Advertisement

Plant Molecular Biology

, Volume 64, Issue 3, pp 329–347 | Cite as

A barley activation tagging system

  • Michael A. AyliffeEmail author
  • Margaret Pallotta
  • Peter Langridge
  • Anthony J. Pryor
Article

Abstract

Activation tagging, as the result of random genomic insertion of either promoter or enhancer sequences, can produce novel, dominant mutations by over-expression of endogenous genes. This powerful genomics tool has been used extensively in dicot species such as Arabidopsis, while rice is the only cereal for which an equivalent system exists. In this study we describe an activation tagging system in barley based upon the maize Ac/Ds transposable element system. A modified Ds element (UbiDs) containing two maize polyubiquitin promoters, transposed in families derived from multiple independent UbiDs transformants and generated new Ds insertion events at frequencies ranging from 0% to 52% per family. The majority of transposed UbiDs elements activated high levels of adjacent flanking sequence transcription. Transposon-mediated expression was detected in all barley cell and tissue types analysed suggesting that this system is applicable to all aspects of plant development and biogenesis. In addition to transcriptional activation, this system is also capable of generating insertional knockout mutants and a UbiDs inactivated allele of the granule bound starch synthase I gene (waxy) was recovered that lead to reduced amylose accumulation. The recovery and analysis of dominant over-expression phenotypes generated by this system will provide a novel approach to understanding gene function in large cereal genomes where gene redundancy may mask conventional loss-of-function mutations.

Keywords

Activation tagging Barley Mutagenesis Overexpression Transposon 

Notes

Acknowledgments

We wish to thank Pat Atkinson, Lejla Buza, Luch Hac, Craig Jackson, Kim Newell, Terese Richardson and Libby Viccars for technical support, Celia Miller and Dr Rosemary White for microscopy assistance, Patricia Warner for flanking sequence isolation and Dr Narayana Upadhyaya for providing pUR224NA and a Ubi-transposase clone. This work was financially supported, in part, by the Grains Research and Development Corporation as part of the Australian Cereal Rust Control Program.

References

  1. An G, Lee S, Kim S-H, Kim S-R (2005) Molecular genetics using T-DNA in rice. Plant Cell Physiol 46:14–22PubMedCrossRefGoogle Scholar
  2. Ahad A, Wolf J, Nick P (2003) Activation-tagged tobacco mutants that are tolerant to antimicrotubular herbicides are cross-resistant to chilling stress. Trans Res 12:615–629CrossRefGoogle Scholar
  3. Ayliffe MA, Frost DV, Finnegan EJ, Lawrence GJ, Anderson PA, Ellis JG (1999) Analysis of alternative transcripts of the flax L6 rust resistance gene. Plant J 17:287–292PubMedCrossRefGoogle Scholar
  4. Ayliffe MA, Pryor AJ (2007) Activation tagging in plants - generation of novel, gain-of-function mutations. Aust J Agric Res vol. 58 (in press)Google Scholar
  5. Bancroft I, Dean C (1993) Transposition pattern of the maize element Ds in Arabidopsis thaliana. Genetics 134:1221–1229PubMedGoogle Scholar
  6. Benfey PN, Chua N-H (1989) The CaMV 35S enhancer contains at least two domains which can confer different developmental and tissue-specific patterns. EMBO J 8:2195–2202PubMedGoogle Scholar
  7. Borevitz JO, Xia Y, Blount J, Dixon RA, Lamb C (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12:2382–2394CrossRefGoogle Scholar
  8. Bouche N, Bouchez D (2001) Arabidopsis gene knockout: phenotypes wanted. Curr Opin Plant Biol 4:111–117PubMedCrossRefGoogle Scholar
  9. Busov VB, Meilan R, Pearce DW, Ma C, Rood SB, Strauss SH (2003) Activation tagging of a dominant gibberellin catabolism gene (GA2-oxidase) from popular that regulates tree stature. Plant Physiol 132:1283–1291PubMedCrossRefGoogle Scholar
  10. Chalfun-Junior A, Franken J, Mes JJ, Marsch-Martinez N, Pereira A, Angenent GC (2005) ASYMETRIC LEAVES2-LIKE1 gene, a member of the AS2/LOB family, controls proximal-distal patterning in Arabidopsis petals. Plant Mol Biol 57:559–575PubMedCrossRefGoogle Scholar
  11. Christensen AH, Sharrock RA, Quail PH (1992) Maize polyubiquitin genes: structure, thermal perturbation of expression and transcript splicing, and promoter activity following transfer to protoplast by electroporation. Plant Mol Biol 18:675–689PubMedCrossRefGoogle Scholar
  12. Chung JH, Whiteley M, Felsenfeld G (1993) A 5′ element of the chicken B-globin domain serves as an insulator in human erythroid cells and protects against position effects in Drosophilia. Cell 74:505–514PubMedCrossRefGoogle Scholar
  13. Collins NC, Drake J, Ayliffe MA, Sun Q, Ellis J, Hulbert S, Pryor T (1999) Molecular characterization of the Rp1-D rust resistance haplotype and its mutants. Plant Cell 11:1365–1376PubMedCrossRefGoogle Scholar
  14. Cooper LD, Marquez-Cedillo L, Singh J, Sturbaum AK, Zhang S, Edwards V, Johnson K, Kleinhofs A, Rangel S, Carollo V, Bregitzer P, Lemaux PG, Hayes PM (2004) Mapping Ds insertions in barley using a sequence-based approach. Mol Gen Genomics 272:181–193CrossRefGoogle Scholar
  15. DeBlock M, Botterman J, Vandewiele M, Dockx J, Thoen C, Gossele V, Rao Movva N, Thompson C, Van Montagu M, Leemans J (1987) Engineering herbicide resistance in plants by expression of a detoxifying enzyme. EMBO J 6:2513–2518Google Scholar
  16. Domon E, Saito A, Takeda K (2002) Comparison of the waxy locus sequence from a non-waxy strain and two waxy mutants of spontaneous and artificial origins in barley. Genes Genet Syst 77:351–359PubMedCrossRefGoogle Scholar
  17. Dooner HK, Belachew A (1989) Transposition pattern of the maize Ac form bz-M2 (Ac) allele in maize. Genetics 122:447–457PubMedGoogle Scholar
  18. Dooner HK, Keller J, Harper E, Ralston E (1991) Variable patterns of transposition of the maize element Activator in tobacco. Plant Cell 3:473–482PubMedCrossRefGoogle Scholar
  19. Fridborg I., Kuusk S, Moritz T, Sundberg E (1999) The Arabidopsis dwarf mutant shi exhibits reduced gibberellin responses conferred by overexpression of a new putative zinc finger protein. Plant Cell 11:1019–1031PubMedCrossRefGoogle Scholar
  20. Furini A, Koncz C, Salamini F, Bartels D (1997) High level transcription of a member of a repeated gene family confers dehydration tolerance to callus tissue of Craterostigma plantagineum. EMBO J 16:3599–3608PubMedCrossRefGoogle Scholar
  21. Gu Z, Steinmetz LM, Gu X, Scharfe C, Davis RW, Li W-H (2003) Role of duplicate genes in genetic robustness against null mutations. Nature 421:63–66PubMedCrossRefGoogle Scholar
  22. Goff SA, Ricke D, Lan T-H, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H, Hadley D, Hutchison D, Martin C, Katagiri F, Lange BM, Moughamer T, Xia Y, Budworth P, Zhong, Miguel T, Paszkowski U, Zhang S, Colbert M, Sun W-L, Chen L, Cooper B, Park S, Wood TC, Mao L, Quail P, Wing R., Dean R, Yu Y, Zharkikh A, Shen R, Sahasrabudhe S, Thomas A, Cannings R, Gutin A, Pruss D, Reid J, Tavtigian S, Mitchell J, Eldredge G, Scholl T, Miller RM, Bhatnagar S, Ade N, Rubano T, Tusneem N, Robinson R, Feldhaus J, Macalma T, Oliphant A, Briggs S (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:92–100PubMedCrossRefGoogle Scholar
  23. Greco R, Ouwerkerk PB, Taal AJ, Favalli C, Beguiristain T, Puigdomenech P, Colombo L, Hoge JH, Pereira A (2001) Early and multiple Ac transpositions in rice suitable for efficient insertional mutagenesis. Plant Mol Biol 46:215–227PubMedCrossRefGoogle Scholar
  24. Hsing Y-I, Chern C-G, Fan M-J, Lu P-C, Chen KT, Lo S-F, Sun P-K, Ho S-L, Lee K-W, Wang Y-C, Huang W-L, Ko S-S, Chen S, Chen J-L, Chung C-I., Lin Y-C, Hour A-L, Wang Y-W, Chang Y-C, Tsai M-W, Lin Y-S, Chen Y-C, Yen H-M, Li C-P, Wey C-K, Tseng C-S, Lai M-H, Huang S-C, Chen L-J, Yu S-M (2007) A rice activation/knockout mutant resource for high throughput functional genomics. Plant Mol Biol 63:351–364PubMedCrossRefGoogle Scholar
  25. International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800Google Scholar
  26. Ito T, Meyerowitz EM (2000) Overexpression of a gene encoding a cytochrome P450, CYP78A9, induces large seedless fruit in Arabidopsis. Plant Cell 12:1541–1550PubMedCrossRefGoogle Scholar
  27. Ito Y, Eiguchi M, Kurata N (2004) Establishment of an enhancer trap system with Ds and GUS for functional genomics in rice. Mol Gen Genomics 271:639–650CrossRefGoogle Scholar
  28. Izawa T, Ohnishi T, Nakano T, Ishida N, Eoki H, Hashimoto H, Itoh K, Terada R, Wu C, Miyazaki C, Endo T, Iida S, Shimamoto K (1997) Transposon tagging in rice. Plant Mol Biol 35:219–229PubMedCrossRefGoogle Scholar
  29. Jeong D-H, An S, Kang H-G, Moon S, Han J-J, Park S, Lee H.S, An K, An G (2002) T-DNA insertional mutagenesis for activation tagging in rice. Plant Physiol 130:1636–1644PubMedCrossRefGoogle Scholar
  30. Jeong D-H, An S, Park S, Kang H-G, Park G-G, Kim S-R, Sim J, Kim Y-O, Kim M-K, Kim S-R, Kim J, Shin M, Jung M, An G (2006) Generation of a flanking sequence-tag database for activation-tagging lines in japonica rice. Plant J 45:123–132PubMedCrossRefGoogle Scholar
  31. Jones JDG, Carland F, Lim E, Ralston E, Dooner HK (1990) Preferential transposition of the maize element Activator to linked chromosomal location in tobacco. Plant Cell 2:701–708PubMedCrossRefGoogle Scholar
  32. 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 286:1962–1965PubMedCrossRefGoogle Scholar
  33. Kakimoto T (1996) CKI1, a histidine kinase homolog implicated in cytokinin signal transduction. Science 274:982–985PubMedCrossRefGoogle Scholar
  34. Kim CM, Je BI, Piao HL, Park SJ, Kim MJ, Park SH, Park JY, Park SH, Lee EK, Chon NS, Won YJ, Lee GH, Nam MH, Yun DW, Lee MC, Cha YS, Lee KH, Eun MY, Han CD (2002) Reprogramming of the activity of the activator/dissociation transposon family during plant regeneration in rice. Mol Cells 14:231–237PubMedGoogle Scholar
  35. Kirik V, Simon M, Huelskamp M, Schiefelbein J (2004) The ENHANCER OF TRY AND CPC1 gene acts redundantly with TRIPTYCHON and CAPRICE in trichome and root hair cell patterning in Arabidopsis. Dev Biol 286:506–513CrossRefGoogle Scholar
  36. Klosgen RB, Gierl A, Schwarz-Sommer Z, Saedler H (1986) Molecular analysis of the waxy locus of Zea mays. Mol Gen Genet 203:237–244CrossRefGoogle Scholar
  37. Koes R, Souer E, van Houwelingen AV, Mur L, Spelt C, Quattrocchio F, Wing J, Oppedijk B, Ahmed S, Maes T, Gerats T, Hoogeveen P, Meesters M, Kloos D, Mol JNM (1995) Targeted Gene Inactivation in Petunia by PCR-Based Selection of Transposon Insertion Mutants. Proc Natl Acad Sci USA 92:8149–8153PubMedCrossRefGoogle Scholar
  38. Kolesnik T, Szeverenyi I., Bachmann D, Kumar CS, Jiang S, Ramamoorthy R, Cai M, Ma ZG, Sundaresan V, Ramachandran S (2004) Establishing an efficient Ac/Ds tagging system in rice: large-scale analysis of Ds flanking sequences. Plant J 37:301–314PubMedGoogle Scholar
  39. Koprek T, McElroy D, Louwerse J, Williams-Carrier R, Lemaux PG (2000) An efficient method for dispersing Ds elements in the barley genome as a tool for determining gene function. Plant J 24:253–263PubMedCrossRefGoogle Scholar
  40. Koprek T, Rangel S, McElroy D, Louwerse JD, Williams-Carrier RE, Lemaux PG (2001) Transposon-mediated single-copy gene delivery leads to increased transgene expression stability in barley. Plant Physiol 125:1354–1362PubMedCrossRefGoogle Scholar
  41. Krysan PJ, Young JC, Sussman MR (1999) T-DNA as an insertional mutagen in Arabidopsis. Plant Cell 11:2283–2290PubMedCrossRefGoogle Scholar
  42. Kumar SC, Narayanan KK (1997) Gene and enhancer trap constructs for isolating genetic regions from rice. Rice Biotechnol Quart 31:17–18Google Scholar
  43. Lee H, Suh SS, Park E, Cho E, Ahn JH, Kin SG, Lee JS, Kwon YM, Lee I (2000) The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev 14:2366–2376PubMedCrossRefGoogle Scholar
  44. Li J, Lease KA, Tax FE, Walker JC (2001) BRS1, a serine carboxypeptidase, regulates BRI1 signalling in Arabidopsis thaliana. Proc Natl Acad Sci USA 98:5916–59121PubMedCrossRefGoogle Scholar
  45. Li J, Wen J, Lease KA, Doke JT, Tax FE, Walker JC (2002) BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110:213–222PubMedCrossRefGoogle Scholar
  46. Liu Y-G, Mitsukawa N, Oosumi T, Whittier R (1995) Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J 8:457–463PubMedCrossRefGoogle Scholar
  47. 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 129:1544–1556PubMedCrossRefGoogle Scholar
  48. Matsubayashi Y, Ogawa M, Morita A, Sakagami Y (2002) An LRR receptor kinase involved in perception of a peptide plant hormone, phytosulfokine. Science 296:1470–1472PubMedCrossRefGoogle Scholar
  49. Messiner 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 22:265–274CrossRefGoogle Scholar
  50. Mora-Garcia S, Vert G, Yin Y, Cano-Delgado A, Cheong H, Chory J (2004) Nuclear protein phosphatases with Kelch-repeat domains modulate the response to brassinosteriods in Arabidopsis. Genes Dev 18:448–460PubMedCrossRefGoogle Scholar
  51. 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 DOI 10.1007/s11103-006-9130-yGoogle Scholar
  52. Nakagawa Y, Machida C, Mahida Y, Toriyama K (2000) Frequency and pattern of transposition of the maize transposable element Ds in transgenic rice plants. Plant Cell Physiol 41:733–742PubMedGoogle Scholar
  53. Nakazawa M, Ichikawa T, Ishikawa A, Kobayashi H, Tsuhara Y, Kawashima M, Suzuki K, Muto S, Matsui M (2003) Activation tagging, a novel tool to dissect the functions of a gene family. Plant J 34:741–750PubMedCrossRefGoogle Scholar
  54. Neff MM, Nguyen SM, Malancharuvil EJ, Fujioka S, Noguchi T, Seto H, Tsubuki M, Honda T, Takasuto S, Yoshida S, Chory J (1999) BAS1: a gene regulating brassinosteroid levels and light responsiveness in Arabidopsis. Proc Natl Acad Sci USA 96:15316–15323PubMedCrossRefGoogle Scholar
  55. Nelson OE, Rines HW (1962) The enzymatic deficiency in the waxy mutant of maize. Biochem Biophys Res Commun 9:297–300PubMedCrossRefGoogle Scholar
  56. Nussaume L, Harrison K, Klimyuk V, Martienssen R, Sundaresan V, Jones JDG (1995) Analysis of splice donor and acceptor site function in a transposable gene trap derived from the maize element Activator. Mol Gen Genet 249:91–101PubMedCrossRefGoogle Scholar
  57. Parinov S, Sundaresan V (2000) Functional genomics in Arabidopsis: large-scale insertional mutagenesis complements the genome sequencing project. Curr Opin Biotechnol 11:157–161PubMedCrossRefGoogle Scholar
  58. Parinov S, Sevugan M, Ye D, Yang W-C, Kumaran M, Sundaresan V (1999) Analysis of flanking sequences from Dissociation insertion lines: a database for reverse genetics in Arabidopsis. Plant Cell 1:2263–2270CrossRefGoogle Scholar
  59. Pohlman RF, Fedoroff NV, Messing J (1984) The nucleotide sequence of the maize controlling element Activator. Cell 37:635–643PubMedCrossRefGoogle Scholar
  60. Raina S, Mahalingham R, Chen F, Federoff N (2002) A collection of sequenced and mapped Ds transposon insertion sites in Arabidopsis thaliana. Plant Mol Biol 50:93–110PubMedCrossRefGoogle Scholar
  61. Rohde W, Becker D, Salamini F (1988) Structural analysis of the waxy locus from Hordeum vulgare. Nucleic Acids Res 16:7185–7186PubMedCrossRefGoogle Scholar
  62. Rorth P (1996) A modular misexpression screen in Drosophilia detecting tissue specific phenotypes. Proc Natl Acad Sci USA 93:12418–12422PubMedCrossRefGoogle Scholar
  63. Rorth P, Szabo K, Bailey A, Laverty T, Rehm J, Rubin GM, Weigmann K, Milan M, Benes V, Ansorge W, Cohen SM (1998) Systematic gain-of-function genetics in Drosophila. Development 125:1049–1057PubMedGoogle Scholar
  64. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual (2nd edn) Cold Spring Harbour Laboratory Press, Cold Spring Harbour, NYGoogle Scholar
  65. Schafer R, Ramsay N, Samach A, Corden S, Putterill J, Carre IA., Coupland G (1998) The late elongated hypocotyl muatation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell 93:1219–1229CrossRefGoogle Scholar
  66. Schneider A, Kirch T, Gigolashvili T, Mock H-P, Sonnewald U, Simon R, Flugge U-I, 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 579:4622–4628PubMedCrossRefGoogle Scholar
  67. Scholz S, Lorz H, Lutticke S (2001) Transposition of the maize Ac transposable element Ac in barley (Hordeum vulgare L.) Mol Gen Genomics 264:653–661Google Scholar
  68. Schroeder HE, Schotz AH, Wardley-Richardson T, Spencer D, Higgins TJV (1993) Transformation and regeneration of two cultivars of pea (Pisum sativum L.) Plant Physiol 101:751–757PubMedCrossRefGoogle Scholar
  69. Shure M, Wessler S, Fedoroff N (1983) Molecular identification and isolation of the waxy locus in maize. Cell 35:225–233PubMedCrossRefGoogle Scholar
  70. Singh J, Zhang S, Chen C, Cooper L, Bregitzer P, Sturbaum A, Hayes PM, Lemaux PG (2006) High frequency Ds remobilization over multiple generations in barley facilitates tagging in large genome cereals. Plant Mol Biol 62:937–950PubMedCrossRefGoogle Scholar
  71. Sundaresan V, Springer P, Volpe T, Haward S, Jones JDG, Dean C, Ma H, Martienssen R (1995) Patterns of gene action in plant development revealed by enhancer trap and gene trap retrotransposable elements. Genes Dev 9:1797–1810PubMedCrossRefGoogle Scholar
  72. Tani H, Chen X, Nurmberg P, Grant JJ, SantaMaria M, Chini A, Gilroy E, Birch PRJ, Loake GJ (2004) Activation tagging in plants: a tool for gene discovery. Funct Integr Genomics 4:258–266PubMedCrossRefGoogle Scholar
  73. The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815Google Scholar
  74. Thompson CJ, Movva NR, Tizard R, Crameri R, Davies JE, Lauwereys M, Botterman J (1987) Characterization of the herbicide-resistance gene bar from Streptomyces hygroscopicus. EMBO J 6:2519–2523PubMedGoogle Scholar
  75. Tingay S, McElroy D, Kalla R, Fieg S, Wang M, Thornton S, Brettell R (1997) Agrobacterium tumefacians-mediated barley transformation. Plant J 11:1369–1376CrossRefGoogle Scholar
  76. Upadhyaya NM, Zhou X-R, Zhu Q-H, Ramm K, Wu L, Eamen A, Sivakumar R, Kato T, Yun D-W, Santhoshkumar C, Narayanan KK, Peacock JW, Dennis ES (2002) An iAc/Ds gene and enhancer trapping system for insertional mutagenesis in rice. Funct Plant Biol 29:547–559CrossRefGoogle Scholar
  77. Upadhyaya NM, Zhu Q-H, Zhou X-R, Eamens AL, Hoque MS, Ramm K, Shivakkumar R, Smith KF, Pan S-T, Li S, Peng K, Kim SJ, Dennis ES (2006) Dissociation (Ds) constructs, mapped Ds launch pads and a transiently-expressed transposase system suitable for localized insertional mutagenesis in rice. Theoret Applied Genet 112:1326–1341CrossRefGoogle Scholar
  78. Van der Fits L, Memelink J (2000) ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science 289:295–297PubMedCrossRefGoogle Scholar
  79. Van der Graaff E, Dulk-Ras AD, Hooykaas PJ, Keller B (2000) Activation tagging of the LEAFY PETIOLE gene affects leaf petiole development in Arabidopsis thaliana. Development 127:4971–4980PubMedGoogle Scholar
  80. Van der Graaff E, Hooykaas PJJ, Keller B (2002) Activation tagging of the two closely linked genes LEP and VAS independently affects vascular cell number. Plant J 32:819–830PubMedCrossRefGoogle Scholar
  81. Weigel D, Ahn JH, Blazquez MA, Borevitz JO, Christensen SK, Fankhauser C, Ferrandiz C, Kardailsky I., Malancharuvil EJ, Neff MM, Nguyen JT, Sato S, Wang Z-Y, Xia Y, Dixon RA, Harrison MJ, Lamb CJ, Yanofsky MF, Chory J (2000) Activation tagging in Arabidopsis. Plant Physiol 122:1003–1013PubMedCrossRefGoogle Scholar
  82. Wen J, Lease KA, Walker JC (2004) DVL, a novel class of small polypepetides: overexpression alters Arabidopsis development. Plant J 37:668–677PubMedCrossRefGoogle Scholar
  83. Wesley SV, Helliwell CA, Smith NA, Wang MB, Rouse DT, Liu Q, Gooding PS, Singh SP, Abbott D, Stoutjesdijk PA, Robinson SP, Gleave AP, Green AG, Waterhouse PM (2001) Construct design for efficient, effective and high-throughput gene silencing in plants. Plant J 27:581–590PubMedCrossRefGoogle Scholar
  84. Wessler SR (1989) The splicing of maize transposable elements from pre-mRNA—a minireview. Gene 82:127–133PubMedCrossRefGoogle Scholar
  85. Wilson K, Long D, Swinburne J, Coupland G (1996) A Dissociation insertion causes a semidominant mutation that increases expression of TINY, an Arabidopsis gene related to APETALA2. Plant Cell 8:659–671PubMedCrossRefGoogle Scholar
  86. 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 139:192–203PubMedCrossRefGoogle Scholar
  87. Zhao Y, Christensen SK, Fankhauser C, Cashman JR, Cohen JD, Weigel D, Chory J (2001) A role for flavin monooxygenase-like exzymes in auxin biosynthesis. Science 291:306–309PubMedCrossRefGoogle Scholar
  88. Zhao T, Palotta M, Langridge P, Prasad M, Graner A, Schulze-Lefert P, Koprek T (2006) Mapped Ds/T-DNA launch pads for functional genomics in barley. Plant J 47:811–826PubMedCrossRefGoogle Scholar
  89. 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 29:797–808PubMedCrossRefGoogle Scholar
  90. Zhou A, Wang H, Walker JC, Li J (2004) BRL1, a leucine-rich repeat receptor-like protein kinase, is functionally redundant with BRI1 in regulating Arabidopsis brassinosteriod signaling. Plant J 40:399–409PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Michael A. Ayliffe
    • 1
    Email author
  • Margaret Pallotta
    • 2
  • Peter Langridge
    • 2
  • Anthony J. Pryor
    • 1
  1. 1.CSIRO Plant IndustryCanberraAustralia
  2. 2.Australian Centre for Plant Functional GenomicsPlant Genomics CentreUrrbraeAustralia

Personalised recommendations