Genetic transformation of Eucalyptus-challenges and future prospects

Tree Biotechnology

Volumn , Issue , 2014, Pages 392-445

  Chauhan, Raj Deepika ^a   Veale, Adri ^b   Cathleen, Ma ^c   Strauss, Steven H ^c   Myburg, Alexander A ^b  

^a DONALD DANFORTH PLANT SCIENCE CENTER   (United States)

^b UNIVERSITY OF PRETORIA   (South Africa)

^c OREGON STATE UNIVERSITY   (United States)

Author keywords

Agrobacterium tumefaciens; Eucalypts; Genetic transformation; In vitro regeneration; Somatic embryogenesis; Transformation rate

Indexed keywords

BACTERIA; GENE TRANSFER; GENES; NUCLEIC ACIDS; PLANTS (BOTANY);

AGROBACTERIUM TUMEFACIENS; EUCALYPTS; GENETIC TRANSFORMATION; IN-VITRO; SOMATIC EMBRYOGENESIS; TRANSFORMATION RATES;

REFORESTATION;

EID: 84942353543     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1201/b16714     Document Type: Chapter

References (171)

1. Aharoni, A., S. Dixit, R. Jetter, E. Thoenes, G. van Arkel and A. Pereira. 2004. The SHINE clade of AP2 domain transcription factors activates wax biosynthesis, alters cuticle properties, and confers drought tolerance when overexpressed in Arabidopsis. Plant Cell 16: 2463-2480.
2. Adam, S. 1987. Obtention de raciness transforméez chez Eucalyptus gunnii H. par Agrobacterium rhizogenes. pp. 7-21. In: Annales de Recherches Sylvicoles, Association Forest-Cellulose.
3. Adam, S. 1989. Ph.D. Etude de la sensibilité d’Eucalyptus gunnii à Agrobacterium rhizogeneset A. tumefaciens; facteurs impliqués dans l’obtention de réponses de transformations et problèmes liés à la régénération de plantes entières transformées. Dissertation, Universite Pierre et Marie Curie, Paris, France. 154 pp.
4. Aggarwal, D., A. Kumar and M.S. Reddy. 2010. Shoot organogenesis in elite clones of Eucalyptus tereticornis. Plant Cell Tiss. Org. Cult. 102: 45-52.
5. Aggarwal, D., A. Kumar and M.S. Reddy. 2011. Agrobacterium tumefaciens mediated genetic transformation of selected elite clone(s) of Eucalyptus tereticornis. Acta Physiol. Plant. 33: 1603-1611.
6. Ainsley, P.J., G.G. Collins and M. Sedgley. 2001. Factors affecting Agrobacterium-mediated gene transfer and the selection of transgenic calli in paper shell almond (Prunus dulcis Mill). J. Hort. Sci. Biotechnol. 7(5): 522-528.
7. Alt-Morbe, J., H. Kithmann and J. Schroder. 1989. Differences in induction of Ti-plasmid virulence genes virG and virD and continued control of virD expression by four external factors. Mol. Plant-Microbe Interact. 2: 301-308.
8. Andrade, G.M. and A.C.M. Brasileiro. 1997. Gene transfer to Eucalypt (Eucalyptus grandis x E. urophylla) through the co-inoculation approach. In: Proceedings of IUFRO Conference on Silviculture and Improvement of Eucalypts, Salvador, Brazil, 24-29 Aug. 1997.
9. Aneja, S. and C. Atal. 1969. Plantlet formation in tissue cultures from lignotubers of Eucalyptus citriodora Hook. Curr. Sci. 38: 69-70.
10. Asbel, L.E. and M.E. Levison. 2000. Cephalosporins, carbapenems and monobactams. Infect. Dis. Clin. North America 14: 435-447.
11. Azmi, A., W. Dewitte, C. Drevet, H. van Onckelen, P. Landre, A.M. Boudet, L. Jouanin and D. Chriqui. 1997. Bud regeneration from Eucalyptus globulus clones and seedlings through hormonal imbalances induced by Agrobacterium tumefaciens strain 82.139. Plant Sci. 127: 81-90.
12. Balestrazzi, A., D. Carbonera and M. Confalonieri. 2000. Agrobacterium tumefaciens-mediated transformation of white poplar (Populus alba L.) and regeneration of transgenic plants. J. Genet. Breed. 54: 263-270.
13. Bandyopadhyay, S., K. Cane, G. Rasmussen and J.D. Hamill. 1999. Efficient plant regeneration from seedling explants of two commercially important temperate eucalypt species-Eucalyptus nitens and E. globulus. Plant Sci. 140: 189-198.
14. Barrueto-Cid, L.P., R.D. Illg and A.E. Piedrabuena. 1994. Regeneration of garlic plants (Allium sativum L., cv. ‘chonan’) via cell culture in liquid medium. In vitro Cell Dev. Biol. 30P: 150-155.
15. Barrueto-Cid, L.P., A.C.M. Machado, S.R.C. Carvalheira and A.C.M. Brasileiro. 1999. Plant regeneration from seedling explants of Eucalyptus grandis × E. urophylla. Plant Cell Tiss. Org. Cult. 56: 17-23.
16. Bennett, I.J. and J.A. McComb. 1982. Propagation of Jarrah (Eucalyptus marginata) by organ and tissue culture. Aust. For. Res. 12: 121-127.
17. Bhaskar, P.B., M. Venkateshwaran, L. Wu, J.M. Ané and J. Jiang. 2009. Agrobacterium-mediated transient gene expression and silencing: A rapid tool for functional gene assay in potato. PLoS ONE 4(6): e5812.
18. Bhatnagar, S. and P. Khurana. 2003. Agrobacterium tumefaciens-mediated transformation of Indian mulberry, Morus indica cv. K2: A time-phased screening strategy. Plant Cell Rep. 21(7): 669-675.
19. Blakely, W.F. 1955. A Key to the Eucalypts. 2nd ed. Forest and Timber Bureau, Canberra, Australia. 359 pp.
20. Boudet, A.M. 2000. Lignins and lignification: Selected issues. Plant Physiol. Biochem. 38(1): 1-16.
21. Boulay, M. 1983. Micropropagation of forest resistant Eucalyptus. pp. 102-107. In: Proceedings from Workshop of Eucalyptus. USDA For. Serv. Gen. Tech. Rep. PSW 69. Sacramento, California, USA.
22. Boulay, M. 1987. Recherches preliminaires sur l’embryogenise somatique d’Eucalyptusgunnii. pp. 23-27. In: Annales de Recherches Silvicoles, Association Forest-Cellulose.
23. Brackpool, A.L. and M.R. Ward. 1990. Optimization of adventitious shoot formation for transformation in Eucalyptus. Abstract A1-23, 7th International Congress on Plant Tissue and Cell Culture, Amsterdam, The Netherlands, 24-29 June 1990.
24. Brooker, I. and D. Kleinig. 1996. Eucalyptus, An Illustrated Guide to Identification. Reed Books, Port Melbourne, Australia. 230 pp.
25. Bunn, E., T. Senaratna, K. Sivasithamparam and K.W. Dixon. 2005. In vitro propagation of Eucalyptus phylacis L. Johnson and K. Hill., a critically endangered relict from Western Australia. In vitro Cell. Dev. Biol. Plant 41: 812-815.
26. Chang, S., R.D. Thomas, L.W. Handley, M.B. Connett and R.L. Hamilton. 2006. Eucalyptus urophylla transformation and selection. U.S. Patent # WO 2006/052554 A2.
27. Chauhan, R.D. and A.A. Myburg. 2011. Unpublished raw data.
28. Chen, J., Y.L. Hu, C.F. Zhou, T. Ni and Z.P. Lin. 2007a. Studies of transformation of GO into Eucalyptus. Linye Shiyong Jishu (Pract. For. Technol.) 6: 3-4.
29. Chen, Z.Z., J.Y. Tsay and J.D. Chung. 1996. Callus culture of Eucalyptus grandis x urophylla and preliminary studies on organogenesis and Agrobacterium -mediated transformation. Taiwan J. For. Sci. 11: 43-52.
30. Chen, Z.Z., S.H. Chang, C.K. Ho, Y.C. Chen, J.B. Tsai and V.L. Chiang. 2001. Plant production of transgenic Eucalyptus camaldulensis carrying the Populus tremuloides cinnamate 4-hydroxylase gene. Taiwan J. For. Sci. 16: 249-258.
31. Chen, Z.Z., C.K. Ho, I.S. Ahn and V.L. Chiang. 2007b. Eucalyptus. pp. 125-134. In: K. Wang (ed.). Methods in Molecular Biology, Vol. 344: Agrobacterium Protocols, Vol. II. Humana Press, Inc., Totowa, New Jersey, USA.
32. Curtis, I.S., J.B. Power and M.R. Davey. 1995. NPT II assays for measuring gene expression and enzyme activity in transgenic plants. pp. 149-159. In: H. Jones (ed.). Methods in Molecular Biology: Plant Gene Transfer and Expression Protocol, Vol. 49. Humana Press, Inc., Totowa, New Jersey, USA.
33. Dan, Y. 2008. Biological functions of antioxidants in plant transformation. In vitro Cell. Dev. Biol. Plant 44: 149-161.
34. deBondt, A., K. Eggeemant, P.V.M. Druast, I. Goderis, J. Vanderteyden and W.F. Brockaert. 1994. Agrobacterium mediated transformation of apple (Malus domestica Bork.) and assessment of factors affecting gene transfer efficiency during early transformation steps. Plant Cell Rep. 13(10): 587-593.
35. de Fossard, R.A. 1974. Tissue culture of Eucalyptus. Aust. For. 37: 43-54.
36. de Fossard, R.A., C. Nitsch, R.J. Cresswell and E.C.M. Lee. 1974. Tissue and organ culture of Eucalyptus. NZJ. For. Sci. 4: 267-278.
37. Dibax, R., C. De L. Eisfeld, L. Cuquel, H. Koehler and M. Quoirin. 2005. Plant regeneration from cotyledonary explants of Eucalyptus camaldulensis. Sci. Agric. 62(4): 406-412.
38. Dibax, R., C. Deschamps, J.C. Bespalhok Filho, L.G.E. Vieire, H.B.C. Molinari, M.K.F. de Campos and M. Quoirin. 2010. Organogenesis and Agrobacterium tumefaciens-mediated transformation of Eucalyptus saligna with P5CS gene. Biol. Plant. 54(1): 6-12.
39. Dillen, W., J. de Clereq, J. Kapila, M. Zambre, M. van Montagu and G. Angenon. 1997. Effect of temperatures on Agrobacterium tumefaciens mediated gene transfer to plants. Plant J. 12: 1459-1463.
40. Durand-Cresswell, R.J., M. Boulay and A. Franclet. 1982. Vegetative propagation of Eucalyptus. pp. 150-181. In: J.M. Bonga and D.J. Durzan (eds.). Tissue Culture in Forestry. Nijhoff, The Hague, The Netherlands.
41. Edwards, G.A., K.J. Fuell, E.M. Laine and I.S. Mussio. 1996. Genetic modification of plants. U.S. Patent # WO/1996/025504.
42. Esmeraldo, M.V., S.B.R.C. Carvalheira, A.A. Brasil, S.A. Figueiredo, L.P. Barrueto-Cid and A.C.M. Brasileiro. 1997. Analysis of different parameters affecting Agrobacterium-mediated transformation of Eucalyptus grandis x Eucalyptus urophylla. In: Proceedings from IUFRO Conference on Silviculture and Improvement of Eucalypts, Salvador, Brazil, 24-29 Aug. 1997.
43. Franclet, A. and M. Boulay. 1989. Rejuvenation and clonal silviculture for Eucalyptus and forest species harvested through short rotation. pp. 267-274. In: J.S. Pereira and J.J. Landsberg (eds.). Biomass Production by Fast Growing Trees. Kluwer Academic Publishers, Amsterdam, The Netherlands.
44. Fullner, K.J. and E.W. Nester. 1996. Temperature affects the T-DNA machinery of Agrobacterium tumefaciens. J. Bacteriol. 178: 1498-1504.
45. Gamborg, O.L., R.A. Miller and K. Ojima. 1968. Nutrient requirements of suspension cultures of Soybean root cells. Exp. Cell. Res. 50: 151-158.
46. George, E.F. and P.D. Sherrington. 1984. Plant Propagation by Tissue Culture: Handbook and Directory of Commercial Laboratories. Exegetics, Basingstoke, UK, 709 p.
47. Gerwal, S., A. Ahuja and C.K. Atal. 1980. In vitro proliferation of shoot apices of Eucalyptus citriodora Hook. Indian J. Exp. Biol. 18: 775-777.
48. Giamakis, A., O. Kretsi, I. Chinou and C.G. Spyropoulos. 2001. Eucalyptus camaldulensis: Volatiles from immature flowers and high production of 1,8-cineole and β-pinene by in vitro cultures. Phytochemistry 58: 351-355.
49. GIT Forestry. 2009. Global Eucalyptus Map, 2009. (Available online: http://git-forestry.com/ download_git_eucalyptus_map.htm).
50. Glocke, P., K. Delaporte, G. Collins and M. Sedgley. 2006. Micropropagation of juvenile tissue of E. erythronema x E. Stricklandii cv. ‘Urbrae Gem’. In vitro Cell. Dev. Biol. Plant 42(2): 139-143.
51. Goncalves, A.N. 1975. The growth and developmental physiology of Eucalyptus in cell and tissue culture systems. M.Sc. Thesis, The Ohio State University, Columbus, Ohio, USA.
52. Gonzalez, E.R., A. de Andrade, A.L. Bertolo, G.C. Lacerda, R.T. Carneiro, V.A.P. Defavari, M.T.V. Labate and C.A. Labate. 2002. Production of transgenic Eucalyptus grandis x Eucalyptus urophylla using the sonication-assisted Agrobacterium transformation (SAAT) system. Funct. Plant Biol. 29: 97-102.
53. González, E., C. Gugliermoni, M. Galvão, M. Fagundes, M. Ferreira, G. Almeida, H. AlvesJose Gonsalves, F. Silva, S. Bentivenha, S. Oda and E. Mello. 2011. Characterization of herbicideresistant Eucalyptus plants expressing phosphinothricin acetyltransferase gene. BMC Proc. 5: P135.
54. Grattapaglia, D. and M. Kirst. 2008. Eucalyptus applied genomics: from gene sequences to breeding tools. New Phytologist. 179: 911-929.
55. Hajari, E., M.P. Watt, D.J. Mycock and B. McAlister. 2006. Plant regeneration from induced callus of improved Eucalyptus clones. S. Afr. J. Bot. 72: 195-201.
56. Hall, N., R.D. Johnston and R. Marryatt. 1963. The Natural Occurrence of the Eucalypts. Leaflet 65, 2nd ed. Forestry and Timber Bureau, Canberra, Australia. 122 pp.
57. Harcourt, R.L., J. Kyozuka, R.B. Floyd, K.S. Bateman, H. Tanaka, V. Decroocq, D.J. Llewellyn, X. Zhu, W.J. Peacock and E.S. Dennis. 2000. Insect and herbicide resistant transgenic eucalypts. Mol. Breed. 6: 307-315.
58. Herve, P., A. Jauneau, M. Paques, J.N. Marien, A.M. Boudet and C.A. Teulières. 2001. Procedure for shoot organogenesis in vitro from leaves and nodes of an elite Eucalyptus gunnii clone: Comparative histology. Plant Sci. 161: 645-653.
59. Hinchee, M., C. Zhang, S. Chang, M. Cunningham, W. Hammond and N. Nehra. 2011. Biotech Eucalyptus can sustainably address society’s need for wood: the example of freeze tolerant Eucalyptus in the southeastern U.S. BMC Proc. 5: I24.
60. Ho, C.K., S.H. Chang, J.Y. Tsay, C.J. Tsai, V.L. Chiang and Z.Z. Chen. 1998. Agrobacterium tumefaciens-mediated transformation of Eucalyptus camaldulensis and production of transgenic plants. Plant Cell Rep. 17: 675-680.
61. Huang, Z.C., F.H. Zeng and X.Y. Lu. 2010. Efficient regeneration of Eucalyptus urophylla from seedling-derived hypocotyls. Biol. Plant. 54(1): 131-134.
62. Hull, R., S.N. Covey and P. Dale. 2000. Genetically modified plants and the 35S promoter: assessing the risks and enhancing the debate. Microbial Ecology in Health and Disease 12: 1-5.
63. Jacquiot, C. 1964a. Applicationde la technique de culture des tissues vegetaux a l’etude de quelques problems de la physiologie de l’abre. Ann. Sci. For. 21: 310-473.
64. Jacquiot, C. 1964b. Structure of excised roots or of organ formed de novo from cambial tissue of trees grown in culture. Rev. Cytol. Biol. Veg 27: 319-322.
65. Jin, S., T. Komari, M.P. Gordon and E.W. Nester. 1987. Genes responsible for the supervirulence phenotype of Agrobacterium tumefaciens A281. J. Bacteriol. 169: 4417-4425.
66. Jin, S., Y.N. Song, W.Y. Deng, M.P. Gordon and E.W. Nester. 1993. The regulatory virA protein of Agrobacterium tumefaciens does not function at elevated temperatures. J. Bacteriol. 175: 6830-6835.
67. Johnston, R.D. and R. Marryatt. 1965. Taxonomy and Nomenclature of Eucalypts. Leaflet 92. Forestry and Timber Bureau, Canberra, Australia. 24 pp.
68. Jones, N.B. and J. van Staden. 1997. Micropropagation of Eucalyptus. pp. 286-329. In: Y.P.S. Bajaj (ed.). Biotechnology in Agriculture and Forestry: High-Tech and Micropropagation V., Vol. 39. Springer-Verlag, Heidelberg, Germany.
69. Kannangara, R., C. Branigan, Y. Liu, T. Penfield, V. Rao, G. Mouille, H. Höfte, M. Pauly, J.L. Riechmann and P. Broun. 2007. The transcription factor WIN1/SHN1 regulates cutin biosynthesis in Arabidopsis thaliana. Plant Cell 19: 1278-1294.
70. Kawaoka, A., K. Nanto, K. Ishii and H. Ebinuma. 2006. Reduction of lignin content by suppression of expression of the LIM domain transcription factor in Eucalyptus camaldulensis. Silv. Genet. 55: 269-277.
71. Kawaoka, A., K. Nanto, K. Sugita, S. Endo, K. Yamada-Watanabe, E. Matsunaga and H. Ebinuma. 2003. Production and analysis of lignin-modifies transgenic Eucalyptus. pp. S10-S16. In: B. Sundberg (ed.). Proceedings of IUFRO Conference on Tree Biotechnology, Umea Plant Science Centre, Umea, Sweden.
72. Kawazu, T., K. Doi and K. Kondo. 2000a. Process for transformation of mature trees of eucalyptus plants. European Patent # 1 050 209 A2.
73. Kawazu, T., K. Doi and K. Kondo. 2000b. Process for transformation of mature trees of Eucalyptus plants. U.S. Patent # 6,563,024 B1.
74. Kawazu, T., K. Doi, T. Ohta, Y. Shinohara, K. Ito and M. Shibata. 1990. Transformation of Eucalyptus (Eucalyptus saligna) using electroporation.Abstract 64, 7th International Congress on Plant Tissue and Cell Culture. Amsterdam, The Netherlands, 24-29 June 1990.
75. Kawazu, T., K. Dol, Y. Tatemichi, K. Ito and M. Shibata. 1996. Regeneration of transgenic plants by nodule culture system in Eucalyptus camaldulensis, tree improvement for sustainable tropical forestry. QFRI-IUFRO Conf., Caloundra, Queensland, Australia 27: 492-497.
76. Kithahara, E.M. and L.S. Caldas. 1975. Shoot and root formation in hypocotyls callus cultures of Eucalyptus. For. Sci. 21: 242-243.
77. Kooter, J.M., M.A. Matzke and P. Meyer. 1999. Listening to the silent genes: transgene silencing, gene regulation and pathogen control. Trends in Plant Sciences 4: 340-347.
78. Kudirka, D.T., S.M. Colburn, M.A. Hinchee and M.S. Wright. 1986. Interactions of Agrobacterium tumefaciens with soybean leaf explants in tissue culture. Can. J. Genet. Cytol. 28: 808-817.
79. Kutty, P.C., G.K.A. Parveez and F. Huyop. 2010. An easy method for Agrobacterium tumefaciensmediated gene transfer to Nicotiana tabacum cv. TAPM26. J. Biol. Sci. 10: 480-489.
80. Laine, E. and A. David. 1994. Regeneration of plant from leaf explants of micropropagated clonal Eucalyptus grandis. Plant Cell Rep. 13: 473-476.
81. Lakshmi Sita, G. and B.S. Rani. 1985. In vitro propagation of Eucalyptus grandis L. by tissue culture. Plant Cell Rep. 4: 63-65.
82. Lakshmi Sita, G. and C.S. Vaidyanathan. 1979. Rapid multiplication of Eucalyptus by multiple shoot production. Curr. Sci. 48: 350-352.
83. Lakshmi Sita, G., S. Rani and K.S. Rao. 1986. Propagation of Eucalyptus grandis by tissue culture. pp. 318-321. In: J.K. Sharma, C.T.S. Nair, S. Kedhamath and S. Kondas (eds.). Eucalyptus in India. Past, Present and Future. Proceedings of a National Seminar, Kerala For.Res. Inst., Peechi, Kerala, India.
84. Llewellyn, D., J. Kyozuko and R. Floyd. 1999. Transgenic eucalypts [Eucalyptus camaldulensis] with insect resistance and herbicide tolerance. pp. 115-120. In: Proceedings of the Second International Wood Biotechnology Symposium, Canberra, Australia.
85. Lloyd, G. and B. McCown. 1981. Commercially feasible micropropagation of mountain laurel Kalmia latifolia by use of shoot tip culture. Proc. Intl. Plant Prop. Soc. 30: 421-427.
86. Luisa, M., F.C. Goncalves and W. Steiner. 1996. Purification and characterization of laccase from a newly isolated wood-decaying fungus. pp. 258-266. In: T.W. Jeffries and I.L. Viikari (eds.). Enzymes for Pulp and Paper Processing. American Chemical Society. Washington, D.C., USA.
87. Ma, C., R. Deepika, A.A. Myburg, M. Ranik and S. H. Strauss. 2011a. Development of Eucalyptus tissue culture conditions for improved in vitro plant health and transformability. In: BMC Proceedings of IUFRO Tree Biotechnology conference, 26th June to 02, July, 2011, Arraial D’ Ajuda, Bahia, Brazil. 153 p.
88. Ma, C. and S.H. Strauss. 2011b. Unpublished raw data.
89. Machado, L.O.R., G.M. de Andrade, L.P. Barrueto-Cid, R.M. Penchel and A.C.M. Brasileiro. 1997. Agrobacterium strain specificity and shooty tumour formation in eucalypt (Eucalyptus grandis × E. urophylla). Plant Cell Rep. 16: 299-303.
90. MacRae, S. 1991. Agrobacterium-mediated transformation of Eucalyptus to improve rooting ability. pp. 117-125. In: A.P.G. Schonau (ed.). The Role of Eucalypts. Proceeding from IUFRO Symposium on Intensive Forestry, Pretoria, South Africa. Southern African Institute of Forestry.
91. MacRae, S. and J. van Staden. 1993. Agrobacterium rhizogenes-mediated transformation to improve rooting ability of eucalypts. Tree Physiol. 12: 411-418.
92. Mamaghani, M.S., M.H. Asareh, M. Omidi, A. Ghamari-Zare and S.H. Shahrzad. 2008. Comparison of direct and indirect regeneration in eucalyptus microtheca m. Iranian Journal of Rangelands and Forests Plant Breeding and Genetic Research 16: 229-237.
93. Mamaghani, M.S., M.H. Assareh, M. Omidi, M. Matinizadeh, A. Ghamari-Zare, S. Shahrzad and M. Forootan. 2009. The effect of thidiazuron level on in vitro regeneration type and peroxidase profile in Eucalyptus microtheca F. Muell. Plant Growth Regul. 59: 199-205.
94. Manders, G., A.V.P. dos Santos, F.B. Utravaz, M.R. Davey and J.B. Power. 1992. Transient gene expression in electroporated protoplasts of Eucalyptus citriodora Hook. Plant Cell 30(1): 69-75.
95. Mansfield, S.D. 2009. Solutions for dissolution-engineering cell walls for deconstruction. Curr. Opin. Biotechnol. 20: 286-294.
96. McComb, J.A. and I.J. Bennett. 1982. Vegetative propagation of eucalypts: Using tissue culture and its application to forest improvement in Western Australia. pp. 721-722. In: A. Fujiwara (ed.). Plant Tissue Culture. Maruzen, Tokyo, Japan.
97. McHughen, A., M. Jordan and G. Feist. 1989. Preculture period prior to Agrobacterium increases production of transgenic plants. J. Plant Physiol. 135: 245-248.
98. Miguel, C.M. and M.M. Oliveira. 1999. Transgenic almond (Prunus dulcis Mill.) plants obtained by Agrobacterium-mediated transformation of leaf explants. Plant Cell Rep. 18: 387-393.
99. Moralejo, M., F. Rochange, A.M. Boudet and C. Teulieres. 1998. Generation of transgenic Eucalyptus globulus plantlets through Agrobacterium tumefaciens mediated transformation. Austr. J. Plant Physiol. 25(2): 207-212.
100. Mourgues, F., E. Chevreau, C. Lambert and A. de Bondt. 1996. Efficient Agrobacterium-mediated transformation and recovery of transgenic plants from pear (Pyrus communis L.). Plant Cell Rep. 16: 245-249.
101. Marques, W.L., M. Salazar, E. Camargo, J. Lepikson-Neto, D.C. Gonçalves, L. Costa do Nascimento, C. Garcia, A. Almeida and G. Pereira. 2011. Exploring a new model of cell wall regulation: identification and expression of two putative SHINEs transcription factors in Eucalyptus. BMC Proc. 5-P166.
102. Mullins, K.V., D.J. Llewellyn, V.J. Hartney, S. Strauss and E.S. Dennis. 1997. Regeneration and transformation of Eucalyptus camaldulensis. Plant Cell Rep. 16: 787-791.
103. Muralidharan, E.M. and A.F. Mascarenhas. 1987. In vitro plantlet formation by organogenesis in Eucalyptus camaldulensis and by somatic embryogenesis in Eucalyptus citriodora. Plant Cell Rep. 6: 256-259.
104. Muralidharan, E.M., P.K. Gupta and A.F. Mascarenhas. 1989. Plantlet production through high frequency somatic embryogenesis in long term cultures of Eucalyptus citriodora. Plant Cell Rep. 8: 41-43.
105. Murashige, T. and F. Skoog. 1962. A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol. Plant. 15: 473-497.
106. Navarro, M., C. Ayax, Y. Martinez, J. Laur, W.E.I. Kayal, C. Marque and C. Teulieres. 2011. Two EguCBF1 genes overexpressed in Eucalyptus display a different impact on stress tolerance and plant development. Plant Biotechnol. J. 9: 50-63.
107. Negri, P., L. Cantoni and L. Manzecchi. 2002. Effects of hormonal conditioning of pear leaf explants on Agrobacterium-mediated transformation efficiency. Acta Hort. (ISHS) 596: 441-445.
108. Nugent, G., S.F. Chandler, P. Whiteman and T.W. Stevenson. 2001. Adventitious bud induction in Eucalyptus globulus Labill. In vitro Cell. Dev. Biol. Plant 37: 388-391.
109. Ouyang, Q., Q.Q. Li and H.S. Peng. 1980. Preliminary report on the development of embryoids fromEucalyptus. Acta Phytophysiol. Sin. 6: 429-432.
110. Ouyang, Q., H.S. Peng and Q.Q. Li. 1981. Studies on the development of embryoids from Eucalyptus callus. Scient. Silv. Sin. 17: l-7.
111. Penford, A.R. and J.L. Willis. 1961. The Eucalypts: Botany, Cultivation, Chemistry, and Utilization. Interscience Publishers, New York, New York, USA. 551 pp.
112. Petroli, C.D., C.P. Sansaloni, J. Carling, D.A. Steane, R.E. Vaillancourt, A.A. Myburg, A.A., Jr. O.B. da Silva, Jr. G.J. Pappas, A. Kilian and D. Grattapaglia. 2012. Genomic characterization of DArT markers based on high-density linkage analysis and physical mapping to the Eucalyptus genome. PLoS One 7: e44684.
113. Pinto, G., S. Silva, Y.S. Park, L. Neves, C. Araújo and C. Santos. 2008. Factors influencing somatic embryogenesis induction in Eucalyptus globulus Labill.: Basal medium and anti-browning agents. Plant Cell Tiss.Org. Cult. 95(1): 79-88.
114. Pokhrel, D. and T. Viraraghavan. 2004. Treatment of pulp and paper mill wastewater-A review. Sci. Total Environ. 333: 37-58.
115. Potenza, C., L. Aleman and C. Sengupta-Gopalan. 2004. Targeting transgene expression in research, agricultural, and environmental applications: Promoters used in plant transformation. In vitro Cellular & Developmental Biology-Plant 40: 1-22.
116. Prakash, M.G. and K. Gurumurthi. 2005a. Agrobacterium mediated genetic transformation and regeneration of transgenic plants in Eucalyptus tereticornis. Plant Cell Biotechnol. Mol. Biol. 61-2: 23-28.
117. Prakash, M.G. and K. Gurumurthi. 2005b. Somatic embryogenesis and plant regeneration in Eucalyptus tereticornis Sm. Curr. Sci 88: 1311-1316.
118. Prakash, M.G. and K. Gurumurthi. 2009. Genetic transformation and regeneration of transgenic plants from precultured cotyledon and hypocotyls explants of Eucalyptus tereticornis Sm. using Agrobacterium tumefaciens. In vitro Cell. Dev. Biol. Plant 45: 429-434.
119. Prakash, M.G. and K. Gurumurthi. 2010. Effects of type of explant and age, plant growth regulators and medium strength on somatic embryogenesis and plant regeneration in Eucalyptus camaldulensis. Plant Cell Tiss.Org. Cult. 100(1): 13-20.
120. Qin, C.-L. and E.G. Kirby. 1990. Induction of shoots and embryo-like structures in cultures derived from juvenile and adult explants of Eucalyptus spp. Abstract Al-74, 7th Intl. Congr. Plant Tiss. Cell Cult. Amsterdam, The Netherlands. 24-29 June 1990.
121. Quisen, R. 2007. Transformacao genetica de Eucalyptus camaldulensis via co-cultivo com Agrobacterium tumefaciens. M.Sc. Thesis. Univasidade Federal Do Parana, Curitiba, Paraná, Brazil. 146 pp.
122. Quisen, R., Y. de Oliveira, M. Pileggi, F. Cuquel and M. Quoirin. 2009. Selective agent and A. tumefaciens overgrowth-control antibiotics in Eucalyptus camaldulensis cotyledonary culture. Braz. Arch. Biol. Technol. (online) 52(6): 1485-1492.
123. Quoirin, M. and R. Quisen. 2006. Advances in genetic transformation of Eucalyptus species. pp. 41-56. In: C. Franche (ed.). Molecular Biology of Tropical Plants. Research Signpost, Kerala, India Resende, M.D.V., F.R. Márcio, Resende Jr., Carolina P. Sansaloni, Cesar D. Petroli, Alexandre A. Missiaggia, Aurelio M. Aguiar, Jupiter M. Abad, Elizabete K. Takahashi, Antonio M.
124. Rosado, Danielle A. Faria,3 Georgios J. Pappas Jr., Andrzej Kilian and Dario Grattapaglia. 2012. Genomic selection for growth and wood quality in Eucalyptus: capturing the missing heritability and accelerating breeding for complex traits in forest trees. New Phytologist 194: 116-128.
125. Rao, K.S. and R. Venkateswara. 1985. Tissue culture of forest trees: Clonal multiplication of Eucalyptus grandis L. Plant Sci. 40: 51-55.
126. Riemenschneider, D.E. 1990. Susceptibility of intra and interspecific hybrid poplars to Agrobacterium tumefaciens strains C 58. Phytopathology 80: 1099-1102.
127. Rivera, A.L., M. Gómez-Lim, F. Fernández and A.M. Loske. 2012. Physical methods for genetic plant transformation. Physics Life Rev. 9: 308-345.
128. Rochange, F. 1996. Transformation génétique chez Eucalyptus globulus Labill: étude comparée de différentes approaches. Ph.D. Thesis. Universite Paul Sabatier, France.
129. Rochange, F., L. Serrano, C. Marque, C. Teulieres and A.M. Boudet. 1995. DNA delivery into Eucalyptus globulus zygotic embryos through biolistics: Optimization of the biological and physical parameters of bombardment for two different particle guns. Plant Cell Rep. 14: 674-678.
130. Roux, J.J.L. and J. van Staden. 1991. Micropropagation and tissue culture of Eucalyptus-A review. Tree Physiol. 9: 435-477.
131. Ruaud, J.N., K. Churchill and S. Pepper. 1997. Somatic embryogenesis initiation in Eucalyptus nitens. Acta Hort. (ISHS) 447: 185-186.
132. Sansaloni, C.P., C.D. Petroli, J. Carling, C.J. Hudson, D.A. Steane, A.A. Myburg, D. Grattapaglia, R.E. Vaillancourt and A. Kilian. 2010. A high-density Diversity Arrays Technology (DArT) microarray for genome-wide genotyping in Eucalyptus. Plant Methods 6: 16.
133. Sangwan, R.S., S. Brown, G. Vasseur and B. Sangwan-Norreel. 1992. Characterization of competent cells and early events of Agrobacterium-mediated genetic transformation in Arabidopsis thaliana. Planta 188: 439-456.
134. Sartoretto, L.M., L. Barrueto-Cid and A.C.M. Brasileiro. 2002. Biolistic transformation of Eucalyptus grandis × E. urophylla callus. Funct. Plant Biol. 298: 917-924.
135. Scorza, R., L. Levy, V. Damsteegt, L.M. Yepes, J.M. Cordts, A. Hadidi, J. Slightum and D. Gonsalves. 1995. Transformation of plum with papaya ringspot virus coat protein gene and reaction of transgenic plant to plum pox virus. J. Am. Soc. Hort. Sci. 120(6): 943-952.
136. Seabra, R.C. and M.S. Pais. 1997. Genetic transformation of European chestnut. Plant Cell Rep. 17(3): 177-182.
137. Seabra, R.C. and M.S. Pais. 1999. Genetic transformation of European chestnut (Castanea sativa Mill.) with genes of interest. Acta Hort. 494: 407-414.
138. Serrano, L., F. Rochange, J.P. Semblat, C. Marque, C. Teulières and A.M. Boudet. 1996. Genetic transformation of Eucalyptus globulus through biolistics: Complementary development of procedures for organogenesis from zygotic embryos and stable transformation of corresponding proliferating tissue. J. Exp. Bot. 47: 285-290.
139. Shani, Z., M. Dekel, B. Cohen, N. Barimboim, N. Kolosovski, A. Safranuvitch, O. Cohen and O. Shoseyov. 2003. Cell wall modification for the enhancement of commercial eucalyptus species. pp. S10-S26. In: B. Sundberg (ed.). Proceedings of Conference on IUFRO Tree Biotechnology. Umea Plant Science Center, Umea, Sweden.
140. Shao, Z.F., W.Y. Chen, H.L. Luo and X.F. Ye. 2002. Studies on the introduction of the cecropind gene into Eucalyptus urophylla to breed the resistant varieties to Pseudomonas solanacearum. Linye Kexue (Scient. Silv. Sin.) 38(2): 92-98.
141. Shpigel, E., L. Roiz, A. Goren and O. Shoseyov. 1998. Bacterial cellulose binding domain modulates in vitro elongation of different plant cells. Plant Physiol. 117(4): 1185-1194.
142. Sierra-Alvarez, R. and G. Lettinga. 1991. The methanogenic toxicity of wastewater lignins and lignin related compounds. J. Chem. Tech. Biotechnol. 50: 443-455.
143. Slee, A.V., J. Connors, M.I.H. Brooker, S.M. Duffy and J.G. West. 2006. EUCLID Eucalypts of Australia. Third Edition CD ROM Centre for Plant Biodiversity Research. CSIRO Publishing, Melbourne.
144. Southerton, S.G. 2007. Early flowering induction and Agrobacteium transformation of hardwood tree species Eucalyptus occidentalis. Funct. Plant Biol. 34: 707-713.
145. Spokevicius, A.V., K.V. Beveren, M.A. Leitch and G. Bossinger. 2005. Agrobacterium mediated in vitro transformation of wood producing stem segments in eucalypts. Plant Cell Rep. 23: 617-624.
146. Sussex, I.M. 1965. The origin and morphogenesis of Eucalyptus cell populations. pp. 383-391. In: P.R. White and A.R. Grove (eds.). Proceedings of the International Conference on Plant Tissue Culture. McCutchan, Berkeley, California, USA.
147. Teasdale, R.D., E. Mouradova, Y. Yang, D.G. He and C. O’Dwyer. 1999. A method of transformation. U.S. Patent # WO1999/048355.
148. Termignoni, R.R., P.J. Wang and C.Y. Hu. 1996. Somatic embryo induction in Eucalyptus dunnii. Plant Cell Tiss.Org. Cult. 45(2): 129-132.
149. Teulieres, C., J. Teissee and A.M. Boudet. 1990. Transient gene expression in protoplasts and intact cells of Eucalyptus gunnii after electrical or chemical treatment. Abstract A2-136, Proceedings of the 7th International Congress on Plant Tissue and Cell Culture. Amsterdam, The Netherlands, 24-29 June 1990.
150. Teulieres, C., J. Grima-Pettenati, C. Curie, J. Teissie and A.M. Boudet. 1991. Transient foreign expression in polyethylene/glycol treated or electropulsated Eucalyptus gunnii protoplasts. Plant Cell Tiss. Org. Cult. 25(2): 125-132.
151. Tibok, A., N.W. Blackhall, J.B. Power and M.R. Devey. 1995. Optimized plant regeneration from callus derived from seedling hypocotyl of Eucalyptus urophylla. Plant Cell 110: 139-145.
152. Tournier, V., S. Grat, C. Marque, W. El Kayal, R. Penchel, G. Andrade, A.M. Boudet and C. Teulieres. 2003. An efficient procedure to stably introduce genes into an economically important pulp tree (Eucalyptus grandis x Eucalyptus urophylla). Transgen. Res. 124: 403-411.
153. Trindade, H. and M.S. Pais. 2003. Meristematic nodule culture: A new pathway for in vitro propagation of Eucalyptus globulus. Trees 17: 308-315.
154. Tsuchihira, A., Y.T. Hanba, N. Kato, T. Doi, T. Kawazu and M. Maeshima. 2010. Effect of overexpression of radish plasma membrane aquaporins on water use efficiency, photosynthesis and growth of Eucalyptus trees. Tree Physiol. 30: 417-430.
155. Uranbey, S., C.S. Sevimay, M.D. Kaya, A. Ppek, C. Sancak, D. Basalma, C. Er and S. Ozcan. 2005. Influence of different co-cultivation temperatures, periods and media on Agrobacterium tumefaciens mediated gene transfer. Biol. Plant. 49(1): 53-57.
156. Valerio, L., D. Carter, J.C. Rodrigues, V. Tournier, J. Gominho, C. Marque, A.M. Boudet, M. Maunders, H. Pereira and C. Teulieres. 2003. Down regulation of cinnamyl alcohol dehydrogenase, a lignification enzyme, in Eucalyptus camaldulensis. Mol. Breed. 12: 157-167.
157. Vanholme, R., V. Storme, B. Vanholme, L. Sundin, J.H. Christensen, G. Goeminne, C. Halpin, A. Rohde, K. Morreel and W. Boerjan. 2012. A systems biology view of responses to lignin biosynthesis perturbations in Arabidopsis. Plant Cell 24: 3506-3529.
158. Wang, S.Q., J. Chen and Y.H. Gan. 2007. Studies of transformation of hrap gene from sweet pepper into Eucalyptus. Zhongnan Linye Keji Daxue Xuebao (J. Centr. S. Univ. For. Technol.) 27(6): 115-118.
159. Warrag, E., M.S. Lesney and D.J. Rockwood. 1991. Nodule culture and regeneration of Eucalyptus grandis hybrids. Plant Cell Rep. 9: 586-589.
160. Watt, M.P., F.C. Blackeway, C.F. Cresswell and B. Herman. 1991. Somatic embryogenesis in Eucalyptus grandis. S. Afr. For. J. 157: 59-65.
161. Watt, M.P., F.C. Blakeway, F.C. Termignoni and S.M. Jain. 1999. Somatic embryogenesis in Eucalyptus grandis and E. dunni. pp. 63-78. In: S.M. Jain, P.K. Gupta and R.J. Newton (eds.). Somatic Embryogenesis in Woody Plants, Vol. 5. Kluwer, Dordrecht, The Netherlands.
162. Whyte, G., K. Howard, H.E. Giles, J. St and T.I. Burgess. 2011. Foliar pests and pathogens of Eucalyptus dunnii plantations in southern Queensland. Australian Forestry 74: 161-169.
163. Williams, K.J. and B.M. Potts. 1996. The natural distribution of Eucalyptus species in Tasmania. Tas. For. 8: 39-165.
164. Winans, S.C., R.A. Kerstetter, J.E. Ward and E.W. Nester. 1989. A protein required for transcriptional regulation of Agrobacterium virulence genes spans the cytoplasmic membrane. J. Bacteriol. 171: 1616-1622.
165. Winton, L.L. 1974. Second Addendum to the Bibliography of Tree Callus Cultures. Genetic and Physiological Notes, Number 19. The Institute of Paper Chemistry, Appleton, Wisconsin, USA.
166. Wu, H., C. Sparks, B. Amoah and H.D. Jones. 2003. Factors influencing successful Agrobacterium -mediated genetic transformation of wheat. Plant Cell Reports 21: 659-668.
167. Yamada Watanabe, K., A. Kawaoka, K. Matsunaga, K. Nanto, K. Sugita, S. Endo, H. Ebinuma and N. Murata. 2003. Molecular breeding of Eucalyptus: Analysis of salt stress tolerance of transgenic Eucalyptus camaldulensis that over expressed choline oxidase gene (coda). pp. S7-S9. In: B. Sundberg (ed.). Proceedings of IUFRO Conference on Tree Biotechnology. Umea Plant Science Center, Umea, Sweden.
168. Zhang, X., D.W. Stebbing, G. Soong, J.N. Saddler and R.P. Beatson. 2002. A combined fungal and enzyme treatment system to remove TMP/newsprint mill white water substances. TAPPI J. 1: 26-32.
169. Zhang, C., K.A. Winkeler, S.A. Miller, T. Wales, Y. Zhao and M. Wood. 2007. Enhancement of cold tolerance in plants. U.S. patent number 20100107473 A1.
170. Zhang, C., B. Kwan, S. Chang and P. Raymond. 2011. Freeze tolerant eucalyptus. U.S. patent no. 20120266326 A1.
171. Zhang, C., K.H. Norris-Caneda, W.H. Rottmann, J.E. Gulledge, S. Chang, B.Y. Kwan, A.M. Thomas, L.C. Mandel, R.T. Kothera, A.D. Victor, L. Pearson and M.A.W. Hinchee. 2012. Control of Pollen-Mediated Gene Flow in Transgenic Trees. Plant Physiology 159: 1319-1334.