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Resources for Reverse Genetics Approaches in Arabidopsis thaliana

  • Bekir ÜlkerEmail author
  • Bernd Weisshaar
Chapter
Part of the Plant Genetics and Genomics: Crops and Models book series (PGG, volume 9)

Abstract

Having many characteristics of an ideal experimental system, Arabidopsis thaliana became a very important model system for flowering plants. Its completed genome sequence data provided scientists the first fundamental tool towards understanding its genome structure and genes that it possess. There are more than 33,000 predicted genes in Arabidopsis and this number is increasing as novel methods develop and our understanding of genome organization and regulation expands. Reverse genetics that aim to reveal the functions of all Arabidopsis genes and the related resources were next most important tools that plant scientists needed. Numerous consortia were formed to supply scientists with such resources and tools necessary to determine the functions of Arabidopsis genes. Thanks to these international community efforts, now there are around 426,000 independent T-DNA/transposon insertion lines representing near saturation of all genes in Arabidopsis available for the research community. Besides insertion lines, several other sophisticated technologies and resources crucial for large-scale gene function studies in Arabidopsis were also developed. In this chapter, we discuss most of these important reverse genetics resources for gene function analysis.

Keywords

Reverse genetics Arabidopsis T-DNA Transposon Activation tagging Knockout T-DNA insertion collections T-DNA vectors Agrobacterium TILLING EcoTILLING Deleteagene Zink finger nuclease Homologous recombination Gene silencing Antisense RNAi MicroRNA miRNA Microarray Gene trap Promoter trap Enhancer trap Overexpression Mutant EMS mutagenesis Fast neutron bombardment SALK Gabi-Kat FLAGdb SAIL 

Abbreviations

Ac/Ds

Activator/dissociation

AchrDNA

Agrobacterium chromosomal DNA

AGI

Arabidopsis genome initiative

AGRICOLA

Arabidopsis genomic RNAi knock-out line analysis

AMAZE/ZIGIA

Arabidopsis En-1 transposon insertion lines from Max-Planck-institute for plant breeding, Cologne

amiRNAs

artificial microRNAs

CaMV

Cauliflower mosaic virus

BLAST

Basic local alignment search tool

DHPLC

High-performance liquid chromatography

dsRNA

double-stranded RNA

EMS

Ethylmethanesulfonate

En/Spm

Enhancer/supressor–mutator

FLAGdb

Functional analysis of the Arabidopsis genome database, also known as INRA/Versailles lines

FST

Flanking sequence tag

GABI-Kat

Genomanalyse im biologischen System Pflanze Arabidopsis T-DNA lines

GFP

Green fluorescent protein

GUS

β-glucuronidase

LUC

Luciferase protein

INDELS

Insertions/deletions

MASC

Multinational Arabidopsis steering committee

MIPS

The Munich Institute for Protein Sequences

miRNAs

microRNAs

NASC

Nottingham Arabidopsis stock centre

PCR

Polymerase chain reaction

SNPs

Single nucleotide polymorphisms

SLAT

Sainsbury laboratory Arabidopsis thaliana transposants

SAIL

Syngenta Arabidopsis insertion library, formerly known as GARLIC (Gilroy Arabidopsis reverse lethal insertion collection)

SALK

SALK institute T-DNA insertion lines

siRNA

small interfering RNA

TAIR

The Arabidopsis information resource

TAIL PCR

Thermal asymmetric interlaced polymerase chain reaction

TAMARA

Transposable element-mediated activation tagging mutagenesis in Arabidopsis

taRNAs

Transacting RNAs

T-DNA

Transferred DNA

TILLING

Targeting-Induced Local Lesions In Genomes

tiling arrays

Arrays that cover the whole genome

Ti plasmid

Tumour inducing plasmid

TT1

Arabidopsis transparent testa 1 protein

uidA

Gene coding for β-glucuronidase

ZFN

Zinc finger nuclease

References

  1. Aarts MG, Corzaan P, Stiekema WJ, Pereira A (1995) A two-element enhancer-inhibitor transposon system in Arabidopsis thaliana. Mol Gen Genet 247:555–564PubMedGoogle Scholar
  2. Aboul-Soud MA, Chen X, 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(4):1163–1175PubMedGoogle Scholar
  3. Agrawal N, Dasaradhi PV, Mohmmed A, Malhotra P, Bhatnagar RK, Mukherjee SK (2003) RNA interference: biology, mechanism, and applications. Microbiol Mol Biol Rev 67:657–685PubMedGoogle Scholar
  4. Alonso JM, Ecker JR (2006) Moving forward in reverse: genetic technologies to enable genome-wide phenomic screens in Arabidopsis. Nat Rev Genet 7:524–536PubMedGoogle Scholar
  5. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657PubMedGoogle Scholar
  6. Altmann T, Felix G, Jessop A, Kauschmann A, Uwer U, Pena-Cortes H, Willmitzer L (1995) Ac/Ds transposon mutagenesis in Arabidopsis thaliana: mutant spectrum and frequency of Ds insertion mutants. Mol Gen Genet 247:646–652PubMedGoogle Scholar
  7. Alvarado MC, Zsigmond LM, Kovacs I, Cseplo A, Koncz C, Szabados LM (2004) Gene trapping with firefly luciferase in Arabidopsis. Tagging of stress-responsive genes. Plant Physiol 134:18–27PubMedGoogle Scholar
  8. Alvarez JP, Pekker I, Goldshmidt A, Blum E, Amsellem Z, Eshed Y (2006) Endogenous and synthetic microRNAs stimulate simultaneous, efficient, and localized regulation of multiple targets in diverse species. Plant Cell 18:1134–1151PubMedGoogle Scholar
  9. Arabidiopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815Google Scholar
  10. Balzergue S, Dubreucq B, Chauvin S, Le-Clainche I, Le Boulaire F, de Rose R, Samson F, Biaudet V, Lecharny A, Cruaud C et al (2001) Improved PCR-walking for large-scale isolation of plant T-DNA borders. Biotechniques 30:496–498, 502, 504PubMedGoogle Scholar
  11. Barkley NA, Wang ML (2008) Application of TILLING and EcoTILLING as reverse genetic approaches to elucidate the function of genes in plants and animals. Curr Genomics 9:212–226PubMedGoogle Scholar
  12. Baulcombe DC, Saunders GR, Bevan MW, Mayo MA, Harrison BD (1986) Expression of biologically-active viral satellite RNA from the nuclear genome of transformed plants. Nature 321:446–449Google Scholar
  13. Bechtold N, Ellis J, Pelletier G (1993) In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. CR Acad Sci Paris Life Sci 316:1194–1199Google Scholar
  14. Birch RG (1997) PLANT TRANSFORMATION: problems and strategies for practical application. Annu Rev Plant Physiol Plant Mol Biol 48:297–326PubMedGoogle Scholar
  15. Bolle C, Herrmann RG, Oelmuller R (1996) Intron sequences are involved in the plastid- and light-dependent expression of the spinach PsaD gene. Plant J 10:919–924PubMedGoogle Scholar
  16. Borevitz JO, Xia Y, Blount J, Dixon RA, Lamb C (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12:2383–2394PubMedGoogle Scholar
  17. Bouchez D, Camillieri C, Caboche M (1993a) A binary vector based on Basta resistance for in planta transformation of Arabidopsis thaliana. C R Acad Sci Paris 316:1188–1193Google Scholar
  18. Bouchez D, Camillieri C, Caboche M (1993b) A binary vector based on Basta resistance for in planta transformation of Arabidopsis thaliana. CR Acad Sci Paris 316:1188–1193Google Scholar
  19. Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320:1185–1190PubMedGoogle Scholar
  20. Caldwell DG, McCallum N, Shaw P, Muehlbauer GJ, Marshall DF, Waugh R (2004) A structured mutant population for forward and reverse genetics in barley (Hordeum vulgare L.). Plant J 40:143-150PubMedGoogle Scholar
  21. Campisi L, Yang Y, Yi Y, Heilig E, Herman B, Cassista AJ, Allen DW, Xiang H, Jack T (1999) Generation of enhancer trap lines in Arabidopsis and characterization of expression patterns in the inflorescence. Plant J 17:699–707PubMedGoogle Scholar
  22. Casadaban MJ, Cohen SN (1979) Lactose genes fused to exogenous promoters in one step using a Mu-lac bacteriophage: in vivo probe for transcriptional control sequences. Proc Natl Acad Sci USA 76:4530–4533PubMedGoogle Scholar
  23. Clough SJ, Bent AF (1998) Floral dip: a simplified method for agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743PubMedGoogle Scholar
  24. Colbert T, Till BJ, Tompa R, Reynolds S, Steine MN, Yeung AT, McCallum CM, Comai L, Henikoff S (2001) High-throughput screening for induced point mutations. Plant Physiol 126:480–484PubMedGoogle Scholar
  25. Comai L, Young K, Till BJ, Reynolds SH, Greene EA, Codomo CA, Enns LC, Johnson JE, Burtner C, Odden AR, Henikoff S (2004) Efficient discovery of DNA polymorphisms in natural populations by ecotilling. Plant J 37:778–786PubMedGoogle Scholar
  26. Cooper JL, Till BJ, Laport RG, Darlow MC, Kleffner JM, Jamai A, El-Mellouki T, Liu S, Ritchie R, Nielsen N, Bilyeu KD, Meksem K, Comai L, Henikoff S (2008) TILLING to detect induced mutations in soybean. BMC Plant Biol 8:9PubMedGoogle Scholar
  27. Deyholos MK, Sieburth LE (2000) Separable whorl-specific expression and negative regulation by enhancer elements within the AGAMOUS second intron. Plant Cell 12:1799–1810PubMedGoogle Scholar
  28. Dierking EC, Bilyeu KD (2009) New sources of soybean seed meal and oil composition traits identified through TILLING. BMC Plant Biol 9:89PubMedGoogle Scholar
  29. Du G, Yonekubo J, Zeng Y, Osisami M, Frohman MA (2006) Design of expression vectors for RNA interference based on miRNAs and RNA splicing. FEBS J 273:5421–5427PubMedGoogle Scholar
  30. Enns LC, Kanaoka MM, Torii KU, Comai L, Okada K, Cleland RE (2005) Two callose synthases, GSL1 and GSL5, play an essential and redundant role in plant and pollen development and in fertility. Plant Mol Biol 58:333–349PubMedGoogle Scholar
  31. Eyal Y, Curie C, McCormick S (1995) Pollen specificity elements reside in 30 bp of the proximal promoters of two pollen-expressed genes. Plant Cell 7:373–384PubMedGoogle Scholar
  32. Fobert PR, Miki BL, Iyer VN (1991) Detection of gene regulatory signals in plants revealed by T-DNA-mediated fusions. Plant Mol Biol 17:837–851PubMedGoogle Scholar
  33. Gelvin SB (2003) Agrobacterium-mediated plant transformation: the biology behind the “gene-jockeying” tool. Microbiol Mol Biol Rev 67:16–37 table of contentsPubMedGoogle Scholar
  34. Gelvin SB, Kim SI (2007) Effect of chromatin upon agrobacterium T-DNA integration and transgene expression. Biochim Biophys Acta 1769:410–421PubMedGoogle Scholar
  35. Ghildiyal M, Zamore PD (2009) Small silencing RNAs: an expanding universe. Nat Rev Genet 10:94–108PubMedGoogle Scholar
  36. Gilchrist EJ, O’Neil NJ, Rose AM, Zetka MC, Haughn GW (2006) TILLING is an effective reverse genetics technique for Caenorhabditis elegans. BMC Genomics 7:262PubMedGoogle Scholar
  37. Gong JM, Waner DA, Horie T, Li SL, Horie R, Abid KB, Schroeder JI (2004) Microarray-based rapid cloning of an ion accumulation deletion mutant in Arabidopsis thaliana. Proc Natl Acad Sci USA 101:15404–15409PubMedGoogle Scholar
  38. Grant JJ, Chini A, Basu D, Loake GJ (2003) Targeted activation tagging of the Arabidopsis NBS-LRR gene, ADR1, conveys resistance to virulent pathogens. Mol Plant Microbe Interact 16:669–680PubMedGoogle Scholar
  39. Greene EA, Codomo CA, Taylor NE, Henikoff JG, Till BJ, Reynolds SH, Enns LC, Burtner C, Johnson JE, Odden AR, Comai L, Henikoff S (2003) Spectrum of chemically induced mutations from a large-scale reverse-genetic screen in Arabidopsis. Genetics 164:731–740PubMedGoogle Scholar
  40. Henikoff S, Till BJ, Comai L (2004) TILLING. Traditional mutagenesis meets functional genomics. Plant Physiol. 135:630–636PubMedGoogle Scholar
  41. Hilson P, Allemeersch J, Altmann T, Aubourg S, Avon A, Beynon J, Bhalerao RP, Bitton F, Caboche M, Cannoot B et al (2004) Versatile gene-specific sequence tags for Arabidopsis functional genomics: transcript profiling and reverse genetics applications. Genome Res 14:2176–2189PubMedGoogle Scholar
  42. Himelblau E, Gilchrist EJ, Buono K, Bizzell C, Mentzer L, Vogelzang R, Osborn T, Amasino RM, Parkin IA, Haughn GW (2009) Forward and reverse genetics of rapid-cycling Brassica oleracea. Theor Appl Genet 118:953–961PubMedGoogle Scholar
  43. Honma MA, Baker BJ, Waddell CS (1993) High-frequency germinal transposition of DsALS in Arabidopsis. Proc Natl Acad Sci USA 90:6242–6246PubMedGoogle Scholar
  44. 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 48:974–985PubMedGoogle Scholar
  45. Ichikawa T, Nakazawa M, Kawashima M, Muto S, Gohda K, Suzuki K, Ishikawa A, Kobayashi H, Yoshizumi T, Tsumoto Y, Tsuhara Y, Iizumi H, Goto Y, Matsui M (2003) Sequence database of 1172 T-DNA insertion sites in Arabidopsis activation-tagging lines that showed phenotypes in T1 generation. Plant J 36:421–429PubMedGoogle Scholar
  46. Ito T, Motohashi R, Kuromori T, Mizukado S, Sakurai T, Kanahara H, Seki M, Shinozaki K (2002) A new resource of locally transposed Dissociation elements for screening gene-knockout lines in silico on the Arabidopsis genome. Plant Physiol 129:1695–1699PubMedGoogle Scholar
  47. 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 46:1149–1153PubMedGoogle Scholar
  48. Jackson AL, Bartz SR, Schelter J, Kobayashi SV, Burchard J, Mao M, Li B, Cavet G, Linsley PS (2003) Expression profiling reveals off-target gene regulation by RNAi. Nat Biotechnol 21:635–637PubMedGoogle Scholar
  49. Jun JH, Kim CS, Cho DS, Kwak JM, Ha CM, Park YS, Cho BH, Patton DA, Nam HG (2002) Random antisense cDNA mutagenesis as an efficient functional genomic approach in higher plants. Planta 214:668–674PubMedGoogle Scholar
  50. Kakimoto T (1996) CKI1, a histidine kinase homolog implicated in cytokinin signal transduction. Science 274:982–985PubMedGoogle Scholar
  51. 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 286:1962–1965PubMedGoogle Scholar
  52. Kertbundit S, De Greve H, Deboeck F, Van Montagu M, Hernalsteens JP (1991) In vivo random beta-glucuronidase gene fusions in Arabidopsis thaliana. Proc Natl Acad Sci USA 88: 5212–5216PubMedGoogle Scholar
  53. Kiegle E, Moore CA, Haseloff J, Tester MA, Knight MR (2000) Cell-type-specific calcium responses to drought, salt and cold in the Arabidopsis root. Plant J 23:267–278PubMedGoogle Scholar
  54. Koncz C, Martini N, Mayerhofer R, Koncz-Kalman Z, Korber H, Redei GP, Schell J (1989) High-frequency T-DNA-mediated gene tagging in plants. Proc Natl Acad Sci USA 86:8467–8471PubMedGoogle Scholar
  55. Koornneef M, Dellaert LW, van der Veen JH (1982) EMS- and radiation-induced mutation frequencies at individual loci in Arabidopsis thaliana (L.) Heynh. Mutat Res 93:109–123PubMedGoogle Scholar
  56. Kuromori T, Hirayama T, Kiyosue Y, Takabe H, Mizukado S, Sakurai T, Akiyama K, Kamiya A, Ito T, Shinozaki K (2004) A collection of 11,800 single-copy Ds transposon insertion lines in Arabidopsis. Plant J 37:897–905PubMedGoogle Scholar
  57. Lacroix B, Tzfira T, Vainstein A, Citovsky V (2006) A case of promiscuity: Agrobacterium’s endless hunt for new partners. Trends Genet 22:29–37PubMedGoogle Scholar
  58. Laubinger S, Zeller G, Henz SR, Sachsenberg T, Widmer CK, Naouar N, Vuylsteke M, Scholkopf B, Ratsch G, Weigel D (2008) At-TAX: a whole genome tiling array resource for developmental expression analysis and transcript identification in Arabidopsis thaliana. Genome Biol 9:R112PubMedGoogle Scholar
  59. LeClere S, Bartel B (2001) A library of Arabidopsis 35S-cDNA lines for identifying novel mutants. Plant Mol Biol 46:695–703PubMedGoogle Scholar
  60. Li X, Lassner M, Zhang Y (2002b) Deleteagene: a fast neutron deletion mutagenesis-based gene knockout system for plants. Comp Funct Genomics 3:158–160PubMedGoogle Scholar
  61. Li Y, Rosso MG, Ulker B, Weisshaar B (2006) Analysis of T-DNA insertion site distribution patterns in Arabidopsis thaliana reveals special features of genes without insertions. Genomics 87:645–652PubMedGoogle Scholar
  62. Li X, Song Y, Century K, Straight S, Ronald P, Dong X, Lassner M, Zhang Y (2001) A fast neutron deletion mutagenesis-based reverse genetics system for plants. Plant J 27:235–242PubMedGoogle Scholar
  63. Li J, Wen J, Lease KA, Doke JT, Tax FE, Walker JC (2002a) BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110: 213–222PubMedGoogle Scholar
  64. Liu YG, Mitsukawa N, Oosumi T, Whittier RF (1995) Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J 8:457–463PubMedGoogle Scholar
  65. 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 129:1544–1556PubMedGoogle Scholar
  66. Martienssen RA (1998) Functional genomics: probing plant gene function and expression with transposons. Proc Natl Acad Sci USA 95:2021–2026PubMedGoogle Scholar
  67. May BP, Martienssen RA (2003) Transposon mutagenesis in the study of plant development. CRC Crit Rev Plant Sci 22:1–35Google Scholar
  68. McCallum CM, Comai L, Greene EA, Henikoff S (2000) Targeted screening for induced mutations. Nat Biotechnol 18:455–457PubMedGoogle Scholar
  69. McElver J, Tzafrir I, Aux G, Rogers R, Ashby C, Smith K, Thomas C, Schetter A, Zhou Q, Cushman MA, Tossberg J, Nickle T, Levin JZ, Law M, Meinke D, Patton D (2001) Insertional mutagenesis of genes required for seed development in Arabidopsis thaliana. Genetics 159:1751–1763PubMedGoogle Scholar
  70. Meinke DW, Cherry JM, Dean C, Rounsley SD, Koornneef M (1998) Arabidopsis thaliana: a model plant for genome analysis. Science 282(662):679–682Google Scholar
  71. Meinke D, Scholl R (2003) The preservation of plant genetic resources. Experiences with Arabidopsis. Plant Physiol 133:1046–1050PubMedGoogle Scholar
  72. Menand B, Desnos T, Nussaume L, Berger F, Bouchez D, Meyer C, Robaglia C (2002) Expression and disruption of the Arabidopsis TOR (target of rapamycin) gene. Proc Natl Acad Sci USA 99:6422–6427PubMedGoogle Scholar
  73. Mengiste T, Amedeo P, Paszkowski J (1997) High-efficiency transformation of Arabidopsis thaliana with a selectable marker gene regulated by the T-DNA 1’ promoter. Plant J 12:945–948PubMedGoogle Scholar
  74. Mizoi J, Nakamura M, Nishida I (2006) Defects in CTP:PHOSPHORYLETHANOLAMINE CYTIDYLYLTRANSFERASE affect embryonic and postembryonic development in Arabidopsis. Plant Cell 18:3370–3385PubMedGoogle Scholar
  75. Moens CB, Donn TM, Wolf-Saxon ER, Ma TP (2008) Reverse genetics in zebrafish by TILLING. Brief Funct Genomic Proteomic 7:454–459PubMedGoogle Scholar
  76. Mun JH, Lee SY, Yu HJ, Jeong YM, Shin MY, Kim H, Lee I, Kim SG (2002) Petunia actin-depolymerizing factor is mainly accumulated in vascular tissue and its gene expression is enhanced by the first intron. Gene 292:233–243PubMedGoogle Scholar
  77. Muskett PR, Clissold L, Marocco A, Springer PS, Martienssen R, Dean C (2003) A resource of mapped dissociation launch pads for targeted insertional mutagenesis in the Arabidopsis genome. Plant Physiol 132:506–516PubMedGoogle Scholar
  78. 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 34:741–750PubMedGoogle Scholar
  79. Neff MM, Nguyen SM, Malancharuvil EJ, Fujioka S, Noguchi T, Seto H, Tsubuki M, Honda T, Takatsuto S, Yoshida S, Chory J (1999) BAS1: a gene regulating brassinosteroid levels and light responsiveness in Arabidopsis. Proc Natl Acad Sci USA 96:15316–15323PubMedGoogle Scholar
  80. Niu QW, Lin SS, Reyes JL, Chen KC, Wu HW, Yeh SD, Chua NH (2006) Expression of artificial micro RNAs in transgenic Arabidopsis thaliana confers virus resistance. Nat Biotechnol 24:1420–1428PubMedGoogle Scholar
  81. Oleykowski CA, Bronson Mullins CR, Godwin AK, Yeung AT (1998) Mutation detection using a novel plant endonuclease. Nucleic Acids Res 26:4597–4602PubMedGoogle Scholar
  82. Ostergaard L, Yanofsky MF (2004) Establishing gene function by mutagenesis in Arabidopsis thaliana. Plant J 39:682–696PubMedGoogle Scholar
  83. Papdi C, Abraham E, Joseph MP, Popescu C, Koncz C, Szabados L (2008) Functional identification of Arabidopsis stress regulatory genes using the controlled cDNA overexpression system. Plant Physiol 147:528–542PubMedGoogle Scholar
  84. 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 11:2263–2270PubMedGoogle Scholar
  85. Paterson AH, Freeling M, Sasaki T (2005) Grains of knowledge: genomics of model cereals. Genome Res 15:1643–1650PubMedGoogle Scholar
  86. Perry JA, Wang TL, Welham TJ, Gardner S, Pike JM, Yoshida S, Parniske M (2003) A TILLING reverse genetics tool and a web-accessible collection of mutants of the legume lotus japonicus. Plant Physiol 131:866–871PubMedGoogle Scholar
  87. Pettersson E, Lundeberg J, Ahmadian A (2009) Generations of sequencing technologies. Genomics 93:105–111PubMedGoogle Scholar
  88. Preuss D, Rhee SY, Davis RW (1994) Tetrad analysis possible in Arabidopsis with mutation of the QUARTET (QRT) genes. Science 264:1458–1460PubMedGoogle Scholar
  89. Puchta H, Hohn B (2005) Green light for gene targeting in plants. Proc Natl Acad Sci USA 102:11961–11962PubMedGoogle Scholar
  90. Perry J, Brachmann A, Welham T, Binder A, Charpentier M, Groth M, Haage K, Markmann K, Wang TL, Parniske M (2009) TILLING in lotus japonicus identified large allelic series for symbiosis genes and revealed a bias in functionally defective EMS alleles towards glycine replacements. Plant Physiol 151(3)1281–1291PubMedGoogle Scholar
  91. Quesada V, Macknight R, Dean C, Simpson GG (2003) Autoregulation of FCA pre-mRNA processing controls Arabidopsis flowering time. EMBO J 22:3142–3152PubMedGoogle Scholar
  92. Rensing SA, Fritzowsky D, Lang D, Reski R (2005) Protein encoding genes in an ancient plant: analysis of codon usage, retained genes and splice sites in a moss, Physcomitrella patens. BMC Genomics 6:43PubMedGoogle Scholar
  93. Robertson D (2004) VIGS vectors for gene silencing: many targets, many tools. Annu Rev Plant Biol 55:495–519PubMedGoogle Scholar
  94. Robinson SJ, Tang LH, Mooney BA, McKay SJ, Clarke WE, Links MG, Karcz S, Regan S, Wu YY, Gruber MY, Cui D, Yu M, Parkin IA (2009) An archived activation tagged population of Arabidopsis thaliana to facilitate forward genetics approaches. BMC Plant Biol 9:101PubMedGoogle Scholar
  95. 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 53:247–259PubMedGoogle Scholar
  96. Rubin GM, Yandell MD, Wortman JR, Gabor Miklos GL, Nelson CR, Hariharan IK, Fortini ME, Li PW, Apweiler R, Fleischmann W et al (2000) Comparative genomics of the eukaryotes. Science 287:2204–2215PubMedGoogle Scholar
  97. Salmeron JM, Oldroyd GE, Rommens CM, Scofield SR, Kim HS, Lavelle DT, Dahlbeck D, Staskawicz BJ (1996) Tomato Prf is a member of the leucine-rich repeat class of plant disease resistance genes and lies embedded within the pto kinase gene cluster. Cell 86:123–133PubMedGoogle Scholar
  98. Samson F, Brunaud V, Balzergue S, Dubreucq B, Lepiniec L, Pelletier G, Caboche M, Lecharny A (2002) FLAGdb/FST: a database of mapped flanking insertion sites (FSTs) of Arabidopsis thaliana T-DNA transformants. Nucleic Acids Res 30:94–97PubMedGoogle Scholar
  99. Schneeberger RG, Zhang K, Tatarinova T, Troukhan M, Kwok SF, Drais J, Klinger K, Orejudos F, Macy K, Bhakta A, Burns J, Subramanian G, Donson J, Flavell R, Feldmann KA (2005) Agrobacterium T-DNA integration in Arabidopsis is correlated with DNA sequence compositions that occur frequently in gene promoter regions. Funct Integr Genomics 5:240–253PubMedGoogle Scholar
  100. 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 579:4622–4628PubMedGoogle Scholar
  101. Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D (2006) Highly specific gene silencing by artificial micro RNAs in Arabidopsis. Plant Cell 18:1121–1133PubMedGoogle Scholar
  102. Seki H, Nishizawa T, Tanaka N, Niwa Y, Yoshida S, Muranaka T (2005) Hairy root-activation tagging: a high-throughput system for activation tagging in transformed hairy roots. Plant Mol Biol 59:793–807PubMedGoogle Scholar
  103. Service RF (2006) Gene sequencing. The race for the $1000 genome. Science 311:1544–1546PubMedGoogle Scholar
  104. Sessions A, Burke E, Presting G, Aux G, McElver J, Patton D, Dietrich B, Ho P, Bacwaden J, Ko C et al (2002) A high-throughput Arabidopsis reverse genetics system. Plant Cell 14:2985–2994PubMedGoogle Scholar
  105. Sheldon CC, Conn AB, Dennis ES, Peacock WJ (2002) Different regulatory regions are required for the vernalization-induced repression of FLOWERING LOCUS C and for the epigenetic maintenance of repression. Plant Cell 14:2527–2537PubMedGoogle Scholar
  106. Shukla VK, Doyon Y, Miller JC, DeKelver RC, Moehle EA, Worden SE, Mitchell JC, Arnold NL, Gopalan S, Meng X et al (2009) Precise genome modification in the crop species Zea mays using zinc-finger nucleases. Nature 459:437–441PubMedGoogle Scholar
  107. Slade AJ, Fuerstenberg SI, Loeffler D, Steine MN, Facciotti D (2005) A reverse genetic, nontransgenic approach to wheat crop improvement by TILLING. Nat Biotechnol 23:75–81PubMedGoogle Scholar
  108. Smits BM, Mudde J, Plasterk RH, Cuppen E (2004) Target-selected mutagenesis of the rat. Genomics 83:332–334PubMedGoogle Scholar
  109. Speulman E, Metz PL, van Arkel G, te Lintel Hekkert B, Stiekema WJ, Pereira A (1999) A two-component enhancer-inhibitor transposon mutagenesis system for functional analysis of the Arabidopsis genome. Plant Cell 11:1853–1866PubMedGoogle Scholar
  110. Steinmetz LM, Davis RW (2004) Maximizing the potential of functional genomics. Nat Rev Genet 5:190–201PubMedGoogle Scholar
  111. Sun T, Goodman HM, Ausubel FM (1992) Cloning the Arabidopsis GA1 locus by genomic subtraction. Plant Cell 4:119–128PubMedGoogle Scholar
  112. Sundaresan V, Springer P, Volpe T, Haward S, Jones JD, Dean C, Ma H, Martienssen R (1995) Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements. Genes Dev 9:1797–1810PubMedGoogle Scholar
  113. Sussman MR, Amasino RM, Young JC, Krysan PJ, Austin-Phillips S (2000) The Arabidopsis knockout facility at the University of Wisconsin-Madison. Plant Physiol 124:1465–1467PubMedGoogle Scholar
  114. Suzuki T, Eiguchi M, Kumamaru T, Satoh H, Matsusaka H, Moriguchi K, Nagato Y, Kurata N (2008) MNU-induced mutant pools and high performance TILLING enable finding of any gene mutation in rice. Mol Genet Genomics 279:213–223PubMedGoogle Scholar
  115. Talame V, Bovina R, Sanguineti MC, Tuberosa R, Lundqvist U, Salvi S (2008) TILLMore, a resource for the discovery of chemically induced mutants in barley. Plant Biotechnol J 6:477–485PubMedGoogle Scholar
  116. Teeri TH, Herrera-Estrella L, Depicker A, Van Montagu M, Palva ET (1986) Identification of plant promoters in situ by T-DNA-mediated transcriptional fusions to the npt-II gene. EMBO J 5:1755–1760PubMedGoogle Scholar
  117. Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, Selbig J, Muller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37:914–939PubMedGoogle Scholar
  118. Thomas CM, Jones DA, English JJ, Carroll BJ, Bennetzen JL, Harrison K, Burbidge A, Bishop GJ, Jones JD (1994) Analysis of the chromosomal distribution of transposon-carrying T-DNAs in tomato using the inverse polymerase chain reaction. Mol Gen Genet 242: 573–585PubMedGoogle Scholar
  119. Till BJ, Colbert T, Tompa R, Enns LC, Codomo CA, Johnson JE, Reynolds SH, Henikoff JG, Greene EA, Steine MN, Comai L, Henikoff S (2003a) High-throughput TILLING for functional genomics. Methods Mol Biol 236:205–220PubMedGoogle Scholar
  120. Till BJ, Cooper J, Tai TH, Colowit P, Greene EA, Henikoff S, Comai L (2007) Discovery of chemically induced mutations in rice by TILLING. BMC Plant Biol 7:19PubMedGoogle Scholar
  121. Till BJ, Reynolds SH, Greene EA, Codomo CA, Enns LC, Johnson JE, Burtner C, Odden AR, Young K, Taylor NE, Henikoff JG, Comai L, Henikoff S (2003) Large-scale discovery of induced point mutations with high-throughput TILLING. Genome Res 13:524–530PubMedGoogle Scholar
  122. Till BJ, Reynolds SH, Weil C, Springer N, Burtner C, Young K, Bowers E, Codomo CA, Enns LC, Odden AR, Greene EA, Comai L, Henikoff S (2004) Discovery of induced point mutations in maize genes by TILLING. BMC Plant Biol 4:12PubMedGoogle Scholar
  123. Tissier AF, Marillonnet S, Klimyuk V, Patel K, Torres MA, Murphy G, Jones JD (1999) Multiple independent defective suppressor-mutator transposon insertions in Arabidopsis: a tool for functional genomics. Plant Cell 11:1841–1852PubMedGoogle Scholar
  124. Topping JF, Agyeman F, Henricot B, Lindsey K (1994) Identification of molecular markers of embryogenesis in Arabidopsis thaliana by promoter trapping. Plant J 5:895–903PubMedGoogle Scholar
  125. Topping JF, Wei W, Lindsey K (1991) Functional tagging of regulatory elements in the plant genome. Development 112:1009–1019PubMedGoogle Scholar
  126. Townsend JA, Wright DA, Winfrey RJ, Fu F, Maeder ML, Joung JK, Voytas DF (2009) High-frequency modification of plant genes using engineered zinc-finger nucleases. Nature 459:442–445PubMedGoogle Scholar
  127. Tschuch C, Schulz A, Pscherer A, Werft W, Benner A, Hotz-Wagenblatt A, Barrionuevo LS, Lichter P, Mertens D (2008) Off-target effects of siRNA specific for GFP. BMC Mol Biol 9:60PubMedGoogle Scholar
  128. Ülker B, Li Y, Rosso MG, Logemann E, Somssich IE, Weisshaar B (2008a) T-DNA-mediated transfer of Agrobacterium tumefaciens chromosomal DNA into plants. Nat Biotechnol 26:1015–1017PubMedGoogle Scholar
  129. Ülker B, Peiter E, Dixon DP, Moffat C, Capper R, Bouche N, Edwards R, Sanders D, Knight H,, Knight MR (2008b) Getting the most out of publicly available T-DNA insertion lines. Plant J 56(4):665–677PubMedGoogle Scholar
  130. 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
  131. Van Montagu M (2003) Jeff schell (1935–2003): steering Agrobacterium-mediated plant gene engineering. Trends Plant Sci 8:353–354PubMedGoogle Scholar
  132. 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 26:1521–1528PubMedGoogle Scholar
  133. Wang S, Sim TB, Kim YS, Chang YT (2004) Tools for target identification and validation. Curr Opin Chem Biol 8:371–377PubMedGoogle Scholar
  134. Weigel D, Ahn JH, Blazquez MA, Borevitz JO, Christensen SK, Fankhauser C, Ferrandiz C, Kardailsky I, Malancharuvil EJ, Neff MM et al (2000) Activation tagging in Arabidopsis. Plant Physiol 122:1003–1013PubMedGoogle Scholar
  135. Wienholds E, van Eeden F, Kosters M, Mudde J, Plasterk RH, Cuppen E (2003) Efficient target-selected mutagenesis in zebrafish. Genome Res 13:2700–2707PubMedGoogle Scholar
  136. 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 8:659–671PubMedGoogle Scholar
  137. Winkler S, Schwabedissen A, Backasch D, Bokel C, Seidel C, Bonisch S, Furthauer M, Kuhrs A, Cobreros L, Brand M, Gonzalez-Gaitan M (2005) Target-selected mutant screen by TILLING in Drosophila. Genome Res 15:718–723PubMedGoogle Scholar
  138. Wisman E, Hartmann U, Sagasser M, Baumann E, Palme K, Hahlbrock K, Saedler H, Weisshaar B (1998) Knock-out mutants from an En-1 mutagenized Arabidopsis thaliana population generate phenylpropanoid biosynthesis phenotypes. Proc Natl Acad Sci USA 95:12432–12437PubMedGoogle Scholar
  139. Wright DA, Townsend JA, Winfrey RJ Jr., Irwin PA, Rajagopal J, Lonosky PM, Hall BD, Jondle MD, Voytas DF (2005) High-frequency homologous recombination in plants mediated by zinc-finger nucleases. Plant J 44:693–705PubMedGoogle Scholar
  140. Wu GZ, Shi QM, Niu Y, Xing MQ, Xue HW (2008) Shanghai RAPESEED Database: a resource for functional genomics studies of seed development and fatty acid metabolism of Brassica. Nucleic Acids Res 36:D1044–D1047PubMedGoogle Scholar
  141. Xin Z, Wang ML, Barkley NA, Burow G, Franks C, Pederson G, Burke J (2008) Applying genotyping (TILLING) and phenotyping analyses to elucidate gene function in a chemically induced sorghum mutant population. BMC Plant Biol 8:103PubMedGoogle Scholar
  142. Yamada K, Lim J, Dale JM, Chen H, Shinn P, Palm CJ, Southwick AM, Wu HC, Kim C, Nguyen M et al (2003) Empirical analysis of transcriptional activity in the Arabidopsis genome. Science 302:842–846PubMedGoogle Scholar
  143. Yu H, Chen X, Hong YY, Wang Y, Xu P, Ke SD, Liu HY, Zhu JK, Oliver DJ, Xiang CB (2008) Activated expression of an Arabidopsis HD-START protein confers drought tolerance with improved root system and reduced stomatal density. Plant Cell 20:1134–1151PubMedGoogle Scholar
  144. Zamore PD, Tuschl T, Sharp PA, Bartel DP (2000) RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 101:25–33PubMedGoogle Scholar
  145. Zhang J, Guo D, Chang Y, You C, Li X, Dai X, Weng Q, Chen G, Liu H, Han B, Zhang Q, Wu C (2007) Non-random distribution of T-DNA insertions at various levels of the genome hierarchy as revealed by analyzing 13 804 T-DNA flanking sequences from an enhancer-trap mutant library. Plant J 49:947–959PubMedGoogle Scholar
  146. Zhang S, Raina S, Li H, Li J, Dec E, Ma H, Huang H, Fedoroff NV (2003) Resources for targeted insertional and deletional mutagenesis in Arabidopsis. Plant Mol Biol 53:133–150PubMedGoogle Scholar
  147. Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632PubMedGoogle Scholar
  148. Zupan J, Muth TR, Draper O, Zambryski P (2000) The transfer of DNA from agrobacterium tumefaciens into plants: a feast of fundamental insights. Plant J 23:11–28PubMedGoogle Scholar

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© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.Plant Molecular Engineering GroupIZMB (Institute of Cellular and Molecular Botany), University of BonnBonnGermany
  2. 2.Faculty of BiologyBielefeld UniversityBielefeldGermany

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