Global Analysis of the RNA-protein Interaction and RNA Secondary Structure Landscapes of the Arabidopsis Nucleus

Overview

Journal Mol Cell

Publisher Cell Press

Specialty Cell Biology

Date 2015 Jan 6

PMID 25557549

Citations 57

Authors

Sager J Gosai

Shawn W Foley

Dongxue Wang

Ian M Silverman

Nur Selamoglu

Andrew D L Nelson

Mark A Beilstein

Fevzi Daldal

Roger B Deal

Brian D Gregory

Affiliations

Soon will be listed here.

Abstract

Posttranscriptional regulation in eukaryotes requires cis- and trans-acting features and factors including RNA secondary structure and RNA-binding proteins (RBPs). However, a comprehensive view of the structural and RBP interaction landscape of nuclear RNAs has yet to be compiled for any organism. Here, we use our ribonuclease-mediated structure and RBP-binding site mapping approaches to globally profile these features in Arabidopsis seedling nuclei in vivo. We reveal anticorrelated patterns of secondary structure and RBP binding throughout nuclear mRNAs that demarcate sites of alternative splicing and polyadenylation. We also uncover a collection of protein-bound sequence motifs, and identify their structural contexts, co-occurrences in transcripts encoding functionally related proteins, and interactions with putative RBPs. Finally, using these motifs, we find that the chloroplast RBP CP29A also interacts with nuclear mRNAs. In total, we provide a simultaneous view of the RNA secondary structure and RBP interaction landscapes in a eukaryotic nucleus.

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References

Rouskin S, Zubradt M, Washietl S, Kellis M, Weissman J . Genome-wide probing of RNA structure reveals active unfolding of mRNA structures in vivo. Nature. 2013; 505(7485):701-5. PMC: 3966492. DOI: 10.1038/nature12894. View

Hacisuleyman E, Goff L, Trapnell C, Williams A, Henao-Mejia J, Sun L . Topological organization of multichromosomal regions by the long intergenic noncoding RNA Firre. Nat Struct Mol Biol. 2014; 21(2):198-206. PMC: 3950333. DOI: 10.1038/nsmb.2764. View

Cech T, Steitz J . The noncoding RNA revolution-trashing old rules to forge new ones. Cell. 2014; 157(1):77-94. DOI: 10.1016/j.cell.2014.03.008. View

Talkish J, May G, Lin Y, Woolford Jr J, McManus C . Mod-seq: high-throughput sequencing for chemical probing of RNA structure. RNA. 2014; 20(5):713-20. PMC: 3988572. DOI: 10.1261/rna.042218.113. View

Silverman I, Li F, Alexander A, Goff L, Trapnell C, Rinn J . RNase-mediated protein footprint sequencing reveals protein-binding sites throughout the human transcriptome. Genome Biol. 2014; 15(1):R3. PMC: 4053792. DOI: 10.1186/gb-2014-15-1-r3. View

Wu H, Su Y, Chen H, Chen Y, Wu C, Lin W . Genome-wide analysis of light-regulated alternative splicing mediated by photoreceptors in Physcomitrella patens. Genome Biol. 2014; 15(1):R10. PMC: 4054894. DOI: 10.1186/gb-2014-15-1-r10. View

Keene J, Tenenbaum S . Eukaryotic mRNPs may represent posttranscriptional operons. Mol Cell. 2002; 9(6):1161-7. DOI: 10.1016/s1097-2765(02)00559-2. View

Ule J, Jensen K, Ruggiu M, Mele A, Ule A, Darnell R . CLIP identifies Nova-regulated RNA networks in the brain. Science. 2003; 302(5648):1212-5. DOI: 10.1126/science.1090095. View

Ye L, Li Y, Fukami-Kobayashi K, Go M, Konishi T, Watanabe A . Diversity of a ribonucleoprotein family in tobacco chloroplasts: two new chloroplast ribonucleoproteins and a phylogenetic tree of ten chloroplast RNA-binding domains. Nucleic Acids Res. 1991; 19(23):6485-90. PMC: 329204. DOI: 10.1093/nar/19.23.6485. View

10.

Kandasamy M, McKinney E, Meagher R . The late pollen-specific actins in angiosperms. Plant J. 1999; 18(6):681-91. DOI: 10.1046/j.1365-313x.1999.00487.x. View

11.

Foissac S, Sammeth M . ASTALAVISTA: dynamic and flexible analysis of alternative splicing events in custom gene datasets. Nucleic Acids Res. 2007; 35(Web Server issue):W297-9. PMC: 1933205. DOI: 10.1093/nar/gkm311. View

12.

Cruz J, Westhof E . The dynamic landscapes of RNA architecture. Cell. 2009; 136(4):604-9. DOI: 10.1016/j.cell.2009.02.003. View

13.

Wahl M, Will C, Luhrmann R . The spliceosome: design principles of a dynamic RNP machine. Cell. 2009; 136(4):701-18. DOI: 10.1016/j.cell.2009.02.009. View

14.

Bailey T, Boden M, Buske F, Frith M, Grant C, Clementi L . MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 2009; 37(Web Server issue):W202-8. PMC: 2703892. DOI: 10.1093/nar/gkp335. View

15.

Raker V, Mironov A, Gelfand M, Pervouchine D . Modulation of alternative splicing by long-range RNA structures in Drosophila. Nucleic Acids Res. 2009; 37(14):4533-44. PMC: 2724269. DOI: 10.1093/nar/gkp407. View

16.

Chen M, Manley J . Mechanisms of alternative splicing regulation: insights from molecular and genomics approaches. Nat Rev Mol Cell Biol. 2009; 10(11):741-54. PMC: 2958924. DOI: 10.1038/nrm2777. View

17.

Du Z, Zhou X, Ling Y, Zhang Z, Su Z . agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res. 2010; 38(Web Server issue):W64-70. PMC: 2896167. DOI: 10.1093/nar/gkq310. View

18.

Heinz S, Benner C, Spann N, Bertolino E, Lin Y, Laslo P . Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell. 2010; 38(4):576-89. PMC: 2898526. DOI: 10.1016/j.molcel.2010.05.004. View

19.

Simpson C, Manthri S, Raczynska K, Kalyna M, Lewandowska D, Kusenda B . Regulation of plant gene expression by alternative splicing. Biochem Soc Trans. 2010; 38(2):667-71. DOI: 10.1042/BST0380667. View

20.

Deal R, Henikoff S . A simple method for gene expression and chromatin profiling of individual cell types within a tissue. Dev Cell. 2010; 18(6):1030-40. PMC: 2905389. DOI: 10.1016/j.devcel.2010.05.013. View