Genetic transformation of conifers and its application in forest biotechnology

Plant Cell Reports

Volumn 22, Issue 1, 2003, Pages 1-15

  Tang, W ^a   Newton, R J ^a  

^a EAST CAROLINA UNIVERSITY   (United States)

Author keywords

Agrobacterium; Conifer; Genetic engineering; Particle bombardment

Indexed keywords

DNA; GENETIC ENGINEERING; HERBICIDES; PLANTS (BOTANY);

GENETIC TRANSFORMATION;

BIOTECHNOLOGY;

BIOTECHNOLOGY; CONIFEROPHYTA; RHIZOBIUM RADIOBACTER; TRANSFECTION; TRANSFORMATION, GENETIC; TREES;

ABIES; AGROBACTERIUM; CONIFEROPHYTA; EMBRYOPHYTA; LARIX; LARIX DECIDUA; PICEA; PICEA ABIES; PICEA GLAUCA; PICEA MARIANA; PINUS RADIATA; PINUS STROBUS; PINUS TAEDA; STROBUS;

EID: 0043286804     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-003-0670-1     Document Type: Review

References (123)

1. Baucher M, Chabbert B, Pilate G, Van Doorsselaere J, Tollier MT, Conil MP, Cornu D, Monties B, Van Montagu M, Inze D, Jouanin L, Boerjan W (1996) Red xylem and higher lignin extractability by down-regulating a cinnamyl alcohol dehydrogenase in poplar. Plant Physiol 112:1479-1490
2. Bekkaoui F, Pilon M, Laine E, Raju DSS, Crosby WL, Dunstan DL (1988) Transient gene expression in electroporated Picea glauca protoplasts. Plant Cell Rep 7:481-484
3. Bekkaoui F, Dalta RSS, Pilon M, Tautorus TE, Crosby WL, Dunstan DI (1990) The effects of promoter on transient expression in conifer cell lines. Theor Appl Genet 79:535-359
4. Benfey PN, Ren L, Chua N-H (1990) Combinational and synergistic properties of CaMV 35S enhancer subdomains. EMBO J 9:1685-1996
5. Bergmann BA, Stomp AM (1992) Effect of host plant genotype and growth rate on Agrobacterium tumefaciens-mediated gall formation in Pinus radiata. Phytopathology 82:1457-1462
6. Birch RG (1997) Plant transformation: problems and strategies for practical application. Annu Rev Plant Physiol Plant Mol Biol 48:297-326
7. Birch RG, Bower R (1994) Principles of gene transfer using particle bombardment. In: Yang N-S, Christou P (eds) Particle bombardment technology for gene transfer. Oxford University Press, New York, pp 3-37
8. Bishop-Hurley SL, Zabkiewicz RJ, Grace L, Gardner RC, Wagner A, Walter C (2001) Conifer genetic engineering: transgenic Pinus radiata (D. Don) and Picea abies (Karst) plants are resistant to the herbicide Buster. Plant Cell Rep 20:235-243
9. Bommineni VR, Chibbar RN, Dalta RSS, Tsang EWT (1993) Transformation of white spruce (Picea glauca) somatic embryos by microprojectile bombardment. Plant Cell Rep 13:17-23
10. Bowler C, Slooten L, Vanderbranden S, De Rycke R, Botterman J, Sybesma C, Van Montagu M, Inze D (1991) Manganese superoxide dismutase can reduce cellular damage mediated by oxygen radicals in transgenic plants. EMBO J 10:1723-1732
11. Campbell MA, Kinlaw CS, Neale DB (1992) Expression of luciferase and β-glucuronidase in Pinus radiata suspension cells using electroporation and particle bombardment. Can J For Res 22:2014-2018
12. Cerda F, Aquea F, Gebauer M, Medina C, Arce-Johnson P (2002) Stable transformation of Pinus radiata embryogenic tissue by Agrobacterium tumefaciens. Plant Cell Tissue Organ Cult 70:251-257
13. Charest PJ, Devantier Y, Ward C, Jones C, Schaffer U (1991) Transient expression of foreign chimeric genes in the gymnosperm hybrid larch following electroporation. Can J Bot 69:1731-1736
14. Charest PJ, Calero N, Lachance D, Dalta RSS, Duchesne LC, Tsang EWT (1993) Microprojectile-DNA delivery in conifer species: factors affecting assessment of transient gene expression using the β-glucuronidase reporter gene. Plant Cell Rep 12:189-193
15. Charest PJ, Devantier Y, Lachance D (1996) Stable genetic transformation of Picea mariana (Black spruce) via microprojectile bombardment. In Vitro Cell Dev Biol 32:91-99
16. Charity JA, Holland L, Donaldson SS, Grace L, Walter C (2002) Agrobacterium-mediated transformation of Pinus radiata organogenic tissue using vacuum-infiltration. Plant Cell Tissue Organ Cult 70:51-60
17. Chiang VL (2002) From rags to riches. Nat Biotechnol 20:557-558
18. Citovsky V, Wong ML, Zambryski P (1989) Cooperative interaction of Agrobacterium VirE2 protein with single-stranded DNA: implications for T-DNA transfer process. Proc Natl Acad Sci USA 86:1193-1197
19. Clapham DH, Ekberg I (1986) Induction of tumours by various strains of Agrobacterium tumefaciens on Abies nordmanniana and Picea abies. Scand J For Res 1:435-437
20. Clapham D, Demel P, Elfstrand M, Koop HU, Sabala I, Von Arnold S (2000) Gene transfer by particle bombardment to embryogenic cultures of Picea abies and the production of transgenic plantlets. Scand J For Res 15:151-160
21. Comai L, Facciotti D, Hiatt WR, Thompson G, Rose RE, Stalker DM (1985) Expression in plants of a mutant aroA gene from Salmonella typhimurium confers tolerance to glyphosate. Nature 317:741-744
22. Dandekar AM, Gupta PK, Durzan DJ, Knauf V (1987) Transformation and foreign gene expression in micropropagated Douglas-fir (Pseudotsuga menziesii). Biotechnology 5:587-590
23. DeCleene M, DeLey J (1976) The host range of crown gall. Bot Rev 42:389-466
24. Dekker-Robertson DL, Libby WJ (1998) American forest policy-global ethical tradeoffs. Bioscience 48:471-477
25. Dillen W, De Clercq J, Kapila J, Zambre M, Van Montagu M, Angenon G (1997) The effect of temperature on Agrobacterium tumefaciens-mediated gene transfer to plants. Plant J 12:1459-1463
26. Diner AM (1999) Genetic transformation of Pinus palustris (longleaf pine). In: Bajaj YPS (ed) Transgenic trees. Biotechnology in agriculture and forestry, vol. 44. Springer, Berlin Heidelberg New York, pp 185-192
27. Diner AM, Karnosky DF (1987) Differential responses of two conifers to in vitro inoculation with Agrobacterium rhizogenes. Eur J Forest Pathol 17:211-216
28. Doblin MS, Kurek I, Jacob-Wilk D, Delmer DP (2002) Cellulose biosynthesis in plants: from genes to rosettes. Plant Cell Physiol 43:1407-1420
29. Duchesne LC, Charest PJ (1991) Transient expression of the β-glucuronidase gene in embryogenic callus of Picea mariana following microprojection. Plant Cell Rep 10:191-194
30. Duchesne LC, Lelu MA, Aderkas PV, Charest PJ (1993) Microprojectile-mediated DNA delivery in haploid and diploid embryogenic cells of Larix spp. Can J For Res 23:312-316
31. Elfstrand M, Fossdal CG, Sitbon F, Olsson O, Lonneborg A, von Arnold S (2001) Overexpression of the endogenous peroxidase-like gene spi 2 in transgenic Norway spruce plants results in increased total peroxidase activity and reduced growth. Plant Cell Rep 20:596-603
32. Ellis D, Roberts D, Sutton B, Lazaroff W, Webb D, Flinn B (1989) Transformation of white spruce and other conifer species by Agrobacterium tumefaciens. Plant Cell Rep 8:16-20
33. Ellis DD, McCabe D, Russell D, Martinell B, McCown BH (1991) Expression of inducible angiosperm promoters in a gymnosperm, Picea glauca (white spruce). Plant Mol Biol 19:19-27
34. Ellis DD, McCabe DE, Mcinnis S, Ramachandran R, Russell DR, Wallace KM, Martinell BJ, Roberts DR, Raffa KF, McCown BH (1993) Stable transformation of Picea glauca by particle acceleration. Biotechnology 11:84-89
35. Fenning TM, Gershenzon J (2002) Where will the wood come from? Plantation forests and the role of biotechnology. Trends Biotechnol 20:291-296
36. Fernando DD, Owens JN, Misra S (2000) Transient gene expression in pine pollen tubes following particle bombardment. Plant Cell Rep 19:224-228
37. Fillatti JJ, Sellmer J, McCown B, Haissig B, Comai L (1987) Agrobacterium mediated transformation and regeneration of Populus. Mol Gen Genet 206:192-199
38. Finer JJ, Vain P, Jones MW, McMullen MD (1992) Development of the particle inflow gun for DNA delivery to plant-cells. Plant Cell Rep 11:323-328
39. Fire A (1999) RNA-triggered gene silencing. Trends Genet 15:358-363
40. Fire A, Xu SQ, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806-811
41. Fladung M (1999) Gene stability in transgenic aspen-Populus. I. Flanking DNA sequences and T-DNA structure. Mol Gen Genet 260:574-581
42. Godwin I, Gordon T, Ford-Lloyd B, Newbury HJ (1991) The effects of acetosyringone and pH on Agrobacterium-mediated transformation vary according to plant species. Plant Cell Rep 9:671-675
43. Goldfarb B, Strauss SH, Howe GT, Zaerr JB (1991) Transient gene expression of microprojectile-introduced DNA in Douglas-fir cotyledons. Plant Cell Rep 10:517-521
44. Gomord V, Faye L (1996) Signals and mechanisms involved in intracellular transport of secreted proteins in plants. Plant Physiol Biochem 34:165-181
45. Gould JH, Zhou YX, Padmanabhan V, Magallanes-Cedeno ME, Newton RJ (2002) Transformation and regeneration of loblolly pine: shoot apex inoculation with Agrobacterium. Mol Breed 10:131-141
46. Grevelding C, Fantes V, Kemper E, Schell J, Masterson R (1993) Single-copy T-DNA insertions in Arabidopsis are the predominant form of integration in root-derived transgenics, whereas multiple insertions are found in leaf discs. Plant Mol Biol 23:847-860
47. Gupta PK, Dandekar AM, Durzan DJ (1988) Somatic proembryo formation and transient expression of a luciferase gene in Douglas fir and loblolly pine protoplasts. Plant Sci 58:85-92
48. Hansen G, Das A, Chilton M-D (1994) Constitutive expression of the virulence genes improves the efficiency of plant transformation by Agrobacterium. Proc Natl Acad Sci USA 91:7603-7607
49. Herschbach C, Kopriva S (2002) Transgenic trees as tools in tree and plant physiology. Trees 16:250-261
50. Hicks GR, Smith HMS, Shieh M, Raikhel NV (1995) Three classes of nuclear import signals bind to plant nuclei. Plant Physiol 107:1055-1058
51. Hoekema A, Hirsch PR, Hooykaas PJJ, Schilperoort RA (1983) A binary plant vector strategy based on separation of vir and T-region of Agrobacterium tumefaciens Ti plasmid. Nature 303:179-180
52. Hood EE, Gelvin SB, Melchers LS, Hoekema A (1993) New Agrobacterium helper plasmids for gene transfer to plants. Transgenic Res 2:208-218
53. Huang Y, Diner AM, Karnosky DF (1991) Agrobacterium rhizogenes-mediated genetic transformation and regeneration of a conifer: Larix decidua. In Vitro Cell Dev Biol 27:201-207
54. Humara J M, Lopez M, Ordas R J (1999) Agrobacterium tumefaciens-mediated transformation of Pinus pinea L. cotyledons: an assessment of factors influencing the efficiency of uidA gene transfer. Plant Cell Rep 19:51-58
55. James DJ, Uratsu S, Cheng J, Negri P, Viss P, Dandekar AM (1993) Acetosyringone and osmoprotectants like betaine or proline synergistically enhance Agrobacterium-mediated transformation of apple. Plant Cell Rep 12:559-563
56. James R, DiFazio S P, Brunner A, Strauss S H (1998) Environmental effects of genetic engineering of woody biomass crops. Biomass Bioenergy 14:403-414
57. Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusion: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901-3907
58. Kim JW, Minamikawa T (1996) Transformation and regeneration of French bean plants by the particle bombardment process. Plant Sci 117:131-138
59. Klimaszewska K, Devantier Y, Lachance D, Lelu MA, Charest PJ (1997) Larix laricina (tamarack): somatic embryogenesis and genetic transformation. Can J For Res 27:538-550
60. Klimaszewska K, Lachance D, Pelletier G, Lelu M-A, Seguin A (2001) Regeneration of transgenic Picea glauca, P. mariana and P. abies after cocultivation of embryogenic tissue with Agrobacterium tumefaciens. In Vitro Cell Dev Biol Plant 37:748-755
61. Koncz C, Schell J (1986) The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimeric genes carried by a novel type of Agrobacterium binary vector. Mol Gen Genet 204:383-396
62. Kumar S, Fladung M (2001) Gene stability in transgenic aspen (Populus). II. Molecular characterization of variable expression of transgene in wild and hybrid aspen. Planta 213:731-740
63. Le VQ, Belles-Isles J, Dusabenyagasani M, Tremblay FM (2001) An improved procedure for production of white spruce (Picea glauca) transgenic plants using Agrobacterium tumefaciens. J Exp Bot 52:2089-2095
64. Leple JC, Brasileiro ACM, Michel MF, Delmotte F, Jouanin L (1992) Transgenic poplars: expression of chimeric genes using four different constructs. Plant Cell Rep 11:137-141
65. Levee V, Lelu MA, Jouanin L, Cornu D, Pilate G (1997) Agrobacterium tumefaciens-mediated transformation of hybrid larch (Larix kaempferixL. decidua) and transgenic plant regeneration. Plant Cell Rep 16:680-685
66. Levee V, Garin E, Klimaszewska K, Seguin A, (1999) Stable genetic transformation of white pine (Pinus strobus L.) after cocultivation of embryogenic tissues with Agrobacterium tumefaciens. Mol Breed 5:429-440
67. Li L, Zhou YH, Cheng XF, Sun JY, Marita JM, Ralph J, Chiang VL (2003) Combinatorial modification of multiple lignin traits in trees through multigene cotransformation. Proc Natl Acad Sci USA 100:4939-4944
68. Lindroth AM, Gronroos R, Clapham D, Svensson J, von Arnold S (1999) Ubiquitous and tissue-specific gus expression in transgenic roots conferred by six different promoters in one coniferous and three angiosperm species. Plant Cell Rep 18:820-828
69. Loopstra CA, Stomp AM, Sederoff RR (1990) Agrobacterium-mediated DNA transfer in sugar pine. Plant Mol Biol 15:1-9
70. Lucier AA, Hinchee M, McCullough RB (2001) Biotechnology and the forest products industry. In: Strauss SH, Bradshaw HD (eds) Proceedings of the first international symposium on ecological and society aspect of transgenic plantations. College of Forestry, Oregon State University, pp 57-61
71. Mathews JH, Campbell MM (2000) The advantages and disadvantages of the application of genetic engineering to forest trees: a discussion. Forestry 73:371-380
72. McAfee BJ, White EE, Pelcher LE, Lapp MS (1993) Root induction in pine (Pinus) and larch (Larix) spp. Using Agrobacterium rhizogenes. Plant Cell Tissue Organ Cult 34:53-62
73. McLean MA, Charest PJ (2000) The regulation of transgenic trees in North America. Silvae Genet 49:233-239
74. Meilan R, Han KH, Ma CP, James RR, Eaton JA, Stanton BJ, Hoien E, Crockett RP, Strauss SH (2000) Development of glyphosate-tolerant hybrid cottonwoods. Tappi J 83:164-166
75. Merkle SA, Dean JFD (2000) Forest tree biotechnology. Curr Opin Biotechnol 11:298-302
76. Morris JW, Castle LA, Morris RO (1989) Efficacy of different Agrobacterium tumefaciens strains in transformation of pinaceous gymnosperms. Physiol Mol Plant Pathol 34:451-461
77. Moyle R, Moody J, Phillips L, Walter C, Wagner A (2002) Isolation and characterization of a Pinus radiata lignin biosynthesis-related O-methyltransferase promoter. Plant Cell Rep 20:1052-1060
78. Mullin TJ, Bertrand S (1998) Environmental release of transgenic trees in Canada - potential benefits and assessment of biosafety. For Chron 74:203-219
79. Newton RJ, Bloom J, Bivans DH, Jain SM (2001) Stable genetic transformation of conifers. Phytomorphology Golden Jubilee Issue, pp 421-434
80. Park SH, Lee BM, Salas MG, Srivatanakul M, Smith RH (2000) Shorter T-DNA or additional virulence genes improve Agrobacterium-mediated transformation. Theor Appl Genet 101:1015-1020
81. Pena L, Sequin A (2001) Recent advances in the genetic transformation of trees. Trends Biotechnol 19:5000-5506
82. Perlak FJ, Fuchs RL, Dean DA, McPherson SL, Fischhoff DA (1991) Modification of the coding sequence enhances plant expression of insect control genes. Proc Natl Acad Sci USA 88:3324-3328
83. Pilate G, Guiney E, Holt K, Petit-Conil M, Lapierre C, Leple JC, Pollet B, Mila I, Webster EA, Marstorp HG, Hopkins DW, Jouanin L, Boerjan W, Schuch W, Cornu D, Halpin C (2002) Field and pulping performances of transgenic trees with altered lignification. Nat Biotechnol 20:607-612
84. Reichel C, Mathur J, Eckes P, Langenkemper K, Koncz C (1996) Enhanced green fluorescence by the expression of an Aequorea victoria green fluorescent protein mutant in mono- and dicotyledonous plant cells. Proc Natl Acad Sci USA 93:5888-5893
85. Reiss B, Sprengle R, Will H, Schaller H (1984) A new sensitive method for qualitative and quantitative assay of neomycin phosphotransferase in crude cell extracts. Gene 30:211-217
86. Richardson JP (1993) Transcription termination. Crit Rev Biochem Mol Biol 28:1-30
87. Robertson D, Weissinger AK, Ackley R, Glover S, Sederoff RR (1992) Genetic transformation of Norway spruce [Picea abies (L.) Karst] using somatic embryo explants by microprojectile bombardment. Plant Mol Biol 19:925-935
88. Rogers H J, Parkes H C (1995) Transgenic plants and the environment. J Exp Bot 46:467-488
89. Rossi L, Horn B, Tinland B (1996) Integration of complete transferred DNA units is dependent on the activity of virulence E2 protein of Agrobacterium tumefaciens. Proc Natl Acad Sci USA 93:126-130
90. Rugh CI, Senecoff JF, Meagher RB, Merkle SA (1998) Development of transgenic yellow poplar for mercury phytoremediation. Nat Biotechnol 16:925-928
91. Sederoff R, Stomp AM, Chilton WS, Moore LW (1986) Gene transfer into loblolly pine by Agrobacterium tumefaciens. Biotechnology 4:647-649
92. Sheikholeslam SN, Weeks DP (1987) Acetosyringone promotes high frequency transformation of Arabidopsis thaliana explants by Agrobacterium tumefaciens. Plant Mol Biol 8:291-298
93. Sheng JS, Citovsky V (1996) Agrobacterium-plant cell DNA transport: have virulence proteins, will travel. Plant Cell 8:1699-1710
94. Shin DI, Podila GK, Huang Y, Karnosky DF (1994) Transgenic larch expressing genes for herbicide and insect resistance. Can J For Res 24:2059-2067
95. Smith RH, Hood EE (1995) Agrobacterium-tumefaciens transformation of monocotyledons. Crop Sci 35:301-309
96. Stachel SE, Messens E, Montague MV, Zambryski P (1985) Identification of the signal molecules produced by wounded plant cells that activate T-DNA transfer in Agrobacterium tumefaciens. Nature 318:624-629
97. Stomp AM, Loopstra C, Chilton WS, Sederoff RR, Moore LW (1990) Extended host range of Agrobacterium tumefaciens in the genus Pinus. Plant Physiol 92:1226-1236
98. Stomp AM, Weissinger A, Sederoff RR (1991) Transient expression from microprojectile-mediated DNA transfer in Pinus taeda. Plant Cell Rep 10:187-190
99. Strauss SH, Bradshaw HD (eds) (2001) Proceedings of the First International Symposium on Ecological and Societal Aspect of Transgenic Plantations. College of Forestry, Oregon State University
100. Strauss SH, Rottmann WH, Brunner AM, Sheppard LA (1995) Genetic engineering of reproductive sterility in forest trees. Mol Breed 1:5-26
101. Strauss SH, DiFazio SP, Meilan R (2001) Genetically modified poplars in context. For Chron 77:271-279
102. Sutton B (2002) Commercial delivery of genetic improvement to conifer plantations using somatic embryogenesis. Ann For Sci 59:657-661
103. Tang W (2000) Peroxidase activity of desiccation-tolerant loblolly pine somatic embryos. In Vitro Cell Dev Biol Plant 36:488-491
104. Tang W (2001) Agrobacterium-mediated transformation and assessment of factors influencing transgene expression in loblolly pine (Pinus taeda L.). Cell Res 11:237-243
105. Tang W, Ouyang F (1999) Plant regeneration via organogenesis from six families of loblolly pine. Plant Cell Tissue Organ Cult 58:223-226
106. Tang W, Ouyang F, Guo ZC (1998) Plant regeneration through organogenesis from callus induced from mature zygotic embryos of loblolly pine. Plant Cell Rep 17:557-560
107. Tang W, Sederoff R, Whetten R (2001) Regeneration of transgenic loblolly pine (Pinus taeda L.) from zygotic embryos transformed with Agrobacterium tumefaciens. Planta 213:981-989
108. Tautorus TE, Bekkaoui F, Pilon M, Dalta RSS, Crosby WL, Fowke LC, Dunstan DI (1989) Factors affecting transient gene in electroporated black spruce (Picea mariana) and jack pine (Pinus banksiana) protoplasts. Theor Appl Genet 78:531-356
109. Tian L, Seguin A, Charest PJ (1997) Expression of the green fluorescent protein gene in conifer tissues. Plant Cell Rep 16:267-271
110. Turner R, Foster GD (1995) The potential of plant viral translational enhancers in biotechnology for increased gene expression. Mol Biotechnol 3:225-236
111. Tzfira T, Citovsky V (2002) Partners-in-infection: host proteins involved in the transformation of plant cells by Agrobacterium. Trends Cell Biol 12:121-129
112. Tzfira T, Yarnitzky O, Vainstein A, Altman A (1996) Agrobacterium rhizogenes-mediated DNA transfer in Pinus halepensis Mill. Plant Cell Rep 16:26-31
113. Tzfira T, Zuker A, Altman A (1998) Forest-tree biotechnology: genetic transformation and its application to future forests. Trends Biotechnol 16:439-446
114. Van Raemdonck D, Jaziri M, Boerjan W, Baucher M (2001) Advances in the improvement of forest trees through biotechnology. Belg J Bot 134:64-78
115. Van Wordragen MF, Dons JJM (1992) Agrobacterium tumefaciens-mediated transformation of recalcitrant crops. Plant Mol Biol Rep 10:12-36
116. Villalobos-Amador E, Rodriguez-Hernandez G, Perez-Molphe-Balch E (2002) Organogenesis and Agrobacterium rhizogenes-induced rooting in Pinus maximartinezii Rzedowsky and P. pinceana Gordon. Plant Cell Rep 20:779-785
117. Walter C, Smith DR, Connett MB, Grace L, White DWR (1994) A biolistic approach for the transfer and expression of a uidA reporter gene in embryogenic cultures of Pinus radiata. Plant Cell Rep 14:69-74
118. Walter C, Grace LJ, Wagner A, White DWR, Walden AR, Donaldson SS, Hinton H, Gardner RC, Smith DR (1998) Stable transformation and regeneration of transgenic plants of Pinus radiata D. Don. Plant Cell Rep 17:460-469
119. Walter C, Grace LJ, Donaldson SS (1999) An efficient biolistic transformation protocol for Picea abies embryogenic tissue and regeneration of transgenic plants. Can J For Res 29:1539-1546
120. Walter C, Charity J, Grace L, Hofig K, Moller R, Wagner A (2002) Gene technologies in Pinus radiata and Picea abies: tools for conifer biotechnology in the 21st century. Plant Cell Tissue Organ Cult 70:3-12
121. Wenck AR, Quinn M, Whetten RW, Pullman G, Sederoff R (1999) High-efficiency Agrobacterium-mediated transformation of Norway spruce (Picea abies) and loblolly pine (Pinus taeda). Plant Mol Biol 39:407-416
122. Wilson SM, Thorpe TA, Moloney MM (1989) PEG-mediated expression of GUS and CAT genes in protoplasts from embryogenic suspension cultures of Picea glauca. Plant Cell Rep 7:704-707
123. Wu L, Ueda T, Messing J (1995) The formation of mRNA 3′-ends in plants. Plant J 8:323-829