Visual analysis of transcriptome data in the context of anatomical structures and biological networks

Frontiers in Plant Science

Volumn 3, Issue NOV, 2012, Pages

  Junker, Astrid ^a   Rohn, Hendrik ^a   Schreiber, Falk ^a,b,c  

^a LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^c MONASH UNIVERSITY   (Australia)

Author keywords

Biological network; Color coding; Data integration; Expression atlas; Omics data visualization; Systems biology graphical notation; Visual analytics

Indexed keywords

EID: 84900840817     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2012.00252     Document Type: Article

References (93)

1. Abramoff, M. D., Magalhães, P. J., and Ram, S. J. (2004). Image processing with imageJ. Biophotonics Int. 11, 36-42.
2. Atias, O., Chor, B., and Chamovitz, D. A. (2009). Large-scale analysis of Arabidopsis transcription reveals a basal co-regulation network. BMC Syst. Biol. 3, 86. doi:10.1186/1752-0509-3-86
3. Benedito, V. A., Torres-Jerez, I., Murray, J. D., Andriankaja, A., Allen, S., Kakar, K., et al. (2008). A gene expression atlas of the model legume Medicago truncatula. Plant J. 55, 504-513.
4. Birnbaum, K., Shasha, D. E., Wang, J. Y., Jung, J. W., Lambert, G. M., Galbraith, D. W., et al. (2003). A gene expression map of the Arabidopsis root. Science 302, 1956-1960.
5. Brandao, M. M., Dantas, L. L., and Silva-Filho, M. C. (2009). AtPIN: Arabidopsis thaliana protein interaction network. BMC Bioinformatics 10, 454. doi:10.1186/1471-2105-10-454
6. Brazma, A., Parkinson, H., Sarkans, U., Shojatalab, M., Vilo, J., Abeygunawardena, N., et al. (2003). ArrayExpress-a public repository for microarray gene expression data at the EBI. Nucleic Acids Res. 31, 68-71.
7. Brooks, L. III., Strable, J., Zhang, X., Ohtsu, K., Zhou, R., Sarkar, A., et al. (2009). Microdissection of shoot meristem functional domains. PLoS Genet. 5, e1000476. doi:10.1371/journal.pgen.1000476
8. Cai, S., and Lashbrook, C. C. (2008). Stamen abscission zone transcriptome profiling reveals new candidates for abscission control: enhanced retention of floral organs in transgenic plants overexpressing Arabidopsis ZINC FINGER PROTEIN2. Plant Physiol. 146, 1305-1321.
9. Card, S. K., Mackinlay, J. D., and Shneiderman, B. (eds). (1999). Readings in Information Visualization: Using Vision to Think. San Francisco: Morgan Kaufmann Publishers Inc.
10. Carr, D. (1999). "Guidelines for designing information visualization applications, " Proceedings of the 1999 Ericsson Conference on Usability Engineering, Stockholm.
11. Caspi, R., Foerster, H., Fulcher, C. A., Hopkinson, R., Ingraham, J., Kaipa, P., et al. (2006). MetaCyc: a multiorganism database of metabolic pathways and enzymes. Nucleic Acids Res. 34, D511-D516.
12. Cerami, E. G., Gross, B. E., Demir, E., Rodchenkov, I., Babur, O., Anwar, N., et al. (2011). Pathway commons, a web resource for biological pathway data. Nucleic Acids Res. 39, D685-D690.
13. Coen, E. S., and Meyerowitz, E. M. (1991). The war of the whorls: genetic interactions controlling flower development. Nature 353, 31-37.
14. Craigon, D. J., James, N., Okyere, J., Higgins, J., Jotham, J., and May, S. (2004). NASCArrays: a repository for microarray data generated by NASC's transcriptomics service. Nucleic Acids Res. 32, D575-D577.
15. Croft, D., O'Kelly, G., Wu, G., Haw, R., Gillespie, M., Matthews, L., et al. (2011). Reactome: a database of reactions, pathways and biological processes. Nucleic Acids Res. 39, D691-D697.
16. Czauderna, T., Klukas, C., and Schreiber, F. (2010). Editing, validating and translating of SBGN maps. Bioinformatics26, 2340-2341.
17. Day, R. C. (2010). Laser microdissection of paraffin-embedded plant tissues for transcript profiling. Methods Mol. Biol. 655, 321-346.
18. Demir, E., Cary, M. P., Paley, S., Fukuda, K., Lemer, C., Vastrik, I., et al. (2010). The BioPAX community standard for pathway data sharing. Nat. Biotechnol. 28, 935-942.
19. Edgar, R., Domrachev, M., and Lash, A. E. (2002). Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30, 207-210.
20. Endo, A., Tatematsu, K., Hanada, K., Duermeyer, L., Okamoto, M., Yonekura-Sakakibara, K., et al. (2012). Tissue-specific transcriptome analysis reveals cell wall metabolism, flavonol biosynthesis and defense responses are activated in the endosperm of germinating Arabidopsis thaliana seeds. Plant Cell Physiol. 53, 16-27.
21. Fei, Z., Tang, X., Alba, R., and Giovannoni, J. (2006). Tomato expression database (TED): a suite of data presentation and analysis tools. Nucleic Acids Res. 34, D766-D770.
22. Ficklin, S. P., and Feltus, F. A. (2011). Gene coexpression network alignment and conservation of gene modules between two grass species: maize and rice. Plant Physiol. 156, 1244-1256.
23. Flanagan, C. A., and Ma, H. (1994). Spatially and temporally regulated expression of the MADS-box gene AGL2 in wild-type and mutant arabidopsis flowers. Plant Mol. Biol. 26, 581-595.
24. Gehlenborg, N., O'Donoghue, S. I., Baliga, N. S., Goesmann, A., Hibbs, M. A., Kitano, H., et al. (2010). Visualization of omics data for systems biology. Nat. Methods 7, S56-S68.
25. Huaiyu, M., Schreiber, F., Le Novère, N., Moodie, S., and Sorokin, A. (2009). Systems biology graphical notation: activity flow language level 1. Nat. Prec. doi: 10.1038/npre.2009.3724.1
26. Hucka, M., Finney, A., Sauro, H. M., Bolouri, H., Doyle, J. C., Kitano, H., et al. (2003). The systems biology markup language (SBML): a medium for representation and exchange of biochemical network models. Bioinformatics 19, 524-531.
27. Jayapandian, M., Chapman, A., Tarcea, V. G., Yu, C., Elkiss, A., Ianni, A., et al. (2007). Michigan molecular interactions (MiMI): putting the jigsaw puzzle together. Nucleic Acids Res. 35, D566-D571.
28. Junker, A., Hartmann, A., Schreiber, F., and Baumlein, H. (2010). An engineer's view on regulation of seed development. Trends Plant Sci. 15, 303-307.
29. Junker, A., Rohn, H., Czauderna, T., Klukas, C., Hartmann, A., and Schreiber, F. (2012). Creating interactive, web-based and data-enriched maps with the systems biology graphical notation. Nat. Protoc. 7, 579-593.
30. Junker, B. H., Klukas, C., and Schreiber, F. (2006). VANTED: A system for advanced data analysis and visualization in the context of biological networks. BMC Bioinformatics 7, 109. doi:10.1186/1471-2105-7-109
31. Kagaya, Y., Toyoshima, R., Okuda, R., Usui, H., Yamamoto, A., and Hattori, T. (2005). LEAFY COTYLEDON1 controls seed storage protein genes through its regulation of FUSCA3 and ABSCISIC ACID INSENSITIVE3. Plant Cell Physiol. 46, 399-406.
32. Kanehisa, M., Goto, S., Furumichi, M., Tanabe, M., and Hirakawa, M. (2010). KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic Acids Res. 38, D355-D360.
33. Kanehisa, M., Goto, S., Sato, Y., Furumichi, M., and Tanabe, M. (2012). KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 40, D109-D114.
34. Kelder, T., Van Iersel, M. P., Hanspers, K., Kutmon, M., Conklin, B. R., Evelo, C. T., et al. (2012). WikiPathways: building research communities on biological pathways. Nucleic Acids Res. 40, D1301-D1307.
35. Kerrien, S., Aranda, B., Breuza, L., Bridge, A., Broackes-Carter, F., Chen, C., et al. (2012). The intact molecular interaction database in 2012. Nucleic Acids Res. 40, D841-D846.
36. Kohler, J., Baumbach, J., Taubert, J., Specht, M., Skusa, A., Ruegg, A., et al. (2006). Graph-based analysis and visualization of experimental results with ONDEX. Bioinformatics 22, 1383-1390.
37. Kroj, T., Savino, G., Valon, C., Giraudat, J., and Parcy, F. (2003). Regulation of storage protein gene expression in Arabidopsis. Development 130, 6065-6073.
38. Le, B. H., Cheng, C., Bui, A. Q., Wagmaister, J. A., Henry, K. F., Pelletier, J., et al. (2010). Global analysis of gene activity during Arabidopsis seed development and identification of seed-specific transcription factors. Proc. Natl. Acad. Sci. U.S.A. 107, 8063-8070.
39. Le Novere, N., Hucka, M., Mi, H. Y., Moodie, S., Schreiber, F., Sorokin, A., et al. (2009). The systems biology graphical notation. Nat. Biotechnol. 27, 735-741.
40. Li, L., Wang, X., Stolc, V., Li, X., Zhang, D., Su, N., et al. (2006). Genome-wide transcription analyses in rice using tiling microarrays. Nat. Genet. 38, 124-129.
41. Libault, M., Farmer, A., Joshi, T., Takahashi, K., Langley, R. J., Franklin, L. D., et al. (2010). An integrated transcriptome atlas of the crop model Glycine max, and its use in comparative analyses in plants. Plant J. 63, 86-99.
42. Liu, X., Lu, T., Yu, S., Li, Y., Huang, Y., Huang, T., et al. (2007). A collection of 10,096 indica rice full-length cDNAs reveals highly expressed sequence divergence between Oryza sativa indica and japonica subspecies. Plant Mol. Biol. 65, 403-415.
43. Liu, Z., and Mara, C. (2010). Regulatory mechanisms for floral homeotic gene expression. Semin. Cell Dev. Biol. 21, 80-86.
44. Ma, S., Gong, Q., and Bohnert, H. J. (2007). An Arabidopsis gene network based on the graphical Gaussian model. Genome Res. 17, 1614-1625.
45. Mao, L., Van Hemert, J. L., Dash, S., and Dickerson, J. A. (2009). Arabidopsis gene co-expression network and its functional modules. BMC Bioinformatics 10, 346. doi:10.1186/1471-2105-10-346
46. Martin, A. R., and Ward, M. O. (1995). "High Dimensional Brushing for Interactive Exploration of Multivariate Data, " Proceedings of the 6th Conference on Visualization' 95, Washington, 271-278.
47. Matas, A. J., Yeats, T. H., Buda, G. J., Zheng, Y., Chatterjee, S., Tohge, T., et al. (2011). Tissue-and cell-type specific transcriptome profiling of expanding tomato fruit provides insights into metabolic and regulatory specialization and cuticle formation. Plant Cell 23, 3893-3910.
48. Meinke, D. W., Franzmann, L. H., Nickle, T. C., and Yeung, E. C. (1994). LEAFY COTYLEDON MUTANTS OF ARABIDOPSIS. Plant Cell 6, 1049-1064.
49. Mi, H., Dong, Q., Muruganujan, A., Gaudet, P., Lewis, S., and Thomas, P. D. (2010). PANTHER version 7: improved phylogenetic trees, orthologs and collaboration with the Gene Ontology Consortium. Nucleic Acids Res. 38, D204-D210.
50. Mochida, K., Uehara-Yamaguchi, Y., Yoshida, T., Sakurai, T., and Shinozaki, K. (2011). Global landscape of a co-expressed gene network in barley and its application to gene discovery in triticeae crops. Plant Cell Physiol. 52, 785-803.
51. Moodie, S., Le Novère, N., Demir, E., Huaiyu, M., and Villeger, A. (2011). Systems biology graphical notation: process description language level 1v3. Nat. Prec. doi:10.1038/npre.2011.3721.4
52. Moreno-Risueno, M. A., Busch, W., and Benfey, P. N. (2010). Omics meet networks-using systems approaches to infer regulatory networks in plants. Curr. Opin. Plant Biol. 13, 126-131.
53. Mutwil, M., Klie, S., Tohge, T., Giorgi, F. M., Wilkins, O., Campbell, M. M., et al. (2011). PlaNet: combined sequence and expression comparisons across plant networks derived from seven species. Plant Cell 23, 895-910.
54. Mutwil, M., Usadel, B., Schutte, M., Loraine, A., Ebenhoh, O., and Persson, S. (2010). Assembly of an interactive correlation network for the Arabidopsis genome using a novel heuristic clustering algorithm. Plant Physiol. 152, 29-43.
55. Nelson, T., Gandotra, N., and Tausta, S. L. (2008). Plant cell types: reporting and sampling with new technologies. Curr. Opin. Plant Biol. 11, 567-573.
56. Nelson, T., Tausta, S. L., Gandotra, N., and Liu, T. (2006). Laser microdissection of plant tissue: what you see is what you get. Annu. Rev. Plant Biol. 57, 181-201.
57. Obayashi, T., Hayashi, S., Saeki, M., Ohta, H., and Kinoshita, K. (2009). ATTED-II provides coexpressed gene networks for Arabidopsis. Nucleic Acids Res. 37, D987-D991.
58. 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.
59. Ogata, H., Goto, S., Sato, K., Fujibuchi, W., Bono, H., and Kanehisa, M. (1999). KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 27, 29-34.
60. Ogata, Y., Suzuki, H., and Shibata, D. (2009). A database for poplar gene co-expression analysis for systematic understanding of biological processes, including stress responses. J. Wood Sci. 55, 395-400.
61. Pelaz, S., Ditta, G. S., Baumann, E., Wisman, E., and Yanofsky, M. F. (2000). B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405, 200-203.
62. Razick, S., Magklaras, G., and Donaldson, I. M. (2008). iRefIndex: a consolidated protein interaction database with provenance. BMC Bioinformatics 9, 405. doi:10.1186/1471-2105-9-405
63. Rohn, H., Klukas, C., and Schreiber, F. (2011). Creating views on integrated multidomain data. Bioinformatics 27, 1839-1845.
64. Santos-Mendoza, M., Dubreucq, B., Baud, S., Parcy, F., Caboche, M., and Lepiniec, L. (2008). Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis. Plant J. 54, 608-620.
65. Schmid, M., Davison, T. S., Henz, S. R., Pape, U. J., Demar, M., Vingron, M., et al. (2005). A gene expression map of Arabidopsis thaliana development. Nat. Genet. 37, 501-506.
66. Schmidt, A., Wuest, S. E., Vijverberg, K., Baroux, C., Kleen, D., and Grossniklaus, U. (2011). Transcriptome analysis of the Arabidopsis megaspore mother cell uncovers the importance of RNA helicases for plant germline development. PLoS Biol. 9, e1001155.
67. Schreiber, F., Colmsee, C., Czauderna, T., Grafahrend-Belau, E., Junker, A., Junker, B. H., et al. (2012). MetaCrop 2.0: managing and exploring information about crop plant metabolism. Nucleic Acid Res. 40, D1173-D1177.
68. Severin, A. J., Woody, J. L., Bolon, Y. T., Joseph, B., Diers, B. W., Farmer, A. D., et al. (2010). RNA-seq atlas ofGlycine max: a guide to the soybean transcriptome. BMC Plant Biol. 10, 160.
69. Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., et al. (2003). Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504.
70. Sherlock, G., Hernandez-Boussard, T., Kasarskis, A., Binkley, G., Matese, J. C., Dwight, S. S., et al. (2001). The stanford microarray database. Nucleic Acids Res. 29, 152-155.
71. Sjodin, A., Street, N. R., Sandberg, G., Gustafsson, P., and Jansson, S. (2009). The populus genome integrative explorer (PopGenIE): a new resource for exploring the populus genome. New Phytol. 182, 1013-1025.
72. Stalling, D., Westerhoff, M., and Hege, H. C. (2005). "Amira: A highly interactive system for visual data analysis, " inThe Visualization Handbook, eds C. D. Hansen and C. R. Johnson (Orlanda, FL: Academic Press, Inc.), 749-767.
73. Stark, C., Breitkreutz, B. J., Reguly, T., Boucher, L., Breitkreutz, A., and Tyers, M. (2006). BioGRID: a general repository for interaction datasets. Nucleic Acids Res. 34, D535-D539.
74. Steinhauser, D., Usadel, B., Luedemann, A., Thimm, O., and Kopka, J. (2004). CSB. DB: a comprehensive systems-biology database. Bioinformatics 20, 3647-3651.
75. Stone, S. L., Braybrook, S. A., Paula, S. L., Kwong, L. W., Meuser, J., Pelletier, J., et al. (2008). Arabidopsis LEAFY COTYLEDON2 induces maturation traits and auxin activity: Implications for somatic embryogenesis. Proc. Natl. Acad. Sci. U.S.A. 105, 3151-3156.
76. Suderman, M., and Hallett, M. (2007). Tools for visually exploring biological networks. Bioinformatics 23, 2651-2659.
77. Szklarczyk, D., Franceschini, A., Kuhn, M., Simonovic, M., Roth, A., Minguez, P., et al. (2011). The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res. 39, D561-D568.
78. Theissen, G., and Saedler, H. (2001). Plant biology. Floral quartets. Nature 409, 469-471.
79. Thiel, J., Riewe, D., Rutten, T., Melzer, M., Friedel, S., Bollenbeck, F., et al. (2012). Differentiation of endosperm transfer cells of barley: a comprehensive analysis at the micro-scale. Plant J. 71, 639-655.
80. To, A., Valon, C., Savino, G., Guilleminot, J., Devic, M., Giraudat, J., et al. (2006). A network of local and redundant gene regulation governs Arabidopsis seed maturation. Plant Cell 18, 1642-1651.
81. Van Iersel, M. P., Kelder, T., Pico, A. R., Hanspers, K., Coort, S., Conklin, B. R., et al. (2008). Presenting and exploring biological pathways with pathvisio. BMC Bioinformatics 9, 399.
82. Van Iersel, M. P., Villeger, A. C., Czauderna, T., Boyd, S. E., Bergmann, F. T., Luna, A., et al. (2012). Software support for SBGN maps: SBGN-ML and LibSBGN. Bioinformatics 28, 2016-2021.
83. Wagner, D., Sablowski, R. W., and Meyerowitz, E. M. (1999). Transcriptional activation of APETALA1 by LEAFY. Science 285, 582-584.
84. Walter, T., Shattuck, D. W., Baldock, R., Bastin, M. E., Carpenter, A. E., Duce, S., et al. (2010). Visualization of image data from cells to organisms. Nat. Methods 7, S26-S41.
85. Ward, M. O., Grinstein, G., and Keim, D. (2010). Interactive Data Visualization: Foundations, Techniques, and Application. London: Transatlantic Publishers, 500.
86. Weigel, D., and Meyerowitz, E. M. (1994). The ABCs of floral homeotic genes. Cell 78, 203-209.
87. 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.
88. Wollmann, H., Mica, E., Todesco, M., Long, J. A., and Weigel, D. (2010). On reconciling the interactions between APETALA2, miR172 and AGAMOUS with the ABC model of flower development. Development 137, 3633-3642.
89. Yamada, K., Lim, J., Dale, J. M., Chen, H., Shinn, P., Palm, C. J., et al. (2003). Empirical analysis of transcriptional activity in the Arabidopsis genome. Science 302, 842-846.
90. Yang, H., Lu, P., Wang, Y., and Ma, H. (2012). The transcriptome landscape of Arabidopsis male meiocytes from high-throughput sequencing: the complexity and evolution of the meiotic process. Plant J. 65, 503-516.
91. Yilmaz, A., Mejia-Guerra, M. K., Kurz, K., Liang, X., Welch, L., and Grotewold, E. (2011). AGRIS: the Arabidopsis Gene Regulatory Information Server, an update. Nucleic Acids Res. 39, D1118-D1122.
92. Yu, H., Luscombe, N. M., Lu, H. X., Zhu, X., Xia, Y., Han, J. D., et al. (2004). Annotation transfer between genomes: protein-protein interologs and protein-DNA regulogs. Genome Res. 14, 1107-1118.
93. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L., and Gruissem, W. (2004). GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621-2632.