Automated conserved non-coding sequence (CNS) discovery reveals differences in gene content and promoter evolution among grasses

Frontiers in Plant Science

Volumn 4, Issue JUL, 2013, Pages

  Turco, Gina ^a,b   Schnable, James C ^a,c   Pedersen, Brent ^a,d   Freeling, Michael ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c DONALD DANFORTH PLANT SCIENCE CENTER   (United States)

^d UNIVERSITY OF COLORADO   (United States)

Author keywords

Comparative genomics; Conserved non coding sequences; Gene regulation; Genome evolution; Maize; Rice; Sorghum

Indexed keywords

EID: 84899149304     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00170     Document Type: Article

References (55)

1. Bailey, T. L. (2011). DREME: motif discovery in transcription factor ChIP-seq data. Bioinformatics 27, 1653-1659. doi: 10.1093/bioinformatics/btr261
2. Baucom, R. S., Estill, J. C., Chaparro, C., Upshaw, N., Jogi, A., Deragon, J. M., et al. (2009). Exceptional diversity, non-random distribution, and rapid evolution of retroelements in the B73 maize genome. PLoS Genet. 5:e1000732. doi: 10.1371/journal.pgen.1000732
3. Baxter, L., Jironkin, A., Hickman, R., Moore, J., Barrington, C., Krusche, P., et al. (2012). Conserved noncoding sequences highlight shared components of regulatory networks in dicotyledonous plants. Plant Cell 24, 3949-3965. doi: 10.1105/tpc.112.103010
4. Blanc, G., and Wolfe, K. H. (2004). Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16, 1679-1691. doi: 10.1105/tpc.021410
5. Bowers, J. E., Chapman, B. A., Rong, J., and Paterson, A. H. (2003). Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422, 433-438. doi: 10.1038/nature01521
6. Brunner, S., Fengler, K., Morgante, M., Tingey, S., and Rafalski, A. (2005). Evolution of DNA sequence nonhomologies among maize inbreds. Plant Cell 17, 343-360. doi: 10.1105/tpc.104.025627
7. Bulger, M., and Groudine, M. (2010). Enhancers: the abundance and function of regulatory sequences beyond promoters. Dev. Biol. 339, 250-257. doi: 10.1016/j.ydbio.2009.11.035
8. Dugas, D. V., Monaco, M. K., Olsen, A., Klein, R. R., Kumari, S., Ware, D., et al. (2011). Functional annotation of the transcriptome of Sorghum bicolor in response to osmotic stress and abscisic acid. BMC Genomics 12:514. doi: 10.1186/1471-2164-12-514
9. Force, A., Lynch, M., Pickett, F. B., Amores, A., Yan, Y. L., and Postlethwait, J. (1999). Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151, 1531-1545.
10. Freeling, M., Rapaka, L., Lyons, E., Pedersen, B., and Thomas, B. C. (2007). G-boxes, bigfoot genes, and environmental response: characterization of intragenomic conserved noncoding sequences in Arabidopsis. Plant Cell 19, 1441-1457. doi: 10.1105/tpc.107.050419
11. Freeling, M., and Subramaniam, S. (2009). Conserved noncoding sequences (CNSs) in higher plants. Curr. Opin. Plant Biol. 12, 126-132. doi: 10.1016/j.pbi.2009.01.005
12. Gao, G., Zhong, Y., Guo, A., Zhu, Q., Tang, W., Zheng, W., et al. (2006). DRTF: a database of rice transcription factors. Bioinformatics 22, 1286-1287. doi: 10.1093/bioinformatics/btl107
13. Gaut, B. S., and Doebley, J. F. (1997). DNA sequence evidence for the segmental allotetraploid origin of maize. Proc. Natl. Acad. Sci. U.S.A. 94, 6809-6814.
14. Harris, R. S. (2007). Improved Pairwise Alignment of Genomic DNA. Ph.D. thesis, The Pennsylvania State University.
15. 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. doi: 10.1093/nar/27.1.297
16. Hollister, J. D., Ross-Ibarra, J., and Gaut, B. S. (2010). Indel-associated mutation rate varies with mating system in flowering plants. Mol. Biol. Evol. 27, 409-416. doi: 10.1093/molbev/msp249
17. Inada, D. C., Bashir, A., Lee, C., Thomas, B. C., Ko, C., Goff, S. A., et al. (2003). Conserved noncoding sequences in the grasses. Genome Res. 13, 2030-2041. doi: 10.1101/gr.1280703
18. International Barley Sequencing Consortium. (2012). A physical, genetic and functional sequence assembly of the barley genome. Nature 491, 711-716. doi: 10.1038/nature11543
19. Jiang, N., Bao, Z., Zhang, X., Eddy, S. R., and Wessler, S. R. (2004). Pack-MULE transposable elements mediate gene evolution in plants. Nature 431, 569-573. doi: 10.1038/nature02953
20. Junion, G., Spivakov, M., Girardot, C., Braun, M., Gustafson, E. H., Birney, E., et al. (2012). A transcription factor collective defines cardiac cell fate and reflects lineage history. Cell 148, 473-486. doi: 10.1016/j.cell.2012.01.030
21. Kaplinsky, N. J., Braun, D. M., Penterman, J., Goff, S. A., and Freeling, M. (2002). Utility and distribution of conserved noncoding sequences in the grasses. Proc. Natl. Acad. Sci. U.S.A. 99, 6147-6151. doi: 10.1073/pnas.052139599
22. Kellogg, E. A. (2001). Evolutionary history of the grasses. Plant Physiol. 125, 1198-1205. doi: 10.1104/125.3.1198
23. Lee, A. P., Kerk, S. Y., Tan, Y. Y., Brenner, S., and Venkatesh, B. (2011). Ancient vertebrate conserved noncoding elements have been evolving rapidly in teleost fishes. Mol. Biol. Evol. 28, 1205-1215. doi: 10.1093/molbev/msq304
24. Li, X., Qian, Q., Fu, Z., Wang, Y., Xiong, G., Zeng, D., et al. (2003). Control of tillering in rice. Nature 422, 618-621. doi: 10.1038/nature01518
25. Loots, G. G., Locksley, R. M., Blankespoor, C. M., Wang, Z. E., Miller, W., Rubin, E. M., et al. (2000). Identification of a coordinate regulator of interleukins 4 13, and 5 by cross-species sequence comparisons. Science 288, 136-140. doi: 10.1126/science.288.5463.136
26. Lyons, E., and Freeling, M. (2008). How to usefully compare homologous plant genes and chromosomes as DNA sequences. Plant J. 53, 661-673. doi: 10.1111/j.1365-313X.2007.03326.x
27. Lyons, E., Pederson, B., Kane, J., and Freeling, M. (2008). The value of nonmodel genomes and an example using SynMap within CoGe to dissect the paleohexaploidy at preceeds the rosids. Trop. Plant Biol. 1, 181-190.
28. Maere, S., De Bodt, S., Raes, J., Casneuf, T., Van Montagu, M., Kuiper, M., et al. (2005). Modeling gene and genome duplications in eukaryotes. Proc. Natl. Acad. Sci. U.S.A. 102, 5454-5459. doi: 10.1073/pnas.0501102102
29. Mayer, K. F., Martis, M., Hedley, P. E., Simkova, H., Liu, H., Morris, J. A., et al. (2011). Unlocking the barley genome by chromosomal and comparative genomics. Plant Cell 23, 1249-1263. doi: 10.1105/tpc.110.082537
30. Montgomery, E. A., Huang, S. M., Langley, C. H., and Judd, B. H. (1991). Chromosome rearrangement by ectopic recombination in Drosophila melanogaster: genome structure and evolution. Genetics 129, 1085-1098.
31. Narusaka, Y., Nakashima, K., Shinwari, Z. K., Sakuma, Y., Furihata, T., Abe, H., et al. (2003). Interaction between two cis-acting elements, Aand DRE, BRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J. 34, 137-148.
32. Ouyang, S., Zhu, W., Hamilton, J., Lin, H., Campbell, M., Childs, K., et al. (2007). The TIGR Rice Genome Annotation Resource: improvements and new features. Nucleic Acids Res. 35, D883-D887. doi: 10.1093/nar/gkl976
33. Paterson, A. H., Bowers, J. E., and Chapman, B. A. (2004). Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc. Natl. Acad. Sci. U.S.A. 101, 9903-9908. doi: 10.1073/pnas.0307901101
34. Pedersen, B. S., Tang, H., and Freeling, M. (2011). Gobe: an interactive, web-based tool for comparative genomic visualization. Bioinformatics 27, 1015-1016. doi: 10.1093/bioinformatics/btr056
35. Raatz, B., Eicker, A., Schmitz, G., Fuss, E., Muller, D., Rossmann, S., et al. (2011). Specific expression of LATERAL SUPPRESSOR is controlled by an evolutionarily conserved 3′ enhancer. Plant J. 68, 400-412. doi: 10.1111/j.1365-313X.2011.04694.x
36. Reineke, A. R., Bornberg-Bauer, E., and Gu, J. (2011). Evolutionary divergence and limits of conserved non-coding sequence detection in plant genomes. Nucleic Acids Res. 39, 6029-6043. doi: 10.1093/nar/gkr179
37. Roberts, A., Pimentel, H., Trapnell, C., and Pachter, L. (2011). Identification of novel transcripts in annotated genomes using RNA-Seq. Bioinformatics 27, 2325-2329. doi: 10.1093/bioinformatics/btr355
38. Robinson, M. D., McCarthy, D. J., and Smyth, G. K. (2010). edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140. doi: 10.1093/bioinformatics/btp616
39. Schnable, J. C., and Freeling, M. (2011). Genes identified by visible mutant phenotypes show increased bias toward one of two subgenomes of maize. PLoS ONE 6:e17855. doi: 10.1371/journal.pone.0017855
40. Schnable, J. C., Freeling, M., and Lyons, E. (2012). Genome-wide analysis of syntenic gene deletion in the grasses. Genome Biol. Evol. 4, 265-277. doi: 10.1093/gbe/evs009
41. Schnable, J. C., Springer, N. M., and Freeling, M. (2011). Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss. Proc. Natl. Acad. Sci. U.S.A. 108, 4069-4074. doi: 10.1073/pnas.1101368108
42. Schnable, P. S., Ware, D., Fulton, R. S., Stein, J. C., Wei, F., Pasternak, S., et al. (2009). The B73 maize genome: complexity, diversity, and dynamics. Science 326, 1112-1115. doi: 10.1126/science.1178534
43. Seoighe, C., and Gehring, C. (2004). Genome duplication led to highly selective expansion of the Arabidopsis thaliana proteome. Trends Genet. 20, 461-464. doi: 10.1016/j.tig.2004.07.008
44. Spangler, J. B., Subramaniam, S., Freeling, M., and Feltus, F. A. (2012). Evidence of function for conserved noncoding sequences in Arabidopsis thaliana. New Phytol. 193, 241-252. doi: 10.1111/j.1469-8137.2011.03916.x
45. Subramaniam, S., Wang, X., Freeling, M., and Pires, J. C. (2013). The fate of Arabidopsis thaliana homeologous CNSs and their motifs in the paleohexaploid Brassica rapa. Genome Biol. Evol. 5, 646-660. doi: 10.1093/gbe/evt035
46. Sun, X., Zou, Y., Nikiforova, V., Kurths, J., and Walther, D. (2010). The complexity of gene expression dynamics revealed by permutation entropy. BMC Bioinformatics 11:607. doi: 10.1186/1471-2105-11-607
47. Swigonova, Z., Lai, J., Ma, J., Ramakrishna, W., Llaca, V., Bennetzen, J. L., et al. (2004). Close split of sorghum and maize genome progenitors. Genome Res. 14, 1916-1923. doi: 10.1101/gr.2332504
48. Tang, H., Lyons, E., Pedersen, B., Schnable, J. C., Paterson, A. H., and Freeling, M. (2011). Screening synteny blocks in pairwise genome comparisons through integer programming. BMC Bioinformatics 12:102. doi: 10.1186/1471-2105-12-102
49. Thomas, B. C., Rapaka, L., Lyons, E., Pedersen, B., and Freeling, M. (2007). Arabidopsis intragenomic conserved noncoding sequence. Proc. Natl. Acad. Sci. U.S.A. 104, 3348-3353. doi: 10.1073/pnas.0611574104
50. Thomas, T. L. (1993). Gene expression during plant embryogenesis and germination: an overview. Plant Cell 5, 1401-1410. doi: 10.1105/tpc.5.10.1401
51. Tran, L., Nakashima, K., Sakuma, Y., and Yamaguchi-Shinozaki, K. (2004). Isolation and functional analysis of Arabidodopsis stress-inducible NAC transcription factors that bind to a draught-responsive cis-element in the early response to dehydration stress1 promoter. Plant Cell 16, 2481-2498.
52. Venkataram, S., and Fay, J. C. (2010). Is transcription factor binding site turnover a sufficient explanation for cis-regulatory sequence divergence? Genome Biol. Evol. 2, 851-858. doi: 10.1093/gbe/evq066
53. Woodhouse, M. R., Schnable, J. C., Pedersen, B. S., Lyons, E., Lisch, D., Subramaniam, S., et al. (2010). Following tetraploidy in maize, a short deletion mechanism removed genes preferentially from one of the two homologs. PLoS Biol. 8:e1000409. doi: 10.1371/journal.pbio.1000409
54. Wu, T. D., and Nacu, S. (2010). Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics 26, 873-881. doi: 10.1093/bioinformatics/btq057
55. Zhang, W., Wu, Y., Schnable, J. C., Zeng, Z., Freeling, M., Crawford, G. E., et al. (2012). High-resolution mapping of open chromatin in the rice genome. Genome Res. 22, 151-162. doi: 10.1101/gr.131342.111