期刊论文详细信息
BMC Genomics
The Chironomus tentans genome sequence and the organization of the Balbiani ring genes
Lars Wieslander2  Neus Visa2  Stefania Giacomello3  Erik Sonnhammer4  Petra Björk2  Joakim Lundeberg1  Björn Nystedt5  Thomas Svensson3  Alexey Kutsenko3 
[1] Science for Life Laboratory, KTH, Royal Institute of Technology, Science for Life Laboratory, SE-171 65 Solna, Sweden;Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, SE-106 91 Stockholm, Sweden;Science for Life Laboratory, Department of Biochemistry and Biophysics, Stockholm University, SE-171 21 Solna, Sweden;Department of Biochemistry and Biophysics, Stockholm University, SE-106 91 Stockholm, Sweden;Science for Life Laboratory, Department of Cell and Molecular Biology, Uppsala University, SE-752 37 Uppsala, Sweden
关键词: Chromosome puffs;    Balbiani ring genes;    Model organisms;    Eukaryotic gene expression;   
Others  :  1139512
DOI  :  10.1186/1471-2164-15-819
 received in 2014-06-13, accepted in 2014-09-22,  发布年份 2014
【 摘 要 】

Background

The polytene nuclei of the dipteran Chironomus tentans (Ch. tentans) with their Balbiani ring (BR) genes constitute an exceptional model system for studies of the expression of endogenous eukaryotic genes. Here, we report the first draft genome of Ch. tentans and characterize its gene expression machineries and genomic architecture of the BR genes.

Results

The genome of Ch. tentans is approximately 200 Mb in size, and has a low GC content (31%) and a low repeat fraction (15%) compared to other Dipteran species. Phylogenetic inference revealed that Ch. tentans is a sister clade to mosquitoes, with a split 150–250 million years ago. To characterize the Ch. tentans gene expression machineries, we identified potential orthologus sequences to more than 600 Drosophila melanogaster (D. melanogaster) proteins involved in the expression of protein-coding genes. We report novel data on the organization of the BR gene loci, including a novel putative BR gene, and we present a model for the organization of chromatin bundles in the BR2 puff based on genic and intergenic in situ hybridizations.

Conclusions

We show that the molecular machineries operating in gene expression are largely conserved between Ch. tentans and D. melanogaster, and we provide enhanced insight into the organization and expression of the BR genes. Our data strengthen the generality of the BR genes as a unique model system and provide essential background for in-depth studies of the biogenesis of messenger ribonucleoprotein complexes.

【 授权许可】

   
2014 Kutsenko et al.; licensee BioMed Central Ltd.

附件列表
Files Size Format View
Figure 1. 55KB Image download
Figure 5. 108KB Image download
Figure 4. 43KB Image download
Figure 3. 62KB Image download
Figure 2. 45KB Image download
Figure 1. 46KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 1.

【 参考文献 】
  • [1]Nebeker AV, Cairns MA, Wise C: Relative sensitivity of Chironomus tentans life stages to copper. Environ Toxicol Chem 1984, 3:151-158.
  • [2]Call DJ, Polkinghorne CN, Brooke TP, Geiger LT, Gorsuch JW, Robillard KA: Silver toxicity to Chironomus tentans in two freshwater sediments. Environ Toxicol Chem 1999, 18:30-39.
  • [3]Ingersoll CG, Brunson EL, Dwyer FJ, Ankley GT, Benoit DA, Norberg-Kling TJ, Burton GA, Hoke RA, Landrum PF, Winger PV: Toxicity and bioaccumulation of sediment-associated contaminants using freshwater invertebrates: a review of methods and applications. Environ Toxicol Chem 1995, 14:1885-1894.
  • [4]Kornberg RD: The eukaryotic gene transcription machinery. Biol Chem 2001, 382:1103-1107.
  • [5]Ramakrishnan V: The ribosome: some hard facts about its structure and hot air about its evolution. Cold Spring Harb Symp Quant Biol 2009, 74:25-33.
  • [6]Bono F, Gehring NH: Assembly, disassembly and recycling: the dynamics of exon junction complexes. RNA Biol 2011, 8:24-29.
  • [7]Will CL, Lührmann R: Spliceosomal structure and function. Cold Spring Harb Perspect Biol 2011, 3:a003707.
  • [8]Müller-McNicoll M, Neugebauer KM: How cells get the message: dynamic assembly and function of mRNA-protein complexes. Nat Rev Genet 2013, 14:275-287.
  • [9]Adams RL, Wente SR: Uncovering nuclear pore complexity with innovation. Cell 2013, 152:1218-1221.
  • [10]Herold N, Will CL, Wolf E, Kastner B, Urlaub H, Lührmann R: Conservation of the protein composition and electron microscopy structure of Drosophila melanogaster and human spliceosomal complexes. Mol Cell Biol 2009, 29:281-301.
  • [11]Daneholt B: Assembly and transport of a premessenger RNP particle. Proc Natl Acad Sci U S A 2001, 98:7012-7017.
  • [12]Björk P, Wieslander L: Nucleocytoplasmic mRNP export is an integral part of mRNP biogenesis. Chromosoma 2011, 120:23-38.
  • [13]Case ST, Wieslander L: Secretory proteins of Chironomus salivary glands: structural motifs and assembly characteristics of a novel biopolymer. In Results and Problems in Cell Differentiation 19 Biopolymers. Edited by Case ST. Berlin Heidelberg: Springer-Verlag; 1992:187-226.
  • [14]Wieslander L: The Balbiani ring multigene family: coding repetitive sequences and evolution of a tissue-specific cell function. Progr Nucleic Acids Res Mol Biol 1994, 48:275-313.
  • [15]Ericsson C, Mehlin H, Björkroth B, Lamb MM, Daneholt B: The ultrastructure of upstream and downstream regions of an active Balbiani ring gene. Cell 1989, 56:631-639.
  • [16]Percipalle P, Fomproix N, Kylberg K, Miralles F, Björkroth B, Daneholt B, Visa N: An actin-ribonucleoprotein interaction is involved in transcription by RNA polymerase II. Proc Natl Acad Sci U S A 2003, 100:6475-6480.
  • [17]Visa N, Izaurralde E, Ferreira J, Daneholt B, Mattaj IW: A nuclear cap-binding complex binds Balbiani ring pre-mRNA cotranscriptionally and accompanies the ribonucleoprotein particle during nuclear export. J Cell Biol 1996, 133:5-14.
  • [18]Baurén G, Wieslander L: Splicing of Balbiani ring 1 gene pre-mRNA occurs simultaneously with transcription. Cell 1994, 76:183-192.
  • [19]Baurén G, Belikov S, Wieslander L: Transcriptional termination in the Balbiani ring 1 gene is closely coupled to 3′-end formation and excision of the 3′-terminal intron. Genes Dev 1998, 12:2759-2769.
  • [20]Mehlin H, Daneholt B, Skoglund U: Structural interaction between the nuclear pore complex and a specific translocating RNP particle. J Cell Biol 1995, 129:1205-1216.
  • [21]Miralles F, Öfverstedt LG, Sabri N, Assouni Y, Hellman U, Skoglund U, Visa N: Electron tomography reveals posttranscriptional binding of pre-mRNPs to specific fibers in the nucleoplasm. J Cell Biol 2000, 148:271-282.
  • [22]Siebrasse JP, Kaminski T, Kubitscheck U: Nuclear export of single native mRNA molecules observed by light sheet fluorescence microscopy. Proc Natl Acad Sci U S A 2012, 109:9426-9431.
  • [23]Wyss C: Chironomus tentans epithelial cell lines sensitive to ecdysteroids, juvenile hormone, insulin and heat shock. Exp Cell Res 1982, 139:309-319.
  • [24]Baurén G, Jing W-Q, Bernholm K, Gu F, Wieslander L: Demonstration of a dynamic, transcription-dependent organization of pre-mRNA splicing factors in polytene nuclei. J Cell Biol 1996, 133:929-941.
  • [25]Wurtz T, Kiseleva E, Nacheva G, Alzhanova-Ericsson A, Rosén A, Daneholt B: Identification of two RNA-binding proteins in Balbiani ring premessenger ribonucleoprotein granules and presence of these proteins in specific subsets of heterogeneous nuclear ribonucleoprotein particles. Mol Cell Biol 1996, 16:1425-1435.
  • [26]Kiesler E, Miralles F, Visa N: HEL/UAP56 binds cotranscriptionally to the Balbiani ring pre-mRNA in an intron-independent manner and accompanies the BR mRNP to the nuclear pore. Curr Biol 2002, 12:859-862.
  • [27]Björk P, Jin S, Zhao J, Singh OP, Persson JO, Hellman U, Wieslander L: Specific combinations of SR proteins associate with single pre-messenger RNAs in vivo and contribute different functions. J Cell Biol 2009, 184:555-568.
  • [28]Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W: Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 2011, 27:578-579.
  • [29]Daneholt B, Edström JE: The content of deoxyribonucleic acid in individual polytene chromosomes of Chironomus tentans. Cytogenetics 1967, 6:350-356.
  • [30]Wieslander L: Number and structure of Balbiani ring 75S RNA transcription units in Chironomus tentans. J Mol Biol 1979, 134:347-367.
  • [31]Derksen J, Wieslander L, van der Ploeg M, Daneholt B: Identification of the Balbiani ring 2 chromomere and determination of the content and compaction of its DNA. Chromosoma 1980, 81:65-84.
  • [32]Parra G, Bradnam K, Ning Z, Keane T, Korf I: Assessing the gene space in draft genomes. Nucleic Acids Res 2009, 37:289-297.
  • [33]Cockburn AF, Mitchell SE: Repetitive DNA interspersion patterns in Diptera. Arch Insect Biocem Phys 1989, 10:105-113.
  • [34]Nene V, Wortman JR, Lawson D, Haas B, Kodira C, Tu ZJ, Loftus B, Xi Z, Megy K, Grabherr M, Ren Q, Zdobnov EM, Lobo NF, Campbell KS, Brown SE, Bonaldo MF, Zhu J, Sinkins SP, Hogenkamp DG, Amedeo P, Arensburger P, Atkinson PW, Bidwell S, Biedler J, Birney E, Bruggner RV, Costas J, Coy MR, Crabtree J, Crawford M, et al.: Genome sequence of Aedes aegypti, a major arbovirus vector. Science 2007, 316:1718-1723.
  • [35]Timoshevskiy V, Kinney NA, de Bruyn BS, Mao C, Tu Z, Severson D, Sharakov IV, Sharakova MV: Genomic composition and evolution of Aedes aegypti chromosomes revealed by the analysis of physically mapped supercontigs. BMC Biol 2014, 12:27. BioMed Central Full Text
  • [36]Arensburger P, Megy K, Waterhouse RM, Abrudan J, Amedio P, Antelo B, Bartholomay L, Biddwell S, Caler E, Camara F, Campbell CL, Campbell KS, Casola C, Castro MT, Chandramouliswaran I, Chapman SB, Christley S, Costas J, Eisenstadt E, Feschotte C, Fraser-Liggett C, Guigo R, Haas B, Hammond M, Hansson BS, Hemingway J, Hill SR, Howarth C, Ignell R, Kennedy RC, et al.: Sequencing of Culex quinquefasciatus establishes a platform for mosquito comparative genomics. Science 2010, 330:86-88.
  • [37]Marsano RM, Leronni D, D’Addabbo P, Viggiano L, Tarasco E, Caizzi R: Mosquitoes LTR retrotransposons: a deeper view into the genomic sequence of Culex quinquefasciatus. PLoS One 2012, 7:e30770.
  • [38]Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R, Nusskern DR, Wincker P, Clark AG, Ribeiro JMC, Wides R, Salzberg SL, Loftus B, Yandell M, Majoros WH, Rusch DB, Lai Z, Kraft CL, Abril JF, Anthouard V, Arensburger P, Atkinson PW, Baden H, de Berardinis V, Baldwin D, Benes V, Biedler J, Blass C, Bolanos R, Boscus D, Barnstead M, et al.: The genome sequence of the malaria mosquito Anopheles gambiae. Science 2002, 298:129-149.
  • [39]Sharakova MV, George P, Brusentsova IV, Leman SC, Bailey JA, Smith CD, Sharakov IV: Genome mapping and characterization of the Anopheles gambiae heterochromatin. BMC Genomics 2010, 11:459. BioMed Central Full Text
  • [40]Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, Amanatidis PG, Scherer SE, Li PW, Hoskins RA, Galle RF, George RA, Lewis SE, Richards S, Ashburner M, Henderson SN, Sutton GG, Wortman JR, Yandell MD, Zhang Q, Chen LX, Brandon RC, Rogers YH, Blazej RG, Champe M, Pfeiffer BD, Wan KH, Doyle C, Baxter EG, Helt G, Nelson CR, et al.: The genome sequence of Drosophila melanogaster. Science 2000, 287:2185-2195.
  • [41]Schmidt ER: The development of a 120 base-pair repetitive DNA sequence in Chironomus thummi is correlated to the duplication of defined chromosomal segments. FEBS Lett 1981, 129:21-24.
  • [42]Schmidt ER: Clustered and interspersed repetitive DNA family of Chironomus. J Mol Biol 1984, 178:1-15.
  • [43]Schaefer J, Schmidt ER: Different repetition frequencies of a 120 base-pair DNA-element and its arrangement in Chironomus thummi thummi and Chironomus thummi piger. Chromosoma 1981, 84:61-66.
  • [44]Ross R, Hankeln T, Schmidt ER: Complex evolution of tandem-repetitive DNA in the Chironomus thummi species group. J Mol Evol 1997, 44:321-326.
  • [45]Mount SM, Burks C, Hertz G, Stormo GD, White O, Fields C: Splicing signals in Drosophila: intron size, information content, and consensus sequences. Nucleic Acids Res 1992, 20:4255-4262.
  • [46]Lim LP, Burge C: A computational analysis of sequence features involved in recognition of short introns. Proc Natl Acad Sci U S A 2001, 98:11193-11198.
  • [47]Talerico M, Berget SM: Intron definition in splicing of small Drosophila introns. Mol Cell Biol 1994, 14:3434-3445.
  • [48]Chen F, Mackey AJ, Stoeckert CJ, Roos DS: OrthoMCL-DB: querying a comprehensive multi-species collection of ortholog groups. Nucleic Acids Res 2006, 34:D363-D368.
  • [49]You M, Yue Z, He W, Yang X, Yang G, Xie M, Zhan D, Baxter SW, Vasseur L, Gurr GM, Douglas CJ, Bai J, Wang P, Cui K, Huang S, Li X, Zhou Q, Wu Z, Chen Q, Liu C, Wang B, Li X, Xu X, Lu C, Hu M, Davey JW, Smith SM, Chen M, Xia X, Tang W, et al.: A heterozygous moth genome provides insights into herbivory and detoxification. Nat Genet 2013, 45:220-225.
  • [50]Conesa A, Götz S, Garcia-Gómez JM, Terol J, Talón M, Robles M: Blast2GO. 2005–2011 (http://www.blast2go.com webcite)
  • [51]Östlund G, Schmitt T, Forslund K, Köstler T, Messina DN, Roopra S, Frings O, Sonnhammer EL: InParanoid 7: new algorithms and tools for eukaryotic orthology analysis. Nucleic Acids Res 2010, 38:D196-D203.
  • [52]Lassmann T, Sonnhammer EL: Kalign - an accurate and fast multiple sequence alignment algorithm. BMC Bioinformatics 2005, 6:298. BioMed Central Full Text
  • [53]Slater GS, Birney E: Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics 2005, 6:31. BioMed Central Full Text
  • [54]Waterhouse RM, Zdobnov EM, Tegenfeldt F, Li J, Kriventseva EV: OrthoDB: the hierarchical catalog of eukaryotic orthologs in 2011. Nucleic Acids Res 2011, 39:D283-D288.
  • [55]Paulsson G, Lendahl U, Galli J, Ericsson C, Wieslander L: The Balbiani ring 3 gene in Chironomus tentans has a diverged repetitive structure split by many introns. J Mol Biol 1990, 211:331-349.
  • [56]Dreesen TD, Bower JR, Case ST: A second gene in a Balbiani ring. J Biol Chem 1985, 260:11824-11830.
  • [57]Lamb MM, Daneholt B: Characterization of active transcription units in Balbiani rings of Chironomus tentans. Cell 1979, 17:835-848.
  • [58]Marcais G, Kingsford C: A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics 2011, 27:764-770.
  • [59]Smit AFA, Hubley R: RepeatModeler Open-1.0. 2008–2010 (http://www.repeatmasker.org webcite)
  • [60]Benson G: Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 1999, 27:573-580.
  • [61]Weizhong L, Godzik A: Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 2006, 22:1658-1659.
  • [62]Smit AFA, Hubley R, Green P: RepeatMasker Open-3.0. 1996–2010 (http://www.repeatmasker.org webcite)
  • [63]Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A: Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat Biotechnol 2011, 29:644-652.
  • [64]Stanke M, Diekhans M, Baertsch R, Haussler D: Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics 2008, 24:637-644.
  • [65]Stamatakis A: RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688-2690.
  • [66]Talavera G, Castresana J: Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 2007, 56:564-577.
  • [67]Galli J, Wieslander L: Two secretory protein genes in Chironomus tentans have arisen by gene duplication and exhibit different developmental expression patterns. J Mol Biol 1993, 231:324-334.
  • [68]Björk P, Wieslander L: Gene expression in polytene nuclei. Methods Mol Biol 2009, 464:29-54.
  文献评价指标  
  下载次数:33次 浏览次数:2次