is restricted to embryogenie cultures. FEBS Lett 87:295–298CrossRefGoogle Scholar
  12. Constabel CP, Bergey DR, Ryan CA (1995) Systemin activates synthesis of wound-inducible tomato leaf polyphenol oxidase via the octadecanoid defense signaling pathway. Proc Natl Acad Sci USA 92:407–411PubMedCrossRefGoogle Scholar
  13. Dijkema C, De Vries SC, Booij H, Schaafoma TJ, Van Kammen A (1988) Substrate utilization by suspension cultures and somatic embryos of Daucus carota L. measured by 13C NMR. Plant Physiol 88:1332–1337PubMedCrossRefGoogle Scholar
  14. Efrose RC, Flemetakis E, Sfichi L, Stedel C, Kouri ED, Udvardi MK, Kotzabasis K, Katinakis P (2008) Characterization of spermidine and spermine synthases in Lotus japonicus: induction and spatial organization of polyamine biosynthesis in nitrogen fixing nodules. Planta 228:37–49PubMedCrossRefGoogle Scholar
  15. Faure O, Mengoli M, Nougarede A, Bagni N (1991) Polyamine pattern and biosynthesis in zygotic and somatic embryo stages of Vitis vinifera. J Plant Physiol 138:545–549CrossRefGoogle Scholar
  16. Fouet O, Allegre M, Argout X, Jeanneau M, Lemainque A, Pavek S, Boland A, Risterucci AM, Loor G, Tahi M et al (2011) Structural characterization and mapping of functional EST-SSR markers in Theobroma cacao. Tree Genet Genomes 7:799–817CrossRefGoogle Scholar
  17. Ge C, Cui X, Wang Y, Hu Y, Fu Z, Zhang D, Cheng Z, Li J (2006) BUD2, encoding an S-adenosylmethionine decarboxylase, is required for Arabidopsis growth and development. Cell Res 16:446–456PubMedCrossRefGoogle Scholar
  18. Gemperlová L, Fischerová L, Cvikrová M, Malá J, Vondráková Z, Martincová O, Vágner M (2009) Polyamine profiles and biosynthesis in somatic embryo development and comparison of germinating somatic and zygotic embryos of Norway spruce. Tree Physiol 29:1287–1298PubMedCrossRefGoogle Scholar
  19. Goyal M, Asthir B (2010) Polyamine catabolism influences antioxidative defense mechanism in shoots and roots of five wheat genotypes under high temperature stress. Plant Growth Regul 60:13–25CrossRefGoogle Scholar
  20. Grotkass C (1997) Aktivität und Aktivierbarkeit von Polyphenoloxidasen in embryogenen und nicht-embryogenen Suspensionskulturen von Euphorbia pulcherrima Willd, Ex Klotsch. Dissertation zur Erlangung des Doktorgrades, Universität Hamburg, p 115Google Scholar
  21. Grotkass C, Lieberei R, Preil W (1995) Polyphenoloxidase-activity and -activation in embryogenic and non-embryogenic suspension cultures of Euphorbia pulcherrima. Plant Cell Rep 14:428–431CrossRefGoogle Scholar
  22. Hadrami El, d’Auzac J (1992) Effects of growth regulators on polyamine content and peroxidase activity in Hevea brasiliensis callus. Ann Bot 69:323–325Google Scholar
  23. Hanzawa Y, Imai A, Michael AJ, Komeda Y, Takahashi T (2002) Characterization of the spermidine synthase-related gene family in Arabidopsis thaliana. FEBS Lett 527:176–180PubMedCrossRefGoogle Scholar
  24. Imai A, Matsuyama T, Hanzawa Y, Akiyama T, Tamaoki M, Saji H, Shirano Y, Kato T, Hayashi H, Shibata D, Tabata S, Komeda Y, Takahashi T (2004) Spermidine synthase genes are essential for survival of Arabidopsis. Plant Physiol 135:1565–1573PubMedCrossRefGoogle Scholar
  25. Jay V, Genestier S, Courduroux J-C (1994) Bioreactor studies of the effect of medium pH on carrot (Daucus carota L.) somatic embryogenesis. Plant Cell Tiss Organ Cult 36:205–209CrossRefGoogle Scholar
  26. Kakkar RK, Sawhney VK (2002) Polyamine research in plants—a changing perspective. Physiol Plant 116:281–292CrossRefGoogle Scholar
  27. Kusano T, Yamaguchi K, Berberich T, Takahashi Y (2007) Advances in polyamine research in 2007. J Plant Res 120:345–350PubMedCrossRefGoogle Scholar
  28. Li Z, Traore A, Maximova SN, Guiltinan MJ (1998) Somatic embryogenesis and plant regeneration from floral explants of cacao (Theobroma cacao L.) using thidiazuron. In Vitro Cell Dev Biol Plant 34:293–299CrossRefGoogle Scholar
  29. Loukanina N, Thorpe TA (2008) Arginine and ornithine decarboxylases in embryonic and non-embryonic carrot cell suspensions. In Vitro Cell Dev Biol Plant 44:59–64CrossRefGoogle Scholar
  30. Maximova SN, Alemanno L, Young A, Ferrière N, Traore A, Guiltinan MJ (2002) Efficiency, genotypic variability, and cellular origin of primary and secondary somatic embryogenesis of Theobroma cacao L. In Vitro Cell Dev Biol Plant 38:252–259CrossRefGoogle Scholar
  31. Mayer AM (1987) Polyphenol oxidases in plants—recent progress. Phytochemistry 26:11–20CrossRefGoogle Scholar
  32. Miller CR, Guiltinan MJ (2003) Perspective on rapid vegetative multiplication for orthotropic scion and rootstock varieties of cocoa. International workshop on cocoa breeding for improved production systems (INGENIC). 19–21 October 2003, Accra, Ghana, pp 189–194Google Scholar
  33. Minocha R, Smith DR, Reeves C, Steele KD, Minocha SC (1999) Polyamine levels during the development of zygotic and somatic embryos of Pinus radiata. Physiol Plant 105:155–164CrossRefGoogle Scholar
  34. Niemenak N, Saare-Surminski K, Rohsius C, Omokolo ND, Lieberei R (2008) Regeneration of somatic embryos in Theobroma cacao L. in temporary immersion bioreactor and analyses of free amino acids in different tissues. Plant Cell Rep 27:667–676PubMedCrossRefGoogle Scholar
  35. Okole BN, Schulz FA (1996) Micro-cross sections of banana and plantains (Musa spp) morphogenesis and regeneration of callus and shoot buds. Plant Sci 116:185–195CrossRefGoogle Scholar
  36. Osternack N, Saare-Surminski K, Preil W, Lieberei R (1999) Induction of somatic embryos, adventitious shoots and roots in hypocotyls tissue of Euphorbia pulcherrima Wild. ex Klotzsch: comparative studies on embryogenic and organogenic competence. J Appl Bot 73:197–201Google Scholar
  37. 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 138:142–152PubMedCrossRefGoogle Scholar
  38. Smith MA, Davies RJ, Reid JB (1985) Role of polyamines in gibberellin-induced internode growth in peas. Plant Physiol 78:92–99PubMedCrossRefGoogle Scholar
  39. Steffens J, Harel E, Hunt M (1994) Polyphenol oxidase. In: Ellis BE, Kuroki GW, Stafford HA (eds) Genetic engineering of plant secondary metabolism. Plenum Press, New York, pp 276–304Google Scholar
  40. Thipyapong P, Hunt MD, Steffens JC (1995) Systemic wound induction of potato (Solanum tuberosum) polyphenol oxidase. Phytochemistry 40:673–676CrossRefGoogle Scholar
  41. Todorova D, Sergiev I, Alexieva V, Karanov E, Smith A, Hall M (2007) Polyamine content in Arabidopsis thaliana (L.) Heynh during recovery after low and high temperature treatment. Plant Growth Regul 51:185–191CrossRefGoogle Scholar
  42. Urano K, Hobo T, Shinozaki K (2005) Arabidopsis ADC genes involved in polyamine biosynthesis are essential for seed development. FEBS Lett 579:1557–1564PubMedCrossRefGoogle Scholar
  43. Van Le B, Thao D, My Nghieng, Gendy C, Vidal J, Van Tran Thanh K (1997) Somatic embryogenesis on thin cell layers of a C4 species, Digitaria sanguinalis (L.) Scop. Plant Cell Tiss Organ Cult 49:201–208CrossRefGoogle Scholar
  44. Vaughn KC, Lax AR, Duke SO (1988) Polyphenol oxidase: the chloroplast oxidase with no established function. Physiol Plant 72:659–665CrossRefGoogle Scholar
  45. Vinocur B, Carmi T, Altman A, Ziv M (2000) Enhanced bud regeneration in aspen (Populus tremula L.) roots cultured in liquid media. Plant Cell Rep 19:1146–1154CrossRefGoogle Scholar
  46. Zapata PJ, Serrano M, Pretel MT, Botella MA (2008) Changes in free polyamine concentration induced by salt stress in seedlings of different species. Plant Growth Regul 56:167–177CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Nicolas Niemenak
    • 1
  • Tita Margaret Awah
    • 2
  • Reinhard Lieberei
    • 3
  1. 1.Laboratory of Plant Physiology, Department of Biological Science, Higher Teachers’ Training CollegeUniversity of Yaounde IYaoundeCameroon
  2. 2.Higher Teachers’ Training CollegeUniversity of BamendaBamendaCameroon
  3. 3.Department of Crop Science and Plant Ecology, Biocenter Klein Flottbek and Botanical GardenUniversity of HamburgHamburgGermany

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