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Journal of Integrative Agriculture  2013, Vol. 12 Issue (5): 737-748    DOI: 10.1016/S2095-3119(13)60260-9
Crop Genetics · Breeding · Germplasm Resources Advanced Online Publication | Current Issue | Archive | Adv Search |
Alterations of Alternative Splicing Patterns of Ser/Arg-Rich (SR) Genes in Response to Hormones and Stresses Treatments in Different Ecotypes of Rice (Oryza sativa)
 ZHANG Peng, DENG Heng, XIAO Fang-ming , LIU Yong-sheng
1.Key Laboratory for Bio-Resource and Eco-Environment, Ministry of Education/State Key Laboratory of Hydraulics and Mountain River
Engineering/College of Life Science, Sichuan University, Chengdu 610064, P.R.China
2.Neijiang Hybrid Rice Research and Development Center, Neijiang 641000, P.R.China
3.Department of Plant, Soil and Entomological Sciences, University of Idaho, Moscow 83844, USA
4.School of Biotechnology and Food Engineering, Hefei University of Technology, Hefei 230009, P.R.China
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摘要  Ser/Arg-rich (SR) genes encode proteins that play pivotal roles in both constitutive and alternative splicing of pre-mRNA. However, not much effort has been made to investigate the alternative splicing of their own pre-mRNA. In this study, we conducted comprehensive analyses of pre-mRNA splicing for 22 SR genes in three rice (Oryza sativa L.) ecotypes indica, japonica and javanica. Using different ecotypes we characterized the variations in expression and splicing patterns of rice SR genes in different tissues and at different developmental stages. In addition, we compared the divergence in expression and splicing patterns of SR genes from seedlings of different rice ecotypes in response to hormones application and environmental stresses. Our results revealed the complexity of alternative splicing of SR genes in rice. The splicing varies in different tissues, in different ecotypes, in response to stresses and hormones. Thus, our study suggested that SR genes were subjected to sophisticated alternative splicing although their encoding proteins were involved in the splicing process.

Abstract  Ser/Arg-rich (SR) genes encode proteins that play pivotal roles in both constitutive and alternative splicing of pre-mRNA. However, not much effort has been made to investigate the alternative splicing of their own pre-mRNA. In this study, we conducted comprehensive analyses of pre-mRNA splicing for 22 SR genes in three rice (Oryza sativa L.) ecotypes indica, japonica and javanica. Using different ecotypes we characterized the variations in expression and splicing patterns of rice SR genes in different tissues and at different developmental stages. In addition, we compared the divergence in expression and splicing patterns of SR genes from seedlings of different rice ecotypes in response to hormones application and environmental stresses. Our results revealed the complexity of alternative splicing of SR genes in rice. The splicing varies in different tissues, in different ecotypes, in response to stresses and hormones. Thus, our study suggested that SR genes were subjected to sophisticated alternative splicing although their encoding proteins were involved in the splicing process.
Keywords:  SR protein       alternative splicing       stress       rice  
Received: 29 August 2012   Accepted:
Fund: 

This work was supported by the National Basic Research Program of China (2011CB100401), the National Science Fund of China for Distinguished Young Scientists (30825030), the National Natural Science Foundation of China (30970260, 30770466 and 30971752), and the Key Project from Chongqing Local Government, China (2010AA1019).

Corresponding Authors:  Correspondence LIU Yong-sheng, E-mail: liuyongsheng1122@yahoo.com.cn   
About author:  ZHANG Peng, E-mail: njzhp825@sohu.com

Cite this article: 

ZHANG Peng, DENG Heng, XIAO Fang-ming , LIU Yong-sheng. 2013. Alterations of Alternative Splicing Patterns of Ser/Arg-Rich (SR) Genes in Response to Hormones and Stresses Treatments in Different Ecotypes of Rice (Oryza sativa). Journal of Integrative Agriculture, 12(5): 737-748.

[1]Barta A, Kalyna M, Reddy A S. 2010. Implementing a rationaland consistent nomenclature for serine/arginine-richprotein splicing factors (SR proteins) in plants. ThePlant Cell, 22, 2926-2929

[2]Black D L. 2003. Mechanisms of alternative pre-messengerRNA splicing. Annunal Review Biochemistry, 72, 291-332

[3]Blencowe B J. 2000. Exonic splicing enhancers: mechanismof action, diversity and role in human genetic diseases.Trends in Biochemical Sciences, 25, 106-110

[4]Cartegni L, Chew S L, Krainer A R. 2002. Listening to silenceand understanding nonsense: exonic mutations thataffect splicing. Nature Reviews Genetics, 3, 285-298

[5]Fan J, Niu X L, Wang Y G, Ren G J, Zhuo T, Yang Y, Lu B R,Liu Y S. 2007. Short, direct repeats (SDRs)-mediatedpost-transcriptional processing of a transcription factorgene OsVP1 in rice (Oryza sativa). Journal ofExperimental Botany, 58, 3811-3817

[6]Filichkin S A, Priest H D, Givan S A, Shen R, Bryant D W,Fox S E, Wong W K. 2010. Genome-wide mapping ofalternative splicing in Arabidopsis thaliana. GenomeResearch, 20, 45-58

[7]Fu X D. 1995. The superfamily of arginine/serine-richsplicing factors. RNA, 1, 663-680

[8]Graveley B R. 2000. Sorting out the complexity of SR proteinfunctions. RNA, 6, 1197-1211

[9]Huang Y, Steitz J A. 2001. Splicing factors SRp20 and 9G8promote the nucleocytoplasmic export of mRNA.Molecular Cell, 7, 899-905

[10]Iida K, Go M. 2006. Survey of conserved alternative splicingevents of mRNAs encoding SR proteins in land plants.Molecular Biology and Evolution, 23, 1085-1094

[11]Iida K, Seki M, Sakurai T, Satou M, Akiyama K, Toyoda T,Konagaya A, Shinozaki K. 2004. Genome-wide analysisof alternative pre-mRNA splicing in Arabidopsisthaliana based on full-length cDNA sequences.Nucleic Acids Research, 32, 5096-5103

[12]Isshiki M, Tsumoto A, Shimamoto K. 2006. The serine/arginine-rich protein family in rice plays important rolesin constitutive and alternative splicing of pre-mRNA.The Plant Cell, 18, 146-158

[13]Kalyna M, Lopato S, Barta A. 2003. Ectopic expression ofatRSZ33 reveals its function in splicing and causes pleiotropic changes in development. MolecularBiology of the Cell, 14, 3565-3577

[14]Kalyna M, Lopato S, Voronin V, Barta A. 2006. Evolutionaryconservation and regulation of particular alternativesplicing events in plant SR proteins. Nucleic AcidsResearch, 34, 4395-4405

[15]Lemaire R, Prasad J, Kashima T, Gustafson J, Manley J L,Lafyatis R. 2002. Stability of a PKCI-1-related mRNA iscontrolled by the splicing factor ASF/SF2: a novelfunction for SR proteins Genes & Development, 16,594-607

[16]Liu J G, Yao Q H, Zhang Z, Peng R H, Xiong A S, Xu F, ZhuH. 2005. Isolation and characterization of a cDNAencoding two novel heat-shock factor OsHSF6 andOsHSF12 in Oryza sativa L. Journal of Biochemistryand Molecular Biology, 38, 602-608

[17]Lopato S, Gattoni R, Fabini G, Stevenin J, Barta A. 1999. Anovel family of plant splicing factors with a Zn knucklemotif: examination of RNA binding and splicingactivities. Plant Molecular Biology, 39, 761-773

[18]Luo D, Niu X L, Wang Y G, Zheng W J, Chang L J, Wang QL, Wei X, Yu G R, Lu B R, Liu Y S. 2007. Functionaldefect at the rice choline monooxygenase locus froman unusual post-transcriptional processing isassociated with the sequence elements of short-directrepeats. New Phytologist, 175, 439-447

[19]Maniatis T, Reed R. 2002. An extensive network of couplingamong gene expression machines. Nature, 416, 499-506

[20]Maniatis T, Tasic B. 2002. Alternative pre-mRNA splicingand proteome expansion in metazoans. Nature, 418,236-243

[21]Modrek B, Resch A, Grasso C, Lee C. 2001. Genome-widedetection of alternative splicing in expressed sequencesin human genes. Nucleic Acids Research, 29, 2850-2859

[22]Niu X L, Luo D, Gao S P, Ren G J, Chang L J, Zhou Y K, LuoX L, Li Y X, Hou P, Tang W, et al. 2010. A conservedunusual posttranscriptional processing mediated byshort, direct repeated (SDR) sequences in plants.Journal of Genetics and Genomics, 37, 85-99

[23]Niu X L, Zheng W J, Lu B R, Ren G J, Huang W Z, Wang SH, Liu J L, Tang Z Z, Luo D, Wang Y G, et al. 2007. Anunusual posttranscriptional processing in two betainealdehyde dehydrogenase loci of cereal crops directedby short, direct repeats in response to stress conditions.Plant Physiology, 143, 1929-1942

[24]Palusa S G, Ali G S, Reddy A S. 2007. Alternative splicing ofpre-mRNAs of arabidopsis serine/arginine-richproteins: regulation by hormones and stresses. ThePlant Journal, 49, 1091-1107

[25]Pan Q, Shai O, Lee L J, Frey B J, Blencowe B J. 2008. Deepsurveying of alternative splicing complexity in thehuman transcriptome by high-throughput sequencing.Nature Genetics, 40, 1413-1415

[26]Quaggiotti S, Ruperti B, Borsa P, Destro T, Malagoli M.2003. Expression of a putative high-affinity NO3-transporter and of an H+-ATPase in relation to wholeplant nitrate transport physiology in two maizegenotypes differently responsive to low nitrogenavailability. The Journal of Experimental Botany, 54,1023-1031

[27]Reddy A S. 2007. Alternative splicing of pre-messengerRNAs in plants in the genomic era. Annual Review ofPlant Biology, 58, 267-294

[28]Reddy A S, Golovkin M V. 2008. Current Topics inMicrobiology and Immunology: Nuclear Pre-mrnaProcessing in Plants. Springer-Verlag, Berlin.Richardson D N, Rogers M F, Labadorf A, Ben-Hur A, GuoH, Paterson A H, Reddy A S. 2011. Comparative analysisof serine/arginine-rich proteins across 27 eukaryotes:insights into sub-family classification and extent ofalternative splicing. PLoS One, 6, e24542.Sanford J R, Gray N K, Beckmann K, Caceres J F. 2004. Anovel role for shuttling SR proteins in mRNA translation.Genes & Development, 18, 755-768

[29]Sanford J R, Longman D, Caceres J F. 2003. Multiple rolesof the SR protein family in splicing regulation. Progressin Molecular Subcellular Biology, 31, 33-58

[30]Sharp P A, Burge C B. 1997. Classification of introns: U2-type or U12-type. Cell, 91, 875-879

[31]Shen H, Green M R. 2006. RS domains contact splicingsignals and promote splicing by a common mechanismin yeast through humans. Genes & Development, 20,1679-1684

[32]Shin C, Feng Y, Manley J L. 2004. Dephosphorylated SRp38acts as a splicing repressor in response to heat shock.Nature, 427, 553-558

[33]Smith C W, Valcarcel J. 2000. Alternative pre-mRNA splicing:the logic of combinatorial control. Trends inBiochemical Sciences, 25, 381-388

[34]Stamm S. 2002. Signals and their transduction pathwaysregulating alternative splicing: a new dimension of thehuman genome. Human Molecular Genetics, 11, 2409-2416

[35]Thomashow M F. 1999. Plant cold acclimation: freezingtolerance genes and regulatory mechanisms. AnnualReview of Plant Physiology, 50, 571-599

[36]Ulm R, Baumann A, Oravecz A, Mate Z, Adam E, Oakeley EJ, Schafer E, Nagy F. 2004. Genome-wide analysis ofgene expression reveals function of the bZIPtranscription factor HY5 in the UV-B response ofArabidopsis. Proceedings of the National Academy ofSciences of the United States of America, 101, 1397-1402

[37]Wang E T, Sandberg R, Luo S, Khrebtukova I, Zhang L,Mayr C, Kingsmore S F, Schroth G P, Burge C B. 2008.Alternative isoform regulation in human tissuetranscriptomes. Nature, 456, 470-476.
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