期刊论文详细信息
BMC Genomics
Genome-wide analysis of alternative splicing in Volvox carteri
Armin Hallmann2  Gunnar Rätsch3  Cheng Soon Ong1  Arash Kianianmomeni2 
[1] Machine Learning Group, NICTA Canberra Research Laboratory, Canberra, Australia;Department of Cellular and Developmental Biology of Plants, University of Bielefeld, Universitätsstr. 25, D-33615 Bielefeld, Germany;Biomedical Data Science Group, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York City, NY 10065, USA
关键词: Transcriptome;    Quantitative real-time RT-PCR;    Lower eukaryotes;    Green algae;    EST analysis;    Differential splicing;    Bioinformatics;   
Others  :  1127225
DOI  :  10.1186/1471-2164-15-1117
 received in 2014-06-30, accepted in 2014-12-11,  发布年份 2014
PDF
【 摘 要 】

Background

Alternative splicing is an essential mechanism for increasing transcriptome and proteome diversity in eukaryotes. Particularly in multicellular eukaryotes, this mechanism is involved in the regulation of developmental and physiological processes like growth, differentiation and signal transduction.

Results

Here we report the genome-wide analysis of alternative splicing in the multicellular green alga Volvox carteri. The bioinformatic analysis of 132,038 expressed sequence tags (ESTs) identified 580 alternative splicing events in a total of 426 genes. The predominant type of alternative splicing in Volvox is intron retention (46.5%) followed by alternative 5′ (17.9%) and 3′ (21.9%) splice sites and exon skipping (9.5%). Our analysis shows that in Volvox at least ~2.9% of the intron-containing genes are subject to alternative splicing. Considering the total number of sequenced ESTs, the Volvox genome seems to provide more favorable conditions (e.g., regarding length and GC content of introns) for the occurrence of alternative splicing than the genome of its close unicellular relative Chlamydomonas. Moreover, many randomly chosen alternatively spliced genes of Volvox do not show alternative splicing in Chlamydomonas. Since the Volvox genome contains about the same number of protein-coding genes as the Chlamydomonas genome (~14,500 protein-coding genes), we assumed that alternative splicing may play a key role in generation of genomic diversity, which is required to evolve from a simple one-cell ancestor to a multicellular organism with differentiated cell types (Mol Biol Evol 31:1402-1413, 2014). To confirm the alternative splicing events identified by bioinformatic analysis, several genes with different types of alternatively splicing have been selected followed by experimental verification of the predicted splice variants by RT-PCR.

Conclusions

The results show that our approach for prediction of alternative splicing events in Volvox was accurate and reliable. Moreover, quantitative real-time RT-PCR appears to be useful in Volvox for analyses of relationships between the appearance of specific alternative splicing variants and different kinds of physiological, metabolic and developmental processes as well as responses to environmental changes.

【 授权许可】

   
2014 Kianianmomeni et al.; licensee BioMed Central.

【 预 览 】
附件列表
Files Size Format View
20150220055408567.pdf 2128KB PDF download
【 参考文献 】
  • [1]Chen L, Bush SJ, Tovar-Corona JM, Castillo-Morales A, Urrutia AO: Correcting for differential transcript coverage reveals a strong relationship between alternative splicing and organism complexity. Mol Biol Evol 2014, 31(6):1402-1413.
  • [2]Stamm S, Ben-Ari S, Rafalska I, Tang Y, Zhang Z, Toiber D, Thanaraj TA, Soreq H: Function of alternative splicing. Gene 2005, 344:1-20.
  • [3]Keren H, Lev-Maor G, Ast G: Alternative splicing and evolution: diversification, exon definition and function. Nat Rev Genet 2010, 11(5):345-355.
  • [4]Reddy AS: Nuclear pre-mRNA splicing in plants. Crit Rev Plant Sci 2001, 20(6):523-571.
  • [5]Reddy AS: Alternative splicing of pre-messenger RNAs in plants in the genomic era. Annu Rev Plant Biol 2007, 58:267-294.
  • [6]Gassmann W: Alternative splicing in plant defense. Curr Top Microbiol Immunol 2008, 326:219-233.
  • [7]Cáceres JF, Kornblihtt AR: Alternative splicing: multiple control mechanisms and involvement in human disease. Trends Genet 2002, 18(4):186-193.
  • [8]Grabowski PJ: Splicing regulation in neurons: tinkering with cell-specific control. Cell 1998, 92(6):709-712.
  • [9]Grabowski PJ, Black DL: Alternative RNA splicing in the nervous system. Prog Neurobiol 2001, 65(3):289-308.
  • [10]Stamm S, Zhang MQ, Marr TG, Helfman DM: A sequence compilation and comparison of exons that are alternatively spliced in neurons. Nucleic Acids Res 1994, 22(9):1515-1526.
  • [11]Licatalosi DD, Darnell RB: RNA processing and its regulation: global insights into biological networks. Nat Rev Genet 2010, 11(1):75-87.
  • [12]Black DL: Mechanisms of alternative pre-messenger RNA splicing. Annu Rev Biochem 2003, 72:291-336.
  • [13]Johnson JM, Castle J, Garrett-Engele P, Kan Z, Loerch PM, Armour CD, Santos R, Schadt EE, Stoughton R, Shoemaker DD: Genome-wide survey of human alternative pre-mRNA splicing with exon junction microarrays. Science 2003, 302(5653):2141-2144.
  • [14]Kampa D, Cheng J, Kapranov P, Yamanaka M, Brubaker S, Cawley S, Drenkow J, Piccolboni A, Bekiranov S, Helt G, Tammana H, Gingeras TR: Novel RNAs identified from an in-depth analysis of the transcriptome of human chromosomes 21 and 22. Genome Res 2004, 14(3):331-342.
  • [15]Pan Q, Shai O, Lee LJ, Frey BJ, Blencowe BJ: Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 2008, 40(12):1413-1415.
  • [16]Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB: Alternative isoform regulation in human tissue transcriptomes. Nature 2008, 456(7221):470-476.
  • [17]Graveley BR, Brooks AN, Carlson JW, Duff MO, Landolin JM, Yang L, Artieri CG, van Baren MJ, Boley N, Booth BW, Brown JB, Cherbas L, Davis CA, Dobin A, Li R, Lin W, Malone JH, Mattiuzzo NR, Miller D, Sturgill D, Tuch BB, Zaleski C, Zhang D, Blanchette M, Dudoit S, Eads B, Green RE, Hammonds A, Jiang L, Kapranov P, et al.: The developmental transcriptome of Drosophila melanogaster. Nature 2011, 471(7339):473-479.
  • [18]Filichkin SA, Priest HD, Givan SA, Shen R, Bryant DW, Fox SE, Wong WK, Mockler TC: Genome-wide mapping of alternative splicing in Arabidopsis thaliana. Genome Res 2010, 20(1):45-58.
  • [19]Marquez Y, Brown JW, Simpson C, Barta A, Kalyna M: Transcriptome survey reveals increased complexity of the alternative splicing landscape in Arabidopsis. Genome Res 2012, 22(6):1184-1195.
  • [20]Barash Y, Calarco JA, Gao W, Pan Q, Wang X, Shai O, Blencowe BJ, Frey BJ: Deciphering the splicing code. Nature 2010, 465(7294):53-59.
  • [21]Ramani AK, Calarco JA, Pan Q, Mavandadi S, Wang Y, Nelson AC, Lee LJ, Morris Q, Blencowe BJ, Zhen M, Fraser AG: Genome-wide analysis of alternative splicing in Caenorhabditis elegans. Genome Res 2011, 21(2):342-348.
  • [22]Zhu W, Schlueter SD, Brendel V: Refined annotation of the Arabidopsis genome by complete expressed sequence tag mapping. Plant Physiol 2003, 132(2):469-484.
  • [23]Iida K, Seki M, Sakurai T, Satou M, Akiyama K, Toyoda T, Konagaya A, Shinozaki K: Genome-wide analysis of alternative pre-mRNA splicing in Arabidopsis thaliana based on full-length cDNA sequences. Nucleic Acids Res 2004, 32(17):5096-5103.
  • [24]Campbell MA, Haas BJ, Hamilton JP, Mount SM, Buell CR: Comprehensive analysis of alternative splicing in rice and comparative analyses with Arabidopsis. BMC Genomics 2006, 7:327. BioMed Central Full Text
  • [25]Hori K, Watanabe Y: Context analysis of termination codons in mRNA that are recognized by plant NMD. Plant Cell Physiol 2007, 48(7):1072-1078.
  • [26]Barbazuk WB, Fu Y, McGinnis KM: Genome-wide analyses of alternative splicing in plants: opportunities and challenges. Genome Res 2008, 18(9):1381-1392.
  • [27]Goodall GJ, Filipowicz W: Different effects of intron nucleotide composition and secondary structure on pre-mRNA splicing in monocot and dicot plants. EMBO J 1991, 10(9):2635-2644.
  • [28]McCullough AJ, Schuler MA: AU-rich intronic elements affect pre-mRNA 5′ splice site selection in Drosophila melanogaster. Mol Cell Biol 1993, 13(12):7689-7697.
  • [29]Lim LP, Burge CB: A computational analysis of sequence features involved in recognition of short introns. Proc Natl Acad Sci U S A 2001, 98(20):11193-11198.
  • [30]Goodall GJ, Filipowicz W: The AU-rich sequences present in the introns of plant nuclear pre-mRNAs are required for splicing. Cell 1989, 58(3):473-483.
  • [31]Arabidopsis Genome Initiative: Analysis of the genome sequence of the lowering plant Arabidopsis thaliana. Nature 2000, 408(6814):796-815.
  • [32]Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, Funke R, Gage D, Harris K, Heaford A, Howland J, Kann L, Lehoczky J, LeVine R, McEwan P, McKernan K, Meldrim J, Mesirov JP, Miranda C, Morris W, Naylor J, Raymond C, Rosetti M, Santos R, Sheridan A, Sougnez C, et al.: Initial sequencing and analysis of the human genome. Nature 2001, 409(6822):860-921.
  • [33]Alexandrov NN, Troukhan ME, Brover VV, Tatarinova T, Flavell RB, Feldmann KA: Features of Arabidopsis genes and genome discovered using full-length cDNAs. Plant Mol Biol 2006, 60(1):69-85.
  • [34]Wang BB, Brendel V: Genomewide comparative analysis of alternative splicing in plants. Proc Natl Acad Sci U S A 2006, 103(18):7175-7180.
  • [35]White O, Soderlund C, Shanmugan P, Fields C: Information contents and dinucleotide compositions of plant intron sequences vary with evolutionary origin. Plant Mol Biol 1992, 19(6):1057-1064.
  • [36]Yu J, Hu S, Wang J, Wong GK, Li S, Liu B, Deng Y, Dai L, Zhou Y, Zhang X, Cao M, Liu J, Sun J, Tang J, Chen Y, Huang X, Lin W, Ye C, Tong W, Cong L, Geng J, Han Y, Li L, Li W, Hu G, Li J, Liu Z, Qi Q, Li T, Wang X, et al.: A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 2002, 296(5565):79-92.
  • [37]Baek JM, Han P, Iandolino A, Cook DR: Characterization and comparison of intron structure and alternative splicing between Medicago truncatula, Populus trichocarpa, Arabidopsis and rice. Plant Mol Biol 2008, 67(5):499-510.
  • [38]Luehrsen KR, Taha S, Walbot V: Nuclear pre-mRNA processing in higher plants. Prog Nucleic Acid Res Mol Biol 1994, 47:149-193.
  • [39]Jordan T, Schornack S, Lahaye T: Alternative splicing of transcripts encoding Toll-like plant resistance proteins - what’s the functional relevance to innate immunity? Trends Plant Sci 2002, 7(9):392-398.
  • [40]Tanabe N, Yoshimura K, Kimura A, Yabuta Y, Shigeoka S: Differential expression of alternatively spliced mRNAs of Arabidopsis SR protein homologs, atSR30 and atSR45a, in response to environmental stress. Plant Cell Physiol 2007, 48(7):1036-1049.
  • [41]Egawa C, Kobayashi F, Ishibashi M, Nakamura T, Nakamura C, Takumi S: Differential regulation of transcript accumulation and alternative splicing of a DREB2 homolog under abiotic stress conditions in common wheat. Genes Genet Syst 2006, 81(2):77-91.
  • [42]Christensen AH, Sharrock RA, Quail PH: Maize polyubiquitin genes: structure, thermal perturbation of expression and transcript splicing, and promoter activity following transfer to protoplasts by electroporation. Plant Mol Biol 1992, 18(4):675-689.
  • [43]Hopf N, Plesofsky-Vig N, Brambl R: The heat shock response of pollen and other tissues of maize. Plant Mol Biol 1992, 19(4):623-630.
  • [44]Mazzucotelli E, Mastrangelo AA, Crosatti C, Guerra D, Stanca AM, Cattivelli L: Abiotic stress response in plants: when post-transcriptional and post-translational regulations control transcription. Plant Sci 2008, 174:420-431.
  • [45]Ali GS, Reddy AS: Regulation of alternative splicing of pre-mRNAs by stresses. Curr Top Microbiol Immunol 2008, 326:257-275.
  • [46]Syed NH, Kalyna M, Marquez Y, Barta A, Brown JW: Alternative splicing in plants - coming of age. Trends Plant Sci 2012, 17(10):616-623.
  • [47]James AB, Syed NH, Bordage S, Marshall J, Nimmo GA, Jenkins GI, Herzyk P, Brown JW, Nimmo HG: Alternative splicing mediates responses of the Arabidopsis circadian clock to temperature changes. Plant Cell 2012, 24(3):961-981.
  • [48]Huber O, Sumper M: Algal-CAMs: isoforms of a cell adhesion molecule in embryos of the alga Volvox with homology to Drosophila fasciclin I. EMBO J 1994, 13(18):4212-4222.
  • [49]Kianianmomeni A, Nematollahi G, Hallmann A: A gender-specific retinoblastoma-related protein in Volvox carteri implies a role for the retinoblastoma protein family in sexual development. Plant Cell 2008, 20(9):2399-2419.
  • [50]Ferris P, Olson BJ, De Hoff PL, Douglass S, Casero D, Prochnik S, Geng S, Rai R, Grimwood J, Schmutz J, Nishii I, Hamaji T, Nozaki H, Pellegrini M, Umen JG: Evolution of an expanded sex-determining locus in Volvox. Science 2010, 328(5976):351-354.
  • [51]Fuhrmann M, Stahlberg A, Govorunova E, Rank S, Hegemann P: The abundant retinal protein of the Chlamydomonas eye is not the photoreceptor for phototaxis and photophobic responses. J Cell Sci 2001, 114(Pt 21):3857-3863.
  • [52]Schroda M, Vallon O, Whitelegge JP, Beck CF, Wollman FA: The chloroplastic GrpE homolog of Chlamydomonas: two isoforms generated by differential splicing. Plant Cell 2001, 13(12):2823-2839.
  • [53]Labadorf A, Link A, Rogers MF, Thomas J, Reddy AS, Ben-Hur A: Genome-wide analysis of alternative splicing in Chlamydomonas reinhardtii. BMC Genomics 2010, 11:114. BioMed Central Full Text
  • [54]Herron MD, Hackett JD, Aylward FO, Michod RE: Triassic origin and early radiation of multicellular volvocine algae. Proc Natl Acad Sci U S A 2009, 106(9):3254-3258.
  • [55]Sanderson MJ: Molecular data from 27 proteins do not support a Precambrian origin of land plants. Am J Bot 2003, 90(6):954-956.
  • [56]Peterson KJ, Butterfield NJ: Origin of the Eumetazoa: testing ecological predictions of molecular clocks against the Proterozoic fossil record. Proc Natl Acad Sci U S A 2005, 102(27):9547-9552.
  • [57]Kirk DL: A twelve-step program for evolving multicellularity and a division of labor. Bioessays 2005, 27(3):299-310.
  • [58]Prochnik SE, Umen J, Nedelcu AM, Hallmann A, Miller SM, Nishii I, Ferris P, Kuo A, Mitros T, Fritz-Laylin LK, Hellsten U, Chapman J, Simakov O, Rensing SA, Terry A, Pangilinan J, Kapitonov V, Jurka J, Salamov A, Shapiro H, Schmutz J, Grimwood J, Lindquist E, Lucas S, Grigoriev IV, Schmitt R, Kirk D, Rokhsar DS: Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science 2010, 329(5988):223-226.
  • [59]Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Marechal-Drouard L, Marshall WF, Qu LH, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren Q, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Cardol P, Cerutti H, Chanfreau G, Chen CL, Cognat V, Croft MT, Dent R, et al.: The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 2007, 318(5848):245-250.
  • [60]Pennisi E: Volvox genome shows it doesn’t take much to be multicellular. Science 2010, 329(5988):128-129.
  • [61]Irimia M, Penny D, Roy SW: Coevolution of genomic intron number and splice sites. Trends Genet 2007, 23(7):321-325.
  • [62]Holland LZ, Short S: Alternative splicing in development and function of chordate endocrine systems: a focus on Pax genes. Integr Comp Biol 2010, 50(1):22-34.
  • [63]Grabowski P: Alternative splicing takes shape during neuronal development. Curr Opin Genet Dev 2011, 21(4):388-394.
  • [64]Lozada-Chávez I, Stadler PF, Prohaska SJ: “Hypothesis for the modern RNA world”: a pervasive non-coding RNA-based genetic regulation is a prerequisite for the emergence of multicellular complexity. Orig Life Evol Biosph 2011, 41(6):587-607.
  • [65]Kim E, Magen A, Ast G: Different levels of alternative splicing among eukaryotes. Nucleic Acids Res 2007, 35(1):125-131.
  • [66]Roy M, Kim N, Xing Y, Lee C: The effect of intron length on exon creation ratios during the evolution of mammalian genomes. RNA 2008, 14(11):2261-2273.
  • [67]Kent WJ: BLAT - the BLAST-like alignment tool. Genome Res 2002, 12(4):656-664.
  • [68]Sparks ME, Brendel V: Incorporation of splice site probability models for non-canonical introns improves gene structure prediction in plants. Bioinformatics 2005, 21 Suppl 3:iii20-iii30.
  • [69]Yu AY, Houry WA: ClpP: a distinctive family of cylindrical energy-dependent serine proteases. FEBS Lett 2007, 581(19):3749-3757.
  • [70]Majeran W, Friso G, van Wijk KJ, Vallon O: The chloroplast ClpP complex in Chlamydomonas reinhardtii contains an unusual high molecular mass subunit with a large apical domain. FEBS J 2005, 272(21):5558-5571.
  • [71]Ekici OD, Paetzel M, Dalbey RE: Unconventional serine proteases: variations on the catalytic Ser/His/Asp triad configuration. Protein Sci 2008, 17(12):2023-2037.
  • [72]Wang J, Hartling JA, Flanagan JM: The structure of ClpP at 2.3 Å resolution suggests a model for ATP-dependent proteolysis. Cell 1997, 91(4):447-456.
  • [73]Bove J, Kim CY, Gibson CA, Assmann SM: Characterization of wound-responsive RNA-binding proteins and their splice variants in Arabidopsis. Plant Mol Biol 2008, 67(1–2):71-88.
  • [74]Moll AG, Lindenmeyer MT, Kretzler M, Nelson PJ, Zimmer R, Cohen CD: Transcript-specific expression profiles derived from sequence-based analysis of standard microarrays. PLoS One 2009, 4(3):e4702.
  • [75]Chamberlain KL, Miller SH, Keller LR: Gene expression profiling of flagellar disassembly in Chlamydomonas reinhardtii. Genetics 2008, 179(1):7-19.
  • [76]Amon P, Haas E, Sumper M: The sex-inducing pheromone and wounding trigger the same set of genes in the multicellular green alga Volvox. Plant Cell 1998, 10(5):781-789.
  • [77]Hallmann A: The pherophorins: common, versatile building blocks in the evolution of extracellular matrix architecture in Volvocales. Plant J 2006, 45(2):292-307.
  • [78]Nematollahi G, Kianianmomeni A, Hallmann A: Quantitative analysis of cell-type specific gene expression in the green alga Volvox carteri. BMC Genomics 2006, 7(1):321. BioMed Central Full Text
  • [79]Fraga D, Meulia T, Fenster S: Real-Time PCR. In Current Protocols Essential Laboratory Techniques. Edited by Gallagher SR, Wiley EA. New York: John Wiley & Sons; 2008.
  • [80]Hilgenfeld R: Regulatory GTPases. Curr Opin Struct Biol 1995, 5(6):810-817.
  • [81]Agirrezabala X, Frank J: Elongation in translation as a dynamic interaction among the ribosome, tRNA, and elongation factors EF-G and EF-Tu. Q Rev Biophys 2009, 42(3):159-200.
  • [82]Kjeldgaard M, Nyborg J: Refined structure of elongation factor EF-Tu from Escherichia coli. J Mol Biol 1992, 223(3):721-742.
  • [83]Kawashima T, Berthet-Colominas C, Wulff M, Cusack S, Leberman R: The structure of the Escherichia coli EF-Tu.EF-Ts complex at 2.5 Å resolution. Nature 1996, 379(6565):511-518.
  • [84]Bourne HR, Sanders DA, McCormick F: The GTPase superfamily: conserved structure and molecular mechanism. Nature 1991, 349(6305):117-127.
  • [85]Berchtold H, Reshetnikova L, Reiser CO, Schirmer NK, Sprinzl M, Hilgenfeld R: Crystal structure of active elongation factor Tu reveals major domain rearrangements. Nature 1993, 365(6442):126-132.
  • [86]Nissen P, Kjeldgaard M, Thirup S, Polekhina G, Reshetnikova L, Clark BF, Nyborg J: Crystal structure of the ternary complex of Phe-tRNAPhe, EF-Tu, and a GTP analog. Science 1995, 270(5241):1464-1472.
  • [87]Adams MW: The structure and mechanism of iron-hydrogenases. Biochim Biophys Acta 1990, 1020(2):115-145.
  • [88]Przybyla AE, Robbins J, Menon N, Peck HD Jr: Structure-function relationships among the nickel-containing hydrogenases. FEMS Microbiol Rev 1992, 8(2):109-135.
  • [89]Happe T, Kaminski A: Differential regulation of the Fe-hydrogenase during anaerobic adaptation in the green alga Chlamydomonas reinhardtii. Eur J Biochem 2002, 269(3):1022-1032.
  • [90]Forestier M, King P, Zhang L, Posewitz M, Schwarzer S, Happe T, Ghirardi ML, Seibert M: Expression of two [Fe]-hydrogenases in Chlamydomonas reinhardtii under anaerobic conditions. Eur J Biochem 2003, 270(13):2750-2758.
  • [91]Peters JW, Lanzilotta WN, Lemon BJ, Seefeldt LC: X-ray crystal structure of the Fe-only hydrogenase (CpI) from Clostridium pasteurianum to 1.8 Angstrom resolution. Science 1998, 282(5395):1853-1858.
  • [92]Shimizu T, Inoue T, Shiraishi H: Cloning and characterization of novel extensin-like cDNAs that are expressed during late somatic cell phase in the green alga Volvox carteri. Gene 2002, 284(1–2):179-187.
  • [93]Kinoshita T, Fukuzawa H, Shimada T, Saito T, Matsuda Y: Primary structure and expression of a gamete lytic enzyme in Chlamydomonas reinhardtii: similarity of functional domains to matrix metalloproteases. Proc Natl Acad Sci U S A 1992, 89(10):4693-4697.
  • [94]Hallmann A, Amon P, Godl K, Heitzer M, Sumper M: Transcriptional activation by the sexual pheromone and wounding: a new gene family from Volvox encoding modular proteins with (hydroxy)proline-rich and metalloproteinase homology domains. Plant J 2001, 26(6):583-593.
  • [95]Heitzer M, Hallmann A: An extracellular matrix-localized metalloproteinase with an exceptional QEXXH metal binding site prefers copper for catalytic activity. J Biol Chem 2002, 277(31):28280-28286.
  • [96]Hooper NM: Families of zinc metalloproteases. FEBS Lett 1994, 354(1):1-6.
  • [97]Soejima H, Zhao W, Mukai T: Epigenetic silencing of the MGMT gene in cancer. Biochem Cell Biol 2005, 83(4):429-437.
  • [98]Kaina B, Christmann M, Naumann S, Roos WP: MGMT: key node in the battle against genotoxicity, carcinogenicity and apoptosis induced by alkylating agents. DNA Repair (Amst) 2007, 6(8):1079-1099.
  • [99]Margison GP, Povey AC, Kaina B, Santibáñez Koref MF: Variability and regulation of O6-alkylguanine-DNA alkyltransferase. Carcinogenesis 2003, 24(4):625-635.
  • [100]Daniels DS, Mol CD, Arvai AS, Kanugula S, Pegg AE, Tainer JA: Active and alkylated human AGT structures: a novel zinc site, inhibitor and extrahelical base binding. EMBO J 2000, 19(7):1719-1730.
  • [101]Daniels DS, Woo TT, Luu KX, Noll DM, Clarke ND, Pegg AE, Tainer JA: DNA binding and nucleotide flipping by the human DNA repair protein AGT. Nat Struct Mol Biol 2004, 11(8):714-720.
  • [102]Duguid EM, Rice PA, He C: The structure of the human AGT protein bound to DNA and its implications for damage detection. J Mol Biol 2005, 350(4):657-666.
  • [103]Dreyfuss G, Kim VN, Kataoka N: Messenger-RNA-binding proteins and the messages they carry. Nat Rev Mol Cell Biol 2002, 3(3):195-205.
  • [104]Maris C, Dominguez C, Allain FH: The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J 2005, 272(9):2118-2131.
  • [105]Cléry A, Blatter M, Allain FH: RNA recognition motifs: boring? not quite. Curr Opin Struct Biol 2008, 18(3):290-298.
  • [106]Oubridge C, Ito N, Evans PR, Teo CH, Nagai K: Crystal structure at 1.92 Å resolution of the RNA-binding domain of the U1A spliceosomal protein complexed with an RNA hairpin. Nature 1994, 372(6505):432-438.
  • [107]Low SC, Berry MJ: Knowing when not to stop: selenocysteine incorporation in eukaryotes. Trends Biochem Sci 1996, 21(6):203-208.
  • [108]Wang P, Heitman J: The cyclophilins. Genome Biol 2005, 6(7):226. BioMed Central Full Text
  • [109]Maleszka R, Lupas A, Hanes SD, Miklos GL: The dodo gene family encodes a novel protein involved in signal transduction and protein folding. Gene 1997, 203(2):89-93.
  • [110]Horowitz DS, Lee EJ, Mabon SA, Misteli T: A cyclophilin functions in pre-mRNA splicing. EMBO J 2002, 21(3):470-480.
  • [111]Ingelfinger D, Gothel SF, Marahiel MA, Reidt U, Ficner R, Luhrmann R, Achsel T: Two protein-protein interaction sites on the spliceosome-associated human cyclophilin CypH. Nucleic Acids Res 2003, 31(16):4791-4796.
  • [112]He Z, Li L, Luan S: Immunophilins and parvulins. superfamily of peptidyl prolyl isomerases in Arabidopsis. Plant Physiol 2004, 134(4):1248-1267.
  • [113]Romano P, Gray J, Horton P, Luan S: Plant immunophilins: functional versatility beyond protein maturation. New Phytol 2005, 166(3):753-769.
  • [114]Kallen J, Spitzfaden C, Zurini MG, Wider G, Widmer H, Wuthrich K, Walkinshaw MD: Structure of human cyclophilin and its binding site for cyclosporin A determined by X-ray crystallography and NMR spectroscopy. Nature 1991, 353(6341):276-279.
  • [115]Pflügl G, Kallen J, Schirmer T, Jansonius JN, Zurini MG, Walkinshaw MD: X-ray structure of a decameric cyclophilin-cyclosporin crystal complex. Nature 1993, 361(6407):91-94.
  • [116]Zydowsky LD, Etzkorn FA, Chang HY, Ferguson SB, Stolz LA, Ho SI, Walsh CT: Active site mutants of human cyclophilin A separate peptidyl-prolyl isomerase activity from cyclosporin A binding and calcineurin inhibition. Protein Sci 1992, 1(9):1092-1099.
  • [117]Cardenas ME, Lim E, Heitman J: Mutations that perturb cyclophilin A ligand binding pocket confer cyclosporin A resistance in Saccharomyces cerevisiae. J Biol Chem 1995, 270(36):20997-21002.
  • [118]Tam LW, Kirk DL: Identification of cell-type-specific genes of Volvox carteri and characterization of their expression during the asexual life cycle. Dev Biol 1991, 145(1):51-66.
  • [119]Meissner M, Stark K, Cresnar B, Kirk DL, Schmitt R: Volvox germline-specific genes that are putative targets of RegA repression encode chloroplast proteins. Curr Genet 1999, 36(6):363-370.
  • [120]Mayfield SP, Bennoun P, Rochaix JD: Expression of the nuclear encoded OEE1 protein is required for oxygen evolution and stability of photosystem II particles in Chlamydomonas reinhardtii. EMBO J 1987, 6(2):313-318.
  • [121]Yi X, McChargue M, Laborde S, Frankel LK, Bricker TM: The manganese-stabilizing protein is required for photosystem II assembly/stability and photoautotrophy in higher plants. J Biol Chem 2005, 280(16):16170-16174.
  • [122]García-Gimeno MA, Muñoz I, Ariño J, Sanz P: Molecular characterization of Ypi1, a novel Saccharomyces cerevisiae type 1 protein phosphatase inhibitor. J Biol Chem 2003, 278(48):47744-47752.
  • [123]Pazour GJ, Agrin N, Leszyk J, Witman GB: Proteomic analysis of a eukaryotic cilium. J Cell Biol 2005, 170(1):103-113.
  • [124]Modrek B, Resch A, Grasso C, Lee C: Genome-wide detection of alternative splicing in expressed sequences of human genes. Nucleic Acids Res 2001, 29(13):2850-2859.
  • [125]Zavolan M, Kondo S, Schonbach C, Adachi J, Hume DA, Hayashizaki Y, Gaasterland T: Impact of alternative initiation, splicing, and termination on the diversity of the mRNA transcripts encoded by the mouse transcriptome. Genome Res 2003, 13(6B):1290-1300.
  • [126]Gupta S, Zink D, Korn B, Vingron M, Haas SA: Genome wide identification and classification of alternative splicing based on EST data. Bioinformatics 2004, 20(16):2579-2585.
  • [127]Okazaki Y, Furuno M, Kasukawa T, Adachi J, Bono H, Kondo S, Nikaido I, Osato N, Saito R, Suzuki H, Yamanaka I, Kiyosawa H, Yagi K, Tomaru Y, Hasegawa Y, Nogami A, Schönbach C, Gojobori T, Baldarelli R, Hill DP, Bult C, Hume DA, Quackenbush J, Schriml LM, Kanapin A, Matsuda H, Batalov S, Beisel KW, Blake JA, Bradt D, et al.: Analysis of the mouse transcriptome based on functional annotation of 60,770 full-length cDNAs. Nature 2002, 420(6915):563-573.
  • [128]Nilsen TW, Graveley BR: Expansion of the eukaryotic proteome by alternative splicing. Nature 2010, 463(7280):457-463.
  • [129]Klaff P, Riesner D, Steger G: RNA structure and the regulation of gene expression. Plant Mol Biol 1996, 32(1–2):89-106.
  • [130]Nackley AG, Shabalina SA, Tchivileva IE, Satterfield K, Korchynskyi O, Makarov SS, Maixner W, Diatchenko L: Human catechol-O-methyltransferase haplotypes modulate protein expression by altering mRNA secondary structure. Science 2006, 314(5807):1930-1933.
  • [131]Kudla G, Murray AW, Tollervey D, Plotkin JB: Coding-sequence determinants of gene expression in Escherichia coli. Science 2009, 324(5924):255-258.
  • [132]Gommans WM, Mullen SP, Maas S: RNA editing: a driving force for adaptive evolution? Bioessays 2009, 31(10):1137-1145.
  • [133]Surdej P, Riedl A, Jacobs-Lorena M: Regulation of mRNA stability in development. Annu Rev Genet 1994, 28:263-282.
  • [134]Gamazon ER, Stranger BE: Genomics of alternative splicing: evolution, development and pathophysiology. Hum Genet 2014, 133(6):679-687.
  • [135]Fedorova L, Fedorov A: Puzzles of the human genome: why do we need our introns? Curr Genomics 2005, 6(8):589-595.
  • [136]Galante PA, Sakabe NJ, Kirschbaum-Slager N, de Souza SJ: Detection and evaluation of intron retention events in the human transcriptome. RNA 2004, 10(5):757-765.
  • [137]Stamm S, Zhu J, Nakai K, Stoilov P, Stoss O, Zhang MQ: An alternative-exon database and its statistical analysis. DNA Cell Biol 2000, 19(12):739-756.
  • [138]Zheng CL, Fu XD, Gribskov M: Characteristics and regulatory elements defining constitutive splicing and different modes of alternative splicing in human and mouse. RNA 2005, 11(12):1777-1787.
  • [139]McGuire AM, Pearson MD, Neafsey DE, Galagan JE: Cross-kingdom patterns of alternative splicing and splice recognition. Genome Biol 2008, 9(3):R50. BioMed Central Full Text
  • [140]Kandul NP, Noor MA: Large introns in relation to alternative splicing and gene evolution: a case study of Drosophila bruno-3. BMC Genet 2009, 10:67.
  • [141]Fox-Walsh KL, Dou Y, Lam BJ, Hung SP, Baldi PF, Hertel KJ: The architecture of pre-mRNAs affects mechanisms of splice-site pairing. Proc Natl Acad Sci U S A 2005, 102(45):16176-16181.
  • [142]Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM: The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 1990, 346(6279):35-39.
  • [143]Hong RL, Hamaguchi L, Busch MA, Weigel D: Regulatory elements of the floral homeotic gene AGAMOUS identified by phylogenetic footprinting and shadowing. Plant Cell 2003, 15(6):1296-1309.
  • [144]Bruggmann R, Bharti AK, Gundlach H, Lai J, Young S, Pontaroli AC, Wei F, Haberer G, Fuks G, Du C, Raymond C, Estep MC, Liu R, Bennetzen JL, Chan AP, Rabinowicz PD, Quackenbush J, Barbazuk WB, Wing RA, Birren B, Nusbaum C, Rounsley S, Mayer KF, Messing J: Uneven chromosome contraction and expansion in the maize genome. Genome Res 2006, 16(10):1241-1251.
  • [145]Kobayashi Y, Dokiya Y, Sugiura M, Niwa Y, Sugita M: Genomic organization and organ-specific expression of a nuclear gene encoding phage-type RNA polymerase in Nicotiana sylvestris. Gene 2001, 279(1):33-40.
  • [146]Tadege M, Sheldon CC, Helliwell CA, Upadhyaya NM, Dennis ES, Peacock WJ: Reciprocal control of flowering time by OsSOC1 in transgenic Arabidopsis and by FLC in transgenic rice. Plant Biotechnol J 2003, 1(5):361-369.
  • [147]Haddrill PR, Charlesworth B, Halligan DL, Andolfatto P: Patterns of intron sequence evolution in Drosophila are dependent upon length and GC content. Genome Biol 2005, 6(8):R67. BioMed Central Full Text
  • [148]Marais G, Nouvellet P, Keightley PD, Charlesworth B: Intron size and exon evolution in Drosophila. Genetics 2005, 170(1):481-485.
  • [149]Irimia M, Rukov JL, Penny D, Roy SW: Functional and evolutionary analysis of alternatively spliced genes is consistent with an early eukaryotic origin of alternative splicing. BMC Evol Biol 2007, 7:188. BioMed Central Full Text
  • [150]Luco RF, Allo M, Schor IE, Kornblihtt AR, Misteli T: Epigenetics in alternative pre-mRNA splicing. Cell 2011, 144(1):16-26.
  • [151]Taneri B, Snyder B, Novoradovsky A, Gaasterland T: Alternative splicing of mouse transcription factors affects their DNA-binding domain architecture and is tissue specific. Genome Biol 2004, 5(10):R75. BioMed Central Full Text
  • [152]Umen JG, Goodenough UW: Control of cell division by a retinoblastoma protein homolog in Chlamydomonas. Genes Dev 2001, 15(13):1652-1661.
  • [153]Umen JG: Evolution of sex and mating loci: an expanded view from volvocine algae. Curr Opin Microbiol 2011, 14(6):634-641.
  • [154]Xiao YL, Smith SR, Ishmael N, Redman JC, Kumar N, Monaghan EL, Ayele M, Haas BJ, Wu HC, Town CD: Analysis of the cDNAs of hypothetical genes on Arabidopsis chromosome 2 reveals numerous transcript variants. Plant Physiol 2005, 139(3):1323-1337.
  • [155]Melamud E, Moult J: Stochastic noise in splicing machinery. Nucleic Acids Res 2009, 37(14):4873-4886.
  • [156]Pickrell JK, Pai AA, Gilad Y, Pritchard JK: Noisy splicing drives mRNA isoform diversity in human cells. PLoS Genet 2010, 6(12):e1001236.
  • [157]Resch A, Xing Y, Alekseyenko A, Modrek B, Lee C: Evidence for a subpopulation of conserved alternative splicing events under selection pressure for protein reading frame preservation. Nucleic Acids Res 2004, 32(4):1261-1269.
  • [158]Adams CR, Stamer KA, Miller JK, McNally JG, Kirk MM, Kirk DL: Patterns of organellar and nuclear inheritance among progeny of two geographically isolated strains of Volvox carteri. Curr Genet 1990, 18(2):141-153.
  • [159]Provasoli L, Pintner IJ: Artificial media for fresh-water algae: problems and suggestions. In The Ecology of Algae, a Symposium Held at the Pymatuning Laboratory of Field Biology on June 18 and 19, 1959. 1st edition. Edited by Tryon CA, Hartman RT. Pittsburgh, PA: The Pymatuning Symposia in Ecology, Special Publication No. 2., University of Pittsburgh; 1959:84-96.
  • [160]Starr RC, Jaenicke L: Purification and characterization of the hormone initiating sexual morphogenesis in Volvox carteri f. nagariensis Iyengar. Proc Natl Acad Sci U S A 1974, 71(4):1050-1054.
  • [161]Sambrook J, Russell DW: Molecular Cloning: A Laboratory Manual (3rd Edition), Vol. 1-3, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 2001.
  • [162]Cresnar B, Mages W, Müller K, Salbaum JM, Schmitt R: Structure and expression of a single actin gene in Volvox carteri. Curr Genet 1990, 18(4):337-346.
  • [163]Bustin SA: Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J Mol Endocrinol 2000, 25(2):169-193.
  • [164]Pfaffl MW: A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29(9):e45.
  文献评价指标  
  下载次数:4次 浏览次数:24次