A conserved unusual posttranscriptional processing mediated by short, direct repeated (SDR) sequences in plants

Xiangli Niu; Di Luo; Shaopei Gao; Guangjun Ren; Lijuan Chang; Yuke Zhou; Xiaoli Luo; Yuxiang Li; Pei Hou; Wei Tang; Bao-Rong Lu; Yongsheng Liu

doi:10.1016/S1673-8527(09)60028-X

Volume 37 Issue 1

Jan. 2010

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Article Navigation > Journal of Genetics and Genomics > 2010 > 37(1): 85-99

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A conserved unusual posttranscriptional processing mediated by short, direct repeated (SDR) sequences in plants

doi: 10.1016/S1673-8527(09)60028-X

a
College of Agricultural and Life Sciences, Chongqing University, Chongqing 400030, China
b
Ministry of Education Key Laboratory for Bio-resource and Eco-environment, College of Life Science and State Key Laboratory of Biotherapy, Sichuan University, Chengdu 610064, China
c
Institute of Crop Research, Sichuan Academy of Agricultural Sciences, Chengdu 610066, China
d
Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Institute of Biodiversity Science, Fudan University, Shanghai 200433, China

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Corresponding author: E-mail address: liuyongsheng1122@yahoo.com.cn (Yongsheng Liu)
Received Date: 2009-09-07
Accepted Date: 2009-12-02
Rev Recd Date: 2009-11-06

Available Online: 2010-02-18

Publish Date: 2010-01-20

Abstract

Abstract

In several stress responsive gene loci of monocot cereal crops, we have previously identified an unusual posttranscriptional processing mediated by paired presence of short direct repeated (SDR) sequences at 5′ and 3′ splicing junctions that are distinct from conventional (U2/U12-type) splicing boundaries. By using the known SDR-containing sequences as probes, 24 plant candidate genes involved in diverse functional pathways from both monocots and dicots that potentially possess SDR-mediated posttranscriptional processing were predicted in the GenBank database. The SDRs-mediated posttranscriptional processing events including cis- and trans-actions were experimentally detected in majority of the predicted candidates. Extensive sequence analysis demonstrates several types of SDR-associated splicing peculiarities including partial exon deletion, exon fragment repetition, exon fragment scrambling and trans-splicing that result in either loss of partial exon or unusual exonic sequence rearrangements within or between RNA molecules. In addition, we show that the paired presence of SDR is necessary but not sufficient in SDR-mediated splicing in transient expression and stable transformation systems. We also show prokaryote is incapable of SDR-mediated premRNA splicing.
- posttranscriptional processing,
- short direct repeat (SDR),
- premRNA splicing,
- plant

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References(41)

References

[1]	Black, D.L. Mechanisms of alternative pre-messenger RNA splicing Annu. Rev. Biochem., 72 (2003),pp. 291-336
[2]	Blencowe, B.J. Exonic splicing enhancers: mechanism of action, diversity and role in human genetic diseases Trends Biochem. Sci., 25 (2000),pp. 106-110
[3]	Cartegni, L., Chew, S.L., Krainer, A.R. Listening to silence and understanding nonsense: exonic mutations that affect splicing Nat. Rev. Genet., 3 (2002),pp. 285-298
[4]	Expert-Bezançon, A., Sureau, A., Durosay, P. et al. hnRNP A1 and SR proteins, ASF/SF2 and SC35 have antagonistic functions in splicing of beta-tropomyosin exon 6B J. Biol. Chem., 279 (2004),pp. 38249-38259
[5]	Fan, J., Niu, X., Zhuo, T. et al. J. Exp. Bot., 58 (2007),pp. 3811-3817
[6]	Graveley, B.R. Sorting out the complexity of SR protein functions RNA, 6 (2000),pp. 1197-1211
[7]	Hall, T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT Nucl. Acids. Symp. Ser., 41 (1999),pp. 95-98
[8]	Hiei, Y., Ohta, S., Komari, T. et al. Plant J., 6 (1994),pp. 271-282
[9]	Johnson, J.M., Castle, J., Garrett-Engele, P. et al. Genome-wide survey of human alternative pre-mRNA splicing with exon junction microarrays Science, 302 (2003),pp. 2141-2144
[10]	Kalyna, M., Lopato, S., Voronin, V. et al. Evolutionary conservation and regulation of particular alternative splicing events in plant SR proteins Nucleic Acids Res., 34 (2006),pp. 4395-4405
[11]	Kan, J.L., Green, M.R. Pre-mRNA splicing of IgM exons M1 and M2 is directed by a juxtaposed splicing enhancer and inhibitor Genes Dev., 13 (1999),pp. 462-471
[12]	Kudla, G., Lipinski, L., Caffin, F. et al. High guanine and cytosine content increases mRNA levels in mammalian cells PLoS Biol., 4 (2006),p. e180
[13]	Ladd, A.N., Cooper, T.A. Finding signals that regulate alternative splicing in the post-genomic era Genome Biol., 3 (2002)
[14]	Lewis, B.P., Green, R.E., Brenner, S.E. Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans Proc. Natl Acad. Sci. USA, 100 (2003),pp. 189-192
[15]	Lim, L.P., Burge, C.B. A computational analysis of sequence features involved in recognition of short introns Proc. Natl. Acad. Sci. USA, 98 (2001),pp. 11193-11198
[16]	Lorković, Z.J., Wieczorek Kirk, D.A., Lambermon, M.H. et al. Pre-mRNA splicing in higher plants Trends Plant Sci., 5 (2000),pp. 160-167
[17]	Luo, D., Niu, X., Wang, Y. et al. New Phytol., 175 (2007),pp. 439-447
[18]	Maniatis, T., Reed, R. An extensive network of coupling among gene expression machines Nature, 416 (2002),pp. 499-506
[19]	Mao, J., Zhang, Y., Sang, Y. et al. Proc. Natl. Acad. Sci. USA, 102 (2005),pp. 12270-12275
[20]	Maquat, L.E. Nonsense-mediated mRNA decay: splicing, translation and mRNP dynamics Nat. Rev. Mol. Cell Biol., 5 (2004),pp. 89-99
[21]	Michaud, S., Reed, R. A functional association between the 5′ and 3′ splice site is established in the earliest prespliceosome complex (E) in mammals Genes Dev., 7 (1993),pp. 1008-1020
[22]	Mitchell, P., Tollervey, D. mRNA stability in eukaryotes Curr. Opin. Genet. Dev., 10 (2000),pp. 193-198
[23]	Modrek, B., Resch, A., Grasso, C. et al. Genome-wide detection of alternative splicing in expressed sequences of human genes Nucleic Acids Res., 29 (2001),pp. 2850-2859
[24]	Mount, S.M. A catalogue of splice junction sequences Nucleic Acids Res., 10 (1982),pp. 459-472
[25]	Niu, X., Zheng, W., Lu, BR. et al. Plant Physiol., 143 (2007),pp. 1229-1942
[26]	Reed, R. Initial splice-site recognition and pairing during pre-mRNA splicing Curr. Opin. Genet. Dev., 6 (1996),pp. 215-220
[27]	Reddy, A.S. Alternative splicing of pre-messenger RNAs in plants in the genomic era Annu. Rev. Plant Biol., 58 (2007),pp. 267-294
[28]	Rooke, N., Markovtsov, V., Cagavi, E. et al. Roles for SR proteins and hnRNP A1 in the regulation of c-src exon N1 Mol. Cell Biol., 23 (2003),pp. 1874-1884
[29]	Russell, A.G., Charette, J.M., Spencer, D.F. et al. An early evolutionary origin for the minor spliceosome Nature, 443 (2006),pp. 863-866
[30]	Sambrook, J.
[31]	Senapathy, P., Shapiro, M.B., Harris, N.L. Splice junctions, branch point sites, and exons: sequence statistics, identification, and applications to genome project Methods Enzymol., 183 (1990),pp. 252-278
[32]	Shao, X., Shepelev, V., Fedorov, A. Bioinformatic analysis of exon repetition, exon scrambling and trans-splicing in humans Bioinformatics, 22 (2006),pp. 692-698
[33]	Smith, C.W., Valcarcel, J. Alternative pre-mRNA splicing: the logic of combinatorial control Trends Biochem. Sci., 25 (2000),pp. 381-388
[34]	Staknis, D., Reed, R. SR proteins promote the first specific recognition of Pre-mRNA and are present together with the U1 small nuclear ribonucleoprotein particle in a general splicing enhancer complex Mol. Cell Biol., 14 (1994),pp. 7670-7682
[35]	Stamm, S. Signals and their transduction pathways regulating alternative splicing: a new dimension of the human genome Hum. Mol. Genet., 11 (2002),pp. 2409-2416
[36]	Stamm, S., Ben-Ari, S., Rafalska, I. et al. Function of alternative splicing Gene, 344 (2005),pp. 1-20
[37]	Sun, H., Chasin, L.A. Multiple splicing defects in an intronic false exon Mol. Cell Biol., 20 (2000),pp. 6414-6425
[38]	Tam, W.Y., Steitz, J.A. Pre-mRNA splicing: the discovery of a new spliceosome doubles the challenge Trends Biochem. Sci., 22 (1997),pp. 132-137
[39]	Thompson, J.D., Gibson, T.J., Plewniak, F. et al. The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools Nucelic Acids Res., 25 (1997),pp. 4876-4882
[40]	Wise, J.A. Guides to the heart of the spliceosome Science, 262 (1993),pp. 1978-1979
[41]	Yang, Y., Li, R., Qi, M. In vivo analysis of plant promoters and transcription factors by agroinfiltration of tobacco leaves Plant J., 22 (2000),pp. 543-551