期刊论文详细信息
BMC Genomics
Homopolymer tract organization in the human malarial parasite Plasmodium falciparum and related Apicomplexan parasites
Paul Horrocks7  Kenneth A Marx2  Karine Le Roch6  Richard D Emes1  Nadia Ponts4  Jeffrey W Bizzaro3  Chia-Ho Cheng5  Karen Russell7 
[1]Advanced Data Analysis Centre, University of Nottingham, Nottingham, UK
[2]Center for Intelligent Biomaterials, University of Massachusetts Lowell, Lowell, MA 01854, USA
[3]Bioinformatics Organization Inc, Hudson, MA 01749, USA
[4]National Institute for Agricultural Research (INRA), UR1264-Mycology and Food Safety (MycSA), CS20032, 33882 Villenave d’Ornon Cedex, France
[5]Currently at Institute for Aging Research, Hebrew SeniorLife, Boston, MA 02131, USA
[6]Department Cell Biology and Neuroscience, University of California, Riverside, CA 92521, USA
[7]Institute for Science and Technology in Medicine, Keele University, Stoke-on-Trent ST5 5BG, Staffordshire, UK
关键词: Gene expression;    Nucleosome;    Malaria;    Intergenic regions;    Poly dA.dT;   
Others  :  1139155
DOI  :  10.1186/1471-2164-15-848
 received in 2014-05-21, accepted in 2014-09-24,  发布年份 2014
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【 摘 要 】

Background

Homopolymeric tracts, particularly poly dA.dT, are enriched within the intergenic sequences of eukaryotic genomes where they appear to act as intrinsic regulators of nucleosome positioning. A previous study of the incomplete genome of the human malarial parasite Plasmodium falciparum reports a higher than expected enrichment of poly dA.dT tracts, far above that anticipated even in this highly AT rich genome. Here we report an analysis of the relative frequency, length and spatial arrangement of homopolymer tracts for the complete P. falciparum genome, extending this analysis to twelve additional genomes of Apicomplexan parasites important to human and animal health. In addition, using nucleosome-positioning data available for P. falciparum, we explore the correlation of poly dA.dT tracts with nucleosome-positioning data over key expression landmarks within intergenic regions.

Results

We describe three apparent lineage-specific patterns of homopolymeric tract organization within the intergenic regions of these Apicomplexan parasites. Moreover, a striking pattern of enrichment of overly long poly dA.dT tracts in the intergenic regions of Plasmodium spp. uniquely extends into protein coding sequences. There is a conserved spatial arrangement of poly dA.dT immediately flanking open reading frames and over predicted core promoter sites. These key landmarks are all relatively depleted in nucleosomes in P. falciparum, as would be expected for poly dA.dT acting as nucleosome exclusion sequences.

Conclusions

Previous comparative studies of homopolymer tract organization emphasize evolutionary diversity; this is the first report of such an analysis within a single phylum. Our data provide insights into the evolution of homopolymeric tracts and the selective pressures at play in their maintenance and expansion.

【 授权许可】

   
2014 Russell et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Dechering KJ, Cuelenaere K, Konings RN, Leunissen JA: Distinct frequency-distributions of homopolymeric DNA tracts in different genomes. Nucl Acids Res 1998, 26:4056-4062.
  • [2]Marx KA, Zhou Y, Kishawi IQ: Evidence for long poly(dA).poly(dT) tracts in D. discoideum DNA at high frequencies and their preferential avoidance of nucleosomal DNA core regions. J Biomol Struct Dyn 2006, 23:429-446.
  • [3]Zhou Y, Bizzaro JW, Marx KA: Homopolymer tract length dependent enrichments in functional regions of 27 eukaryotes and their novel dependence on the organism DNA (G + C)% composition. BMC Genomics 2004, 5:95-104. BioMed Central Full Text
  • [4]Field Y, Kaplan N, Fondufe-Mittendorf Y, Moore IK, Sharon E, Lubling Y, Widom J, Segal E: Distinct modes of regulation by chromatin encoded through nucleosome positioning signals. PLoS Comp Biol 2008, 4:e1000216.
  • [5]Mavrich TN, Ioshikhes IP, Venters BJ, Jiang C, Tomsho LP, Qi J, Schuster SC, Albert I, Pugh BF: A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome. Genome Res 2008, 18:1073-1083.
  • [6]Dai J, Chuang RY, Kelly TJ: DNA replication origins in the Schizosaccharomyces pombe genome. Proc Natl Acad Sci U S A 2005, 102:337-342.
  • [7]Segal E, Widom J: Poly(dA:dT) tracts: major determinants of nucleosome organization. Curr Opin Struct Biol 2009, 19:65-71.
  • [8]Cohanim AB, Haran TE: The coexistence of the nucleosome positioning code with the genetic code on eukaryotic genomes. Nucl Acids Res 2009, 37:6466-6476.
  • [9]Radman-Livaja M, Rando OJ: Nucleosome positioning: how is it established, and why does it matter? Dev Biol 2010, 339:258-266.
  • [10]Segal E, Widom J: What controls nucleosome positions? Trends Genet 2009, 25:335-343.
  • [11]Zhang Z, Wippo CJ, Wal M, Ward E, Korber P, Pugh BF: A packing mechanism for nucleosome organization reconstituted across a eukaryotic genome. Science 2011, 332:977-980.
  • [12]Polson HEJ, Blackman MJ: A role for poly (dA) poly(dT) tracts in directing activity of the Plasmodium falciparum calmodulin gene promoter. Mol Biochem Parasitol 2005, 141:179-189.
  • [13]Porter ME: Positive and negative effects of deletions and mutations within the 5’ flanking sequences of Plasmodium falciparum DNA polymerase delta. Mol Biochem Parasitol 2002, 122:9-19.
  • [14]Ponts N, Harris EY, Prudhomme J, Wick I, Eckhardt-Ludka C, Hicks GR, Hardiman G, Lonardi S, Le Roch KG: Nucleosome landscape and control of transcription in the human malaria parasite. Genome Res 2010, 20:228-238.
  • [15]Westenberger SJ, Cui L, Dharia N, Winzeler E, Cui L: Genome-wide nucleosome mapping of Plasmodium falciparum reveals histone-rich coding and histone-poor intergenic regions and chromatin remodeling of core and subtelomeric genes. BMC Genomics 2009, 10:610-621. BioMed Central Full Text
  • [16]Bunnik EM, Polishko A, Prudhomme J, Ponts N, Gill SS, Lonardi S, Le Roch KG: DNA-encoded nucleosome occupancy is associated with transcription levels in the human malaria parasite Plasmodium falciparum. BMC Genomics 2014, 15:347-353. BioMed Central Full Text
  • [17]Cui L, Miao J: Chromatin-mediated epigenetic regulation in the malaria parasite Plasmodium falciparum. Euk Cell 2010, 9:1138-1149.
  • [18]Duffy MF, Selvarajah SA, Josling GA, Petter M: The role of chromatin in Plasmodium gene expression. Cell Microbiol 2012, 14:819-828.
  • [19]Ay F, Bunnik EM, Varoquaux N, Bol SM, Prudhomme J, Vert JP, Noble WS, Le Roch KG: Three-dimensional modeling of the P. falciparum genome during the erythrocytic cycle reveals a strong connection between genome architecture and gene expression. Genome Res 2014, 24:974-988.
  • [20]Ponts N, Harris EY, Lonardi S, Le Roch KG: Nucleosome occupancy at transcription start sites in the human malaria parasite: a hard-wired evolution of virulence? Inf Gen Evol 2011, 11:716-724.
  • [21]Horrocks P, Wong E, Russell K, Emes RD: Control of gene expression in Plasmodium falciparum - ten years on. Mol Biochem Parasitol 2009, 164:9-25.
  • [22]Russell K, Hasenkamp S, Emes R, Horrocks P: Analysis of the spatial and temporal arrangement of transcripts over intergenic regions in the human malarial parasite Plasmodium falciparum. BMC Genomics 2013, 14:267-277. BioMed Central Full Text
  • [23]Siegel TN, Hon CC, Zhang Q, Lopez-Rubio JJ, Scheidig-Benatar C, Martins RM, Sismeiro O, Coppee JY, Scherf A: Strand-specific RNA-Seq reveals widespread and developmentally regulated transcription of natural antisense transcripts in Plasmodium falciparum. BMC Genomics 2014, 15:150-159. BioMed Central Full Text
  • [24]Abrahamsen MS, Templeton TJ, Enomoto S, Abrahante JE, Zhu G, Lancto CA, Deng M, Liu C, Widmer G, Tzipori S, Buck GA, Xu P, Bankier AT, Dear PH, Konfortov BA, Spriggs HF, Iyer L, Anantharaman V, Aravind L, Kapur V: Complete genome sequence of the apicomplexan Cryptosporidium parvum. Science 2004, 304:441-445.
  • [25]Brayton KA, Lau AO, Herndon DR, Hannick L, Kappmeyer LS, Berens SJ, Bidwell SL, Brown WC, Crabtree J, Fadrosh D, Feldblum T, Forberger HA, Haas BJ, Howell JM, Khouri H, Koo H, Mann DJ, Norimine J, Paulsen IT, Radune D, Ren Q, Smith RK Jr, Suarez CE, White O, Wortman JR, Knowles DP Jr, McElwain TF, Nene VM: Genome sequence of Babesia bovis and comparative analysis of apicomplexan hemoprotozoa. PLoS Path 2007, 3:1401-1413.
  • [26]Carlton JM, Adams JH, Silva JC, Bidwell SL, Lorenzi H, Caler E, Crabtree J, Angiuoli SV, Merino EF, Amedeo P, Cheng Q, Coulson RM, Crabb BS, Del Portillo HA, Essien K, Feldblyum TV, Fernandez-Becerra C, Gilson PR, Gueye AH, Guo X, Kang'a S, Kooij TW, Korsinczky M, Meyer EV, Nene V, Paulsen I, White O, Ralph SA, Ren Q, Sargeant TJ, et al.: Comparative genomics of the neglected human malaria parasite Plasmodium vivax. Nature 2008, 455:757-763.
  • [27]Carlton JM, Adams JH, Silva JC, Bidwell SL, Lorenzi H, Caler E, Crabtree J, Angiuoli SV, Merino EF, Amedeo P, Cheng Q, Coulson RM, Crabb BS, Del Portillo HA, Essien K, Feldblyum TV, Fernandez-Becerra C, Gilson PR, Gueye AH, Guo X, Kang'a S, Kooij TW, Korsinczky M, Meyer EV, Nene V, Paulsen I, White O, Ralph SA, Ren Q, Sargeant TJ, et al.: Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii. Nature 2002, 419:512-519.
  • [28]Gardner MJ, Bishop R, Shah T, de Villiers EP, Carlton JM, Hall N, Ren Q, Paulsen IT, Pain A, Berriman M, Wilson RJ, Sato S, Ralph SA, Mann DJ, Xiong Z, Shallom SJ, Weidman J, Jiang L, Lynn J, Weaver B, Shoaibi A, Domingo AR, Wasawo D, Crabtree J, Wortman JR, Haas B, Angiuoli SV, Creasy TH, Lu C, Suh B, et al.: Genome sequence of Theileria parva, a bovine pathogen that transforms lymphocytes. Science 2005, 309:134-137.
  • [29]Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, Paulsen IT, James K, Eisen JA, Rutherford K, Salzberg SL, Craig A, Kyes S, Chan MS, Nene V, Shallom SJ, Suh B, Peterson J, Angiuoli S, Pertea M, Allen J, Selengut J, Haft D, Mather MW, Vaidya AB, Martin DM, et al.: Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 2002, 419:498-511.
  • [30]Pain A, Bohme U, Berry AE, Mungall K, Finn RD, Jackson AP, Mourier T, Mistry J, Pasini EM, Aslett MA, Balasubrammaniam S, Borgwardt K, Brooks K, Carret C, Carver TJ, Cherevach I, Chillingworth T, Clark TG, Galinski MR, Hall N, Harper D, Harris D, Hauser H, Ivens A, Janssen CS, Keane T, Larke N, Lapp S, Marti M, Moule S, et al.: The genome of the simian and human malaria parasite Plasmodium knowlesi. Nature 2008, 455:799-803.
  • [31]Pain A, Böhme U, Berry AE, Mungall K, Finn RD, Jackson AP, Mourier T, Mistry J, Pasini EM, Aslett MA, Balasubrammaniam S, Borgwardt K, Brooks K, Carret C, Carver TJ, Cherevach I, Chillingworth T, Clark TG, Galinski MR, Hall N, Harper D, Harris D, Hauser H, Ivens A, Janssen CS, Keane T, Larke N, Lapp S, Marti M, Moule S, et al.: Genome of the host-cell transforming parasite Theileria annulata compared with T. parva. Science 2005, 309:131-133.
  • [32]Reid AJ, Vermont SJ, Cotton JA, Harris D, Hill-Cawthorne GA, Könen-Waisman S, Latham SM, Mourier T, Norton R, Quail MA, Sanders M, Shanmugam D, Sohal A, Wasmuth JD, Brunk B, Grigg ME, Howard JC, Parkinson J, Roos DS, Trees AJ, Berriman M, Pain A, Wastling JM: Comparative genomics of the apicomplexan parasites Toxoplasma gondii and Neospora caninum: Coccidia differing in host range and transmission strategy. PLoS Path 2012, 8:e1002567.
  • [33]Xu P, Widmer G, Wang Y, Ozaki LS, Alves JM, Serrano MG, Puiu D, Manque P, Akiyoshi D, Mackey AJ, Pearson WR, Dear PH, Bankier AT, Peterson DL, Abrahamsen MS, Kapur V, Tzipori S, Buck GA: The genome of Cryptosporidium hominis. Nature 2004, 431:1107-1112.
  • [34]Bizzaro JW, Marx KA: Poly: a quantitative analysis tool for simple sequence repeat (SSR) tracts in DNA. BMC Bioinformatics 2003, 4:22-25. BioMed Central Full Text
  • [35]Brick K, Watanabe J, Pizzi E: Core promoters are predicted by their distinct physicochemical properties in the genome of Plasmodium falciparum. Genome Biol 2008, 9(12):178-184. BioMed Central Full Text
  • [36]Denver DR, Morris K, Kewalramani A, Harris KE, Chow A, Estes S, Lynch M, Thomas WK: Abundance, distribution, and mutation rates of homopolymeric nucleotide runs in the genome of Caenorhabditis elegans. J Mol Evol 2004, 58:584-595.
  • [37]Katti MV, Ranjekar PK, Gupta VS: Differential distribution of simple sequence repeats in eukaryotic genome sequences. Mol Biol Evol 2001, 18:1161-1167.
  • [38]Toth G, Gaspari Z, Jurka J: Microsatellites in different eukaryotic genomes: survey and analysis. Genome Res 2000, 10:967-981.
  • [39]Hancock JM: The contribution of slippage-like processes to genome evolution. J Mol Evol 1995, 41:1038-1047.
  • [40]Nadir E, Margalit H, Gallily T, Ben-Sasson SA: Microsatellite spreading in the human genome: evolutionary mechanisms and structural implications. Proc Natl Acad Sci U S A 1996, 93:6470-6475.
  • [41]Tautz D, Trick M, Dover GA: Cryptic simplicity in DNA is a major source of genetic variation. Nature 1986, 322:652-656.
  • [42]Wilder J, Hollocher H: Mobile elements and the genesis of microsatellites in dipterans. Mol Biol Evol 2001, 18:384-392.
  • [43]DeBarry JD, Kissinger JC: Jumbled genomes: missing Apicomplexan synteny. Mol Biol Evol 2011, 28:2855-2871.
  • [44]Durand PM, Oelofse AJ, Coetzer TL: An analysis of mobile genetic elements in three Plasmodium species and their potential impact on the nucleotide composition of the P. falciparum genome. BMC Genomics 2006, 7:282-287. BioMed Central Full Text
  • [45]Roy SW, Hartl DL: Very little intron loss/gain in Plasmodium: intron loss/gain mutation rates and intron number. Genome Res 2006, 16:750-756.
  • [46]Roy SW, Penny D: Large-scale intron conservation and order-of-magnitude variation in intron loss/gain rates in apicomplexan evolution. Genome Res 2006, 16:1270-1275.
  • [47]Chang GS, Noegel AA, Mavrich TN, Müller R, Tomsho L, Ward E, Felder M, Jiang C, Eichinger L, Glockner G, Glöckner G, Schuster SC, Pugh BF: Unusual combinatorial involvement of poly-A/T tracts in organizing genes and chromatin in Dictyostelium. Genome Res 2012, 22:1098-1106.
  • [48]Sims JS, Militello KT, Sims PA, Patel VP, Kasper JM, Wirth DF: Patterns of gene-specific and total transcriptional activity during the Plasmodium falciparum intraerythrocytic developmental cycle. Euk Cell 2009, 8(3):327-338.
  • [49]Gopalakrishnan AM, Nyindodo LA, Ross Fergus M, Lopez-Estrano C: Plasmodium falciparum: preinitiation complex occupancy of active and inactive promoters during erythrocytic stage. Exp Parasitol 2009, 121:46-54.
  • [50]Kishore SP, Perkins SL, Templeton TJ, Deitsch KW: An unusual recent expansion of the C-terminal domain of RNA polymerase II in primate malaria parasites features a motif otherwise found only in mammalian polymerases. J Mol Evol 2009, 68:706-714.
  • [51]Bartfai R, Hoeijmakers WA, Salcedo-Amaya AM, Smits AH, Janssen-Megens E, Kaan A, Treeck M, Gilberger TW, Francoijs KJ, Stunnenberg HG: H2A.Z demarcates intergenic regions of the Plasmodium falciparum epigenome that are dynamically marked by H3K9ac and H3K4me3. PLoS Path 2010, 6(12):e1001223.
  • [52]Depledge DP, Lower RP, Smith DF: RepSeq-a database of amino acid repeats present in lower eukaryotic pathogens. BMC Bioinformatics 2007, 8:122-127. BioMed Central Full Text
  • [53]Frugier M, Bour T, Ayach M, Santos MA, Rudinger-Thirion J, Theobald-Dietrich A, Pizzi E: Low Complexity Regions behave as tRNA sponges to help co-translational folding of plasmodial proteins. FEBS Lett 2010, 584:448-454.
  • [54]Pizzi E, Frontali C: Divergence of noncoding sequences and of insertions encoding nonglobular domains at a genomic region well conserved in plasmodia. J Mol Evol 2000, 50:474-480.
  • [55]Pizzi E, Frontali C: Low-complexity regions in Plasmodium falciparum proteins. Genome Res 2001, 11:218-229.
  • [56]Zilversmit MM, Volkman SK, DePristo MA, Wirth DF, Awadalla P, Hartl DL: Low-complexity regions in Plasmodium falciparum: missing links in the evolution of an extreme genome. Mol Biol Evol 2010, 27:2198-2209.
  • [57]Carter R, Nijhout MM: Control of gamete formation (exflagellation) in malaria parasites. Science 1977, 195:407-409.
  • [58]Janse CJ, van der Klooster PF, van der Kaay HJ, van der Ploeg M, Overdulve JP: DNA synthesis in Plasmodium berghei during asexual and sexual development. Mol Biochem Parasitol 1986, 20:173-182.
  • [59]Janse CJ, Van der Klooster PF, Van der Kaay HJ, Van der Ploeg M, Overdulve JP: Rapid repeated DNA replication during microgametogenesis and DNA synthesis in young zygotes of Plasmodium berghei. Trans Roy Soc Trop Med Hyg 1986, 80:154-157.
  • [60]Schmitt MW, Venkatesan RN, Pillaire MJ, Hoffmann JS, Sidorova JM, Loeb LA: Active site mutations in mammalian DNA polymerase delta alter accuracy and replication fork progression. J Biol Chem 2010, 285:32264-32272.
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