New BAR tools for mining expression data and exploring Cis-elements in Arabidopsis thaliana

Plant Journal

Volumn 88, Issue 3, 2016, Pages 490-504

  Austin, Ryan S ^a,b   Hiu, Shu ^a   Waese, Jamie ^a   Ierullo, Matthew ^a   Pasha, Asher ^a   Wang, Ting Ting ^a   Fan, Jim ^a   Foong, Curtis ^a   Breit, Robert ^a   Desveaux, Darrell ^a   Moses, Alan ^a   Provart, Nicholas J ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b LONDON RESEARCH AND DEVELOPMENT CENTRE   (Canada)

Author keywords

Arabidopsis thaliana; cis element prediction; coexpression analysis; gene expression markers; promoter analysis; reporter constructs; technical advance

Indexed keywords

BIOLOGY; PLANTS (BOTANY);

ARABIDOPSIS THALIANA; CIS-ELEMENTS; CO-EXPRESSION; PROMOTER ANALYSIS; REPORTER CONSTRUCTS; TECHNICAL ADVANCES;

GENE EXPRESSION;

ARABIDOPSIS; DATA MINING; GENE EXPRESSION REGULATION; GENETIC DATABASE; GENETICS; METABOLISM; PHYSIOLOGY; PROMOTER REGION; SOFTWARE;

ARABIDOPSIS; DATA MINING; DATABASES, GENETIC; GENE EXPRESSION REGULATION, PLANT; PROMOTER REGIONS, GENETIC; SOFTWARE;

EID: 84990817914     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.13261     Document Type: Article

References (69)

1. Amrine, K.C.H., Blanco-Ulate, B. and Cantu, D. (2015) Discovery of core biotic stress responsive genes in Arabidopsis by weighted gene co-expression network analysis. PLoS ONE, 10, e0118731.
2. Bailey, T.L., Williams, N., Misleh, C. and Li, W.W. (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res. 34, W369–W373.
3. Bassel, G.W., Lan, H., Glaab, E., Gibbs, D.J., Gerjets, T., Krasnogor, N., Bonner, A.J., Holdsworth, M.J. and Provart, N.J. (2011) Genome-wide network model capturing seed germination reveals coordinated regulation of plant cellular phase transitions. Proc. Natl Acad. Sci. USA, 108, 9709–9714.
4. Bauer, A.W., Kirby, W.M., Sherris, J.C. and Turck, M. (1966) Antibiotic susceptibility testing by a standardized single disk method. Am. J. Clin. Pathol. 45, 493–496.
5. Chen, I.-P., Haehnel, U., Altschmied, L., Schubert, I. and Puchta, H. (2003) The transcriptional response of Arabidopsis to genotoxic stress – a high-density colony array study (HDCA). Plant J. 35, 771–786.
6. Chomczynski, P. and Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156–159.
7. Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743.
8. Cooke, R. and Penon, P. (1990) In vitro transcription from cauliflower mosaic virus promoters by a cell-free extract from tobacco cells. Plant Mol. Biol. 14, 391–405.
9. 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.
10. Cutler, S.R., Ehrhardt, D.W., Griffitts, J.S. and Somerville, C.R. (2000) Random GFP:cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency. Proc. Natl Acad. Sci. USA, 97, 3718–3723.
11. Dangl, J.L. and Jones, J.D. (2001) Plant pathogens and integrated defence responses to infection. Nature, 411, 826–833.
12. Deng, W., Buzas, D.M., Ying, H., Robertson, M., Taylor, J., Peacock, W.J., Dennis, E.S. and Helliwell, C. (2013) Arabidopsis polycomb repressive complex 2 binding sites contain putative GAGA factor binding motifs within coding regions of genes. BMC Genomics, 14, 593.
13. Ezcurra, I., Ellerström, M., Wycliffe, P., Stålberg, K. and Rask, L. (1999) Interaction between composite elements in the napA promoter: both the B-box ABA-responsive complex and the RY/G complex are necessary for seed-specific expression. Plant Mol. Biol. 40, 699–709.
14. Fauteux, F., Blanchette, M. and Stromvik, M.V. (2008) Seeder: discriminative seeding DNA motif discovery. Bioinformatics, 24, 2303–2307.
15. Gentleman, R.C., Carey, V.J., Bates, D.M. et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80.
16. Goda, H., Sasaki, E., Akiyama, K. et al. (2008) The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access. Plant J. 55, 526–542.
17. Gómez-Gómez, L. and Boller, T. (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell, 5, 1003–1011.
18. Granok, H., Leibovitch, B.A., Shaffer, C.D. and Elgin, S.C.R. (1995) Chromatin: Ga-Ga over GAGA factor. Curr. Biol. 5, 238–241.
19. Grau, J., Posch, S., Grosse, I. and Keilwagen, J. (2013) A general approach for discriminative de novo motif discovery from high-throughput data. Nucleic Acids Res. 41, e197.
20. Greenberg, J.T. and Yao, N. (2004) The role and regulation of programmed cell death in plant-pathogen interactions. Cell. Microbiol. 6, 201–211.
21. Gurr, S.J. and Rushton, P.J. (2005) Engineering plants with increased disease resistance: how are we going to express it? Trends Biotech. 23, 283–290.
22. Harbison, C.T., Benjamin Gordon, D., Lee, T.I. et al. (2004) Transcriptional regulatory code of a eukaryotic genome. Nature, 431, 99–104.
23. Haudry, A., Platts, A.E., Vello, E. et al. (2013) An atlas of over 90,000 conserved noncoding sequences provides insight into crucifer regulatory regions. Nat. Genet. 45, 891–898.
24. Higo, K., Ugawa, Y., Iwamoto, M. and Higo, H. (1998) PLACE: a database of plant cis-acting regulatory DNA elements. Nucleic Acids Res. 26, 358–359.
25. Higo, K., Ugawa, Y., Iwamoto, M. and Korenaga, T. (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res. 27, 297–300.
26. Honys, D. and Twell, D. (2003) Comparative analysis of the Arabidopsis pollen transcriptome. Plant Physiol. 132, 640–652.
27. Huggins, P., Zhong, S., Shiff, I. et al. (2011) DECOD: fast and accurate discriminative DNA motif finding. Bioinformatics, 27, 2361–2367.
28. Hughes, J.D., Estep, P.W., Tavazoie, S. and Church, G.M. (2000) Computational identification of cis-regulatory elements associated with groups of functionally related genes in Saccharomyces cerevisiae. J. Mol. Biol. 296, 1205–1214.
29. Jacobson, E.M., Li, P., Leon-del-Rio, A., Rosenfeld, M.G. and Aggarwal, A.K. (1997) Structure of Pit-1 POU domain bound to DNA as a dimer: unexpected arrangement and flexibility. Genes Dev. 11, 198–212.
30. Jones, J.D.G. and Dangl, J.L. (2006) The plant immune system. Nature, 444, 323–329.
31. Karimi, M., Inzé, D. and Depicker, A. (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193–195.
32. Kilian, J., Whitehead, D., Horak, J., Wanke, D., Weinl, S., Batistic, O., D'Angelo, C., Bornberg-Bauer, E., Kudla, J. and Harter, K. (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J. 50, 347–363.
33. Korkuć, P., Schippers, J.H.M. and Walther, D. (2014) Characterization and identification of cis-regulatory elements in Arabidopsis based on single-nucleotide polymorphism information. Plant Physiol. 164, 181–200.
34. Lee, I., Ambaru, B., Thakkar, P., Marcotte, E.M. and Rhee, S.Y. (2010) Rational association of genes with traits using a genome-scale gene network for Arabidopsis thaliana. Nat. Biotechnol. 28, 149–156.
35. Leonhardt, N., Kwak, J.M., Robert, N., Waner, D., Leonhardt, G. and Schroeder, J.I. (2004) Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphatase 2C mutant. Plant Cell, 16, 596–615.
36. Liu, Y., Wei, L., Batzoglou, S., Brutlag, D.L., Liu, J.S. and Shirley Liu, X. (2004) A suite of web-based programs to search for transcriptional regulatory motifs. Nucleic Acids Res. 32, W204–W207.
37. van Loon, L.C. and van Kammen, A. (1970) Polyacrylamide disc electrophoresis of the soluble leaf proteins from Nicotiana tabacum var. ‘Samsun’ and ‘Samsun NN’. II. Changes in protein constitution after infection with tobacco mosaic virus. Virology, 40, 190–211.
38. Ma, S., Shah, S., Bohnert, H.J., Snyder, M. and Dinesh-Kumar, S.P. (2013) Incorporating motif analysis into gene co-expression networks reveals novel modular expression pattern and new signaling pathways. PLoS Genet. 9, e1003840.
39. Mathelier, A., Zhao, X., Zhang, A.W. et al. (2013) JASPAR 2014: an extensively expanded and updated open-access database of transcription factor binding profiles. Nucleic Acids Res. 42, D142–D147.
40. Mikkelsen, M.D. and Thomashow, M.F. (2009) A role for circadian evening elements in cold-regulated gene expression in Arabidopsis. Plant J. 60, 328–339.
41. Nakabayashi, K., Okamoto, M., Koshiba, T., Kamiya, Y. and Nambara, E. (2005) Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. Plant J. 41, 697–709.
42. Nakashima, K., Fujita, Y., Katsura, K., Maruyama, K., Narusaka, Y., Seki, M., Shinozaki, K. and Yamaguchi-Shinozaki, K. (2006) Transcriptional regulation of ABI3- and ABA-responsive genes including RD29B and RD29A in seeds, germinating embryos, and seedlings of Arabidopsis. Plant Mol. Biol. 60, 51–68.
43. Nomura, K., Melotto, M. and He, S.-Y. (2005) Suppression of host defense in compatible plant-Pseudomonas syringae interactions. Curr. Opin. Plant Biol. 8, 361–368.
44. Obayashi, T., Nishida, K., Kasahara, K. and Kinoshita, K. (2011) ATTED-II updates: condition-specific gene coexpression to extend coexpression analyses and applications to a broad range of flowering plants. Plant Cell Physiol. 52, 213–219.
45. Patel, R.Y. and Stormo, G.D. (2014) Discriminative motif optimization based on perceptron training. Bioinformatics, 30, 941–948.
46. Pavesi, G., Mauri, G. and Pesole, G. (2001) An algorithm for finding signals of unknown length in DNA sequences. Bioinformatics, 17(Suppl 1), S207–S214.
47. Pearce, S., Ferguson, A., King, J. and Wilson, Z.A. (2015) FlowerNet: a gene expression correlation network for anther and pollen development. Plant Physiol. 167, 1717–1730.
48. Redhead, E. and Bailey, T.L. (2007) Discriminative motif discovery in DNA and protein sequences using the DEME algorithm. BMC Bioinformatics, 8, 385.
49. Schmid, M., Davison, T.S., Henz, S.R., Pape, U.J., Demar, M., Vingron, M., Schölkopf, B., Weigel, D. and Lohmann, J.U. (2005) A gene expression map of Arabidopsis thaliana development. Nat. Genet. 37, 501–506.
50. Schneider, T.D. and Stephens, R.M. (1990) Sequence logos: a new way to display consensus sequences. Nucleic Acids Res. 18, 6097–6100.
51. Simcha, D., Price, N.D. and Geman, D. (2012) The limits of de novo DNA motif discovery. PLoS ONE, 7, e47836.
52. Sinha, S. and Tompa, M. (2003) YMF: a program for discovery of novel transcription factor binding sites by statistical overrepresentation. Nucleic Acids Res. 31, 3586–3588.
53. Spencer, M.W.B., Casson, S.A. and Lindsey, K. (2007) Transcriptional profiling of the Arabidopsis embryo. Plant Physiol. 143, 924–940.
54. Srinivasasainagendra, V., Page, G.P., Mehta, T., Coulibaly, I. and Loraine, A.E. (2008) CressExpress: a tool for large-scale mining of expression data from Arabidopsis. Plant Physiol. 147, 1004–1016.
55. Stormo, G.D. and Fields, D.S. (1998) Specificity, free energy and information content in protein-DNA interactions. Trends Biochem. Sci. 23, 109–113.
56. Suh, M.C., Lacey Samuels, A., Jetter, R., Kunst, L., Pollard, M., Ohlrogge, J. and Beisson, F. (2005) Cuticular lipid composition, surface structure, and gene expression in Arabidopsis stem epidermis. Plant Physiol. 139, 1649–1665.
57. Sullivan, A.M., Arsovski, A.A., Lempe, J. et al. (2014) Mapping and dynamics of regulatory DNA and transcription factor networks in A. thaliana. Cell Rep. 8, 2015–2030.
58. Thijs, G., Lescot, M., Marchal, K., Rombauts, S., De Moor, B., Rouzé, P. and Moreau, Y. (2001) A higher-order background model improves the detection of promoter regulatory elements by Gibbs sampling. Bioinformatics, 17, 1113–1122.
59. Toufighi, K., Brady, S.M., Austin, R., Ly, E. and Provart, N.J. (2005) The botany array resource: E-Northerns, Expression Angling, and promoter analyses. Plant J. 43, 153–163.
60. Truernit, E., Stadler, R., Baier, K. and Sauer, N. (1999) A male gametophyte-specific monosaccharide transporter in Arabidopsis. Plant J. 17, 191–201.
61. Usadel, B., Obayashi, T., Mutwil, M., Giorgi, F.M., Bassel, G.W., Tanimoto, M., Chow, A., Steinhauser, D., Persson, S. and Provart, N.J. (2009) Co-expression tools for plant biology: opportunities for hypothesis generation and caveats. Plant Cell Environ. 32, 1633–1651.
62. Weirauch, M.T., Yang, A., Albu, M. et al. (2014) Determination and inference of eukaryotic transcription factor sequence specificity. Cell, 158, 1431–1443.
63. Whitington, T., Frith, M.C., Johnson, J. and Bailey, T.L. (2011) Inferring transcription factor complexes from ChIP-Seq data. Nucleic Acids Res. 39, e98.
64. Winter, D., Vinegar, B., Nahal, H., Ammar, R., Wilson, G.V. and Provart, N.J. (2007) An ‘electronic fluorescent pictograph’ browser for exploring and analyzing large-scale biological data sets. PLoS ONE, 2, e718.
65. Winter, C.M., Austin, R.S., Blanvillain-Baufumé, S. et al. (2011) LEAFY target genes reveal floral regulatory logic, cis motifs, and a link to biotic stimulus response. Dev. Cell, 20, 430–443.
66. Yang, Y., Costa, A., Leonhardt, N., Siegel, R.S. and Schroeder, J.I. (2008) Isolation of a strong Arabidopsis guard cell promoter and its potential as a research tool. Plant Methods, 4, 6.
67. Yao, Z., Macquarrie, K.L., Fong, A.P. et al. (2014) Discriminative motif analysis of high-throughput datasets. Bioinformatics, 30, 775–783.
68. Zhang, H., Liang, W., Yang, X., Luo, X., Jiang, N., Ma, H. and Zhang, D. (2010) Carbon starved anther encodes a MYB domain protein that regulates sugar partitioning required for rice pollen development. Plant Cell Online, 22, 672–689.
69. Zipfel, C. and Felix, G. (2005) Plants and animals: a different taste for microbes? Curr. Opin. Plant Biol. 8, 353–360.