Advertisement

TDZ-Induced Morphogenesis Pathways in Woody Plant Culture

  • Tatyana I. Novikova
  • Yulianna G. Zaytseva
Chapter

Abstract

Thidiazuron (TDZ) possesses a unique property to stimulate both the auxin- and cytokinin-like activities to induce in vitro morphogenesis pathways in the different explants of many species. An additional advantage of TDZ in low concentrations for many recalcitrant woody species in comparison to common amino purine cytokinins is a higher efficiency in overcoming monopodial growth habits by stimulating the axillary shoot development in in vitro culture. The application of TDZ for in vitro woody tissue culture inducts the wide range of morphological reactions including somatic embryogenesis and shoot organogenesis followed by root organogenesis, which occurs directly or through callus formation. These responses suggested that TDZ-induced regeneration systems could be used as the models for studying the fundamental aspects of plant biology and better understanding the developmental pathways. Despite the progress of recent biochemical, physiological, and molecular researches of TDZ effect on plant regeneration through organogenesis and somatic embryogenesis, the data on chronological sequences of morphological events are still limited. The abnormality formation of de novo structures is known to be undesirable side effect of TDZ. Therefore, the morpho-histological approach based on the observation of developmental route under TDZ at microscopic level and detailed histological analysis is necessary to reveal the type of morphogenic response (organogenic or embryogenic), improve the regeneration efficiency, and create systems of large-scale propagation for woody species. The chapter discusses the data on TDZ-induced regeneration systems in various woody tissue cultures analyzed by morpho-histological approach as a valuable tool to perform morphogenesis studies.

Keywords

Thidiazuron Shoot organogenesis Somatic embryogenesis Morpho-histological analysis 

Notes

Acknowledgments

The reported study was funded by the Russian Foundation for Basic Research (RFBR) according to the research project № 17-04-00782.

References

  1. Ahmad N, Anis M (2007) Rapid clonal multiplication of a woody tree, Vitex negundo L. through axillary shoots proliferation. Agrofor Syst 71:195–200. https://doi.org/10.1007/s10457-007-9078-1 CrossRefGoogle Scholar
  2. Ahmed MR, Anis M (2012) Role of TDZ in the quick regeneration of multiple shoots from nodal explant of Vitex trifolia L. – an important medicinal plant. Appl Biochem Biotechnol 168:957–966. https://doi.org/10.1007/s12010-012-9799-0 PubMedCrossRefGoogle Scholar
  3. Ahuja MR (1993) Micropropagation a la carte. In: Ahuja MR (ed) Micropropagation of woody plants, forestry series, vol 41. Kluwer Academic, Dordrecht, pp 3–9CrossRefGoogle Scholar
  4. Ainsley PJ, Collins GG, Sedgeley M (2000) Adventitious shoot regeneration from leaf explants of almond (Prunus dulcis mill.) In Vitro Cell Dev Biol-Plant 36:470–474. https://doi.org/10.1007/s11627-000-0084-5 CrossRefGoogle Scholar
  5. Atta R, Laurens L, Boucheron-Dubuisson E et al (2009) Pluripotency of Arabidopsis xylem pericycle underlies shoot regeneration from root and hypocotyl explants grown in vitro. Plant J 57:626–644. https://doi.org/10.1111/j.1365-313X.2008.03715.x PubMedCrossRefGoogle Scholar
  6. Azad MAK, Yokota S, Ohkubo T et al (2005) In vitro regeneration of the medicinal woody plant Phellodendron amurense Rupr. through excised leaves. Plant Cell Tissue Organ Cult 80:43–50. https://doi.org/10.1007/s11240-004-8809-5 CrossRefGoogle Scholar
  7. Bairu MW, Kane ME (2011) Physiological and developmental problems encountered by in vitro cultured plants. Plant Growth Regul 63:101–103. https://doi.org/10.1007/s10725-011-9565-2 CrossRefGoogle Scholar
  8. Baránek M, Čechová J, Raddová J et al (2015) Dynamics and reversibility of the DNA methylation landscape of grapevine plants (Vitis vinifera) stressed by in vitro cultivation and thermotherapy. PLoS One 10(5):e0126638. https://doi.org/10.1371/journal.pone.0126638 PubMedPubMedCentralCrossRefGoogle Scholar
  9. Baskaran P, Kumari A, Van Staden J (2015) Embryogenesis and synthetic seed production in Mondia whitei. Plant Cell Tissue Organ Cult 121:205–214. https://doi.org/10.1007/s11240-014-0695-x CrossRefGoogle Scholar
  10. Bassuner BM, Lam R, Lukowitz W, Yeung EC (2007) Auxin and root initiation in somatic embryos of Arabidopsis. Plant Cell Rep 26:1–11Google Scholar
  11. Bhagwat B, David Lane W (2004) In vitro shoot regeneration from leaves of sweet cherry (Prunus avium) ‘Lapins’ and ‘Sweetheart’. Plant Cell Tissue Organ Cult 78:173–181. https://doi.org/10.1023/B:TICU.0000022552.12449.71 CrossRefGoogle Scholar
  12. Blando F, Onlu S, Colella G et al (2013) Plant regeneration from immature seeds of Eugenia myrtifolia Sims. In Vitro Cell Dev Biol-Plant 49:388–395. https://doi.org/10.1007/s11627-013-9502-3 CrossRefGoogle Scholar
  13. Briggs BA, MCculloch SM, Edick LA (1988) Micropropagation of azalea using thidiazuron. Acta Hortic 226:205–208CrossRefGoogle Scholar
  14. Brijwal L, Pandey A, Tamta S (2015) In vitro propagation of the endangered species Berberis aristata DC. via leaf-derived callus. In Vitro Cell Dev Biol-Plant 51:637–647. https://doi.org/10.1007/s11627-015-9716-7 CrossRefGoogle Scholar
  15. Butenko RG (1999) Biology of higher plant cells in vitro and biotechnologies on their bases. FBC-Press, MoscowGoogle Scholar
  16. Casanova E, Valdes AE, Fernandez B et al (2004) Levels and immunolocalization of endogenous cytokinins in thidiazuron-induced shoot organogenesis in carnation. J Plant Physiol 161(1):95–104PubMedCrossRefGoogle Scholar
  17. Cheepala S, Sharma N, Sahi S (2004) Rapid in vitro regeneration of Sesbania drummondii. Biol Plant 48(1):13–18. https://doi.org/10.1023/B:BIOP.0000024269.72171.42 CrossRefGoogle Scholar
  18. Chhabra G, Chaudhary D, Varma M et al (2008) TDZ-induced direct shoot organogenesis and somatic embryogenesis on cotyledonary node explants of lentil (Lens culinaris Medik.) Physiol Mol Biol Plants 14(4):347–353. https://doi.org/10.1007/s12298-008-0033-z PubMedCrossRefGoogle Scholar
  19. Christianson ML, Warnick DA (1985) Temporal requirement for phytohormone balance in the control of organogenesis in vitro. Dev Biol 112:494–497. https://doi.org/10.1016/0012-1606(85)90423-3 CrossRefGoogle Scholar
  20. Clark SE, Running MP, Meyerowitz EM (1993) CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development 119:397–418PubMedGoogle Scholar
  21. Corredoira E, Ballester A, Vieitez AM (2008) Thidiazuron-induced high-frequency plant regeneration from leaf explants of Paulownia tomentosa mature trees. Plant Cell Tissue Organ Cult 95:197–208. https://doi.org/10.1007/s11240-008-9433-6 CrossRefGoogle Scholar
  22. Cuenca B, Ballester A, Vieitez AM (2000) In vitro adventitious bud regeneration from internode segments of beech. Plant Cell Tissue Organ Cult 60:213–220CrossRefGoogle Scholar
  23. D’Onofrio C, Morini S (2005) Development of adventitious shoots from in vitro grown Cydonia oblonga leaves as influenced by different cytokinins and treatment duration. Biol Plant 49(1):17–21. https://doi.org/10.1007/s10535-005-7021-8 CrossRefGoogle Scholar
  24. Dai W, Su Y, Castillo C et al (2011) Plant regeneration from in vitro leaf tissues of Viburnum dentatum L. Plant Cell Tissue Organ Cult 104:257–262. https://doi.org/10.1007/s11240-010-9829-y CrossRefGoogle Scholar
  25. De Oliveira C, Degenhardt-Goldbach J, de França Bettencourt GM et al (2017) Micropropagation of Eucalyptus grandis 3 E. urophylla AEC 224 clone. J For Res 28(1):29–39. https://doi.org/10.1007/s11676-016-0282-6 CrossRefGoogle Scholar
  26. Debnath SC (2003) Improved shoot organogenesis from hypocotyl segments of lingonberry (Vaccinium vitis-idaea L.) In Vitro Cell Dev Biol-Plant 39:490–495. https://doi.org/10.1079/IVP2003458 CrossRefGoogle Scholar
  27. Debnath SC (2009) A two-step procedure for adventitious shoot regeneration on excised leaves of lowbush blueberry. In Vitro Cell Dev Biol-Plant 45:122–128. https://doi.org/10.1007/s11627-008-9186-2 CrossRefGoogle Scholar
  28. Dhavala A, Rathore TS (2010) Micropropagation of Embelia ribes Burm f. through proliferation of adult plant axillary shoots. In Vitro Cell Dev Biol-Plant 46:180–191. https://doi.org/10.1007/s11627-010-9285-8 CrossRefGoogle Scholar
  29. Distabanjong KI, Geneve RL (1997) Multiple shoot formation from cotyledonary node segments of eastern redbud. Plant Cell Tissue Organ Cult 47:247–254CrossRefGoogle Scholar
  30. Dobrowolska I, Andrade GM, Clapham D et al (2017) Histological analysis reveals the formation of shoots rather than embryos in regenerating cultures of Eucalyptus globulus. Plant Cell Tissue Organ Cult 128:319–326. https://doi.org/10.1007/s11240-016-1111-5 CrossRefGoogle Scholar
  31. Dolendro Singh N, Sahoo L, Sarin NB et al (2003) The effect of TDZ on organogenesis and somatic embryogenesis pigeonpea (Cajanus cajan L. Millsp.) Plant Sci 164:341–347. https://doi.org/10.1016/S0168-9452(02)00418-1 CrossRefGoogle Scholar
  32. Durkovic J, Misalova A (2008) Micropropagation of temperate noble hardwoods: an overview. Funct Plant Sci Biotechnol 2:1–19Google Scholar
  33. Elhiti M, Stasolla C, Wang A (2013) Molecular regulation of plant somatic embryogenesis. In Vitro Cell Dev Biol-Plant 49:631–642. https://doi.org/10.1007/s11627-013-9547-3 CrossRefGoogle Scholar
  34. Faisal M, Ahmad N, Anis M (2005) Shoot multiplication in Rauvolfia tetraphylla L. using thidiazuron. Plant Cell Tissue Organ Cult 80:187–190. https://doi.org/10.1007/s11240-004-0567-x CrossRefGoogle Scholar
  35. Fehér A (2015) Somatic embryogenesis – stress-induced remodeling of plant cell fate. Biochim Biophys Acta-Gene Regul Mech 1849:385–402. https://doi.org/10.1016/j.bbagrm.2014.07.005 CrossRefGoogle Scholar
  36. Feyissa T, Welander M, Negash L (2005) In vitro regeneration of Hagenia abyssinica (Bruce) J.F. Gmel. (Rosaceae) from leaf explants. Plant Cell Rep 24:392–400. https://doi.org/10.1007/s00299-005-0949-5 PubMedCrossRefGoogle Scholar
  37. Fiola JA, Hassan MA, Swartz HJ et al (1990) Effect of thidiazuron, light fluence rates and kanamycin on in vitro shoot organogenesis from excised Rubus cotyledons and leaves. Plant Cell Tissue Organ Cult 20:223–228Google Scholar
  38. Gahan PB, George EF (2008) Adventitious regeneration. In: George EF, Hall MA, De Klerk GJ (eds) Plant propagation by tissue culture, 3rd edn. Springer, Dordrecht, pp 355–401Google Scholar
  39. Gaspar T, Kevers C, Bisbis B et al (2000) Loss of plant organogenic totipotency in the course of in vitro neoplastic progression. In Vitro Cell Dev-Plant 36:171–181CrossRefGoogle Scholar
  40. Geneve RL (2005) Comparative adventitious shoot induction in Kentucky coffeetree root and petiole explants treated with thidiazuron and benzylaminopurine. In Vitro Cell Dev Biol-Plant 41:489–493. https://doi.org/10.1079/IVP2005669 CrossRefGoogle Scholar
  41. Genkov T, Iordanka I (1995) Effect of cytokinin-active phenylurea derivatives on shoot multiplication perioxidase and superoxide dismutase activities of in vitro cultured carnation. Bulg J Plant Physiol 21:73–83Google Scholar
  42. Germana MA, Lambardi M (2016) In vitro embryogenesis in higher plants. Springer Science+Business Media, New YorkCrossRefGoogle Scholar
  43. Giri CC, Shyamkumar B, Anjaneyulu C (2004) Progress in tissue culture, genetic transformation and applications of biotechnology to trees: an overview. Trees 18:115–135. https://doi.org/10.1007/s00468-003-0287-6 CrossRefGoogle Scholar
  44. Graner EM, Oberschelp GPJ, Brondani GE et al (2013) TDZ pulsing evaluation on the in vitro morphogenesis of peach palm. Physiol Mol Biol Plants 19(2):283–288. https://doi.org/10.1007/s12298-012-0160-4 PubMedPubMedCentralCrossRefGoogle Scholar
  45. Gu XF, Zhang JR (2005) An efficient adventitious shoot regeneration system for Zhanhua winter jujube (Zizyphus jujuba Mill.) using leaf explants. Plant Cell Rep 23:775–779. https://doi.org/10.1007/s00299-005-0920-5 PubMedCrossRefGoogle Scholar
  46. Guo B, He W, Zhao Y et al (2017) Changes in endogenous hormones and H2O2 burst during shoot organogenesis in TDZ-treated Saussurea involucrate explants. Plant Cell Tissue Organ Cult 128:1–8. https://doi.org/10.1007/s11240-016-1069-3 CrossRefGoogle Scholar
  47. Hazarika BN (2006) Morpho-physiological disorders in in vitro culture of plants. Sci Hortic 108:105–120CrossRefGoogle Scholar
  48. Hicks G (1994) Shoot induction and organogenesis in vitro: a developmental perspective. In Vitro Cell Dev Bio-Plant 30(1):10–15CrossRefGoogle Scholar
  49. Hosseini-Nasr M, Rashid A (2003) Thidiazuron-induced high-frequency shoot regeneration from root region of Robinia pseudoacacia L. seedlings. Biol Plant 47(4):593–596CrossRefGoogle Scholar
  50. Huetteman CA, Preece JE (1993) Thidiazuron – a potent cytokinin for woody plant-tissue culture. Plant Cell Tissue Org Cult 33(2):105–119CrossRefGoogle Scholar
  51. Husain MK, Anis M, Shahzad A (2007) In vitro propagation of Indian Kino (Pterocarpus marsupium Roxb.) using thidiazuron. In Vitro Cell Dev Biol-Plant 43:59–64. https://doi.org/10.1007/s11627-006-9011-8 CrossRefGoogle Scholar
  52. Ipekci Z, Gozukirmizi N (2003) Direct somatic embryogenesis and synthetic seed production from Paulownia elongate. Plant Cell Rep 22:16–24. https://doi.org/10.1007/s00299-003-0650-5 PubMedCrossRefGoogle Scholar
  53. Ipekci Z, Gozukirmizi N (2004) Indirect somatic embryogenesis and plant regeneration from leaf and internode explants of Paulownia elongate. Plant Cell Tissue Organ Cult 79:341–345CrossRefGoogle Scholar
  54. Isah T (2015) Adjustments to in vitro culture conditions and associated anomalies in plants. Acta Biol Cracov Ser Bot 57(2):9–28. https://doi.org/10.1515/abcsb-2015-0026 Google Scholar
  55. Isah T (2016) Induction of somatic embryogenesis in woody plants. Acta Physiol Plant 38(5):1–22. https://doi.org/10.1007/s11738-016-2134-6 CrossRefGoogle Scholar
  56. Jiménez VM (2001) Regulation of in vitro somatic embryogenesis with emphasis on the role of endogenous hormones. Rev Bras Fisiol Veg 13(2):196–223CrossRefGoogle Scholar
  57. Jones MPA, Yi Z, Murch SJ et al (2007) Thidiazuron-induced regeneration of Echinacea purpurea L.: micropropagation in solid and liquid culture systems. Plant Cell Rep 26:13–19PubMedCrossRefGoogle Scholar
  58. José MCS, Cernadas MJ, Corredoira E (2014) Histology of the regeneration of Paulownia tomentosa (Paulowniaceae) by organogenesis. Rev Biol Trop 62(2):809–818CrossRefGoogle Scholar
  59. Kadota M, Niimi Y (2003) Effects of cytokinin types and their concentrations on shoot proliferation and hyperhydricity in in vitro pear cultivar shoots. Plant Cell Tissue Organ Cult 72:261–265. https://doi.org/10.1023/A:1022378511659 CrossRefGoogle Scholar
  60. Khan MI, Anis M (2012) Modulation of in vitro morphogenesis in nodal segments of Salix tetrasperma Roxb. through the use of TDZ, different media types and culture regimes. Agrofor Syst 86:95–103. https://doi.org/10.1007/s10457-012-9512-x CrossRefGoogle Scholar
  61. Kim MK, Sommer HE, Bongarten BC et al (1997a) High-frequency induction of adventitious shoots from hypocotyl segments of Liquidambar styraciflua L. by thidiazuron. Plant Cell Rep 16:536–540Google Scholar
  62. Kim M-S, Schumann CM, Klopfenstein NB (1997b) Effects of thidiazuron and benzyladenine on axillary shoot proliferation of three green ash (Fraxinus pennsylvanica Marsh.) clones. Plant Cell Tissue Organ Cult 48:45–52. https://doi.org/10.1023/A:1005856720650 CrossRefGoogle Scholar
  63. Kim K-M, Kim MY, Yun PY et al (2007) Production of multiple shoots and plant regeneration from leaf segments of fig tree (Ficus carica L.) J Plant Biol 50(4):440–446. https://doi.org/10.1007/BF03030680 CrossRefGoogle Scholar
  64. Kucharska D, Orlikowska T (2009) Enhancement of in vitro organogenetic capacity of rose by preculture of donor shoots on the medium with thidiazuron. Acta Physiol Plant 31:495–500. https://doi.org/10.1007/s11738-008-0258-z CrossRefGoogle Scholar
  65. Li Z, Traore A, Maximova S et al (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
  66. Li B-Q, Feng C-H, Hu L-Y et al (2014) Shoot regeneration and cryopreservation of shoot tips of apple (Malus) by encapsulation–dehydration. In Vitro Cell Dev Biol-Plant 50:357–368. https://doi.org/10.1007/s11627-014-9616-2 CrossRefGoogle Scholar
  67. Liu X, Pijut PM (2008) Plant regeneration from in vitro leaves of mature black cherry (Prunus serotina). Plant Cell Tissue Organ Cult 94:113–123. https://doi.org/10.1007/s11240-008-9393-x CrossRefGoogle Scholar
  68. Lo KH, Giles KL, Sawhney VK (1997) Histological changes associated with acquisition of competence for shoot regeneration in leaf discs of Saintpaulia ionantha x confuse hybrid (African violet) cultured in vitro. Plant Cell Rep 16:421–425Google Scholar
  69. Lu CY (1993) The use of thidiazuron in tissue culture. In Vitro Cell Dev Biol-Plant 29:92–96CrossRefGoogle Scholar
  70. Ma G, Lu J, Da Silva JAT et al (2011) Shoot organogenesis and somatic embryogenesis from leaf and shoot explants of Ochna integerrima (Lour). Plant Cell Tissue Organ Cult 104:157–162CrossRefGoogle Scholar
  71. Marriott P, Sarasan V (2010) Novel micropropagation and weaning methods for the integrated conservation of a critically endangered tree species, Medusagyne oppositifolia. In Vitro Cell Dev Biol-Plant 46:516–523. https://doi.org/10.1007/s11627-010-9321-8 CrossRefGoogle Scholar
  72. Mehta UJ, Sahasrabudhe N, Hazra S (2005) Thidiazuron-induced morphogenesis in tamarind seedlings. In Vitro Cell Dev Biol-Plant 41:240–243. https://doi.org/10.1079/IVP2004611 CrossRefGoogle Scholar
  73. Meng L, Zhang S, Lemaux P (2005) Developing a molecular understanding of in vitro and in planta shoot organogenes. In: Trigiano RN, Gray DJ (eds) Plant development and biotechnology. CRC Press, Boca Raton, pp 39–54Google Scholar
  74. Mithila J, Hall JC, Victor JMR, Saxena PK (2003) Thidiazuron induces shoot organogenesis at low concentrations and somatic embryogenesis at high concentrations on leaf and petiole explants of African violet (Saintpaulia ionantha Wendl.) Plant Cell Rep 21(5):408–414PubMedCrossRefGoogle Scholar
  75. Mok DWS, Turner JE, Mujer CV (1987) Biological and biochemical effects of cytokinin-active phenylurea derivatives in tissue culture systems. HortSci 22(6):1194–1197Google Scholar
  76. Moyo M, Aremu AO, Van Staden J (2015) Insights into the multifaceted application of microscopic techniques in plant tissue culture systems. Planta 242:773–790. https://doi.org/10.1007/s00425-015-2359-4 PubMedCrossRefGoogle Scholar
  77. Mulwa RM, Bhalla PL (2006) In vitro plant regeneration from immature cotyledon explants of macadamia (Macadamia tetraphylla L. Johnson). Plant Cell Rep 25:1281–1286. https://doi.org/10.1007/s00299-006-0182-x PubMedCrossRefGoogle Scholar
  78. Murch SJ, Saxena PK (2001) Molecular fate of thidiazuron and its effects on auxin transport in hypocotyls tissues of Pelargonium xhortorum Bailey. Plant Growth Regul 35(3):269–275CrossRefGoogle Scholar
  79. Murch SJ, KrishnaRaj S, Saxena PK (1997) Thidiazuron-induced morphogenesis of regal geraniums (Pelargonium domesticum): a potential stress response. Physiol Plant 101:183–191CrossRefGoogle Scholar
  80. Murthy BNS, Murch SJ, Saxena PK (1998) Thidiazuron: a potent regulator of in vitro plant morphogenesis. In Vitro Cell Dev Biol-Plant 34(4):267–275. https://doi.org/10.1007/BF02822732 CrossRefGoogle Scholar
  81. Noël N, Leplé J-C, Pilate G (2002) Optimization of in vitro micropropagation and regeneration for Populus × interamericana and Populus × euramericana hybrids (P. deltoides, P. trichocarpa, and P. nigra). Plant Cell Rep 20:1150–1155. https://doi.org/10.1007/s00299-002-0465-9 CrossRefGoogle Scholar
  82. Novikova TI, Poluboyarova TV (2013) Thidiazuron-induced shoot organogenesis of Disanthus cercidiofolius maxim. (Hamamelidaceae). In: Abstracts of the X international conference on plant cell biology in vitro and biotechnology, Kazan Institute of Biochemistry and Biophysics, Kazan, 14–18 October 2013Google Scholar
  83. Pal A, Negi VS, Borthakur D (2012) Efficient in vitro regeneration of Leucaena leucocephala using immature zygotic embryos as explants. Agrofor Syst 84:131–140. https://doi.org/10.1007/s10457-011-9438-8
  84. Panda BM, Hazra S (2012) In vitro morphogenic response in cotyledon explants of Semecarpus anacardium L. Plant Biotechnol Rep 6:141–148. https://doi.org/10.1007/s11816-011-0207-y CrossRefGoogle Scholar
  85. Parveen S, Shahzad A (2010) TDZ–induced high frequency shoot regeneration in Cassia sophera Linn. via cotyledonary node explants. Physiol Mol Biol Plants 16(2):201–205. https://doi.org/10.1007/s12298-010-0022-x PubMedPubMedCentralCrossRefGoogle Scholar
  86. Paul S, Dam A, Bhattacharyya A et al (2011) An efficient regeneration system via direct and indirect somatic embryogenesis for the medicinal tree Murraya koenigii. Plant Cell Tissue Organ Cult 105:271–283. https://doi.org/10.1007/s11240-010-9864-8 CrossRefGoogle Scholar
  87. Pavingerova D (2009) The influence of thidiazuron on shoot regeneration from leaf explants of fifteen cultivars of Rhododendron. Biol Plant 54:797–799CrossRefGoogle Scholar
  88. Phillips GC (2004) In vitro morphogenesis in plants – recent advances. In Vitro Cell Dev Biol-Plant 40(4):342–345. https://doi.org/10.1079/IVP2004555 CrossRefGoogle Scholar
  89. Pinto G, Santos C, Neves L, Araújo C (2002) Somatic embryogenesis and plant regeneration in Eucalyptus globulus Labill. Plant Cell Rep 21:208–213CrossRefGoogle Scholar
  90. Raghu AV, Geetha SP, Gerald M et al (2006) Ravindran PN direct shoot organogenesis from leaf explants of Embelia ribes Burm. f.: a vulnerable medicinal plant. J For Res 11:57–60. https://doi.org/10.1007/s10310-005-0188-1 CrossRefGoogle Scholar
  91. Rai VR (2002) Rapid clonal propagation of Nothapodytes foetida (Wight) sleumer – a threatened medicinal tree. In Vitro Cell Dev Biol-Plant 38:347–351. https://doi.org/10.1079/IVP2002300 CrossRefGoogle Scholar
  92. Rani DN, Nair GM (2006) Effects of plant growth regulators on high frequency shoot multiplication and callus regeneration of an important Indian medicinal plant, nirgundi (Vitex negundo L.) In Vitro Cell Dev Biol-Plant 42:69–73. https://doi.org/10.1079/IVP2005727 CrossRefGoogle Scholar
  93. Ranyaphiaa RA, Maoaa AA, Borthakurb SK (2011) Direct organogenesis from leaf and internode explants of in vitro raised wintergreen plant (Gaultheria fragrantissima). ScienceAsia 37:186–194. https://doi.org/10.2306/scienceasia1513-1874.2011.37.186
  94. Rastogi S, Rizvi SMH, Singh RP et al (2008) In vitro regeneration of Leucaena leucocephala by organogenesis and somatic embryogenesis. Biol Plant 52:743–748. https://doi.org/10.1007/s10535-008-0144-y CrossRefGoogle Scholar
  95. Ravikumar G (2001) Forest biotechnology: development and prospects. Plant Cell Biotech Mol Biol 1:13–28Google Scholar
  96. Ravishankar Rai V, McComb J (2002) Direct somatic embryogenesis from mature embryos of sandalwood. Plant Cell Tissue Organ Cult 69:65–70. https://doi.org/10.1023/A:1015037920529 CrossRefGoogle Scholar
  97. Ružić DV, Vujović TI (2008) The effects of cytokinin types and their concentration on in vitro multiplication of sweet cherry cv. Lapins (Prunus avium L.) Hortic Sci 3:12–21Google Scholar
  98. Salaj J, Petrovská B, Obert B et al (2005) Histological study of embryo-like structures initiated from hypocotyl segments of flax (Linum usitatissimum L.) Plant Cell Rep 24(10):590–595PubMedCrossRefGoogle Scholar
  99. Sandal I, Bhattacharya A, Ahuja PS (2001) An efficient liquid culture system for tea shoot proliferation. Plant Cell Tissue Organ Cult 65:75–80. https://doi.org/10.1023/A:1010662306067 CrossRefGoogle Scholar
  100. Shaik NM, Arha M, Nookaraju A et al (2009) Improved method of in vitro regeneration in Leucaena leucocephala – a leguminous pulpwood tree species. Physiol Mol Biol Plants 15(4):311–318. https://doi.org/10.1007/s12298-009-0035-5 PubMedPubMedCentralCrossRefGoogle Scholar
  101. Sivanesan I, Song JY, Hwang SJ et al (2011) Micropropagation of Cotoneaster wilsonii Nakai—a rare endemic ornamental plant. Plant Cell Tissue Organ Cult 105:55–63. https://doi.org/10.1007/s11240-010-9841-2 CrossRefGoogle Scholar
  102. Siwach P, Gill AR (2011) Enhanced shoot multiplication in Ficus religiosa L. in the presence of adenine sulphate, glutamine and phloroglucinol. Physiol Mol Biol Plants 17(3):271–280. https://doi.org/10.1007/s12298-011-0074-6 PubMedPubMedCentralCrossRefGoogle Scholar
  103. Skoog F, Miller CO (1957) Chemical regulation of growth and organ formation in plant tissue cultured in vitro. Symp Soc Exp Biol 11:118–131PubMedGoogle Scholar
  104. Sriskandarajah S, Lundquist P (2009) High frequency shoot organogenesis and somatic embryogenesis in juvenile and adult tissues of seabuckthorn (Hippophae rhamnoides L.) Plant Cell Tissue Organ Cult 99:259–268. https://doi.org/10.1007/s11240-009-9597-8 CrossRefGoogle Scholar
  105. Stevens ME, Pijut PM (2012) Hypocotyl derived in vitro regeneration of pumpkin ash (Fraxinus profunda). Plant Cell Tissue Organ Cult 108:129–135. https://doi.org/10.1007/s11240-011-0021-9 CrossRefGoogle Scholar
  106. Sugiyama M (1999) Organogenesis in vitro. Curr Opin Plant Biol 2:61–64. https://doi.org/10.1016/S1369-5266(99)80012-0 PubMedCrossRefGoogle Scholar
  107. Sujatha PK, Hazra S (2007) Micropropagation of mature Pongamia pinnata. In Vitro Cell Dev Biol-Plant 43:608–613. https://doi.org/10.1007/s11627-007-9049-2 CrossRefGoogle Scholar
  108. Sujatha K, Panda BM, Hazra S (2008) De novo organogenesis and plant regeneration in Pongamia pinnata, oil producing tree legume. Trees 22:711–716. https://doi.org/10.1007/s00468-008-0230-y CrossRefGoogle Scholar
  109. Thomas JC, Katterman FR (1986) Cytokinin activity induced by thidiazuron. Plant Physiol 81:681–683PubMedPubMedCentralCrossRefGoogle Scholar
  110. Traore A, Maximova SN, Guiltinan MJ (2003) Micropropagation of Theobroma cacao L. using somatic embryo-derived plants. In Vitro Cell Dev Biol-Plant 39:332–337CrossRefGoogle Scholar
  111. Tzfira T, Zuker A, Altman A (1998) Forest tree biotechnology, genetic transformation and its application to future forests. Trends Biotechnol 16:439–446CrossRefGoogle Scholar
  112. Varshney A, Anis M (2014) Trees: propagation and conservation: biotechnological approaches for propagation of a multipurpose tree, Balanites aegyptiaca. Springer, New DelhiGoogle Scholar
  113. Vasil IK (2008) A history of plant biotechnology: from the cell theory of Schleiden and Schwann to biotech crops. Plant Cell Rep 27:1423–1440. https://doi.org/10.1007/s00299-008-0571-4 PubMedCrossRefGoogle Scholar
  114. Vengadesan G, Pijut PM (2009) In vitro propagation of northern red oak (Quercus rubra L.) In Vitro Cell Dev Biol-Plant 45:474–482. https://doi.org/10.1007/s11627-008-9182-6 CrossRefGoogle Scholar
  115. Vengadesan G, Ganapathi A, Anand RP et al (2003) In vitro propagation of Acacia sinuata (Lour.) Merr. from nodal segments of a 10-year-old tree. In Vitro Cell Dev Biol-Plant 39:409–414. https://doi.org/10.1079/IVP2003421 CrossRefGoogle Scholar
  116. Verdeil JL, Alemanno L, Niemenak N et al (2007) Pluripotent versus totipotent plant stem cells: dependence versus autonomy? Trends Plant Sci 12(6):245–252. https://doi.org/10.1016/j.tplants.2007.04.002 PubMedCrossRefGoogle Scholar
  117. Vieitez AM, San José MC (1996) Adventitious shoot regeneration from Fagus sylvatica leaf explants in vitro. In Vitro Cell Dev Biol-Plant 32(3):140–147. https://doi.org/10.1007/BF02822757
  118. Vila S, Gonzalez A, Rey H et al (2003) Somatic embryogenesis and plant regeneration from immature zygotic embryos of Melia azedarach (Meliaceae). In Vitro Cell Dev Biol-Plant 39:283–287. https://doi.org/10.1079/IVP2002377 CrossRefGoogle Scholar
  119. Vila SK, Rey HY, Mroginski LA (2007) Factors affecting somatic embryogenesis induction and conversion in “Paradise Tree” (Melia azedarach L.) J Plant Growth Regul 26:268–277. https://doi.org/10.1007/s00344-007-9007-6 CrossRefGoogle Scholar
  120. Vinocur B, Carmi T, Altman A et al (2000) Enhanced bud regeneration in aspen (Populus tremula L.) roots cultured in liquid media. Plant Cell Rep 19:1146–1154CrossRefGoogle Scholar
  121. Visser C, Qureshi JA, Gill R et al (1992) Morpho-regulatory role of thidiazuron: substitution of auxin and cytokinin requirement for the induction of somatic embryogenesis in geranium hypocotyls culture. Plant Physiol 99:1704–1707PubMedPubMedCentralCrossRefGoogle Scholar
  122. von Arnold S, Sabala I, Bozhkov P et al (2002) Developmental pathways of somatic embryogenesis. Plant Cell Tissue Organ Cult 69:233–249CrossRefGoogle Scholar
  123. Wang SY, Steffens GL, Faust M (1986) Breaking bud dormancy in apple with a plant bioregulator, thidiazuron. Phytochemistry 25:311–317CrossRefGoogle Scholar
  124. Wang H, Liu H, Wang W et al (2008) Effects of thidiazuron, basal medium and light quality on adventitious shoot regeneration from in vitro cultured stem of Populus alba×P. berolinensis. J For Res 19(3):257–259. https://doi.org/10.1007/s11676-008-0042-3 CrossRefGoogle Scholar
  125. Wei F, Zhao F, Tian B (2017) In vitro regeneration of Populus tomentosa from petioles. J For Res 28:465–471. https://doi.org/10.1007/s11676-016-0319-x
  126. Wilhelm E (1999) Micropropagation of juvenile sycamore maple via adventitious shoot formation by use of thidiazuron. Plant Cell Tissue Organ Cult 57:57–60CrossRefGoogle Scholar
  127. Willemsen V, Scheres B (2004) Mechanisms of pattern formation in plant embryogenesis. Annu Rev Genet 38:587–614PubMedCrossRefGoogle Scholar
  128. Woo SM, Wetzstein HY (2008) Morphological and histological evaluations of in vitro regeneration in Elliottia racemosa leaf explants induced on media with thidiazuron. J Am Soc Hortic 133(2):167–172Google Scholar
  129. Xie D, Hong Y (2001) In vitro regeneration of Acacia mangium via organogenesis. Plant Cell Tissue Organ Cult 66:167–173CrossRefGoogle Scholar
  130. Xu L, Liu GF, Bao MZ (2007) Adventitious shoot regeneration from in vitro leaves of formosan sweetgum (Liquidambar formosana L.) HortSci 42(3):721–723Google Scholar
  131. Yancheva SD, Golubowicz S, Fisher E et al (2003) Auxin type and timing of application determine the activation of the developmental program during in vitro organogenesis in apple. Plant Sci 165:299–309CrossRefGoogle Scholar
  132. Zaytseva YG, Novikova TI (2015) Conservation and propagation of Rhododendron schlippenbachii using biotechnological methods. Rastitel’nyj Mir Aziatskoj Rossii (Plant Life of Asian Russia) 4:79–85Google Scholar
  133. Zaytseva YG, Poluboyarova TV, Novikova TI (2016) Effects of thidiazuron on in vitro morphogenic response of Rhododendron sichotense Pojark. and Rhododendron catawbiense cv. Grandiflorum leaf explants. In Vitro Cell Dev Biol-Plant 52:56–63. https://doi.org/10.1007/s11627-015-9737-2 CrossRefGoogle Scholar
  134. Zhang C, Fu S, Tang G et al (2013) Factors influencing direct shoot regeneration from mature leaves of Jatropha curcas, an important biofuel plant. In Vitro Cell Dev Biol-Plant 49:529–540. https://doi.org/10.1007/s11627-013-9530-z CrossRefGoogle Scholar
  135. Zhou H, Li M, Zhao X et al (2010) Plant regeneration from in vitro leaves of the peach rootstock ‘Nemaguard’ (Prunus persica 3 P. davidiana). Plant Cell Tissue Organ Cult 101:79–87. https://doi.org/10.1007/s11240-010-9666-z CrossRefGoogle Scholar
  136. Zhuravlev YN, Omelko AM (2008) Plant morphogenesis in vitro. Russ J Plant Physiol 55(5):579–596. https://doi.org/10.1134/S1021443708050014

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.Biotechnology Laboratory, Central Siberian Botanical GardenSiberian Branch of the Russian Academy of SciencesNovosibirskRussian Federation

Personalised recommendations