5.9
CiteScore
5.9
Impact Factor
Volume 49 Issue 12
Dec.  2022
Turn off MathJax
Article Contents

Systematic annotation of conservation states provides insights into regulatory regions in rice

doi: 10.1016/j.jgg.2022.04.003
Funds:

The authors acknowledge the High Performance Computing Center of Nanjing University for providing high-performance computing (HPC) resources. This work is supported by the Nanjing University Deng Feng Scholars Program, the Priority Academic Program Development (PAPD) of Jiangsu Higher Education Institutions, and the National Natural Science Foundation of China (32070656).

  • Received Date: 2021-12-18
  • Accepted Date: 2022-04-12
  • Rev Recd Date: 2022-04-08
  • Publish Date: 2022-04-22
  • Plant genomes contain a large fraction of noncoding sequences. The discovery and annotation of conserved noncoding sequences (CNSs) in plants is an ongoing challenge. Here we report the application of comparative genomics to systematically identify CNSs in 50 well-annotated Gramineae genomes using rice (Oryza sativa) as the reference. We conduct multiple-way whole-genome alignments to the rice genome. The rice genome is annotated as 20 conservation states (CSs) at single-nucleotide resolution using a multivariate hidden Markov model (ConsHMM) based on the multiple-genome alignments. Different states show distinct enrichments for various genomic features, and the conservation scores of CSs are highly correlated with the level of associated chromatin accessibility. We find that at least 33.5% of the rice genome is highly under selection, with more than 70% of the sequence lying outside of coding regions. A catalog of 855,366 regulatory CNSs is generated, and they significantly overlapped with putative active regulatory elements such as promoters, enhancers, and transcription factor binding sites. Collectively, our study provides a resource for elucidating functional noncoding regions of the rice genome and an evolutionary aspect of regulatory sequences in higher plants.
  • loading
  • Alföldi, J.,Lindblad-Toh, K., 2013. Comparative genomics as a tool to understand evolution and disease. Genome Res. 23, 1063-1068
    Arneson, A.,Ernst, J., 2019. Systematic discovery of conservation states for single-nucleotide annotation of the human genome. Commun. Biol. 2, 248
    Blanchette, M., Kent, W.J., Riemer, C., Elnitski, L., Smit, A.F., Roskin, K.M., Baertsch, R., Rosenbloom, K., Clawson, H., Green, E.D., Haussler D., Miller W., 2004. Aligning multiple genomic sequences with the threaded blockset aligner. Genome Res. 14, 708-715
    Bolger, A.M., Lohse, M.,Usadel, B., 2014. Trimmomatic: A flexible trimmer for illumina sequence data. Bioinformatics 30, 2114-2120
    Bolser, D., Staines, D.M., Pritchard, E.,Kersey, P., 2016. Ensembl plants: Integrating tools for Visualizing, Mining, and Analyzing Plant Genomics Data, Plant bioinformatics: Methods and protocols. pp, 115-140
    Bossolini, E., Wicker, T., Knobel, P.A.,Keller, B., 2007. Comparison of orthologous loci from small grass genomes brachypodium and rice: Implications for wheat genomics and grass genome annotation. Plant J. 49, 704-717
    Butler, D.,Pockley, P., 2000. … as monsanto makes rice genome public. Nature 404, 534-534
    Chen, S., Lin, X.H., Xu, C.G.,Zhang, Q., 2000. Improvement of bacterial blight resistance of ‘minghui 63’, an elite restorer line of hybrid rice, by molecular marker-assisted selection. Crop Sci. 40, 239-244
    Das, S.,Hirano, M., 2012. Comparative genomics and genome evolution. Curr. Genomics 13, 85-85
    Emms, D.M.,Kelly, S., 2019. Orthofinder: Phylogenetic orthology inference for comparative genomics. Genome Biol. 20, 238
    Ernst, J.,Kellis, M., 2012. Chromhmm: Automating chromatin-state discovery and characterization. Nat. Methods 9, 215-216
    Fan, X., Zhu, J., Schadt, E.E.,Liu, J.S., 2007. Statistical power of phylo-hmm for evolutionarily conserved element detection. BMC Bioinform. 8, 374
    Fang, Y., Wang, X., Wang, L., Pan, X., Xiao, J., Wang, X.-e., Wu, Y.,Zhang, W., 2016. Functional characterization of open chromatin in bidirectional promoters of rice. Sci. Rep. 6, 32088
    Flynn Jullien, M., Hubley, R., Goubert, C., Rosen, J., Clark Andrew, G., Feschotte, C.,Smit Arian, F., 2020. Repeatmodeler2 for automated genomic discovery of transposable element families. Proc. Natl. Acad. Sci. U.S.A. 117, 9451-9457
    Fu, L., Zhou, X., Yu, R., Wu, Z., Zhang, P., Chen, M., Kaufmann, K., & Chen, D. (2021). ChIP-Hub: an Integrative Platform for Exploring Plant Regulome. Nature Portfolio
    Frazer, K.A., Elnitski, L., Church, D.M., Dubchak, I.,Hardison, R.C., 2003. Cross-species sequence comparisons: A review of methods and available resources. Genome Res. 13, 1-12
    Freeling, M.,Subramaniam, S., 2009. Conserved noncoding sequences (cnss) in higher plants. Curr. Opin. Plant Biol. 12, 126-132
    Ganguly, D.R., Hickey, L.T.,Crisp, P.A., 2022. Harnessing genetic variation at regulatory regions to fine-tune traits for climate-resilient crops. Mol Plant 15, 222-224
    Goodstein, D.M., Shu, S., Howson, R., Neupane, R., Hayes, R.D., Fazo, J., Mitros, T., Dirks, W., Hellsten, U., Putnam, N., et al., 2012. Phytozome: A comparative platform for green plant genomics. Nucleic Acids Res. 40, D1178-D1186
    Guo, H.,Moose, S.P., 2003. Conserved noncoding sequences among cultivated cereal genomes identify candidate regulatory sequence elements and patterns of promoter evolution. Plant Cell 15, 1143-1158
    Harris, R.S. 2007. Improved pairwise alignment of genomic DNA. The Pennsylvania State University
    Haudry, A., Platts, A.E., Vello, E., Hoen, D.R., Leclercq, M., Williamson, R.J., Forczek, E., Joly-Lopez, Z., Steffen, J.G., Hazzouri, K.M., et al., 2013. An atlas of over 90,000 conserved noncoding sequences provides insight into crucifer regulatory regions. Nat. Genet. 45, 891-898
    Hendelman, A., Zebell, S., Rodriguez-Leal, D., Dukler, N., Robitaille, G., Wu, X., Kostyun, J., Tal, L., Wang, P., Bartlett, M.E., et al., 2021. Conserved pleiotropy of an ancient plant homeobox gene uncovered by cis-regulatory dissection. Cell 184, 1724-1739.e16
    Hubisz, M.J., Pollard, K.S.,Siepel, A., 2011. Phast and rphast: Phylogenetic analysis with space/time models. Brief. Bioinformatics 12, 41-51
    Inada, D.C., Bashir, A., Lee, C., Thomas, B.C., Ko, C., Goff, S.A.,Freeling, M., 2003. Conserved noncoding sequences in the grasses. Genome Res. 13, 2030-2041
    Inukai, Y., Sakamoto, T., Ueguchi-Tanaka, M., Shibata, Y., Gomi, K., Umemura, I., Hasegawa, Y., Ashikari, M., Kitano, H.,Matsuoka, M., 2005. Crown rootless1, which is essential for crown root formation in rice, is a target of an auxin response factor in auxin signaling. Plant Cell 17, 1387-1396
    Kaplinsky, N.J., Braun, D.M., Penterman, J., Goff, S.A.,Freeling, M., 2002. Utility and distribution of conserved noncoding sequences in the grasses. Proc. Natl. Acad. Sci. U.S.A. 99, 6147-6151
    Kent, W.J., Baertsch, R., Hinrichs, A., Miller, W.,Haussler, D., 2003. Evolution's cauldron: Duplication, deletion, and rearrangement in the mouse and human genomes. Proc. Natl. Acad. Sci. U.S.A. 100, 11484-11489
    Konishi, S., Izawa, T., Lin, S.Y., Ebana, K., Fukuta, Y., Sasaki, T.,Yano, M., 2006. An snp caused loss of seed shattering during rice domestication. Science 312, 1392-1396
    Langmead, B.,Salzberg, S.L., 2012. Fast gapped-read alignment with bowtie 2. Nat. Methods 9, 357-359
    Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G.,Durbin, R., 2009a. The sequence alignment/map format and samtools. Bioinformatics 25, 2078-2079
    Li, X., Tan, L., Wang, L., Hu, S.,Sun, C., 2009b. Isolation and characterization of conserved non-coding sequences among rice (oryza sativa l.) paralogous regions. Mol. Genet. Genom. 281, 11-18
    Liang, Z., Zhang, Q., Ji, C., Hu, G., Zhang, P., Wang, Y., Yang, L.,Gu, X., 2021. Reorganization of the 3d chromatin architecture of rice genomes during heat stress. BMC Biol. 19, 53
    Liu, H., Wang, S., Yu, X., Yu, J., He, X., Zhang, S., Shou, H.,Wu, P., 2005. Arl1, a lob-domain protein required for adventitious root formation in rice. Plant J. 43, 47-56
    Liu, L., Gallagher, J., Arevalo, E.D., Chen, R., Skopelitis, T., Wu, Q., Bartlett, M.,Jackson, D., 2021. Enhancing grain-yield-related traits by CRISPR-Cas9 promoter editing of maize cle genes. Nat. Plants 7, 287-294
    Lockton, S.,Gaut, B.S., 2005. Plant conserved non-coding sequences and paralogue evolution. Trends Genet. 21, 60-65
    Lu, Z., Marand, A.P., Ricci, W.A., Ethridge, C.L., Zhang, X.,Schmitz, R.J., 2019. The prevalence, evolution and chromatin signatures of plant regulatory elements. Nat. Plants 5, 1250-1259
    Margulies, E.H.,Birney, E., 2008. Approaches to comparative sequence analysis: Towards a functional view of vertebrate genomes. Nat. Rev. Genet. 9, 303-313
    Meyer, R.S.,Purugganan, M.D., 2013. Evolution of crop species: Genetics of domestication and diversification. Nat. Rev. Genet. 14, 840-852
    Quinlan, A.R.,Hall, I.M., 2010. Bedtools: A flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841-842
    Sasaki, T., Matsumoto, T., Yamamoto, K., Sakata, K., Baba, T., Katayose, Y., Wu, J., Niimura, Y., Cheng, Z., Nagamura, Y., et al., 2002. The genome sequence and structure of rice chromosome 1. Nature 420, 312-316
    Schmitz, R.J., Grotewold, E.,Stam, M., 2022. Cis-regulatory sequences in plants: Their importance, discovery, and future challenges. Plant Cell 34, 718-741
    Shen, Y.-J., Jiang, H., Jin, J.-P., Zhang, Z.-B., Xi, B., He, Y.-Y., Wang, G., Wang, C., Qian, L., Li, X., et al., 2004. Development of genome-wide DNA polymorphism database for map-based cloning of rice genes. Plant Physiol. 135, 1198-1205
    Siepel, A., Bejerano, G., Pedersen, J.S., Hinrichs, A.S., Hou, M., Rosenbloom, K., Clawson, H., Spieth, J., Hillier, L.W., Richards, S., et al., 2005. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res. 15, 1034-1050
    Snetkova, V., Pennacchio, L.A., Visel, A.,Dickel, D.E., 2022. Perfect and imperfect views of ultraconserved sequences. Nat. Rev. Genet. 23, 182-194
    Song, B., Buckler, E.S., Wang, H., Wu, Y., Rees, E., Kellogg, E.A., Gates, D.J., Khaipho-Burch, M., Bradbury, P.J., Ross-Ibarra, J., et al., 2021. Conserved noncoding sequences provide insights into regulatory sequence and loss of gene expression in maize. Genome Res. 31, 1245-1257
    Tang, H., Bowers, J.E., Wang, X., Ming, R., Alam, M.,Paterson, A.H., 2008. Synteny and collinearity in plant genomes. Science 320, 486-488
    Tarailo-Graovac, M.,Chen, N., 2009. Using repeatmasker to identify repetitive elements in genomic sequences. Curr Protoc Bioinformatics Chapter 4, Unit 4.10
    Taramino, G., Sauer, M., Stauffer, J.L., Jr., Multani, D., Niu, X., Sakai, H.,Hochholdinger, F., 2007. The maize (zea mays l.) rtcs gene encodes a lob domain protein that is a key regulator of embryonic seminal and post-embryonic shoot-borne root initiation. Plant J. 50, 649-659
    Turco, G., Schnable, J., Pedersen, B.,Freeling, M., 2013. Automated conserved non-coding sequence (cns) discovery reveals differences in gene content and promoter evolution among grasses. Front. Plant Sci. 4, 170
    Van de Velde, J., Van Bel, M., Vaneechoutte, D.,Vandepoele, K., 2016. A collection of conserved noncoding sequences to study gene regulation in flowering plants Plant Physiol. 171, 2586-2598
    Wang, J., Yu, H., Weng, X., Xie, W., Xu, C., Li, X., Xiao, J.,Zhang, Q., 2014. An expression quantitative trait loci-guided co-expression analysis for constructing regulatory network using a rice recombinant inbred line population. J. Exp. Bot. 65, 1069-1079
    Wang, L., Ming, L., Liao, K., Xia, C., Sun, S., Chang, Y., Wang, H., Fu, D., Xu, C., Wang, Z., et al., 2021. Bract suppression regulated by the mir156/529-spls-nl1-pla1 module is required for the transition from vegetative to reproductive branching in rice. Mol Plant 14, 1168-1184
    Wang, L., Xie, W., Chen, Y., Tang, W., Yang, J., Ye, R., Liu, L., Lin, Y., Xu, C., Xiao, J., et al., 2010. A dynamic gene expression atlas covering the entire life cycle of rice. Plant J. 61, 752-766
    Wilkins, O., Hafemeister, C., Plessis, A., Holloway-Phillips, M.-M., Pham, G.M., Nicotra, A.B., Gregorio, G.B., Jagadish, S.V.K., Septiningsih, E.M., Bonneau, R., et al., 2016. Egrins (environmental gene regulatory influence networks) in rice that function in the response to water deficit, high temperature, and agricultural environments. Plant Cell 28, 2365-2384
    Yan, W.H., Chen, D.J., Schumacher, J., Durantini, D., Engelhorn, J., Chen, M., Carles, C.C.,Kaufmann, K., 2019. Dynamic control of enhancer activity drives stage-specific gene expression during flower morphogenesis. Nat. Commun. 10, 1705
    Zhang, J., Chen, L.-L., Xing, F., Kudrna, D.A., Yao, W., Copetti, D., Mu, T., Li, W., Song, J.-M., Xie, W., et al., 2016. Extensive sequence divergence between the reference genomes of two elite indica rice varieties zhenshan 97 and minghui 63. Proc. Natl. Acad. Sci. U.S.A. 113, E5163-E5171
    Zhang, L.B., Zhu, Q., Wu, Z.Q., Ross-Ibarra, J., Gaut, B.S., Ge, S.,Sang, T., 2009. Selection on grain shattering genes and rates of rice domestication. New Phytol. 184, 708-720
    Zhang, T.Q., Chen, Y., Liu, Y., Lin, W.H.,Wang, J.W., 2021. Single-cell transcriptome atlas and chromatin accessibility landscape reveal differentiation trajectories in the rice root. Nat. Commun. 12, 2053
    Zhang, W., Wu, Y., Schnable, J.C., Zeng, Z., Freeling, M., Crawford, G.E.,Jiang, J., 2012. High-resolution mapping of open chromatin in the rice genome. Genome Res. 22, 151-162
    Zhang, Y., Liu, T., Meyer, C.A., Eeckhoute, J., Johnson, D.S., Bernstein, B.E., Nusbaum, C., Myers, R.M., Brown, M., Li, W., et al., 2008. Model-based analysis of chip-seq (macs). Genome Biol. 9, R137
    Zhao, L., Xie, L., Zhang, Q., Ouyang, W., Deng, L., Guan, P., Ma, M., Li, Y., Zhang, Y., Xiao, Q., et al., 2020. Integrative analysis of reference epigenomes in 20 rice varieties. Nat. Commun. 11, 2658
    Zhu, T., Liao, K., Zhou, R., Xia, C.,Xie, W., 2020. Atac-seq with unique molecular identifiers improves quantification and footprinting. Commun. Biol. 3, 675
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Article Metrics

    Article views (290) PDF downloads (19) Cited by ()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return