Complete representation of a tapeworm genome reveals chromosomes capped by centromeres, necessitating a dual role in segregation and protection
Background Chromosome-level assemblies are indispensable for accurate gene prediction, synteny assessment, and understanding higher-order genome architecture. Reference and draft genomes of key helminth species have been published, but little is yet known about the biology of their chromosomes. Here...
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description | Background Chromosome-level assemblies are indispensable for accurate gene prediction, synteny assessment, and understanding higher-order genome architecture. Reference and draft genomes of key helminth species have been published, but little is yet known about the biology of their chromosomes. Here, we present the complete genome of the tapeworm Hymenolepis microstoma, providing a reference quality, end-to-end assembly that represents the first fully assembled genome of a spiralian/lophotrochozoan, revealing new insights into chromosome evolution. Results Long-read sequencing and optical mapping data were added to previous short-read data enabling complete re-assembly into six chromosomes, consistent with karyology. Small genome size (169 Mb) and lack of haploid variation (1 SNP/3.2 Mb) contributed to exceptionally high contiguity with only 85 gaps remaining in regions of low complexity sequence. Resolution of repeat regions reveals novel gene expansions, micro-exon genes, and spliced leader trans-splicing, and illuminates the landscape of transposable elements, explaining observed length differences in sister chromatids. Syntenic comparison with other parasitic flatworms shows conserved ancestral linkage groups indicating that the H. microstoma karyotype evolved through fusion events. Strikingly, the assembly reveals that the chromosomes terminate in centromeric arrays, indicating that these motifs play a role not only in segregation, but also in protecting the linear integrity and full lengths of chromosomes. Conclusions Despite strong conservation of canonical telomeres, our results show that they can be substituted by more complex, species-specific sequences, as represented by centromeres. The assembly provides a robust platform for investigations that require complete genome representation. |
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Reference and draft genomes of key helminth species have been published, but little is yet known about the biology of their chromosomes. Here, we present the complete genome of the tapeworm Hymenolepis microstoma, providing a reference quality, end-to-end assembly that represents the first fully assembled genome of a spiralian/lophotrochozoan, revealing new insights into chromosome evolution. Results Long-read sequencing and optical mapping data were added to previous short-read data enabling complete re-assembly into six chromosomes, consistent with karyology. Small genome size (169 Mb) and lack of haploid variation (1 SNP/3.2 Mb) contributed to exceptionally high contiguity with only 85 gaps remaining in regions of low complexity sequence. Resolution of repeat regions reveals novel gene expansions, micro-exon genes, and spliced leader trans-splicing, and illuminates the landscape of transposable elements, explaining observed length differences in sister chromatids. Syntenic comparison with other parasitic flatworms shows conserved ancestral linkage groups indicating that the H. microstoma karyotype evolved through fusion events. Strikingly, the assembly reveals that the chromosomes terminate in centromeric arrays, indicating that these motifs play a role not only in segregation, but also in protecting the linear integrity and full lengths of chromosomes. Conclusions Despite strong conservation of canonical telomeres, our results show that they can be substituted by more complex, species-specific sequences, as represented by centromeres. The assembly provides a robust platform for investigations that require complete genome representation.</description><identifier>ISSN: 1741-7007</identifier><identifier>EISSN: 1741-7007</identifier><identifier>DOI: 10.1186/s12915-020-00899-w</identifier><identifier>PMID: 33167983</identifier><language>eng</language><publisher>LONDON: Springer Nature</publisher><subject>Animals ; Assembly ; Biology ; Centromere - metabolism ; Centromeres ; Chromatids ; Chromosome assembly ; Chromosome Segregation ; Chromosomes ; Chromosomes - metabolism ; Complexity ; Deoxyribonucleic acid ; DNA ; DNA Transposable Elements - genetics ; Estimates ; Evolution ; Flatworms ; Gene expression ; Gene mapping ; Genetic aspects ; Genome, Helminth ; Genomes ; Hymenolepis ; Hymenolepis - genetics ; Karyology ; Karyotypes ; Laboratories ; Life Sciences & Biomedicine ; Life Sciences & Biomedicine - Other Topics ; Representations ; Science & Technology ; Single-nucleotide polymorphism ; Sister chromatids ; Splicing ; Structure ; Synteny ; Tapeworms ; Telomere loss ; Telomeres ; Worms</subject><ispartof>BMC biology, 2020-11, Vol.18 (1), p.165-165, Article 165</ispartof><rights>COPYRIGHT 2020 BioMed Central Ltd.</rights><rights>2020. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>The Author(s) 2020</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>true</woscitedreferencessubscribed><woscitedreferencescount>14</woscitedreferencescount><woscitedreferencesoriginalsourcerecordid>wos000590705200001</woscitedreferencesoriginalsourcerecordid><citedby>FETCH-LOGICAL-c697t-da5f932b354d9361313dca1c7ef8194c5996078d6712349c15e56aa4d2364a6f3</citedby><cites>FETCH-LOGICAL-c697t-da5f932b354d9361313dca1c7ef8194c5996078d6712349c15e56aa4d2364a6f3</cites><orcidid>0000-0003-2391-9573 ; 0000-0002-9581-0377 ; 0000-0001-9167-7532</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7653826/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7653826/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,729,782,786,866,887,2104,2116,27931,27932,28255,53798,53800</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33167983$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Olson, Peter D.</creatorcontrib><creatorcontrib>Tracey, Alan</creatorcontrib><creatorcontrib>Baillie, Andrew</creatorcontrib><creatorcontrib>James, Katherine</creatorcontrib><creatorcontrib>Doyle, Stephen R.</creatorcontrib><creatorcontrib>Buddenborg, Sarah K.</creatorcontrib><creatorcontrib>Rodgers, Faye H.</creatorcontrib><creatorcontrib>Holroyd, Nancy</creatorcontrib><creatorcontrib>Berriman, Matt</creatorcontrib><title>Complete representation of a tapeworm genome reveals chromosomes capped by centromeres, necessitating a dual role in segregation and protection</title><title>BMC biology</title><addtitle>BMC BIOL</addtitle><addtitle>BMC Biol</addtitle><description>Background Chromosome-level assemblies are indispensable for accurate gene prediction, synteny assessment, and understanding higher-order genome architecture. Reference and draft genomes of key helminth species have been published, but little is yet known about the biology of their chromosomes. Here, we present the complete genome of the tapeworm Hymenolepis microstoma, providing a reference quality, end-to-end assembly that represents the first fully assembled genome of a spiralian/lophotrochozoan, revealing new insights into chromosome evolution. Results Long-read sequencing and optical mapping data were added to previous short-read data enabling complete re-assembly into six chromosomes, consistent with karyology. Small genome size (169 Mb) and lack of haploid variation (1 SNP/3.2 Mb) contributed to exceptionally high contiguity with only 85 gaps remaining in regions of low complexity sequence. Resolution of repeat regions reveals novel gene expansions, micro-exon genes, and spliced leader trans-splicing, and illuminates the landscape of transposable elements, explaining observed length differences in sister chromatids. Syntenic comparison with other parasitic flatworms shows conserved ancestral linkage groups indicating that the H. microstoma karyotype evolved through fusion events. Strikingly, the assembly reveals that the chromosomes terminate in centromeric arrays, indicating that these motifs play a role not only in segregation, but also in protecting the linear integrity and full lengths of chromosomes. Conclusions Despite strong conservation of canonical telomeres, our results show that they can be substituted by more complex, species-specific sequences, as represented by centromeres. The assembly provides a robust platform for investigations that require complete genome representation.</description><subject>Animals</subject><subject>Assembly</subject><subject>Biology</subject><subject>Centromere - metabolism</subject><subject>Centromeres</subject><subject>Chromatids</subject><subject>Chromosome assembly</subject><subject>Chromosome Segregation</subject><subject>Chromosomes</subject><subject>Chromosomes - metabolism</subject><subject>Complexity</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA Transposable Elements - genetics</subject><subject>Estimates</subject><subject>Evolution</subject><subject>Flatworms</subject><subject>Gene expression</subject><subject>Gene mapping</subject><subject>Genetic aspects</subject><subject>Genome, Helminth</subject><subject>Genomes</subject><subject>Hymenolepis</subject><subject>Hymenolepis - genetics</subject><subject>Karyology</subject><subject>Karyotypes</subject><subject>Laboratories</subject><subject>Life Sciences & Biomedicine</subject><subject>Life Sciences & Biomedicine - Other Topics</subject><subject>Representations</subject><subject>Science & Technology</subject><subject>Single-nucleotide polymorphism</subject><subject>Sister chromatids</subject><subject>Splicing</subject><subject>Structure</subject><subject>Synteny</subject><subject>Tapeworms</subject><subject>Telomere loss</subject><subject>Telomeres</subject><subject>Worms</subject><issn>1741-7007</issn><issn>1741-7007</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>AOWDO</sourceid><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><sourceid>DOA</sourceid><recordid>eNqNkstu1TAURSMEoqXwAwxQJCYgSPErdjxBqq54VKpUidfUcuyTNFVip3bSS7-CX8ZpSulFDKoMYp-svY-ytbPsOUaHGFf8XcRE4rJABBUIVVIW2wfZPhYMFwIh8fDOeS97EuM5QqQUgj7O9ijFXMiK7me_Nn4Ye5ggDzAGiOAmPXXe5b7JdT7pEbY-DHkLzg8Lcwm6j7k5C37wMY3SWY8j2Ly-yk0Spzkkm7e5AwMxdouba5OVnXWfB99D3rk8QhugXRdpZ_Mx-AnMcn2aPWrSBnh28z7Ivn_88G3zuTg5_XS8OTopDJdiKqwuG0lJTUtmJeWYYmqNxkZAU2HJTCklR6KyXGBCmTS4hJJrzSyhnGne0IPsePW1Xp-rMXSDDlfK605dD3xolQ5TZ3pQja0ZYETrFCerUtAMi4oJzDVjJalt8nq_eo1zPYC9jkH3O6a7X1x3plp_qQQvaUV4Mnh1YxD8xQxxUkMXDfS9duDnqAgrJV02yoS-_Ac993NwKapEcZzcUFX-pVqdfqBzjU97zWKqjjgjRCDOF-rwP1R6LAyd8Q6aLs13BK93BImZ4OfU6jlGdfz1y_3Z0x-7LFlZE3yMAZrb7DBSS9XVWnWVqq6uq662SfTibuq3kj_dTkC1AluofRNNB87ALYYQKiUSqCTphPCmW3u_8bObkvTN_aX0N80oGX8</recordid><startdate>20201109</startdate><enddate>20201109</enddate><creator>Olson, Peter D.</creator><creator>Tracey, Alan</creator><creator>Baillie, Andrew</creator><creator>James, Katherine</creator><creator>Doyle, Stephen R.</creator><creator>Buddenborg, Sarah K.</creator><creator>Rodgers, Faye H.</creator><creator>Holroyd, Nancy</creator><creator>Berriman, Matt</creator><general>Springer Nature</general><general>BioMed Central Ltd</general><general>BioMed Central</general><general>BMC</general><scope>AOWDO</scope><scope>BLEPL</scope><scope>DTL</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>4U-</scope><scope>7QG</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>M7P</scope><scope>MBDVC</scope><scope>P64</scope><scope>PADUT</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0003-2391-9573</orcidid><orcidid>https://orcid.org/0000-0002-9581-0377</orcidid><orcidid>https://orcid.org/0000-0001-9167-7532</orcidid></search><sort><creationdate>20201109</creationdate><title>Complete representation of a tapeworm genome reveals chromosomes capped by centromeres, necessitating a dual role in segregation and protection</title><author>Olson, Peter D. ; Tracey, Alan ; Baillie, Andrew ; James, Katherine ; Doyle, Stephen R. ; Buddenborg, Sarah K. ; Rodgers, Faye H. ; Holroyd, Nancy ; Berriman, Matt</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c697t-da5f932b354d9361313dca1c7ef8194c5996078d6712349c15e56aa4d2364a6f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Animals</topic><topic>Assembly</topic><topic>Biology</topic><topic>Centromere - metabolism</topic><topic>Centromeres</topic><topic>Chromatids</topic><topic>Chromosome assembly</topic><topic>Chromosome Segregation</topic><topic>Chromosomes</topic><topic>Chromosomes - metabolism</topic><topic>Complexity</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>DNA Transposable Elements - genetics</topic><topic>Estimates</topic><topic>Evolution</topic><topic>Flatworms</topic><topic>Gene expression</topic><topic>Gene mapping</topic><topic>Genetic aspects</topic><topic>Genome, Helminth</topic><topic>Genomes</topic><topic>Hymenolepis</topic><topic>Hymenolepis - genetics</topic><topic>Karyology</topic><topic>Karyotypes</topic><topic>Laboratories</topic><topic>Life Sciences & Biomedicine</topic><topic>Life Sciences & Biomedicine - Other Topics</topic><topic>Representations</topic><topic>Science & Technology</topic><topic>Single-nucleotide polymorphism</topic><topic>Sister chromatids</topic><topic>Splicing</topic><topic>Structure</topic><topic>Synteny</topic><topic>Tapeworms</topic><topic>Telomere loss</topic><topic>Telomeres</topic><topic>Worms</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Olson, Peter D.</creatorcontrib><creatorcontrib>Tracey, Alan</creatorcontrib><creatorcontrib>Baillie, Andrew</creatorcontrib><creatorcontrib>James, Katherine</creatorcontrib><creatorcontrib>Doyle, Stephen R.</creatorcontrib><creatorcontrib>Buddenborg, Sarah K.</creatorcontrib><creatorcontrib>Rodgers, Faye H.</creatorcontrib><creatorcontrib>Holroyd, Nancy</creatorcontrib><creatorcontrib>Berriman, Matt</creatorcontrib><collection>Web of Science - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>BMC biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Olson, Peter D.</au><au>Tracey, Alan</au><au>Baillie, Andrew</au><au>James, Katherine</au><au>Doyle, Stephen R.</au><au>Buddenborg, Sarah K.</au><au>Rodgers, Faye H.</au><au>Holroyd, Nancy</au><au>Berriman, Matt</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Complete representation of a tapeworm genome reveals chromosomes capped by centromeres, necessitating a dual role in segregation and protection</atitle><jtitle>BMC biology</jtitle><stitle>BMC BIOL</stitle><addtitle>BMC Biol</addtitle><date>2020-11-09</date><risdate>2020</risdate><volume>18</volume><issue>1</issue><spage>165</spage><epage>165</epage><pages>165-165</pages><artnum>165</artnum><issn>1741-7007</issn><eissn>1741-7007</eissn><abstract>Background Chromosome-level assemblies are indispensable for accurate gene prediction, synteny assessment, and understanding higher-order genome architecture. Reference and draft genomes of key helminth species have been published, but little is yet known about the biology of their chromosomes. Here, we present the complete genome of the tapeworm Hymenolepis microstoma, providing a reference quality, end-to-end assembly that represents the first fully assembled genome of a spiralian/lophotrochozoan, revealing new insights into chromosome evolution. Results Long-read sequencing and optical mapping data were added to previous short-read data enabling complete re-assembly into six chromosomes, consistent with karyology. Small genome size (169 Mb) and lack of haploid variation (1 SNP/3.2 Mb) contributed to exceptionally high contiguity with only 85 gaps remaining in regions of low complexity sequence. Resolution of repeat regions reveals novel gene expansions, micro-exon genes, and spliced leader trans-splicing, and illuminates the landscape of transposable elements, explaining observed length differences in sister chromatids. Syntenic comparison with other parasitic flatworms shows conserved ancestral linkage groups indicating that the H. microstoma karyotype evolved through fusion events. Strikingly, the assembly reveals that the chromosomes terminate in centromeric arrays, indicating that these motifs play a role not only in segregation, but also in protecting the linear integrity and full lengths of chromosomes. Conclusions Despite strong conservation of canonical telomeres, our results show that they can be substituted by more complex, species-specific sequences, as represented by centromeres. The assembly provides a robust platform for investigations that require complete genome representation.</abstract><cop>LONDON</cop><pub>Springer Nature</pub><pmid>33167983</pmid><doi>10.1186/s12915-020-00899-w</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0003-2391-9573</orcidid><orcidid>https://orcid.org/0000-0002-9581-0377</orcidid><orcidid>https://orcid.org/0000-0001-9167-7532</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Assembly Biology Centromere - metabolism Centromeres Chromatids Chromosome assembly Chromosome Segregation Chromosomes Chromosomes - metabolism Complexity Deoxyribonucleic acid DNA DNA Transposable Elements - genetics Estimates Evolution Flatworms Gene expression Gene mapping Genetic aspects Genome, Helminth Genomes Hymenolepis Hymenolepis - genetics Karyology Karyotypes Laboratories Life Sciences & Biomedicine Life Sciences & Biomedicine - Other Topics Representations Science & Technology Single-nucleotide polymorphism Sister chromatids Splicing Structure Synteny Tapeworms Telomere loss Telomeres Worms |
title | Complete representation of a tapeworm genome reveals chromosomes capped by centromeres, necessitating a dual role in segregation and protection |
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