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Natl. Acad. Sci. U.S.A."],"published-print":{"date-parts":[[2019,2,19]]},"abstract":"<jats:p>\n                    The positioning of chromosomes in the nucleus of a eukaryotic cell is highly organized and has a complex and dynamic relationship with gene expression. In the human malaria parasite\n                    <jats:italic>Plasmodium falciparum<\/jats:italic>\n                    , the clustering of a family of virulence genes correlates with their coordinated silencing and has a strong influence on the overall organization of the genome. To identify conserved and species-specific principles of genome organization, we performed Hi-C experiments and generated 3D genome models for five\n                    <jats:italic>Plasmodium<\/jats:italic>\n                    species and two related apicomplexan parasites.\n                    <jats:italic>Plasmodium<\/jats:italic>\n                    species mainly showed clustering of centromeres, telomeres, and virulence genes. In\n                    <jats:italic>P. falciparum<\/jats:italic>\n                    , the heterochromatic virulence gene cluster had a strong repressive effect on the surrounding nuclear space, while this was less pronounced in\n                    <jats:italic>Plasmodium vivax<\/jats:italic>\n                    and\n                    <jats:italic>Plasmodium berghei<\/jats:italic>\n                    , and absent in\n                    <jats:italic>Plasmodium yoelii<\/jats:italic>\n                    . In\n                    <jats:italic>Plasmodium knowlesi<\/jats:italic>\n                    , telomeres and virulence genes were more dispersed throughout the nucleus, but its 3D genome showed a strong correlation with gene expression. The\n                    <jats:italic>Babesia microti<\/jats:italic>\n                    genome showed a classical Rabl organization with colocalization of subtelomeric virulence genes, while the\n                    <jats:italic>Toxoplasma gondii<\/jats:italic>\n                    genome was dominated by clustering of the centromeres and lacked virulence gene clustering. Collectively, our results demonstrate that spatial genome organization in most\n                    <jats:italic>Plasmodium<\/jats:italic>\n                    species is constrained by the colocalization of virulence genes.\n                    <jats:italic>P. falciparum<\/jats:italic>\n                    and\n                    <jats:italic>P. knowlesi<\/jats:italic>\n                    , the only two\n                    <jats:italic>Plasmodium<\/jats:italic>\n                    species with gene families involved in antigenic variation, are unique in the effect of these genes on chromosome folding, indicating a potential link between genome organization and gene expression in more virulent pathogens.\n                  <\/jats:p>","DOI":"10.1073\/pnas.1810815116","type":"journal-article","created":{"date-parts":[[2019,2,5]],"date-time":"2019-02-05T16:26:54Z","timestamp":1549384014000},"page":"3183-3192","update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":103,"title":["Comparative 3D genome organization in apicomplexan parasites"],"prefix":"10.1073","volume":"116","author":[{"given":"Evelien M.","family":"Bunnik","sequence":"first","affiliation":[{"name":"Department of Microbiology, Immunology &amp; Molecular Genetics, The University of Texas Health Science Center at San Antonio, San Antonio, TX 78229;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0298-0172","authenticated-orcid":false,"given":"Aarthi","family":"Venkat","sequence":"additional","affiliation":[{"name":"Division of Vaccine Discovery, La Jolla Institute for Immunology, La Jolla, CA 92037;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jianlin","family":"Shao","sequence":"additional","affiliation":[{"name":"Division of Vaccine Discovery, La Jolla Institute for Immunology, La Jolla, CA 92037;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kathryn E.","family":"McGovern","sequence":"additional","affiliation":[{"name":"Division of Biomedical Sciences, School of Medicine, University of California, Riverside, CA 92521;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gayani","family":"Batugedara","sequence":"additional","affiliation":[{"name":"Department of Molecular, Cell and Systems Biology, University of California, Riverside, CA 92521;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Danielle","family":"Worth","sequence":"additional","affiliation":[{"name":"Division of Biomedical Sciences, School of Medicine, University of California, Riverside, CA 92521;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jacques","family":"Prudhomme","sequence":"additional","affiliation":[{"name":"Department of Molecular, Cell and Systems Biology, University of California, Riverside, CA 92521;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stacey A.","family":"Lapp","sequence":"additional","affiliation":[{"name":"International Center for Malaria Research, Education and Development, Emory Vaccine Center, Yerkes National Primate Research Center, Emory University, Atlanta, GA 30329;"},{"name":"Division of Infectious Diseases, Department of Medicine, Emory University, Atlanta, GA 30329;"},{"name":"Malaria Host-Pathogen Interaction Center, Emory University, Atlanta, GA 30329;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chiara","family":"Andolina","sequence":"additional","affiliation":[{"name":"Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine Research Building, University of Oxford, Oxford OX3 7FZ, United Kingdom;"},{"name":"Shoklo Malaria Research Unit, Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Mae Sot, 63110 Tak, Thailand;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Leila S.","family":"Ross","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, Columbia University Medical Center, New York, NY 10032;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lauren","family":"Lawres","sequence":"additional","affiliation":[{"name":"Department of Internal Medicine, Section of Infectious Diseases, Yale School of Medicine, New Haven, CT 06520;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Declan","family":"Brady","sequence":"additional","affiliation":[{"name":"School of Life Sciences, Queens Medical Centre, University of Nottingham, Nottingham NG7 2UH, United 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Columbia University Medical Center, New York, NY 10032;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emma H.","family":"Wilson","sequence":"additional","affiliation":[{"name":"Division of Biomedical Sciences, School of Medicine, University of California, Riverside, CA 92521;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rita","family":"Tewari","sequence":"additional","affiliation":[{"name":"School of Life Sciences, Queens Medical Centre, University of Nottingham, Nottingham NG7 2UH, United Kingdom;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mary R.","family":"Galinski","sequence":"additional","affiliation":[{"name":"International Center for Malaria Research, Education and Development, Emory Vaccine Center, Yerkes National Primate Research Center, Emory University, Atlanta, GA 30329;"},{"name":"Division of Infectious Diseases, Department of Medicine, Emory University, Atlanta, GA 30329;"},{"name":"Malaria Host-Pathogen 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Syst Biol 56, 684\u2013689 (2007).","journal-title":"Syst Biol"},{"key":"e_1_3_4_2_2","unstructured":"; WHO World malaria report 2017. Available at https:\/\/www.who.int\/malaria\/publications\/world-malaria-report-2017\/en\/. Accessed March 15 2018. (2017)."},{"key":"e_1_3_4_3_2","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1086\/524888","article-title":"Plasmodium knowlesi malaria in humans is widely distributed and potentially life threatening","volume":"46","author":"Cox-Singh J","year":"2008","unstructured":"J Cox-Singh, , Plasmodium knowlesi malaria in humans is widely distributed and potentially life threatening. Clin Infect Dis 46, 165\u2013171 (2008).","journal-title":"Clin Infect Dis"},{"key":"e_1_3_4_4_2","doi-asserted-by":"crossref","first-page":"627","DOI":"10.20506\/rst.34.2.2385","article-title":"Babesiosis","volume":"34","author":"Beugnet F","year":"2015","unstructured":"F Beugnet, Y Moreau, Babesiosis. 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PLoS One 9, e90203 (2014).","journal-title":"PLoS One"},{"key":"e_1_3_4_6_2","doi-asserted-by":"crossref","first-page":"S57","DOI":"10.1017\/S0031182014001528","article-title":"Large, rapidly evolving gene families are at the forefront of host-parasite interactions in Apicomplexa","volume":"142","author":"Reid AJ","year":"2015","unstructured":"AJ Reid, Large, rapidly evolving gene families are at the forefront of host-parasite interactions in Apicomplexa. Parasitology 142, S57\u2013S70 (2015).","journal-title":"Parasitology"},{"key":"e_1_3_4_7_2","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1017\/S0031182017001135","article-title":"Plasmodium knowlesi: A superb in vivo nonhuman primate model of antigenic variation in malaria","volume":"145","author":"Galinski MR","year":"2018","unstructured":"MR Galinski, , Plasmodium knowlesi: A superb in vivo nonhuman primate model of antigenic variation in malaria. Parasitology; MAHPIC CONSORTIUM 145, 85\u2013100 (2018).","journal-title":"Parasitology"},{"key":"e_1_3_4_8_2","doi-asserted-by":"crossref","first-page":"625","DOI":"10.1146\/annurev-micro-090816-093841","article-title":"Variant gene expression and antigenic variation by malaria parasites","volume":"71","author":"Deitsch KW","year":"2017","unstructured":"KW Deitsch, R Dzikowski, Variant gene expression and antigenic variation by malaria parasites. Annu Rev Microbiol 71, 625\u2013641 (2017).","journal-title":"Annu Rev Microbiol"},{"key":"e_1_3_4_9_2","doi-asserted-by":"crossref","first-page":"16276","DOI":"10.1038\/nmicrobiol.2016.276","article-title":"Antibody-independent mechanisms regulate the establishment of chronic Plasmodium infection","volume":"2","author":"Brugat T","year":"2017","unstructured":"T Brugat, , Antibody-independent mechanisms regulate the establishment of chronic Plasmodium infection. Nat Microbiol 2, 16276 (2017).","journal-title":"Nat Microbiol"},{"key":"e_1_3_4_10_2","doi-asserted-by":"crossref","first-page":"23449","DOI":"10.1038\/srep23449","article-title":"Characterization of the Plasmodium Interspersed Repeats (PIR) proteins of Plasmodium chabaudi indicates functional diversity","volume":"6","author":"Yam XY","year":"2016","unstructured":"XY Yam, , Characterization of the Plasmodium Interspersed Repeats (PIR) proteins of Plasmodium chabaudi indicates functional diversity. Sci Rep 6, 23449 (2016).","journal-title":"Sci Rep"},{"key":"e_1_3_4_11_2","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1016\/j.molbiopara.2009.12.010","article-title":"The pir multigene family of Plasmodium: Antigenic variation and beyond","volume":"170","author":"Cunningham D","year":"2010","unstructured":"D Cunningham, J Lawton, W Jarra, P Preiser, J Langhorne, The pir multigene family of Plasmodium: Antigenic variation and beyond. Mol Biochem Parasitol 170, 65\u201373 (2010).","journal-title":"Mol Biochem Parasitol"},{"key":"e_1_3_4_12_2","doi-asserted-by":"crossref","first-page":"498","DOI":"10.1038\/nature01097","article-title":"Genome sequence of the human malaria parasite Plasmodium falciparum","volume":"419","author":"Gardner MJ","year":"2002","unstructured":"MJ Gardner, , Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419, 498\u2013511 (2002).","journal-title":"Nature"},{"key":"e_1_3_4_13_2","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1186\/s12915-014-0086-0","article-title":"A comprehensive evaluation of rodent malaria parasite genomes and gene expression","volume":"12","author":"Otto TD","year":"2014","unstructured":"TD Otto, , A comprehensive evaluation of rodent malaria parasite genomes and gene expression. BMC Biol 12, 86 (2014).","journal-title":"BMC Biol"},{"key":"e_1_3_4_14_2","doi-asserted-by":"crossref","first-page":"757","DOI":"10.1038\/nature07327","article-title":"Comparative genomics of the neglected human malaria parasite Plasmodium vivax","volume":"455","author":"Carlton JM","year":"2008","unstructured":"JM Carlton, , Comparative genomics of the neglected human malaria parasite Plasmodium vivax. Nature 455, 757\u2013763 (2008).","journal-title":"Nature"},{"key":"e_1_3_4_15_2","doi-asserted-by":"crossref","first-page":"2783","DOI":"10.1128\/IAI.68.5.2783-2790.2000","article-title":"Serological expression cloning of novel immunoreactive antigens of Babesia microti","volume":"68","author":"Lodes MJ","year":"2000","unstructured":"MJ Lodes, , Serological expression cloning of novel immunoreactive antigens of Babesia microti. Infect Immun 68, 2783\u20132790 (2000).","journal-title":"Infect Immun"},{"key":"e_1_3_4_16_2","doi-asserted-by":"crossref","first-page":"e72657","DOI":"10.1371\/journal.pone.0072657","article-title":"Whole genome mapping and re-organization of the nuclear and mitochondrial genomes of Babesia microti isolates","volume":"8","author":"Cornillot E","year":"2013","unstructured":"E Cornillot, , Whole genome mapping and re-organization of the nuclear and mitochondrial genomes of Babesia microti isolates. PLoS One 8, e72657 (2013).","journal-title":"PLoS One"},{"key":"e_1_3_4_17_2","doi-asserted-by":"crossref","first-page":"35284","DOI":"10.1038\/srep35284","article-title":"Genome-wide diversity and gene expression profiling of Babesia microti isolates identify polymorphic genes that mediate host-pathogen interactions","volume":"6","author":"Silva JC","year":"2016","unstructured":"JC Silva, , Genome-wide diversity and gene expression profiling of Babesia microti isolates identify polymorphic genes that mediate host-pathogen interactions. Sci Rep 6, 35284 (2016).","journal-title":"Sci Rep"},{"key":"e_1_3_4_18_2","doi-asserted-by":"crossref","first-page":"10147","DOI":"10.1038\/ncomms10147","article-title":"Local admixture of amplified and diversified secreted pathogenesis determinants shapes mosaic Toxoplasma gondii genomes","volume":"7","author":"Lorenzi H","year":"2016","unstructured":"H Lorenzi, , Local admixture of amplified and diversified secreted pathogenesis determinants shapes mosaic Toxoplasma gondii genomes. Nat Commun 7, 10147 (2016).","journal-title":"Nat Commun"},{"key":"e_1_3_4_19_2","doi-asserted-by":"crossref","first-page":"1285","DOI":"10.1016\/S0020-7519(01)00261-2","article-title":"Surface antigens of Toxoplasma gondii: Variations on a theme","volume":"31","author":"Lekutis C","year":"2001","unstructured":"C Lekutis, DJ Ferguson, ME Grigg, M Camps, JC Boothroyd, Surface antigens of Toxoplasma gondii: Variations on a theme. Int J Parasitol 31, 1285\u20131292 (2001).","journal-title":"Int J Parasitol"},{"key":"e_1_3_4_20_2","doi-asserted-by":"crossref","first-page":"4129","DOI":"10.1073\/pnas.80.13.4129","article-title":"Antigenic variation of Plasmodium knowlesi malaria: Identification of the variant antigen on infected erythrocytes","volume":"80","author":"Howard RJ","year":"1983","unstructured":"RJ Howard, JW Barnwell, V Kao, Antigenic variation of Plasmodium knowlesi malaria: Identification of the variant antigen on infected erythrocytes. Proc Natl Acad Sci USA 80, 4129\u20134133 (1983).","journal-title":"Proc Natl Acad Sci USA"},{"key":"e_1_3_4_21_2","doi-asserted-by":"crossref","first-page":"857","DOI":"10.1084\/jem.67.6.857","article-title":"The agglutination of Plasmodium knowlesi by immune serum","volume":"67","author":"Eaton MD","year":"1938","unstructured":"MD Eaton, The agglutination of Plasmodium knowlesi by immune serum. J Exp Med 67, 857\u2013870 (1938).","journal-title":"J Exp Med"},{"key":"e_1_3_4_22_2","doi-asserted-by":"crossref","first-page":"1286","DOI":"10.1038\/2081286a0","article-title":"Immunity to malaria: Antigenic variation in chronic infections of Plasmodium knowlesi","volume":"208","author":"Brown KN","year":"1965","unstructured":"KN Brown, IN Brown, Immunity to malaria: Antigenic variation in chronic infections of Plasmodium knowlesi. Nature 208, 1286\u20131288 (1965).","journal-title":"Nature"},{"key":"e_1_3_4_23_2","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1016\/S1097-2765(00)80304-4","article-title":"Antigenic variation in malaria: A 3\u2032 genomic alteration associated with the expression of a P. knowlesi variant antigen","volume":"3","author":"al-Khedery B","year":"1999","unstructured":"B al-Khedery, JW Barnwell, MR Galinski, Antigenic variation in malaria: A 3\u2032 genomic alteration associated with the expression of a P. knowlesi variant antigen. Mol Cell 3, 131\u2013141 (1999).","journal-title":"Mol Cell"},{"key":"e_1_3_4_24_2","doi-asserted-by":"crossref","first-page":"e78014","DOI":"10.1371\/journal.pone.0078014","article-title":"Spleen-dependent regulation of antigenic variation in malaria parasites: Plasmodium knowlesi SICAvar expression profiles in splenic and asplenic hosts","volume":"8","author":"Lapp SA","year":"2013","unstructured":"SA Lapp, , Spleen-dependent regulation of antigenic variation in malaria parasites: Plasmodium knowlesi SICAvar expression profiles in splenic and asplenic hosts. PLoS One 8, e78014 (2013).","journal-title":"PLoS One"},{"key":"e_1_3_4_25_2","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1038\/28660","article-title":"Developmental selection of var gene expression in Plasmodium falciparum","volume":"394","author":"Chen Q","year":"1998","unstructured":"Q Chen, , Developmental selection of var gene expression in Plasmodium falciparum. Nature 394, 392\u2013395 (1998).","journal-title":"Nature"},{"key":"e_1_3_4_26_2","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1016\/0035-9203(74)90187-4","article-title":"Antigenic variation and immunity to Plasmodium knowlesi: Antibodies which induce antigenic variation and antibodies which destroy parasites","volume":"68","author":"Brown KN","year":"1974","unstructured":"KN Brown, LA Hills, Antigenic variation and immunity to Plasmodium knowlesi: Antibodies which induce antigenic variation and antibodies which destroy parasites. Trans R Soc Trop Med Hyg 68, 139\u2013142 (1974).","journal-title":"Trans R Soc Trop Med Hyg"},{"key":"e_1_3_4_27_2","doi-asserted-by":"crossref","first-page":"e2012061","DOI":"10.4084\/mjhid.2012.061","article-title":"Pathogenesis of malaria in tissues and blood","volume":"4","author":"Autino B","year":"2012","unstructured":"B Autino, Y Corbett, F Castelli, D Taramelli, Pathogenesis of malaria in tissues and blood. Mediterr J Hematol Infect Dis 4, e2012061 (2012).","journal-title":"Mediterr J Hematol Infect Dis"},{"key":"e_1_3_4_28_2","doi-asserted-by":"crossref","first-page":"1018","DOI":"10.1038\/35039531","article-title":"Frequent ectopic recombination of virulence factor genes in telomeric chromosome clusters of P. falciparum","volume":"407","author":"Freitas-Junior LH","year":"2000","unstructured":"LH Freitas-Junior, , Frequent ectopic recombination of virulence factor genes in telomeric chromosome clusters of P. falciparum. 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Cell Host Microbe 5, 179\u2013190 (2009).","journal-title":"Cell Host Microbe"},{"key":"e_1_3_4_30_2","doi-asserted-by":"crossref","first-page":"974","DOI":"10.1101\/gr.169417.113","article-title":"Three-dimensional modeling of the P. falciparum genome during the erythrocytic cycle reveals a strong connection between genome architecture and gene expression","volume":"24","author":"Ay F","year":"2014","unstructured":"F Ay, , Three-dimensional modeling of the P. falciparum genome during the erythrocytic cycle reveals a strong connection between genome architecture and gene expression. 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Cell 159, 1665\u20131680 (2014).","journal-title":"Cell"},{"key":"e_1_3_4_33_2","doi-asserted-by":"crossref","first-page":"2701","DOI":"10.1093\/bioinformatics\/bty164","article-title":"GenomeDISCO: A concordance score for chromosome conformation capture experiments using random walks on contact map graphs","volume":"34","author":"Ursu O","year":"2018","unstructured":"O Ursu, , GenomeDISCO: A concordance score for chromosome conformation capture experiments using random walks on contact map graphs. Bioinformatics 34, 2701\u20132707 (2018).","journal-title":"Bioinformatics"},{"key":"e_1_3_4_34_2","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1186\/s13059-015-0831-x","article-title":"HiC-Pro: An optimized and flexible pipeline for Hi-C data processing","volume":"16","author":"Servant N","year":"2015","unstructured":"N Servant, , HiC-Pro: An optimized and flexible pipeline for Hi-C data processing. Genome Biol 16, 259 (2015).","journal-title":"Genome Biol"},{"key":"e_1_3_4_35_2","doi-asserted-by":"crossref","first-page":"999","DOI":"10.1038\/nmeth.2148","article-title":"Iterative correction of Hi-C data reveals hallmarks of chromosome organization","volume":"9","author":"Imakaev M","year":"2012","unstructured":"M Imakaev, , Iterative correction of Hi-C data reveals hallmarks of chromosome organization. Nat Methods 9, 999\u20131003 (2012).","journal-title":"Nat Methods"},{"key":"e_1_3_4_36_2","doi-asserted-by":"crossref","first-page":"i26","DOI":"10.1093\/bioinformatics\/btu268","article-title":"A statistical approach for inferring the 3D structure of the genome","volume":"30","author":"Varoquaux N","year":"2014","unstructured":"N Varoquaux, F Ay, WS Noble, JP Vert, A statistical approach for inferring the 3D structure of the genome. Bioinformatics 30, i26\u2013i33 (2014).","journal-title":"Bioinformatics"},{"key":"e_1_3_4_37_2","doi-asserted-by":"crossref","first-page":"999","DOI":"10.1101\/gr.160374.113","article-title":"Statistical confidence estimation for Hi-C data reveals regulatory chromatin contacts","volume":"24","author":"Ay F","year":"2014","unstructured":"F Ay, TL Bailey, WS Noble, Statistical confidence estimation for Hi-C data reveals regulatory chromatin contacts. Genome Res 24, 999\u20131011 (2014).","journal-title":"Genome Res"},{"key":"e_1_3_4_38_2","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1126\/science.aal3327","article-title":"De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds","volume":"356","author":"Dudchenko O","year":"2017","unstructured":"O Dudchenko, , De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. Science 356, 92\u201395 (2017).","journal-title":"Science"},{"key":"e_1_3_4_39_2","doi-asserted-by":"crossref","first-page":"778","DOI":"10.1101\/gr.213652.116","article-title":"Improving and correcting the contiguity of long-read genome assemblies of three plant species using optical mapping and chromosome conformation capture data","volume":"27","author":"Jiao WB","year":"2017","unstructured":"WB Jiao, , Improving and correcting the contiguity of long-read genome assemblies of three plant species using optical mapping and chromosome conformation capture data. Genome Res 27, 778\u2013786 (2017).","journal-title":"Genome Res"},{"key":"e_1_3_4_40_2","doi-asserted-by":"crossref","first-page":"1143","DOI":"10.1038\/nbt.2768","article-title":"High-throughput genome scaffolding from in vivo DNA interaction frequency","volume":"31","author":"Kaplan N","year":"2013","unstructured":"N Kaplan, J Dekker, High-throughput genome scaffolding from in vivo DNA interaction frequency. Nat Biotechnol 31, 1143\u20131147 (2013).","journal-title":"Nat Biotechnol"},{"key":"e_1_3_4_41_2","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1017\/S0031182017001329","article-title":"PacBio assembly of a Plasmodium knowlesi genome sequence with Hi-C correction and manual annotation of the SICAvar gene family","volume":"145","author":"Lapp SA","year":"2018","unstructured":"SA Lapp, , PacBio assembly of a Plasmodium knowlesi genome sequence with Hi-C correction and manual annotation of the SICAvar gene family. Parasitology; MaHPIC consortium 145, 71\u201384 (2018).","journal-title":"Parasitology"},{"key":"e_1_3_4_42_2","doi-asserted-by":"crossref","first-page":"3767","DOI":"10.1073\/pnas.1006741108","article-title":"Toxoplasma gondii sequesters centromeres to a specific nuclear region throughout the cell cycle","volume":"108","author":"Brooks CF","year":"2011","unstructured":"CF Brooks, , Toxoplasma gondii sequesters centromeres to a specific nuclear region throughout the cell cycle. Proc Natl Acad Sci USA 108, 3767\u20133772 (2011).","journal-title":"Proc Natl Acad Sci USA"},{"key":"e_1_3_4_43_2","doi-asserted-by":"crossref","first-page":"e32671","DOI":"10.1371\/journal.pone.0032671","article-title":"Toxoplasma gondii chromodomain protein 1 binds to heterochromatin and colocalises with centromeres and telomeres at the nuclear periphery","volume":"7","author":"Gissot M","year":"2012","unstructured":"M Gissot, , Toxoplasma gondii chromodomain protein 1 binds to heterochromatin and colocalises with centromeres and telomeres at the nuclear periphery. PLoS One 7, e32671 (2012).","journal-title":"PLoS One"},{"key":"e_1_3_4_44_2","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1038\/nature08973","article-title":"A three-dimensional model of the yeast genome","volume":"465","author":"Duan Z","year":"2010","unstructured":"Z Duan, , A three-dimensional model of the yeast genome. Nature 465, 363\u2013367 (2010).","journal-title":"Nature"},{"key":"e_1_3_4_45_2","doi-asserted-by":"crossref","first-page":"8164","DOI":"10.1093\/nar\/gkq955","article-title":"Mapping of long-range associations throughout the fission yeast genome reveals global genome organization linked to transcriptional regulation","volume":"38","author":"Tanizawa H","year":"2010","unstructured":"H Tanizawa, , Mapping of long-range associations throughout the fission yeast genome reveals global genome organization linked to transcriptional regulation. Nucleic Acids Res 38, 8164\u20138177 (2010).","journal-title":"Nucleic Acids Res"},{"key":"e_1_3_4_46_2","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1038\/nature21429","article-title":"3D structures of individual mammalian genomes studied by single-cell Hi-C","volume":"544","author":"Stevens TJ","year":"2017","unstructured":"TJ Stevens, , 3D structures of individual mammalian genomes studied by single-cell Hi-C. Nature 544, 59\u201364 (2017).","journal-title":"Nature"},{"key":"e_1_3_4_47_2","doi-asserted-by":"crossref","first-page":"3849","DOI":"10.1093\/nar\/gks012","article-title":"On the assessment of statistical significance of three-dimensional colocalization of sets of genomic elements","volume":"40","author":"Witten DM","year":"2012","unstructured":"DM Witten, WS Noble, On the assessment of statistical significance of three-dimensional colocalization of sets of genomic elements. Nucleic Acids Res 40, 3849\u20133855 (2012).","journal-title":"Nucleic Acids Res"},{"key":"e_1_3_4_48_2","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1126\/science.1181369","article-title":"Comprehensive mapping of long-range interactions reveals folding principles of the human genome","volume":"326","author":"Lieberman-Aiden E","year":"2009","unstructured":"E Lieberman-Aiden, , Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326, 289\u2013293 (2009).","journal-title":"Science"},{"key":"e_1_3_4_49_2","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1007\/s10577-010-9177-0","article-title":"The fractal globule as a model of chromatin architecture in the cell","volume":"19","author":"Mirny LA","year":"2011","unstructured":"LA Mirny, The fractal globule as a model of chromatin architecture in the cell. Chromosome Res 19, 37\u201351 (2011).","journal-title":"Chromosome Res"},{"key":"e_1_3_4_50_2","doi-asserted-by":"crossref","first-page":"E3061","DOI":"10.1073\/pnas.1612256114","article-title":"Form and function of topologically associating genomic domains in budding yeast","volume":"114","author":"Eser U","year":"2017","unstructured":"U Eser, , Form and function of topologically associating genomic domains in budding yeast. Proc Natl Acad Sci USA 114, E3061\u2013E3070 (2017).","journal-title":"Proc Natl Acad Sci USA"},{"key":"e_1_3_4_51_2","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1186\/s12864-015-1225-x","article-title":"Asexual expansion of Toxoplasma gondii merozoites is distinct from tachyzoites and entails expression of non-overlapping gene families to attach, invade, and replicate within feline enterocytes","volume":"16","author":"Hehl AB","year":"2015","unstructured":"AB Hehl, , Asexual expansion of Toxoplasma gondii merozoites is distinct from tachyzoites and entails expression of non-overlapping gene families to attach, invade, and replicate within feline enterocytes. BMC Genomics 16, 66 (2015).","journal-title":"BMC Genomics"},{"key":"e_1_3_4_52_2","doi-asserted-by":"crossref","first-page":"706","DOI":"10.1007\/s00239-009-9245-2","article-title":"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","volume":"68","author":"Kishore SP","year":"2009","unstructured":"SP Kishore, SL Perkins, TJ Templeton, KW Deitsch, 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 68, 706\u2013714 (2009).","journal-title":"J Mol Evol"},{"key":"e_1_3_4_53_2","doi-asserted-by":"crossref","first-page":"e1003854","DOI":"10.1371\/journal.ppat.1003854","article-title":"Recruitment of PfSET2 by RNA polymerase II to variant antigen encoding loci contributes to antigenic variation in P. falciparum","volume":"10","author":"Ukaegbu UE","year":"2014","unstructured":"UE Ukaegbu, , Recruitment of PfSET2 by RNA polymerase II to variant antigen encoding loci contributes to antigenic variation in P. falciparum. PLoS Pathog 10, e1003854 (2014).","journal-title":"PLoS Pathog"},{"key":"e_1_3_4_54_2","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1038\/nature12361","article-title":"PfSETvs methylation of histone H3K36 represses virulence genes in Plasmodium falciparum","volume":"499","author":"Jiang L","year":"2013","unstructured":"L Jiang, , PfSETvs methylation of histone H3K36 represses virulence genes in Plasmodium falciparum. Nature 499, 223\u2013227 (2013).","journal-title":"Nature"},{"key":"e_1_3_4_55_2","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1186\/1471-2164-15-350","article-title":"Toxoplasma gondii merozoite gene expression analysis with comparison to the life cycle discloses a unique expression state during enteric development","volume":"15","author":"Behnke MS","year":"2014","unstructured":"MS Behnke, TP Zhang, JP Dubey, LD Sibley, Toxoplasma gondii merozoite gene expression analysis with comparison to the life cycle discloses a unique expression state during enteric development. BMC Genomics 15, 350 (2014).","journal-title":"BMC Genomics"},{"key":"e_1_3_4_56_2","doi-asserted-by":"crossref","first-page":"e1007035","DOI":"10.1371\/journal.ppat.1007035","article-title":"Transcriptional repression by ApiAP2 factors is central to chronic toxoplasmosis","volume":"14","author":"Radke JB","year":"2018","unstructured":"JB Radke, , Transcriptional repression by ApiAP2 factors is central to chronic toxoplasmosis. PLoS Pathog 14, e1007035 (2018).","journal-title":"PLoS Pathog"},{"key":"e_1_3_4_57_2","doi-asserted-by":"crossref","first-page":"e06974","DOI":"10.7554\/eLife.06974","article-title":"Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites","volume":"4","author":"Woo YH","year":"2015","unstructured":"YH Woo, , Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites. eLife 4, e06974 (2015).","journal-title":"eLife"},{"key":"e_1_3_4_58_2","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1016\/j.chom.2014.07.004","article-title":"Heterochromatin protein 1 secures survival and transmission of malaria parasites","volume":"16","author":"Brancucci NMB","year":"2014","unstructured":"NMB Brancucci, , Heterochromatin protein 1 secures survival and transmission of malaria parasites. Cell Host Microbe 16, 165\u2013176 (2014).","journal-title":"Cell Host Microbe"},{"key":"e_1_3_4_59_2","doi-asserted-by":"crossref","first-page":"e1000784","DOI":"10.1371\/journal.ppat.1000784","article-title":"A major role for the Plasmodium falciparum ApiAP2 protein PfSIP2 in chromosome end biology","volume":"6","author":"Flueck C","year":"2010","unstructured":"C Flueck, , A major role for the Plasmodium falciparum ApiAP2 protein PfSIP2 in chromosome end biology. PLoS Pathog 6, e1000784 (2010).","journal-title":"PLoS Pathog"},{"key":"e_1_3_4_60_2","doi-asserted-by":"crossref","first-page":"5414","DOI":"10.1073\/pnas.0408883102","article-title":"Antigenic variation in Plasmodium falciparum is associated with movement of var loci between subnuclear locations","volume":"102","author":"Ralph SA","year":"2005","unstructured":"SA Ralph, C Scheidig-Benatar, A Scherf, Antigenic variation in Plasmodium falciparum is associated with movement of var loci between subnuclear locations. Proc Natl Acad Sci USA 102, 5414\u20135419 (2005).","journal-title":"Proc Natl Acad Sci USA"},{"key":"e_1_3_4_61_2","doi-asserted-by":"crossref","first-page":"1361","DOI":"10.1093\/gbe\/evw081","article-title":"The genome of Haemoproteus tartakovskyi and its relationship to human malaria parasites","volume":"8","author":"Bensch S","year":"2016","unstructured":"S Bensch, , The genome of Haemoproteus tartakovskyi and its relationship to human malaria parasites. 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