Alternative splicing at NAGNAG acceptors in Arabidopsis thaliana SR and SR-related protein-coding genes

Schindler, Stefanie; Szafranski, Karol; Hiller, Michael; Ali, Gul; Palusa, Saiprasad G.; Backofen, Rolf; Platzer, Matthias; Reddy, Anireddy S. N.

doi:10.1186/1471-2164-9-159

Alternative splicing at NAGNAG acceptors in Arabidopsis thaliana SR and SR-related protein-coding genes

Journal Article · Thu Apr 10 00:00:00 EDT 2008 · BMC Genomics

DOI:https://doi.org/10.1186/1471-2164-9-159· OSTI ID:1626462

Schindler, Stefanie ^[1]; Szafranski, Karol ^[2]; Hiller, Michael ^[3]; Ali, Gul ^[4]; Palusa, Saiprasad G. ^[4]; Backofen, Rolf ^[3]; Platzer, Matthias ^[2]; Reddy, Anireddy S. N. ^[4]

Leibniz Institute for Age Research – Fritz Lipmann Institute, Jena (Germany); DOE/OSTI
Leibniz Institute for Age Research – Fritz Lipmann Institute, Jena (Germany)
Albert-Ludwigs-Univ. Freiburg (Germany). Inst. of Computer Science, Bioinformatics Group
Colorado State Univ., Fort Collins, CO (United States). Dept. of Biology and Program in Molecular Plant Biology

Several recent studies indicate that alternative splicing in Arabidopsis and other plants is a common mechanism for post-transcriptional modulation of gene expression. However, few analyses have been done so far to elucidate the functional relevance of alternative splicing in higher plants. Representing a frequent and universal subtle alternative splicing event among eukaryotes, alternative splicing at NAGNAG acceptors contributes to transcriptome diversity and therefore, proteome plasticity. Alternatively spliced NAGNAG acceptors are overrepresented in genes coding for proteins with RNA-recognition motifs (RRMs). As SR proteins, a family of RRMcontaining important splicing factors, are known to be extensively alternatively spliced in Arabidopsis, we analyzed alternative splicing at NAGNAG acceptors in SR and SR-related genes. In a comprehensive analysis of the Arabidopsis thaliana genome, we identified 6,772 introns that exhibit a NAGNAG acceptor motif. Alternative splicing at these acceptors was assessed using available EST data, complemented by a sequence-based prediction method. Of the 36 identified introns within 30 SR and SR-related protein-coding genes that have a NAGNAG acceptor, we selected 15 candidates for an experimental analysis of alternative splicing under several conditions. We provide experimental evidence for 8 of these candidates being alternatively spliced. Quantifying the ratio of NAGNAG-derived splice variants under several conditions, we found organ-specific splicing ratios in adult plants and changes in seedlings of different ages. Splicing ratio changes were observed in response to heat shock and most strikingly, cold shock. Interestingly, the patterns of differential splicing ratios are similar for all analyzed genes. NAGNAG acceptors frequently occur in the Arabidopsis genome and are particularly prevalent in SR and SR-related protein-coding genes. A lack of extensive EST coverage can be compensated by using the proposed sequence-based method to predict alternative splicing at these acceptors. Our findings indicate that the differential effects on NAGNAG alternative splicing in SR and SR-related genes are organ- and condition-specific rather than gene-specific.

View Accepted Manuscript (DOE)

Research Organization:: Colorado State Univ., Fort Collins, CO (United States)

Sponsoring Organization:: Deutsche Forschungsgemeinschaft (DFG); Federal Ministry of Education and Research (BMBF); USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: FG02-04ER15556

OSTI ID:: 1626462

Journal Information:: BMC Genomics, Journal Name: BMC Genomics Journal Issue: 1 Vol. 9; ISSN 1471-2164

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

References (42)

Splicing of precursors to mRNA in higher plants: mechanism, regulation and sub-nuclear organisation of the spliceosomal machinery Simpson, G. G.; Filipowicz, W. Plant Molecular Biology, Vol. 32, Issue 1-2 https://doi.org/10.1007/bf00039375	journal	October 1996
Function of alternative splicing Stamm, Stefan; Ben-Ari, Shani; Rafalska, Ilona Gene, Vol. 344 https://doi.org/10.1016/j.gene.2004.10.022	journal	January 2005
Characterization of alternative oxidase (AOX) gene expression in response to methyl salicylate and methyl jasmonate pre-treatment and low temperature in tomatoes Fung, Raymond W. M.; Wang, Chien Y.; Smith, David L. Journal of Plant Physiology, Vol. 163, Issue 10 https://doi.org/10.1016/j.jplph.2005.11.003	journal	October 2006
The evolving roles of alternative splicing Lareau, Liana F.; Green, Richard E.; Bhatnagar, Rajiv S. Current Opinion in Structural Biology, Vol. 14, Issue 3 https://doi.org/10.1016/j.sbi.2004.05.002	journal	June 2004
Widespread and subtle: alternative splicing at short-distance tandem sites Hiller, Michael; Platzer, Matthias Trends in Genetics, Vol. 24, Issue 5 https://doi.org/10.1016/j.tig.2008.03.003	journal	May 2008
Plant serine/arginine-rich proteins and their role in pre-mRNA splicing Reddy, A. Trends in Plant Science, Vol. 9, Issue 11 https://doi.org/10.1016/j.tplants.2004.09.007	journal	November 2004
Pre-mRNA splicing in higher plants Lorković, Zdravko J.; Wieczorek Kirk, Dominika A.; Lambermon, Mark H. L. Trends in Plant Science, Vol. 5, Issue 4 https://doi.org/10.1016/s1360-1385(00)01595-8	journal	April 2000
Sorting out the complexity of SR protein functions Graveley, Brenton R. RNA, Vol. 6, Issue 9 https://doi.org/10.1017/s1355838200000960	journal	September 2000
Alternative Nonallelic Deletion Is Constitutive of Ruminant αs1-Casein Ferranti, Pasquale; Lilla, Sergio; Chianese, Lina Journal of Protein Chemistry, Vol. 18, Issue 5 https://doi.org/10.1023/a:1020659518748	journal	July 1999
Unproductive splicing of SR genes associated with highly conserved and ultraconserved DNA elements Lareau, Liana F.; Inada, Maki; Green, Richard E. Nature, Vol. 446, Issue 7138 https://doi.org/10.1038/nature05676	journal	March 2007
Widespread occurrence of alternative splicing at NAGNAG acceptors contributes to proteome plasticity Hiller, Michael; Huse, Klaus; Szafranski, Karol Nature Genetics, Vol. 36, Issue 12 https://doi.org/10.1038/ng1469	journal	October 2004
Listening to silence and understanding nonsense: exonic mutations that affect splicing Cartegni, Luca; Chew, Shern L.; Krainer, Adrian R. Nature Reviews Genetics, Vol. 3, Issue 4 https://doi.org/10.1038/nrg775	journal	April 2002
A plethora of plant serine/arginine-rich proteins: redundancy or evolution of novel gene functions? Kalyna, M.; Barta, A. Biochemical Society Transactions, Vol. 32, Issue 4 https://doi.org/10.1042/bst0320561	journal	August 2004
Genomewide comparative analysis of alternative splicing in plants Wang, B. -B.; Brendel, V. Proceedings of the National Academy of Sciences, Vol. 103, Issue 18 https://doi.org/10.1073/pnas.0602039103	journal	April 2006
Identification of a plant serine-arginine-rich protein similar to the mammalian splicing factor SF2/ASF. Lazar, G.; Schaal, T.; Maniatis, T. Proceedings of the National Academy of Sciences, Vol. 92, Issue 17 https://doi.org/10.1073/pnas.92.17.7672	journal	August 1995
An SC35-like Protein and a Novel Serine/Arginine-rich Protein Interact with Arabidopsis U1-70K Protein Golovkin, Maxim; Reddy, Anireddy S. N. Journal of Biological Chemistry, Vol. 274, Issue 51 https://doi.org/10.1074/jbc.274.51.36428	journal	December 1999
Ectopic Expression of atRSZ33 Reveals Its Function in Splicing and Causes Pleiotropic Changes in Development Kalyna, Maria; Lopato, Sergiy; Barta, Andrea Molecular Biology of the Cell, Vol. 14, Issue 9 https://doi.org/10.1091/mbc.e03-02-0109	journal	September 2003
Profile hidden Markov models Eddy, S. R. Bioinformatics, Vol. 14, Issue 9 https://doi.org/10.1093/bioinformatics/14.9.755	journal	October 1998
Alternative Splicing at NAGNAG Acceptor Sites Shares Common Properties in Land Plants and Mammals Iida, K.; Shionyu, M.; Suso, Y. Molecular Biology and Evolution, Vol. 25, Issue 4 https://doi.org/10.1093/molbev/msn015	journal	February 2008
Analysis of the RNA-recognition motif and RS and RGG domains: conservation in metazoan pre-mRNA splicing factors Birney, Ewan; Kumar, Sanjay; Krainer, Adrian R. Nucleic Acids Research, Vol. 21, Issue 25 https://doi.org/10.1093/nar/21.25.5803	journal	January 1993
A clean data set of EST-confirmed splice sites from Homo sapiens and standards for clean-up procedures Thanaraj, T. A. Nucleic Acids Research, Vol. 27, Issue 13 https://doi.org/10.1093/nar/27.13.2627	journal	July 1999
Genome analysis: RNA recognition motif (RRM) and K homology (KH) domain RNA-binding proteins from the flowering plant Arabidopsis thaliana LorkoviM, Z. J. Nucleic Acids Research, Vol. 30, Issue 3 https://doi.org/10.1093/nar/30.3.623	journal	February 2002
Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies Haas, B. J. Nucleic Acids Research, Vol. 31, Issue 19 https://doi.org/10.1093/nar/gkg770	journal	October 2003
RARGE: a large-scale database of RIKEN Arabidopsis resources ranging from transcriptome to phenome Sakurai, T. Nucleic Acids Research, Vol. 33, Issue Database issue https://doi.org/10.1093/nar/gki014	journal	December 2004
Alternative splicing regulation at tandem 3' splice sites Akerman, M. Nucleic Acids Research, Vol. 34, Issue 1 https://doi.org/10.1093/nar/gkj408	journal	January 2006
Evolutionary conservation and regulation of particular alternative splicing events in plant SR proteins Kalyna, Maria; Lopato, Sergiy; Voronin, Viktor Nucleic Acids Research, Vol. 34, Issue 16 https://doi.org/10.1093/nar/gkl570	journal	August 2006
Different levels of alternative splicing among eukaryotes Kim, Eddo; Magen, Alon; Ast, Gil Nucleic Acids Research, Vol. 35, Issue 1 https://doi.org/10.1093/nar/gkl924	journal	December 2006
SR proteins and splicing control. Manley, J. L.; Tacke, R. Genes & Development, Vol. 10, Issue 13 https://doi.org/10.1101/gad.10.13.1569	journal	July 1996
atSRp30, one of two SF2/ASF-like proteins from Arabidopsis thaliana, regulates splicing of specific plant genes Lopato, S.; Kalyna, M.; Dorner, S. Genes & Development, Vol. 13, Issue 8 https://doi.org/10.1101/gad.13.8.987	journal	April 1999
Spidey: A Tool for mRNA-to-Genomic Alignments Wheelan, Sarah J.; Church, Deanna M.; Ostell, James M. Genome Research, Vol. 11, Issue 11 https://doi.org/10.1101/gr.195301	journal	October 2001
The Serine/Arginine-Rich Protein Family in Rice Plays Important Roles in Constitutive and Alternative Splicing of Pre-mRNA Isshiki, Masayuki; Tsumoto, Ayako; Shimamoto, Ko The Plant Cell, Vol. 18, Issue 1 https://doi.org/10.1105/tpc.105.037069	journal	December 2005
Intron retention is a major phenomenon in alternative splicing in Arabidopsis Ner-Gaon, Hadas; Halachmi, Ronit; Savaldi-Goldstein, Sigal The Plant Journal, Vol. 39, Issue 6 https://doi.org/10.1111/j.1365-313x.2004.02172.x	journal	September 2004
Wobble Splicing Reveals the Role of the Branch Point Sequence-to-NAGNAG Region in 3′ Tandem Splice Site Selection Tsai, Kuo-Wang; Tarn, Woan-Yuh; Lin, Wen-chang Molecular and Cellular Biology, Vol. 27, Issue 16 https://doi.org/10.1128/mcb.00363-07	journal	August 2007
Mechanisms of Alternative Pre-Messenger RNA Splicing Black, Douglas L. Annual Review of Biochemistry, Vol. 72, Issue 1 https://doi.org/10.1146/annurev.biochem.72.121801.161720	journal	June 2003
Comprehensive analysis of alternative splicing in rice and comparative analyses with Arabidopsis Campbell, Matthew A.; Haas, Brian J.; Hamilton, John P. BMC Genomics, Vol. 7, Issue 1 https://doi.org/10.1186/1471-2164-7-327	journal	December 2006
Experimental validation of novel genes predicted in the un-annotated regions of the Arabidopsis genome Moskal, William A.; Wu, Hank C.; Underwood, Beverly A. BMC Genomics, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2164-8-18	journal	January 2007
ATP, phosphorylation and transcription regulate the mobility of plant splicing factors Ali, Gul Shad; Reddy, Annireddy S. N. Journal of Cell Science, Vol. 119, Issue 17 https://doi.org/10.1242/jcs.03144	journal	September 2006
Genomic splice-site analysis reveals frequent alternative splicing close to the dominant splice site Dou, Yimeng; Fox-Walsh, Kristi L.; Baldi, Pierre F. RNA, Vol. 12, Issue 12 https://doi.org/10.1261/rna.151106	journal	October 2006
Evolutionary conservation of minor U12-type spliceosome between plants and humans LorkoviĆ, Zdravko J.; Lehner, Reinhard; Forstner, Christina RNA, Vol. 11, Issue 7 https://doi.org/10.1261/rna.2440305	journal	June 2005
Assessing the fraction of short-distance tandem splice sites under purifying selection Hiller, Michael; Szafranski, Karol; Sinha, Rileen RNA, Vol. 14, Issue 4 https://doi.org/10.1261/rna.883908	journal	February 2008
A Simple Physical Model Predicts Small Exon Length Variations Chern, Tzu-Ming; van Nimwegen, Erik; Kai, Chikatoshi PLoS Genetics, Vol. 2, Issue 4 https://doi.org/10.1371/journal.pgen.0020045	journal	April 2006
Characterization of a Novel Arginine/Serine-Rich Splicing Factor in Arabidopsis Lopato, Sergiy; Waigmann, Elisabeth; Barta, Andrea The Plant Cell, Vol. 8, Issue 12 https://doi.org/10.2307/3870466	journal	December 1996

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Accurate prediction of NAGNAG alternative splicing Sinha, Rileen; Nikolajewa, Swetlana; Szafranski, Karol Nucleic Acids Research, Vol. 37, Issue 11 https://doi.org/10.1093/nar/gkp220	journal	April 2009
Comparative analysis indicates that alternative splicing in plants has a limited role in functional expansion of the proteome Severing, Edouard I.; van Dijk, Aalt DJ; Stiekema, Willem J. BMC Genomics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2164-10-154	journal	January 2009
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Alternative Splicing of RNA Triplets Is Often Regulated and Accelerates Proteome Evolution Bradley, Robert K.; Merkin, Jason; Lambert, Nicole J. PLoS Biology, Vol. 10, Issue 1 https://doi.org/10.1371/journal.pbio.1001229	journal	January 2012
A Subtle Alternative Splicing Event Gives Rise to a Widely Expressed Human RNase k Isoform Karousis, Evangelos D.; Sideris, Diamantis C. PLoS ONE, Vol. 9, Issue 5 https://doi.org/10.1371/journal.pone.0096557	journal	May 2014
Deciphering the Plant Splicing Code: Experimental and Computational Approaches for Predicting Alternative Splicing and Splicing Regulatory Elements Reddy, Anireddy S. N.; Rogers, Mark F.; Richardson, Dale N. Frontiers in Plant Science, Vol. 3 https://doi.org/10.3389/fpls.2012.00018	journal	January 2012
Analysis of pollen-specific alternative splicing in Arabidopsis thaliana via semi-quantitative PCR Estrada, April D.; Freese, Nowlan H.; Blakley, Ivory C. https://doi.org/10.7287/peerj.preprints.594v2	posted_content	March 2015
nagnag: Identification and quantification of NAGNAG alternative splicing using RNA-Seq data Yan, Xiaoyan; Sablok, Gaurav; Feng, Gang FEBS Letters, Vol. 589, Issue 15 https://doi.org/10.1016/j.febslet.2015.05.029	journal	May 2015
Physiological state co-regulates thousands of mammalian mRNA splicing events at tandem splice sites and alternative exons Szafranski, Karol; Fritsch, Claudia; Schumann, Frank Nucleic Acids Research, Vol. 42, Issue 14 https://doi.org/10.1093/nar/gku532	journal	July 2014
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59 BASIC BIOLOGICAL SCIENCES
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NAGNAG Acceptor
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Alternative splicing at NAGNAG acceptors in Arabidopsis thaliana SR and SR-related protein-coding genes

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