Transposon Activation Tagging in Plants for Gene Function Discovery

  • Matthias FladungEmail author
Part of the Progress in Botany book series (BOTANY, volume 77)


In the last 20 years, activation tagging or gain-of-function mutagenesis has become a very powerful tool to reveal gene functions in plant reverse genetics. The idea behind activation tagging is to overexpress endogenous genes by random insertion of a DNA sequence as a tag-carrying enhancer or promoter, but without changing transcript patterns. The approaches employed so far mainly comprise two different DNA molecules as tag, either T-DNA or transposable elements (transposons). T-DNA activation tagging is strongly based on classical transformation approaches and is only feasible for plant species with well-developed transformation protocols. The basis for transposon tagging is the breakthrough observation that transposable elements are active in heterologous plant species following transformation and are able to pass chromosome boundaries. Thus, only few transgenic lines are needed for transposon-based activation tagging. Examples for successful transposon activation tagging are provided for some plant species, with particular focus on the tree genus Populus.


Transgenic Line Transposable Element Terpenoid Indole Alkaloid Heat Shock Promoter TMS2 Gene 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



I would like to thank Dr. Trevor Fenning (Northern Research Station, Midlothian, Scotland, UK) and Dina Führmann (Thünen-Institute, Scientific Information Centre, Braunschweig, Germany) for critically reading the manuscript and English language editing. Thanks also to all scientists and technicians who contributed to this work on transposon-based activation tagging (S. Kumar, F. Deutsch, O. Polak) and funding agencies (Federal Ministry of Education and Research [BMBF], German Research Foundation [DFG]) for financial support.


  1. Aarts MGM, Dirkse WG, Stiekema WJ, Pereira A (1993) Transposon tagging of a male sterility gene in Arabidopsis. Nature 363:715–717. doi: 10.1038/363715a0 PubMedCrossRefGoogle Scholar
  2. Aboul-Soud MAM, Chen XW, Kang JG, Yun BW, Raja MU, Malik SI, Loake GJ (2009) Activation tagging of ADR2 conveys a spreading lesion phenotype and resistance to biotrophic pathogens. New Phytol 183:1163–1175. doi: 10.1111/j.1469-8137.2009.02902.x PubMedCrossRefGoogle Scholar
  3. Ahad A, Wolf J, Nick P (2003) Activation-tagged tobacco mutants that are tolerant to antimicrotubular herbicides are cross-resistant to chilling stress. Transgenic Res 12:615–629. doi: 10.1023/A:1025814814823 PubMedCrossRefGoogle Scholar
  4. Ahmad A, Niwa Y, Hatakeyama M, Goto S, Kobayashi K, Kobayashi H (2007) Saturated activation tagging for hunting salt-tolerant genes in Arabidopsis. Plant Cell Physiol 48:S140Google Scholar
  5. André D, Colau D, Schell J, Van Montagu M, Hernalsteens JP (1986) Gene tagging in plants by a T-DNA insertion mutagen that generates APH(3′)II-plant gene fusions. Mol Gen Genet 204:512–518. doi: 10.1007/BF00331033 CrossRefGoogle Scholar
  6. Ayliffe MA, Pryor AJ (2007) Activation tagging in plants—generation of novel, gain-of-function mutations. Aust J Agric Res 58:490–497. doi: 10.1071/Ar06154 CrossRefGoogle Scholar
  7. Ayliffe MA, Pryor AJ (2009) Transposon-based activation tagging in cereals. Funct Plant Biol 36:915–921. doi: 10.1071/Fp09130 CrossRefGoogle Scholar
  8. Ayliffe MA, Pallotta M, Langridge P, Pryor AJ (2007) A barley activation tagging system. Plant Mol Biol 64:329–347. doi: 10.1007/s11103-007-9157-8 PubMedCrossRefGoogle Scholar
  9. Baker B, Schell J, Loerz H, Fedoroff N (1986) Transposition of the maize controlling element activator in tobacco. Proc Natl Acad Sci USA 83:4844–4848PubMedPubMedCentralCrossRefGoogle Scholar
  10. Baker B, Coupland G, Fedoroff N, Starlinger P, Schell J (1987) Phenotypic assay for excision of the maize controlling element Ac in tobacco. EMBO J 6:1547–1554PubMedPubMedCentralGoogle Scholar
  11. Balcells L, Sundberg E, Coupland G (1994) A heat-shock promoter fusion to the Ac transposase gene drives inducible transposition of a Ds element during Arabidopsis embryo development. Plant J 5:755–764. doi: 10.1111/j.1365-313X.1994.00755.x CrossRefGoogle Scholar
  12. Bancroft I, Jones JDG, Dean C (1993) Heterologous transposon tagging of the Drl1 locus in Arabidopsis. Plant Cell 5:631–638, PubMedPubMedCentralCrossRefGoogle Scholar
  13. Belzile F, Yoder JI (1992) Pattern of somatic transposition in a high copy Ac tomato line. Plant J 2:173–179. doi: 10.1046/j.1365-313X.1992.t01-40-00999.x PubMedGoogle Scholar
  14. Boeke JD, Sandmeyer SB (2009) Yeast transposable elements. In: The molecular and cellular biology of the yeast saccharomyces: genome dynamics, protein synthesis, and energetics. Cold Spring Harbor monographs, vol 21A, pp 193–261. doi: 10.1101/087969363.21A.193
  15. Bolle C, Schneider A, Leister D (2011) Perspectives on systematic analyses of gene function in Arabidopsis thaliana: new tools, topics and trends. Curr Genomics 12:1–14. doi: 10.2174/138920211794520187 PubMedPubMedCentralCrossRefGoogle Scholar
  16. Borevitz JO, Xia YJ, Blount J, Dixon RA, Lamb C (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12:2383–2393. doi: 10.1105/tpc.12.12.2383 PubMedPubMedCentralCrossRefGoogle Scholar
  17. Brutnell TP (2002) Transposon tagging in maize. Funct Integr Genomics 2:4–12. doi: 10.1007/s10142-001-0044-0 PubMedCrossRefGoogle Scholar
  18. Busov VB, Meilan R, Pearce DW, Ma C, Rood SB, Strauss SH (2003) Activation tagging of a dominant gibberellin catabolism gene (GA2-oxidase) from poplar that regulates tree stature. Plant Physiol 132:1283–1291. doi:10.1104/pp. 103.020354PubMedPubMedCentralCrossRefGoogle Scholar
  19. Busov V, Fladung M, Groover A, Strauss SH (2005) Insertional mutagenesis in Populus: relevance and feasibility. Tree Genet Genomes 1:135–142. doi: 10.1007/s11295-005-0019-8 CrossRefGoogle Scholar
  20. Busov V, Yordanov Y, Gou J, Meilan R, Ma C, Regan S, Strauss S (2011) Activation tagging is an effective gene tagging system in Populus. Tree Genet Genomes 7:91–101. doi: 10.1007/s11295-010-0317-7 CrossRefGoogle Scholar
  21. Cardon GH, Frey M, Saedler H, Gierl A (1993) Definition and characterization of an artificial En-based Spm-based transposon tagging system in transgenic tobacco. Plant Mol Biol 23:157–178. doi: 10.1007/Bf00021428 PubMedCrossRefGoogle Scholar
  22. Carpenter R, Coen ES (1990) Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus. Genes Dev 4:1483–1493. doi: 10.1101/gad.4.9.1483 PubMedCrossRefGoogle Scholar
  23. Carter JD, Pereira A, Dickerman AW, Veilleux RE (2013) An active Ac/Ds transposon system for activation tagging in tomato cultivar M82 using clonal propagation. Plant Physiol 162:145–156. doi:10.1104/pp. 113.213876PubMedPubMedCentralCrossRefGoogle Scholar
  24. Chang C, Kwok SF, Bleecker AB, Meyerowitz EM (1993) Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science 262:539–544. doi: 10.1126/science.8211181 PubMedCrossRefGoogle Scholar
  25. Charlesworth B, Sniegowski P, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371:215–220. doi: 10.1038/371215a0 PubMedCrossRefGoogle Scholar
  26. Charng YC, Wu G, Hsieh CS, Chuang HN, Huang JY, Yeh LC, Shieh YH, Tu J (2007) The inducible transposon system for rice functional genomics. Bot Stud 48:1–11Google Scholar
  27. Chen S, Jin W, Wang M, Zhang F, Zhou J, Jia Q, Wu Y, Liu F, Wu P (2003) Distribution and characterization of over 1000 T-DNA tags in rice genome. Plant J 36:105–113. doi: 10.1046/j.1365-313X.2003.01860.x PubMedCrossRefGoogle Scholar
  28. Chuck G, Robbins T, Nijjar C, Ralston E, Courtney-Gutterson N, Dooner HK (1993) Tagging and cloning of a petunia flower colour gene with the maize transposable element Activator. Plant Cell 5:371–378, PubMedPubMedCentralCrossRefGoogle Scholar
  29. Coomber SA, Feldmann KA (1993) Gene tagging in transgenic plants. In: Kung SD, Wu R (eds) Transgenic plants, vol 1. Academic, New York, NY, pp 225–240Google Scholar
  30. Czarnecka E, Gurley WB, Nagao RT, Mosquera LA, Key JL (1985) DNA-sequence and transcript mapping of a soybean gene encoding a small heat-shock protein. Proc Natl Acad Sci USA 82:3726–3730. doi: 10.1073/pnas.82.11.3726 PubMedPubMedCentralCrossRefGoogle Scholar
  31. DeLong A, Calderon-Urrea A, Dellaporta SL (1993) Sex determination gene TASSELSEED2 of maize encodes a short-chain alcohol dehydrogenase required for stage-specific floral organ abortion. Cell 74:757–768. doi: 10.1016/0092-8674(93)90522-R PubMedCrossRefGoogle Scholar
  32. Dimitri P, Junakovic N (1999) Revising the selfish DNA hypothesis: new evidence on accumulation of transposable elements in heterochromatin. Trends Genet 15:123–124. doi: 10.1016/S0168-9525(99)01711-4 PubMedCrossRefGoogle Scholar
  33. Dinesh-Kumar SP, Whitham S, Choi D, Hehl R, Corr C, Baker B (1995) Transposon tagging of tobacco mosaic-virus resistance gene-N—its possible role in the Tmv-N-mediated signal-transduction pathway. Proc Natl Acad Sci USA 92:4175–4180. doi: 10.1073/pnas.92.10.4175 PubMedPubMedCentralCrossRefGoogle Scholar
  34. Döring HP, Starlinger P (1986) Molecular genetics of transposable elements in plants. Annu Rev Genet 20:175–200PubMedCrossRefGoogle Scholar
  35. Fedoroff NV (2000) Transposons and genome evolution in plants. Proc Natl Acad Sci USA 97:7002–7007. doi: 10.1073/pnas.97.13.7002 PubMedPubMedCentralCrossRefGoogle Scholar
  36. Fedoroff NV (2012) Transposable elements, epigenetics, and genome evolution. Science 338:758–767. doi: 10.1126/science.338.6108.758 PubMedCrossRefGoogle Scholar
  37. Feldmann KA (1991) T-DNA insertion mutagenesis in Arabidopsis: mutational spectrum. Plant J 1:71–82. doi: 10.1111/j.1365-313X.1991.00071.x CrossRefGoogle Scholar
  38. Fladung M (1990) Transformation of diploid and tetraploid potato clones with the rolC gene of Agrobacterium rhizogenes and characterization of transgenic plants. Plant Breed 104:295–304. doi: 10.1111/j.1439-0523.1990.tb00439.x CrossRefGoogle Scholar
  39. Fladung M (1999) Gene stability in transgenic aspen-Populus. I. Flanking DNA sequences and T-DNA structure. Mol Gen Genet 260:574–581. doi: 10.1007/s004380050931 PubMedCrossRefGoogle Scholar
  40. Fladung M (2011) Analysis of re-integrated Ac element positions in the genome of Populus provides a basis for Ac/Ds-transposon activation tagging in trees. Trees 25:551–557. doi: 10.1007/s00468-010-0511-0 CrossRefGoogle Scholar
  41. Fladung M (2014) Prospects of using a modified Ac/Ds transposon system from maize for activation tagging in the tree species Populus. In: Ramawat KG, Mérillon JM, Ahuja MR (eds) Tree biotechnology. CRC Press, Boca Raton, FL, pp 469–482Google Scholar
  42. Fladung M, Ahuja MR (1997) Excision of the maize transposable element Ac in periclinal leaves of 35S-Ac-rolC transgenic aspen-Populus. Plant Mol Biol 33:1097–1103. doi: 10.1023/a:1005788706864 PubMedCrossRefGoogle Scholar
  43. Fladung M, Polak O (2012) Ac/Ds-transposon activation tagging in poplar: a powerful tool for gene discovery. BMC Genomics 13:61. doi: 10.1186/1471-2164-13-61 PubMedPubMedCentralCrossRefGoogle Scholar
  44. Fladung M, Muhs HJ, Ahuja MR (1996) Morphological changes observed in transgenic Populus carrying the rolC gene from Agrobacterium rhizogenes. Silvae Genet 45:349–354Google Scholar
  45. Fladung M, Großmann K, Ahuja MR (1997) Alterations in hormonal and developmental characteristics in transgenic Populus conditioned by the rolC gene from Agrobacterium rhizogenes. J Plant Physiol 150:420–427. doi: 10.1016/S0176-1617(97)80092-2 CrossRefGoogle Scholar
  46. Fladung M, Deutsch F, Hönicka H, Kumar S (2004) DNA and transposon tagging in aspen. Plant Biol 6:5–11. doi: 10.1055/s-2003-44745 PubMedCrossRefGoogle Scholar
  47. Fobert PR, Labbe H, Cosmopoulos J, Gottlob-McHugh S, Ouellet T, Hattori J, Sunohara G, Iyer VN, Miki BL (1994) T-DNA tagging of a seed coat-specific cryptic promoter in tobacco. Plant J 6:567–577. doi: 10.1046/j.1365-313X.1994.6040567.x PubMedCrossRefGoogle Scholar
  48. Gierl A, Saedler H (1992) Plant transposable elements and gene tagging. Plant Mol Biol 19:39–49. doi: 10.1007/BF00015605 PubMedCrossRefGoogle Scholar
  49. Giordano J, Ge Y, Gelfand Y, Abrusán G, Benson G, Warburton PE (2007) Evolutionary history of mammalian transposons determined by genome-wide defragmentation. PLoS Comput Biol 3(7), e137. doi: 10.1371/journal.pcbi.0030137 PubMedPubMedCentralCrossRefGoogle Scholar
  50. Goff SA, Ricke D, Lan TH et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:92–100. doi: 10.1126/science.1068275 PubMedCrossRefGoogle Scholar
  51. Greco R, Ouwerkerk PBF, Taal AJC, Favalli C, Beguiristain T, Puigdomenech P, Colombo L, Hoge JHC, Pereira A (2001) Early and multiple Ac transpositions in rice suitable for efficient insertional mutagenesis. Plant Mol Biol 46:215–227. doi: 10.1023/A:1010607318694 PubMedCrossRefGoogle Scholar
  52. Greco R, Ouwerkerk PBF, De Kam RJ, Sallaud C, Favalli C, Colombo L, Guiderdoni E, Meijer AH, Hoge JHC, Pereira A (2003) Transpositional behaviour of an Ac/Ds system for reverse genetics in rice. Theor Appl Genet 108:10–24. doi: 10.1007/s00122-003-1416-8 PubMedCrossRefGoogle Scholar
  53. Groover A, Fontana JR, Dupper G, Ma C, Martienssen R, Strauss S, Meilan R (2004) Gene and enhancer trap tagging of vascular-expressed genes in poplar trees. Plant Physiol 134:1742–1751, PubMedPubMedCentralCrossRefGoogle Scholar
  54. Harrison EJ, Bush M, Plett JM, McPhee DP, Vitez R, O’Malley B, Sharma V, Bosnich W, Seguin A, MacKay J, Regan S (2007) Diverse developmental mutants revealed in an activation tagged population of poplar. Can J Bot 85:1071–1087. doi: 10.1139/B07-063 CrossRefGoogle Scholar
  55. Hayashi H, Czaja I, Lubenow H, Schell J, Walden R (1992) Activation of a plant gene by T-DNA tagging: auxin-independent growth in vitro. Science 258:1350–1353. doi: 10.1126/science.1455228 PubMedCrossRefGoogle Scholar
  56. Hehl R (1994) Transposon tagging in heterologous host plants. Trends Genet 11:385–386. doi: 10.1016/0168-9525(94)90041-8 CrossRefGoogle Scholar
  57. Hehl R, Baker B (1989) Induced transposition of Ds by a stable Ac in crosses of transgenic tobacco plants. Mol Gen Genet 217:53–59. doi: 10.1007/BF00330942 PubMedCrossRefGoogle Scholar
  58. Ho HS, Vishwakarma RK, Chen ECF, Tsay HS (2013) Activation tagging in Salvia miltiorrhiza can cause increased leaf size and accumulation of tanshinone I and IIA in its roots. Bot Stud 54:37. doi: 10.1186/1999-3110-54-37 CrossRefGoogle Scholar
  59. Howe GT, Strauss SH, Goldfarb B (1991) Insertion of the maize transposable element Ac into poplar. In: Ahuja MR (ed) Woody plant biotechnology. Plenum, New York, NY, pp 283–294CrossRefGoogle Scholar
  60. Howe GT, Goldfarb B, Strauss SH (1994) Agrobacterium-mediated transformation of hybrid poplar suspension cultures and regeneration of transformed plants. Plant Cell Tiss Org Cult 36:59–71. doi: 10.1007/BF00048316 CrossRefGoogle Scholar
  61. Huang SS, Cerny RE, Bhat DS, Brown SM (2001) Cloning of an Arabidopsis patatin-like gene, STURDY, by activation T-DNA tagging. Plant Physiol 125:573–584. doi: 10.1104/Pp.125.2.573 PubMedPubMedCentralCrossRefGoogle Scholar
  62. Huang CRL, Burns KH, Boeke JD (2012) Active transposition in genomes. Annu Rev Genet 46:651–675. doi: 10.1146/annurev-genet-110711-155616 PubMedPubMedCentralCrossRefGoogle Scholar
  63. Ichikawa T, Nakazawa M, Kawashima M, Iizumi H, Kuroda H, Kondou Y, Tsuhara Y, Suzuki K, Ishikawa A, Seki M, Fujita M, Motohashi R, Nagata N, Takagi T, Shinozaki K, Matsui M (2006) The FOX hunting system: an alternative gain-of-function gene hunting technique. Plant J 48:974–985. doi: 10.1111/j.1365-313X.2006.02924.x PubMedCrossRefGoogle Scholar
  64. Imaizumi R, Sato S, Kameya N, Nakamura I, Nakamura Y, Tabata S, Ayabe SI, Aoki T (2005) Activation tagging approach in a model legume, Lotus japonicus. J Plant Res 118:391–399. doi: 10.1007/10265-005-0231-5 PubMedCrossRefGoogle Scholar
  65. Ito T, Motohashi R, Kuromori T, Noutoshi Y, Seki M, Kamiya A, Mizukado S, Sakurai T, Shinozaki K (2005) A Resource of 5,814 dissociation transposon-tagged and sequence-indexed lines of Arabidopsis transposed from start loci on chromosome 5. Plant Cell Physiol 46:1149–1153. doi: 10.1093/pcp/pci112 PubMedCrossRefGoogle Scholar
  66. James DW Jr, Lim E, Keller J, Plooy I, Ralston E, Dooner HK (1995) Directed tagging of the Arabidopsis FATTY ACID ELONGATION1 (FAE1) gene with the maize transposon activator. Plant Cell 7:309–319, PubMedPubMedCentralCrossRefGoogle Scholar
  67. Jeon JS, An G (2001) Gene tagging in rice: a high throughput system for functional genomics. Plant Sci 161:211–219. doi: 10.1016/S0168-9452(01)00414-9 PubMedCrossRefGoogle Scholar
  68. Jeon JS, Lee S, Jung KH et al (2000) T-DNA insertional mutagenesis for functional genomics in rice. Plant J 22:561–570. doi: 10.1046/j.1365-313x.2000.00767.x PubMedCrossRefGoogle Scholar
  69. Jeong DH, An SY, Kang HG, Moon S, Han JJ, Park S, Lee HS, An KS, An GH (2002) T-DNA insertional mutagenesis for activation tagging in rice. Plant Physiol 130:1636–1644. doi: 10.1104/Pp.014357 PubMedPubMedCentralCrossRefGoogle Scholar
  70. Jeong DH, An SY, Park S, Kang HG, Park GG, Kim SR, Sim J, Kim YO, Kim MK, Kim SR, Kim J, Shin M, Jung M, An GH (2006) Generation of a flanking sequence-tag database for activation-tagging lines in japonica rice. Plant J 45:123–132. doi: 10.1111/j.1365-313X.2005.02610.x PubMedCrossRefGoogle Scholar
  71. Jones JDG, Bishop G, Carroll B, Dickinson M, English J, Harrison K, Jones D, Scofield S, Thomas CM (1992) Prospects for establishing a tomato gene tagging system using the maize transposon Activator (Ac). Proc R Soc Edinb 99B:107–119, Google Scholar
  72. Jones DA, Thomas CM, Hammond-Kosack KE, Balint-Kurti PJ, Jones JD (1994) Isolation of the tomato cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266:789–793. doi: 10.1126/science.7973631 PubMedCrossRefGoogle Scholar
  73. Kakimoto T (1996) CKI1, a histidine kinase homolog implicated in cytokinin signal transduction. Science 274:982–985. doi: 10.1126/science.274.5289.982 PubMedCrossRefGoogle Scholar
  74. Kang B, Wang H, Nam KH, Li JY, Li JM (2010) Activation-tagged suppressors of a weak brassinosteroid receptor mutant. Mol Plant 3:260–268. doi: 10.1093/Mp/Ssp099 PubMedPubMedCentralCrossRefGoogle Scholar
  75. Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D (1999) Activation tagging of the floral inducer FT. Science 286:1962–1965. doi: 10.1126/science.286.5446.1962 PubMedCrossRefGoogle Scholar
  76. Karlin-Neumann GA, Brussian JA, Tobin EM (1991) Phytochrome control of the tms2 gene in transgenic Arabidopsis: a strategy for selecting mutants in the signal transduction pathway. Plant Cell 3:573–582PubMedPubMedCentralCrossRefGoogle Scholar
  77. Kim SG, Lee S, Kim YS, Yun DJ, Woo JC, Park CM (2010) Activation tagging of an Arabidopsis SHI-RELATED SEQUENCE gene produces abnormal anther dehiscence and floral development. Plant Mol Biol 74:337–351. doi: 10.1007/s11103-010-9677-5 PubMedCrossRefGoogle Scholar
  78. Knapp S, Larondelle Y, Rossberg M, Furtek D, Theres K (1988) Transgenic tomato lines containing Ds elements at defined genomic positions as tools for targeted transposon tagging. Mol Gen Genet 243:666–673Google Scholar
  79. Koncz C, Martini N, Mayerhofer R, Koncz-Kalman Z, Körber H, Redei GP, Schell J (1989) High-frequency T-DNA-mediated gene tagging in plants. Proc Natl Acad Sci USA 86:8467–8471. doi: 10.1073/pnas.86.21.8467 PubMedPubMedCentralCrossRefGoogle Scholar
  80. Koncz C, Mayerhofer R, Koncz-Kalman Z, Nawrath C, Reiss B, Redei GP, Schell J (1990) Isolation of a gene encoding a novel chloroplast protein by T-DNA tagging in Arabidopsis thaliana. EMBO J 9:1337–1346PubMedPubMedCentralGoogle Scholar
  81. 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. doi: 10.1007/s004250100535 PubMedCrossRefGoogle Scholar
  82. Kumar S, Fladung M (2003a) Somatic mobility of the maize element Ac and its usability for gene tagging in aspen. Plant Mol Biol 51:643–650. doi: 10.1023/a:1022505808929 PubMedCrossRefGoogle Scholar
  83. Kumar S, Fladung M (2003b) Forest tree transgenesis and functional genomics: from fast forward to reverse genetics. Silvae Genet 52:229–232Google Scholar
  84. Labrador M, Corces VG (1997) Transposable element-host interactions: regulation of insertion and excision. Annu Rev Genet 31:381–404. doi: 10.1146/annurev.genet.31.1.381 PubMedCrossRefGoogle Scholar
  85. Lawrence GJ, Finnegan EJ, Ayliff MA, Ellis JG (1995) The L6 gene for flax rust resistance is related to the Arabidopsis bacterial resistance gene RPS2 and the tobacco viral resistance gene N. Plant Cell 7:1195–1206.
  86. Lee CY, Agrawal DC, Wang CS, Yu SM, Chen JJW, Tsay HS (2008) T-DNA activation tagging as a tool to isolate Salvia miltiorrhiza transgenic lines for higher yields of tanshinones. Planta Med 74:780–786. doi: 10.1055/s-2008-1074527 PubMedCrossRefGoogle Scholar
  87. Lee S, Persson DP, Hansen TH, Husted S, Schjoerring JK, Kim YS, Jeon US, Kim YK, Kakei Y, Masuda H, Nishizawa NK, An G (2011) Bio-available zinc in rice seeds is increased by activation tagging of nicotianamine synthase. Plant Biotechnol J 9:865–873. doi: 10.1111/j.1467-7652.2011.00606.x PubMedCrossRefGoogle Scholar
  88. Li Y, Rosso MG, Strizhov N, Viehoever P, Weisshaar B (2003) GABI-Kat SimpleSearch: a flanking sequence tag (FST) database for the identification of T-DNA insertion mutants in Arabidopsis thaliana. Bioinformatics 19:1441–1442. doi: 10.1093/bioinformatics/btg170 PubMedCrossRefGoogle Scholar
  89. Lisch D (2013) How important are transposons for plant evolution? Nat Rev Genet 14:49–61. doi: 10.1038/nrg3374 PubMedCrossRefGoogle Scholar
  90. Lu GH, Wang XP, Liu JH et al (2014a) Application of T-DNA activation tagging to identify glutamate receptor-like genes that enhance drought tolerance in plants. Plant Cell Rep 33:617–631. doi: 10.1007/s00299-014-1586-7 PubMedCrossRefGoogle Scholar
  91. Lu N, Carter JD, Medina TB, Holt SH, Manrique-Carpintero NC, Upham KT, Pereira A, Shulaev V, Veilleux RE (2014b) Transposon based activation tagging in diploid strawberry and monoploid derivatives of potato. Plant Cell Rep 33:1203–1216. doi: 10.1007/s00299-014-1610-y PubMedCrossRefGoogle Scholar
  92. Marsch-Martinez N, Greco R, Van Arkel G, Herrera-Estrella L, Pereira A (2002) Activation tagging using the En-I maize transposon system in Arabidopsis. Plant Physiol 129:1544–1556. doi: 10.1104/Pp.003327 PubMedPubMedCentralCrossRefGoogle Scholar
  93. Martienssen RA (1998) Functional genomics: probing plant gene function and expression with transposons. Proc Natl Acad Sci USA 95:2021–2026PubMedPubMedCentralCrossRefGoogle Scholar
  94. Martin C, Carpenter R, Sommer H, Saedler H, Coen ES (1985) Molecular analysis of instability in flower pigmentation of Antirrhinum majus, following isolation of the Pallida locus by transposon tagging. EMBO J 4:1625–1630PubMedPubMedCentralGoogle Scholar
  95. Masaki T, Tsukagoshi H, Mitsui N, Nishii T, Hattori T, Morikami A, Nakamura K (2005) Activation tagging of a gene for a protein with novel class of CCT-domain activates expression of a subset of sugar-inducible genes in Arabidopsis thaliana. Plant J 43:142–152. doi: 10.1111/j.1365-313X.2005.02439.x PubMedCrossRefGoogle Scholar
  96. Mathews H, Clendennen SK, Caldwell CG, Liu XL, Connors K, Matheis N, Schuster DK, Menasco DJ, Wagoner W, Lightner J, Wagner DR (2003) Activation tagging in tomato identifies a transcriptional regulator of anthocyanin biosynthesis, modification, and transport. Plant Cell 15:1689–1703. doi: 10.1105/Tpc.012963 PubMedPubMedCentralCrossRefGoogle Scholar
  97. McClintock B (1950) The origin and behavior of mutable loci in maize. Proc Natl Acad Sci 36:344–355PubMedPubMedCentralCrossRefGoogle Scholar
  98. McKenzie N, Dale PJ (2004) Mapping of transposable element Dissociation inserts in Brassica oleracea following plant regeneration from streptomycin selection of callus. Theor Appl Genet 109:333–341. doi: 10.1007/s00122-004-1629-5 PubMedCrossRefGoogle Scholar
  99. McLaughlin M, Walbot V (1987) Cloning of a mutable bz2 allele of maize by transposon tagging and differential hybridization. Genetics 117:771–776PubMedPubMedCentralGoogle Scholar
  100. Meissner R, Chague V, Zhu Q, Emmanuel E, Elkind Y, Levy AA (2000) A high throughput system for transposon tagging and promoter trapping in tomato. Plant J 22:265–274. doi: 10.1046/j.1365-313x.2000.00735.x PubMedCrossRefGoogle Scholar
  101. Mori M, Tomita C, Sugimoto K, Ooka H, Onodera H, Kajiwawra H, Tanaka H, Sekimoto H, Hirochika H, Kikuchi S (2003) Construction of the large scale activation tagging lines and characterization of a lesion mimic mutant. Plant Cell Physiol 44:S129Google Scholar
  102. Mori M, Nakamura H, Ichikawa H (2006) Characterization of the short grain mutant (Sg1) isolated by rice activation tagging. Plant Cell Physiol 47:S177Google Scholar
  103. Mori M, Tomita C, Sugimoto K, Hasegawa M, Hayashi N, Dubouzet JG, Ochiai H, Sekimoto H, Hirochika H, Kikuchi S (2007) Isolation and molecular characterization of a Spotted leaf 18 mutant by modified activation-tagging in rice. Plant Mol Biol 63:847–860. doi: 10.1007/s11103-006-9130-y PubMedCrossRefGoogle Scholar
  104. Murray EE, Rocheleau T, Eberle M, Stock C, Sekar V, Adang M (1991) Transposition of the maize activator element in transgenic rice plants. Plant Mol Biol 16:1035–1050PubMedCrossRefGoogle Scholar
  105. Nakajima K, Miyashima S, Waki T, Hashimoto T (2006) Identification of genes implicated in Arabidopsis root patterning by a GAL4/UAS activation tagging system. Plant Cell Physiol 47:S97CrossRefGoogle Scholar
  106. Nakazawa M, Ichikawa T, Ishikawa A, Suzuki K, Kobayashi H, Tsuhara Y, Kawashima M, Muto S, Matsui M (2003) Activation tagging, a novel tool to dissect the functions of a gene family. Plant Cell Physiol 44:S128Google Scholar
  107. Nilsson O, Moritz T, Sundberg B, Sandberg G, Olsson O (1996) Expression of the Agrobacterium rolC gene in a deciduous forest tree alters growth and development and leads to stem fasciation. Plant Physiol 112:493–502, PubMedPubMedCentralGoogle Scholar
  108. Niwa Y, Goto S, Nakano T, Sakaiya M, Hirano T, Tsukaya H, Komeda Y, Kobayashi H (2006) Arabidopsis mutants by activation tagging in which photosynthesis genes are expressed in dedifferentiated calli. Plant Cell Physiol 47:319–331. doi: 10.1093/Pcp/Pci242 PubMedCrossRefGoogle Scholar
  109. Ostergaard L, Yanofsky MF (2004) Establishment gene function by mutagenesis in Arabidopsis thaliana. Plant J 39:682–696. doi: 10.1111/j.1365-313X.2004.02149.x PubMedCrossRefGoogle Scholar
  110. Ouwerkerk PBF, de Kam RJ, Hoge JHC, Meijer AH (2001) Glucocorticoid-inducible gene expression in rice. Planta 213:370–378. doi: 10.1007/s004250100583 PubMedCrossRefGoogle Scholar
  111. Parinov S, Sevugan M, Ye D, Yang WC, Kumaran M, Sundaresan V (1999) Analysis of flanking sequences from Dissociation insertion lines: a database for reverse genetics in Arabidopsis. Plant Cell 11:2263–2270, PubMedPubMedCentralCrossRefGoogle Scholar
  112. Pereira A, Aarts M, van Agtmaal S, Stiekema WJ, Jacobson E (1991) Waxy variegation in transgenic potato. Maydica 36:323–327Google Scholar
  113. Perrella G, Cremona G, Consiglio F, Errico A, Bressan RA, Conicella C (2006) Screening for mutations affecting sexual reproduction after activation tagging in Arabidopsis thaliana. J Appl Genet 47:109–111. doi: 10.1007/BF03194608 PubMedCrossRefGoogle Scholar
  114. Plett JM, Wilkins O, Campbell MM, Ralph SG, Regan S (2010) Endogenous overexpression of Populus MYB186 increases trichome density, improves insect pest resistance, and impacts plant growth. Plant J 64:419–432. doi: 10.1111/j.1365-313X.2010.04343.x PubMedCrossRefGoogle Scholar
  115. Pogorelko GV, Fursova OV, Ogarkova OA, Tarasov VA (2008) A new technique for activation tagging in Arabidopsis. Gene 414:67–75. doi: 10.1016/j.gene.2008.02.008 PubMedCrossRefGoogle Scholar
  116. Qu S, Desai A, Wing R, Sundaresan V (2008) A versatile transposon-based activation tag vector system for functional genomics in cereals and other monocot plants. Plant Physiol 146:189–199. doi:10.1104/pp. 107.111427PubMedPubMedCentralCrossRefGoogle Scholar
  117. Quattrocchio F, Wing J, van der Woude K, Souer E, de Vetten N, Mol J, Koes R (1999) Molecular analysis of the anthocyanin2 gene of Petunia and its role in the evolution of flower color. Plant Cell 11:1433–1444, PubMedPubMedCentralCrossRefGoogle Scholar
  118. Raina S, Mahalingam R, Chen FQ, Fedoroff N (2002) A collection of sequenced and mapped Ds transposon insertion sites in Arabidopsis thaliana. Plant Mol Biol 50:93–110. doi: 10.1023/A:1016099215667 PubMedCrossRefGoogle Scholar
  119. Rommens CMT, Kneppers TJA, Haring MA, Nijkamp HJJ, Hille J (1991) A transposon tagging strategy with Ac on plant-cell level in heterologous plant species. Plant Sci 74:99–106CrossRefGoogle Scholar
  120. Rosin FM, Watanabe N, Cacas JL, Kato N, Arroyo JM, Fang Y, May B, Vaughn M, Simorowski J, Ramu U, McCombie RW, Spector DL, Martienssen RA, Lam E (2008) Genome-wide transposon tagging reveals location-dependent effects on transcription and chromatin organization in Arabidopsis. Plant J 55:514–525. doi: 10.1111/j.1365-313X.2008.03517.x PubMedCrossRefGoogle Scholar
  121. Rosso MG, Li Y, Strizhov N, Reiss B, Dekker K, Weisshaar B (2003) An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics. Plant Mol Biol 53:247–259. doi: 10.1023/B:PLAN.0000009297.37235.4a PubMedCrossRefGoogle Scholar
  122. Sakurai T, Satou M, Akiyama K, Iida K, Seki M, Kuromori T, Ito T, Konagaya A, Toyoda T, Shinozaki K (2005) RARGE: a large-scale database of RIKEN Arabidopsis resources ranging from transcriptome to phenome. Nucleic Acids Res 33:D647–D650. doi: 10.1093/nar/gki014 PubMedPubMedCentralCrossRefGoogle Scholar
  123. Schmidt RJ, Burr FA, Burr B (1987) Transposon tagging and molecular analysis of the maize regulatory locus opaque-2. Science 238:960–963. doi: 10.1126/science.2823388 PubMedCrossRefGoogle Scholar
  124. Schmülling T, Schell J, Spena A (1988) Single genes from Agrobacterium rhizogenes influence plant development. EMBO J 7:2621–2629PubMedPubMedCentralGoogle Scholar
  125. Schneider A, Kirch T, Gigolashvili T, Mock HP, Sonnewald U, Simon R, Flugge UI, Werr W (2005) A transposon-based activation-tagging population in Arabidopsis thaliana (TAMARA) and its application in the identification of dominant developmental and metabolic mutations. FEBS Lett 579:4622–4628. doi: 10.1016/j.febslet.2005.07.030 PubMedCrossRefGoogle Scholar
  126. Schneuwly S, Kuroiwa A, Gehring WJ (1987) Molecular analysis of the dominant homeotic Antennapedia phenotype. EMBO J 6:201–206PubMedPubMedCentralGoogle Scholar
  127. Scholz SC, Lörz H, Lütticke S (2001) Transposition of the maize transposable element Ac in barley (Hordeum vulgare L.). Mol Gen Genet 264:653–661. doi: 10.1007/s004380000351 PubMedCrossRefGoogle Scholar
  128. Seki M, Narusaka M, Kamiya A, Ishida J, Satou M, Sakurai T, Nakajima M, Enju A, Akiyama K, Oono Y, Muramatsu M, Hayashizaki Y, Kawai J, Carninci P, Itoh M, Ishii Y, Arakawa T, Shibata K, Shinagawa A, Shinozaki K (2002) Functional annotation of a full-length Arabidopsis cDNA collection. Science 296:141–145. doi: 10.1126/science.1071006 PubMedCrossRefGoogle Scholar
  129. Settles AM (2009) Transposon tagging and reverse genetics. In: Kriz AL, Larkins BA (eds) Molecular genetic approaches to maize improvement, biotechnology in agriculture and forestry, vol 63. Springer, Berlin, pp 143–159CrossRefGoogle Scholar
  130. Spena A, Aalen RB, Schulze SC (1989) Cell-autonomous behavior of the rolC gene of Agrobacterium rhizogenes during leaf development: a visual assay for transposon excision in transgenic plants. Plant Cell 1:1157–1164, PubMedPubMedCentralCrossRefGoogle Scholar
  131. Spradling AC, Rubin GM (1982) Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218:341–347. doi: 10.1126/science.6289435 PubMedCrossRefGoogle Scholar
  132. Suzuki Y, Uemura S, Saito Y, Murofushi N, Schmitz G, Theres K, Yamaguchi I (2001) A novel transposon tagging element for obtaining gain-of-function mutants based on a self-stabilizing Ac derivative. Plant Mol Biol 45:123–131. doi: 10.1023/A:1006455130098 PubMedCrossRefGoogle Scholar
  133. Szabados L, Kovács I, Oberschall A, Ábrahám E, Kerekes I, Zsigmond L, Nagy R, Alvarado M, Krasovskaja I, Gál M, Berente A, Rédei GP, Haim AB, Koncz C (2002) Distribution of 1000 sequenced T-DNA tags in the Arabidopsis genome. Plant J 32:233–242. doi: 10.1046/j.1365-313X.2002.01417.x PubMedCrossRefGoogle Scholar
  134. Tacke E, Korfhage C, Michel D, Maddaloni M, Motto M, Lanzini S, Salamini F, Döring HP (1995) Transposon tagging of the maize Glossy2 locus with the transposable element En/Spm. Plant J 8:907–917. doi: 10.1046/j.1365-313X.1995.8060907.x PubMedCrossRefGoogle Scholar
  135. Tani H, Chen X, Nurmberg P, Grant JJ, SantaMaria M, Chini A, Gilroy E, Birch PR, Loake GJ (2004) Activation tagging in plants: a tool for gene discovery. Funct Integr Genomics 4:258–266. doi: 10.1007/s10142-004-0112-3 PubMedCrossRefGoogle Scholar
  136. Trupiano D, Yordanov Y, Regan S, Meilan R, Tschaplinski T, Scippa GS, Busov V (2013) Identification, characterization of an AP2/ERF transcription factor that promotes adventitious, lateral root formation in Populus. Planta 238:271–282. doi: 10.1007/s00425-013-1890-4 PubMedCrossRefGoogle Scholar
  137. Tsay HS, Ho HM, Gupta SK, Wang CS, Chen PT, Chen ECF (2012) Development of pollen mediated activation tagging system for Phalaenopsis and Doritaenopsis. Electron J Biotechnol 15(4):9. doi: 10.2225/vol15-issue4-fulltext-1 Google Scholar
  138. Tuskan GA, Difazio S, Jansson S et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604. doi: 10.1126/science.1128691 PubMedCrossRefGoogle Scholar
  139. van der Fits L, Hilliou F, Memelink J (2001) T-DNA activation tagging as a tool to isolate regulators of a metabolic pathway from a genetically non-tractable plant species. Transgenic Res 10:513–521PubMedCrossRefGoogle Scholar
  140. van der Graaff E, Den Dulk-Ras A, Hooykaas PJJ, Keller B (2000) Activation tagging of the LEAFY PETIOLE gene affects leaf petiole development in Arabidopsis thaliana. Development 127:4971–4980PubMedGoogle Scholar
  141. Van Sluys MA, Temp J, Fedoroff N (1987) Studies on the introduction and mobility of the maize activator element in Arabidopsis thaliana and Daucus carota. EMBO J 6:3881–3889PubMedPubMedCentralGoogle Scholar
  142. Waki T, Miyashima S, Nakanishi M, Ikeda Y, Hashimoto T, Nakajima K (2013) A GAL4-based targeted activation tagging system in Arabidopsis thaliana. Plant J 73:357–367. doi: 10.1111/Tpj.12049 PubMedCrossRefGoogle Scholar
  143. Walbot V (1992) Strategies for mutagenesis and gene cloning using transposon tagging and T-DNA insertional mutagenesis. Annu Rev Plant Physiol Plant Mol Biol 43:49–82CrossRefGoogle Scholar
  144. Walden R, Fritze K, Hayashi H, Miklashevichs E, Harling H, Schell J (1994) Activation tagging—a means of isolating genes implicated as playing a role in plant-growth and development. Plant Mol Biol 26:1521–1528. doi: 10.1007/978-94-011-0239-1_16 PubMedCrossRefGoogle Scholar
  145. Wan SY, Wu JX, Zhang ZG, Sun XH, Lv Y, Gao C, Ning YD, Ma J, Guo YP, Zhang Q, Zheng X, Zhang CY, Ma ZY, Lu TG (2009) Activation tagging, an efficient tool for functional analysis of the rice genome. Plant Mol Biol 69:69–80. doi: 10.1007/s11103-008-9406-5 PubMedCrossRefGoogle Scholar
  146. Weigel D, Ahn JH, Blazquez MA, Borevitz JO, Christensen SK, Frankhauser C, Ferrandiz C, Kardailsky I, Malancharuvil EJ, Neff MM, Nguyen JT, Sato S, Wang ZY, Xia Y, Dixon RA, Harrison MJ, Lamb CJ, Yanofsky MF, Chory J (2000) Activation tagging in Arabidopsis. Plant Pysiol 122:1003–1013, Google Scholar
  147. Whitham S, Dinesh-Kumar SP, Choi D, Hehl R, Corr C, Baker B (1994) The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell 78:1101–1115. doi: 10.1016/0092-8674(94)90283-6 PubMedCrossRefGoogle Scholar
  148. Woodward C, Bemis SM, Hill EJ, Sawa S, Koshiba T, Torii KU (2005) Interaction of auxin and ERECTA in elaborating Arabidopsis inflorescence architecture revealed by the activation tagging of a new member of the YUCCA family putative flavin monooxygenases. Plant Physiol 139:192–203, PubMedPubMedCentralCrossRefGoogle Scholar
  149. Yoder JI, Palys J, Alpert K, Lassner M (1988) Ac transposition in transgenic tomato plants. Mol Gen Genet 213:291–296CrossRefGoogle Scholar
  150. Yordanov YS, Ma C, Strauss SH, Busov VB (2014) EARLY BUD-BREAK 1 (EBB1) is a regulator of release from seasonal dormancy in poplar trees. Proc Natl Acad Sci USA 111:10001–10006. doi: 10.1073/pnas.1405621111 PubMedPubMedCentralCrossRefGoogle Scholar
  151. Yu J, Hu S, Wang J et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296:79–92. doi: 10.1126/science.1068037 PubMedCrossRefGoogle Scholar
  152. Zubko E, Adams CJ, Machaekova I, Malbeck J, Scollan C, Meyer P (2002) Activation tagging identifies a gene from Petunia hybrida responsible for the production of active cytokinins in plants. Plant J 29:797–808. doi: 10.1046/j.1365-313X.2002.01256.x PubMedCrossRefGoogle Scholar

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© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Thünen-Institute of Forest GeneticsGrosshansdorfGermany

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