Microarray-Based Identification of Transcription Factor Target Genes

Methods in Molecular Biology

Volumn 754, Issue , 2011, Pages 119-141

  Gorte, Maartje ^a   Horstman, Anneke ^b   Page, Robert B ^c   Heidstra, Renze ^a   Stromberg, Arnold ^d   Boutilier, Kim ^b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b Plant Research International   (Netherlands)

^c AUBURN UNIVERSITY AT MONTGOMERY   (United States)

^d UNIVERSITY OF KENTUCKY   (United States)

Author keywords

cycloheximide; inducible gene expression systems; Microarray; relative quantification, quantitative real time RT PCR, endogenous reference gene, amplification efficiency; target gene; transcription factor

Indexed keywords

EID: 79960736391     PISSN: 10643745     EISSN: 19406029     Source Type: Book Series    
DOI: 10.1007/978-1-61779-154-3_7     Document Type: Chapter

References (82)

1. Gregory, B. D., and Belostotsky, D. A. (2009) Whole-genome microarrays: applications and technical issues. Methods Mol. Biol. 553, 39–56.
2. Wang, Z., Gerstein, M., and Snyder, M. (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet. 10, 57–63.
3. Collas, P. (2010) The current state of chromatin immunoprecipitation. Mol. Biotechnol. 45, 87–100.
4. Kirmizis, A., and Farnham, P. J. (2004) Genomic approaches that aid in the identification of transcription factor target genes. Exp. Biol. Med. (Maywood). 229, 705–721.
5. Aranda, A., and Pascual, A. (2001) Nuclear hormone receptors and gene expression. Physiol. Rev. 81, 1269–1304.
6. Gomez-Mena, C., de Folter, S., Costa, M. M. R., Angenent, G. C., and Sablowski, R. (2005) Transcriptional program controlled by the floral homeotic gene AGAMOUS during early organogenesis. Development 132, 429–438.
7. Wagner, D., Wellmer, F., Dilks, K., William, D., Smith, M. R., Kumar, P. P., Riechmann, J. L., Greenland, A. J., and Meyerowitz, E. M. (2004) Floral induction in tissue culture: a system for the analysis of LEAFY-dependent gene regulation. Plant J. 39, 273–282.
8. Passarinho, P., Ketelaar, T., Xing, M., van Arkel, J., Maliepaard, C., Hendriks, M. W., Joosen, R., Lammers, M., Herdies, L., den Boer, B., van der Geest, L., and Boutilier, K. (2008) BABY BOOM target genes provide diverse entry points into cell proliferation and cell growth pathways. Plant Mol. Biol. 68, 225–237.
9. Rohila, J. S., Chen, M., Cerny, R., and Fromm, M. E. (2004) Improved tandem affinity purification tag and methods for isolation of protein heterocomplexes from plants. Plant J. 38, 172–181.
10. Craft, J., Samalova, M., Baroux, C., Townley, H., Martinez, A., Jepson, I., Tsiantis, M., and Moore, I. (2005) New pOp/LhG4 vectors for stringent glucocorticoid-dependent transgene expression in Arabidopsis. Plant J. 41, 899–918.
11. Hanson, J., Hanssen, M., Wiese, A., Hendriks, M. M., and Smeekens, S. (2008) The sucrose regulated transcription factor bZIP11 affects amino acid metabolism by regulating the expression of ASPARAGINE SYNTHETASE1 and PROLINE DEHY-DROGENASE2. Plant J. 53, 935–949.
12. Aoyama, T., and Chua, N. H. (1997) A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J. 11, 605–612.
13. Levesque, M. P., Vernoux, T., Busch, W., Cui, H., Wang, J. Y., Blilou, I., Hassan, H., Nakajima, K., Matsumoto, N., Lohmann, J. U., Scheres, B., and Benfey, P. N. (2006) Whole-genome analysis of the SHORT-ROOT developmental pathway in Arabidopsis. PLoS Biol. 4, e143.
14. Hay, A., Jackson, D., Ori, N., and Hake, S. (2003) Analysis of the competence to respond to KNOTTED1 activity in Arabidopsis leaves using a steroid induction system. Plant Physiol. 131, 1671–1680.
15. Sundstrom, J. F., Nakayama, N., Glimelius, K., and Irish, V. F. (2006) Direct regulation of the floral homeotic APETALA1 gene by APETALA3 and PISTILLATA in Arabidopsis. Plant J. 46, 593–600.
16. Ikeda, Y., Banno, H., Niu, Q. W., Howell, S. H., and Chua, N. H. (2006) The ENHANCER OF SHOOT REGENERATION 2 gene in Arabidopsis regulates CUP-SHAPED COTYLEDON 1 at the transcriptional level and controls cotyledon development. Plant Cell Physiol. 47, 1443–1456.
17. Che, P., Lall, S., and Howell, S. H. (2008) Acquiring competence for shoot development in Arabidopsis: ARR2 directly targets A-type ARR genes that are differentially activated by CIM preincubation. Plant Signal. Behav. 3, 99–101.
18. Zuo, J., Niu, Q. W., and Chua, N. H. (2000) Technical advance: an estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J. 24, 265–273.
19. Tornero, P., Chao, R. A., Luthin, W. N., Goff, S. A., and Dangl, J. L. (2002) Large-scale structure–function analysis of the Arabidopsis RPM1 disease resistance protein. Plant Cell 14, 435–450.
20. Zuo, J., and Chua, N. H. (2000) Chemical-inducible systems for regulated expression of plant genes. Curr. Opin. Biotechnol. 11, 146–151.
21. Gatz, C., and Lenk, I. (1998) Promoters that respond to chemical inducers. Trends Plant Sci. 3, 352–358.
22. Ko, J. H., Kim, W. C., and Han, K. H. (2009) Ectopic expression of MYB46 identifies transcriptional regulatory genes involved in secondary wall biosynthesis in Arabidopsis. Plant J. 60, 649–665.
23. Zentella, R., Zhang, Z. L., Park, M., Thomas, S. G., Endo, A., Murase, K., Fleet, C. M., Jikumaru, Y., Nambara, E., Kamiya, Y., and Sun, T. P. (2007) Global analysis of della direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19, 3037–3057.
24. Kang, H. G., Fang, Y., and Singh, K. B. (1999) A glucocorticoid-inducible transcription system causes severe growth defects in Arabidopsis and induces defense-related genes. Plant J. 20, 127–133.
25. Ouwerkerk, P. B., de Kam, R. J., Hoge, J. H., and Meijer, A. H. (2001) Glucocorticoid-inducible gene expression in rice. Planta 213, 370–378.
26. Andersen, S. U., Cvitanich, C., Hougaard, B. K., Roussis, A., Gronlund, M., Jensen, D. B., Frokjaer, L. A., and Jensen, E. O. (2003) The glucocorticoid-inducible GVG system causes severe growth defects in both root and shoot of the model legume Lotus japonicus. Mol. Plant Microbe Interact. 16, 1069–1076.
27. Weijers, D., Van Hamburg, J. P., Van Rijn, E., Hooykaas, P. J., and Offringa, R. (2003) Diphtheria toxin-mediated cell ablation reveals interregional communication during Arabidopsis seed development. Plant Physiol. 133, 1882–1892.
28. Galweiler, L., Conlan, R. S., Mader, P., Palme, K., and Moore, I. (2000) Technical advance: the DNA-binding activity of gal4 is inhibited by methylation of the gal4 binding site in plant chromatin. Plant J. 23, 143–157.
29. Engineer, C. B., Fitzsimmons, K. C., Schmuke, J. J., Dotson, S. B., and Kranz, R. G. (2005) Development and evaluation of a Gal4-mediated LUC/GFP/GUS enhancer trap system in Arabidopsis. BMC Plant Biol. 5, 9.
30. Liu, C., Chen, H., Er, H. L., Soo, H. M., Kumar, P. P., Han, J. H., Liou, Y. C., and Yu, H. (2008) Direct interaction of AGL24 and SOC1 integrates flowering signals in Arabidopsis. Development 135, 1481–1491.
31. Matsuo, N., Mase, H., Makino, M., Takahashi, H., and Banno, H. (2009) Identification of ENHANCER OF SHOOT REGENERATION 1-upregulated genes during in vitro shoot regeneration. Plant Biotechnol. 26, 385–393.
32. Pre, M., Atallah, M., Champion, A., De Vos, M., Pieterse, C. M. J., and Memelink, J. (2008) The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense. Plant Physiol. 147, 1347–1357.
33. Balazadeh, S., Siddiqui, H., Allu, A. D., Matallana-Ramirez, L. P., Caldana, C., Mehrnia, M., Zanor, M. I., Kohler, B., and Mueller-Roeber, B. (2010) A gene regulatory network controlled by the NAC transcription factor ANAC092/AtNAC2/ORE1 during salt-promoted senescence. Plant J. 62, 250–264.
34. Turner, R., and Foster, G. D. (1995) The potential exploitation of plant viral translational enhancers in biotechnology for increased gene-expression. Mol. Biotechnol. 3, 225–236.
35. Zhong, R., Richardson, E. A., and Ye, Z. H. (2007) The MYB46 transcription factor is a direct target of SND1 and regulates secondary wall biosynthesis in Arabidopsis. Plant Cell 19, 2776–2792.
36. McKeehan, W., and Hardesty, B. (1969) The mechanism of cycloheximide inhibition of protein synthesis in rabbit reticulo-cytes. Biochem. Biophys. Res. Commun. 36, 625–630.
37. Lee, D. J., Park, J. W., Lee, H. W., and Kim, J. (2009) Genome-wide analysis of the auxin-responsive transcriptome downstream of iaa1 and its expression analysis reveal the diversity and complexity of auxin-regulated gene expression. J. Exp. Bot. 60, 3935–3957.
38. Ravni, A., Eiden, L. E., Vaudry, H., Gonzalez, B. J., and Vaudry, D. (2006) Cycloheximide treatment to identify components of the transitional transcriptome in PACAP-induced PC12 cell differentiation. J. Neurochem. 98, 1229–1241.
39. Abel, S., Nguyen, M. D., and Theologis, A. (1995) The PS-IAA4/5-like family of early auxin-inducible mRNAs in Arabidopsis thaliana. J. Mol. Biol. 251, 533–549.
40. Theologis, A., Huynh, T. V., and Davis, R. W. (1985) Rapid induction of specific mRNAs by auxin in pea epicotyl tissue. J. Mol. Biol. 183, 53–68.
41. Herrick, D., Parker, R., and Jacobson, A. (1990) Identification and comparison of stable and unstable mRNAs in Saccharomyces cerevisiae. Mol. Cell Biol. 10, 2269–2284.
42. Kiddle, S. J., Windram, O. P., McHattie, S., Mead, A., Beynon, J., Buchanan-Wollaston, V., Denby, K. J., and Mukherjee, S. (2010) Temporal clustering by affinity propagation reveals transcriptional modules in Arabidopsis thaliana. Bioinformatics 26, 355–362.
43. Herzenberg, L. A., Sweet, R. G., and Herzenberg, L. A. (1976) Fluorescence-activated cell sorting. Sci. Am. 234, 108–117.
44. Bargmann, B. O., and Birnbaum, K. D. (2009) Fluorescence activated cell sorting of plant protoplasts. JoVE. 36. http://www. jove.com/index/Details.stp?ID=1673. doi: 10.3791/1673.
45. Birnbaum, K., Jung, J. W., Wang, J. Y., Lambert, G. M., Hirst, J. A., Galbraith, D. W., and Benfey, P. N. (2005) Cell type-specific expression profiling in plants via cell sorting of protoplasts from fluorescent reporter lines. Nat. Methods 2, 615–619.
46. Birnbaum, K., Shasha, D. E., Wang, J. Y., Jung, J. W., Lambert, G. M., Galbraith, D. W., and Benfey, P. N. (2003) A gene expression map of the Arabidopsis root. Science 302, 1956–1960.
47. Yadav, R. K., Girke, T., Pasala, S., Xie, M., and Reddy, G. V. (2009) Gene expression map of the Arabidopsis shoot apical meristem stem cell niche. Proc. Natl. Acad. Sci. USA 106, 4941–4946.
48. Sheen, J. (2001) Signal transduction in maize and Arabidopsis mesophyll protoplasts. Plant Physiol. 127, 1466–1475.
49. Rajeevan, M. S., Ranamukhaarachchi, D. G., Vernon, S. D., and Unger, E. R. (2001) Use of real-time quantitative PCR to validate the results of cDNA array and differential display PCR technologies. Methods 25, 443–451.
50. Chuaqui, R. F., Bonner, R. F., Best, C. J., Gillespie, J. W., Flaig, M. J., Hewitt, S. M., Phillips, J. L., Krizman, D. B., Tangrea, M. A., Ahram, M., Linehan, W. M., Knezevic, V., and Emmert-Buck, M. R. (2002) Post-analysis follow-up and validation of microarray experiments. Nat. Genet. 32 Suppl., 509–514.
51. Canales, R. D., Luo, Y., Willey, J. C., Auster-miller, B., Barbacioru, C. C., Boysen, C., Hunkapiller, K., Jensen, R. V., Knight, C. R., Lee, K. Y., Ma, Y., Maqsodi, B., Papallo, A., Peters, E. H., Poulter, K., Ruppel, P. L., Samaha, R. R., Shi, L., Yang, W., Zhang, L., and Goodsaid, F. M. (2006) Evaluation of DNA microarray results with quantitative gene expression platforms. Nat. Biotechnol. 24, 1115–1122.
52. Bustin, S. A. (2002) Quantification of mRNA using real-time reverse transcription PCR (RT-PCR): trends and problems. J. Mol. Endocrinol. 29, 23–39.
53. Pfaffl, M. A. (2006) Relative quantification, in Real-time PCR (Dorak, M. T., Ed.), pp 63–82. Taylor and Francis, New York, NY.
54. Karlen, Y., McNair, A., Perseguers, S., Mazza, C., and Mermod, N. (2007) Statistical significance of quantitative PCR. BMC Bioinformatics 8, 131.
55. Bustin, S. A., and Nolan, T. (2004) Pitfalls of quantitative real-time reverse-transcription polymerase chain reaction. J. Biomol. Tech. 15, 155–166.
56. Bustin, S. A., Benes, V., Garson, J. A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M. W., Shipley, G. L., Vandesompele, J., and Wittwer, C. T. (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55, 611–622.
57. Bustin, S. A., Benes, V., Nolan, T., and Pfaffl, M. W. (2005) Quantitative real-time RT-PCR—a perspective. J. Mol. Endocrinol. 34, 597–601.
58. Wong, M. L., and Medrano, J. F. (2005) Real-time PCR for mRNA quantitation. Biotechniques 39, 75–85.
59. Czechowski, T., Stitt, M., Altmann, T., Udvardi, M. K., and Scheible, W. R. (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139, 5–17.
60. Gutierrez, L., Mauriat, M., Guenin, S., Pelloux, J., Lefebvre, J. F., Louvet, R., Rusterucci, C., Moritz, T., Guerineau, F., Bellini, C., and Van Wuytswinkel, O. (2008) The lack of a systematic validation of reference genes: a serious pitfall undervalued in reverse transcription-polymerase chain reaction (RT-PCR) analysis in plants. Plant Biotechnol. J. 6, 609–618.
61. Freeman, W. M., Walker, S. J., and Vrana, K. E. (1999) Quantitative RT-PCR: pitfalls and potential. Biotechniques 26, 112–125.
62. Beckman, K. B., Lee, K. Y., Golden, T., and Melov, S. (2004) Gene expression profiling in mitochondrial disease: assessment of microarray accuracy by high-throughput Q-PCR. Mitochondrion 4, 453–470.
63. Leibfried, A., To, J. P., Busch, W., Stehling, S., Kehle, A., Demar, M., Kieber, J. J., and Lohmann, J. U. (2005) WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature 438, 1172–1175.
64. Schlereth, A., Moller, B., Liu, W., Kientz, M., Flipse, J., Rademacher, E. H., Schmid, M., Jurgens, G., and Weijers, D. (2010) MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464, 913–916.
65. Ye, Q., Zhu, W., Li, L., Zhang, S., Yin, Y., Ma, H., and Wang, X. (2010) Brassinosteroids control male fertility by regulating the expression of key genes involved in Arabidopsis anther and pollen development. Proc. Natl. Acad. Sci. USA 107, 6100–6105.
66. Kaufmann, K., Muino, J. M., Osteras, M., Farinelli, L., Krajewski, P., and Angenent, G. C. (2010) Chromatin immunoprecipitation (ChIP) of plant transcription factors followed by sequencing (ChIP-SEQ) or hybridization to whole genome arrays (ChIP-CHIP). Nat. Protoc. 5, 457–472.
67. Fu, W. J., Stromberg, A. J., Viele, K., Carroll, R. J., and Wu, G. (2010) Statistics and bioinformatics in nutritional sciences: analysis of complex data in the era of systems biology. J. Nutr. Biochem. 21, 561–572.
68. Peng, X., Wood, C. L., Blalock, E. M., Chen, K. C., Landfield, P. W., and Stromberg, A. J. (2003) Statistical implications of pooling RNA samples for microarray experiments. BMC Bioinformatics 4, 26.
69. Benjamini, Y., and Hochberg, Y. (1995) Controlling the false discovery rate – a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Methodol. 57, 289–300.
70. Liu, H., Tarima, S., Borders, A. S., Getchell, T. V., Getchell, M. L., and Stromberg, A. J. (2005) Quadratic regression analysis for gene discovery and pattern recognition for non-cyclic short time-course microarray experiments. BMC Bioinformatics 6, 106.
71. Skern, R., Frost, P., and Nilsen, F. (2005) Relative transcript quantification by quantitative PCR: roughly right or precisely wrong? BMC Mol. Biol. 6, 10.
72. Yuan, J. S., Reed, A., Chen, F., and Stewart, C. N., Jr. (2006) Statistical analysis of real-time PCR data. BMC Bioinformatics 7, 85.
73. Yuan, J. S., Wang, D., and Stewart, C. N., Jr. (2008) Statistical methods for efficiency adjusted real-time PCR quantification. Biotechnol. J. 3, 112–123.
74. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402–408.
75. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., and Speleman, F. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, RESEARCH0034.
76. Andersen, C. L., Jensen, J. L., and Orntoft, T. F. (2004) Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 64, 5245–5250.
77. Pfaffl, M. W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
78. Hellemans, J., Mortier, G., De Paepe, A., Speleman, F., and Vandesompele, J. (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 8, R19.
79. Burns, M. J., Nixon, G. J., Foy, C. A., and Harris, N. (2005) Standardisation of data from real-time quantitative PCR methods – evaluation of outliers and comparison of calibration curves. BMC Biotechnol. 5, 31.
80. Peirson, S. N., Butler, J. N., and Foster, R. G. (2003) Experimental validation of novel and conventional approaches to quantitative real-time PCR data analysis. Nucleic Acids Res. 31, e73.
81. Ramakers, C., Ruijter, J. M., Deprez, R. H., and Moorman, A. F. (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339, 62–66.
82. Cikos, S., Bukovska, A., and Koppel, J. (2007) Relative quantification of mRNA: comparison of methods currently used for real-time PCR data analysis. BMC Mol. Biol. 8, 113.