Paired-end analysis of transcription start sites in Arabidopsis reveals plant-specific promoter signatures

Plant Cell

Volumn 26, Issue 7, 2014, Pages 2746-2760

  Morton, Taj ^a   Petricka, Jalean ^b,c   Corcoran, David L ^b   Li, Song ^b   Winter, Cara M ^b   Carda, Alexa ^b   Benfey, Philip N ^b   Ohler, Uwe ^b,d,e,f   Megraw, Molly ^a,b,g  

^a 1148 Kelley Engineering Center Corvallis   (United States)

^b DUKE UNIVERSITY   (United States)

^c CARLETON COLLEGE   (United States)

^d Duke University   (United States)

^e DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^g OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; MESSENGER RNA; PLANT DNA; PLANT RNA; TRANSCRIPTION FACTOR;

ARABIDOPSIS; BINDING SITE; BIOLOGICAL MODEL; CLUSTER ANALYSIS; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NUCLEOTIDE MOTIF; PLANT GENOME; PLANT ROOT; PROCEDURES; PROMOTER REGION; SPECIES DIFFERENCE; TATA BOX; TRANSCRIPTION INITIATION SITE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BINDING SITES; CLUSTER ANALYSIS; DNA, PLANT; GENE EXPRESSION REGULATION, PLANT; GENOME, PLANT; MODELS, GENETIC; NUCLEOTIDE MOTIFS; PLANT ROOTS; PROMOTER REGIONS, GENETIC; RNA, MESSENGER; RNA, PLANT; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; TATA BOX; TRANSCRIPTION FACTORS; TRANSCRIPTION INITIATION SITE;

EID: 84907338600     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.125617     Document Type: Article

References (54)

1. Arabidopsis Genome Initiative (2000). Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-815.
2. Batut, P., Dobin, A., Plessy, C., Carninci, P., and Gingeras, T.R. (2013). High-fidelity promoter profiling reveals widespread alternative promoter usage and transposon-driven developmental gene expression. Genome Res. 23: 169-180.
3. Beissbarth, T., and Speed, T.P. (2004). GOstat: find statistically overrepresented Gene Ontologies within a group of genes. Bioinformatics 20: 1464-1465.
4. Berardini, T.Z., et al. (2004). Functional annotation of the Arabidopsis genome using controlled vocabularies. Plant Physiol. 135: 745-755.
5. Bhattacharyya, M., Das, M., and Bandyopadhyay, S. (2012). miRT: a database of validated transcription start sites of human microRNAs. Genomics Proteomics Bioinformatics 10: 310-316.
6. Brady, S.M., Orlando, D.A., Lee, J.Y., Wang, J.Y., Koch, J., Dinneny, J.R., Mace, D., Ohler, U., and Benfey, P.N. (2007). A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318: 801-806.
7. Bruex, A., Kainkaryam, R.M., Wieckowski, Y., Kang, Y.H., Bernhardt, C., Xia, Y., Zheng, X., Wang, J.Y., Lee, M.M., Benfey, P., Woolf, P.J., and Schiefelbein, J. (2012). A gene regulatory network for root epidermis cell differentiation in Arabidopsis. PLoS Genet. 8: e1002446.
8. Bryne, J.C., Valen, E., Tang, M.H., Marstrand, T., Winther, O., da Piedade, I., Krogh, A., Lenhard, B., and Sandelin, A. (2008). JASPAR, the open access database of transcription factor-binding profiles: new content and tools in the 2008 update. Nucleic Acids Res. 36: D102-D106.
9. Carninci, P., et al. (2006). Genome-wide analysis of mammalian promoter architecture and evolution. Nat. Genet. 38: 626-635.
10. Carninci, P., et al; FANTOM Consortium; RIKEN Genome Exploration Research Group and Genome Science Group (Genome Network Project Core Group) (2005). The transcriptional landscape of the mammalian genome. Science 309: 1559-1563.
11. Civán, P., and Svec, M. (2009). Genome-wide analysis of rice (Oryza sativa L. subsp. japonica) TATA box and Y Patch promoter elements. Genome 52: 294-297.
12. David, L., Huber, W., Granovskaia, M., Toedling, J., Palm, C.J., Bofkin, L., Jones, T., Davis, R.W., and Steinmetz, L.M. (2006). A high-resolution map of transcription in the yeast genome. Proc. Natl. Acad. Sci. USA 103: 5320-5325.
13. Deaton, A.M., and Bird, A. (2011). CpG islands and the regulation of transcription. Genes Dev. 25: 1010-1022.
14. Frith, M.C., Valen, E., Krogh, A., Hayashizaki, Y., Carninci, P., and Sandelin, A. (2008). A code for transcription initiation in mammalian genomes. Genome Res. 18: 1-12.
15. Gowda, M., Li, H., Alessi, J., Chen, F., Pratt, R., and Wang, G.L. (2006). Robust analysis of 59-transcript ends (59-RATE): a novel technique for transcriptome analysis and genome annotation. Nucleic Acids Res. 34: e126.
16. Grasser, K.E., ed (2006). Regulation of Transcription in Plants. (Oxford, UK: Wiley-Blackwell).
17. Griffiths-Jones, S., Grocock, R.J., van Dongen, S., Bateman, A., and Enright, A.J. (2006). miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res. 34: D140-D144.
18. Grünberg, S., and Hahn, S. (2013). Structural insights into transcription initiation by RNA polymerase II. Trends Biochem. Sci. 38: 603-611.
19. Hoskins, R.A., et al. (2011). Genome-wide analysis of promoter architecture in Drosophila melanogaster. Genome Res. 21: 182-192.
20. Jorjani, H., and Zavolan, M. (2014). TSSer: an automated method to identify transcription start sites in prokaryotic genomes from differential RNA sequencing data. Bioinformatics 30: 971-974.
21. Juven-Gershon, T., and Kadonaga, J.T. (2010). Regulation of gene expression via the core promoter and the basal transcriptional machinery. Dev. Biol. 339: 225-229.
22. Kadonaga, J.T. (2004). Regulation of RNA polymerase II transcription by sequence-specific DNA binding factors. Cell 116: 247-257.
23. Kadonaga, J.T. (2012). Perspectives on the RNA polymerase II core promoter. Wiley interdisciplinary reviews. Dev. Biol. 1: 40-51.
24. Kapranov, P. (2009). From transcription start site to cell biology. Genome Biol. 10: 217.
25. Koh, K., Kim, S.-J., and Boyd, S. (2007). An interior-point method for large-scale l1-regularized logistic regression. Mach. Learn. Res. 8: 1519-1555.
26. Lamesch, P., et al. (2012). The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res. 40: D1202-D1210.
27. Lan, P., Li, W., Lin, W.-D., Santi, S., and Schmidt, W. (2013). Mapping gene activity of Arabidopsis root hairs. Genome Biol. 14: R67.
28. Li, S., Liberman, L.M., Mukherjee, N., Benfey, P.N., and Ohler, U. (2013). Integrated detection of natural antisense transcripts using strand-specific RNA sequencing data. Genome Res. 23: 1730-1739.
29. Lobo, J.M., Jiménez-Valverde, A., and Real, R. (2008). AUC: a misleading measure of the performance of predictive distribution models. Glob. Ecol. Biogeogr. 17: 145-151.
30. Marco, A., Ninova, M., Ronshaugen, M., and Griffiths-Jones, S. (2013). Clusters of microRNAs emerge by new hairpins in existing transcripts. Nucleic Acids Res. 41: 7745-7752.
31. Megraw, M., Baev, V., Rusinov, V., Jensen, S.T., Kalantidis, K., and Hatzigeorgiou, A.G. (2006). MicroRNA promoter element discovery in Arabidopsis. RNA 12: 1612-1619.
32. Megraw, M., Mukherjee, S., and Ohler, U. (2013). Sustained-input switches for transcription factors and microRNAs are central building blocks of eukaryotic gene circuits. Genome Biol. 14: R85.
33. Megraw, M., Pereira, F., Jensen, S.T., Ohler, U., and Hatzigeorgiou, A.G. (2009). A transcription factor affinity-based code for mammalian transcription initiation. Genome Res. 19: 644-656.
34. Morton, T., and Megraw, M. (2014). 3PEAT TFBS-Scanner Toolset, http://megraw.cgrb.oregonstate.edu/software/3PEAT/.
35. Nakamura, M., Tsunoda, T., and Obokata, J. (2002). Photosynthesis nuclear genes generally lack TATA-boxes: a tobacco photosystem I gene responds to light through an initiator. Plant J. 29: 1-10.
36. Nepal, C., et al. (2013). Dynamic regulation of the transcription initiation landscape at single nucleotide resolution during vertebrate embryogenesis. Genome Res. 23: 1938-1950.
37. Ni, T., Corcoran, D.L., Rach, E.A., Song, S., Spana, E.P., Gao, Y., Ohler, U., and Zhu, J. (2010). A paired-end sequencing strategy to map the complex landscape of transcription initiation. Nat. Methods 7: 521-527.
38. Park, D., Morris, A.R., Battenhouse, A., and Iyer, V.R. (2014). Simultaneous mapping of transcript ends at single-nucleotide resolution and identification of widespread promoter-associated non-coding RNA governed by TATA elements. Nucleic Acids Res. 42: 3736-3749.
39. Rach, E.A., Winter, D.R., Benjamin, A.M., Corcoran, D.L., Ni, T., Zhu, J., and Ohler, U. (2011). Transcription initiation patterns indicate divergent strategies for gene regulation at the chromatin level. PLoS Genet. 7: e1001274.
40. Rach, E.A., Yuan, H.-Y., Majoros, W.H., Tomancak, P., and Ohler, U. (2009). Motif composition, conservation and condition-specificity of single and alternative transcription start sites in the Drosophila genome. Genome Biol. 10: R73.
41. Rogers, K., and Chen, X. (2013). Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell 25: 2383-2399.
42. Saini, H.K., Griffiths-Jones, S., and Enright, A.J. (2007). Genomic analysis of human microRNA transcripts. Proc. Natl. Acad. Sci. USA 104: 17719-17724.
43. Saxonov, S., Berg, P., and Brutlag, D.L. (2006). A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters. Proc. Natl. Acad. Sci. USA 103: 1412-1417.
44. Shahmuradov, I.A., Solovyev, V.V., and Gammerman, A.J. (2005). Plant promoter prediction with confidence estimation. Nucleic Acids Res. 33: 1069-1076.
45. Shahmuradov, I.A., Gammerman, A.J., Hancock, J.M., Bramley, P.M., and Solovyev, V.V. (2003). PlantProm: a database of plant promoter sequences. Nucleic Acids Res. 31: 114-117.
46. Shiraki, T., et al. (2003). Cap analysis gene expression for high-throughput analysis of transcriptional starting point and identification of promoter usage. Proc. Natl. Acad. Sci. USA 100: 15776-15781.
47. Smale, S.T., and Kadonaga, J.T. (2003). The RNA polymerase II core promoter. Annu. Rev. Biochem. 72: 449-479.
48. Thomas, M.C., and Chiang, C.M. (2006). The general transcription machinery and general cofactors. Crit. Rev. Biochem. Mol. Biol. 41: 105-178.
49. Wingender, E. (2008). The TRANSFAC project as an example of framework technology that supports the analysis of genomic regulation. Brief. Bioinform. 9: 326-332.
50. Xie, Z., Allen, E., Fahlgren, N., Calamar, A., Givan, S.A., and Carrington, J.C. (2005). Expression of Arabidopsis MIRNA genes. Plant Physiol. 138: 2145-2154.
51. Yamamoto, Y.Y., Ichida, H., Abe, T., Suzuki, Y., Sugano, S., and Obokata, J. (2007). Differentiation of core promoter architecture between plants and mammals revealed by LDSS analysis. Nucleic Acids Res. 35: 6219-6226.
52. Yamamoto, Y.Y., Yoshioka, Y., Hyakumachi, M., and Obokata, J. (2011). Characteristics of core promoter types with respect to gene structure and expression in Arabidopsis thaliana. DNA Res. 18: 333-342.
53. Yamamoto, Y.Y., Yoshitsugu, T., Sakurai, T., Seki, M., Shinozaki, K., and Obokata, J. (2009). Heterogeneity of Arabidopsis core promoters revealed by high-density TSS analysis. Plant J. 60: 350-362.
54. Yamashita, R., Sathira, N.P., Kanai, A., Tanimoto, K., Arauchi, T., Tanaka, Y., Hashimoto, S., Sugano, S., Nakai, K., and Suzuki, Y. (2011). Genome-wide characterization of transcriptional start sites in humans by integrative transcriptome analysis. Genome Res. 21: 775-789.