Extreme telomere length dimorphism in the Tasmanian devil and related marsupials suggests parental control of telomere length
Telomeres, specialised structures that protect chromosome ends, play a critical role in preserving chromosome integrity. Telomere dynamics in the Tasmanian devil (Sarcophilus harrisii) are of particular interest in light of the emergence of devil facial tumour disease (DFTD), a transmissible maligna...
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creator | Bender, Hannah S Murchison, Elizabeth P Pickett, Hilda A Deakin, Janine E Strong, Margaret A Conlan, Carly McMillan, Daniel A Neumann, Axel A Greider, Carol W Hannon, Gregory J Reddel, Roger R Graves, Jennifer A Marshall |
description | Telomeres, specialised structures that protect chromosome ends, play a critical role in preserving chromosome integrity. Telomere dynamics in the Tasmanian devil (Sarcophilus harrisii) are of particular interest in light of the emergence of devil facial tumour disease (DFTD), a transmissible malignancy that causes rapid mortality and threatens the species with extinction. We used fluorescent in situ hybridisation to investigate telomere length in DFTD cells, in healthy Tasmanian devils and in four closely related marsupial species. Here we report that animals in the Order Dasyuromorphia have chromosomes characterised by striking telomere length dimorphism between homologues. Findings in sex chromosomes suggest that telomere length dimorphism may be regulated by events in the parental germlines. Long telomeres on the Y chromosome imply that telomere lengthening occurs during spermatogenesis, whereas telomere diminution occurs during oogenesis. Although found in several somatic cell tissue types, telomere length dimorphism was not found in DFTD cancer cells, which are characterised by uniformly short telomeres. This is, to our knowledge, the first report of naturally occurring telomere length dimorphism in any species and suggests a novel strategy of telomere length control. Comparative studies in five distantly related marsupials and a monotreme indicate that telomere dimorphism evolved at least 50 million years ago. |
doi_str_mv | 10.1371/journal.pone.0046195 |
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Telomere dynamics in the Tasmanian devil (Sarcophilus harrisii) are of particular interest in light of the emergence of devil facial tumour disease (DFTD), a transmissible malignancy that causes rapid mortality and threatens the species with extinction. We used fluorescent in situ hybridisation to investigate telomere length in DFTD cells, in healthy Tasmanian devils and in four closely related marsupial species. Here we report that animals in the Order Dasyuromorphia have chromosomes characterised by striking telomere length dimorphism between homologues. Findings in sex chromosomes suggest that telomere length dimorphism may be regulated by events in the parental germlines. Long telomeres on the Y chromosome imply that telomere lengthening occurs during spermatogenesis, whereas telomere diminution occurs during oogenesis. Although found in several somatic cell tissue types, telomere length dimorphism was not found in DFTD cancer cells, which are characterised by uniformly short telomeres. This is, to our knowledge, the first report of naturally occurring telomere length dimorphism in any species and suggests a novel strategy of telomere length control. Comparative studies in five distantly related marsupials and a monotreme indicate that telomere dimorphism evolved at least 50 million years ago.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0046195</identifier><identifier>PMID: 23049977</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Biological evolution ; Biology ; Cancer ; Cell cycle ; Cell division ; Chromosomes ; Comparative studies ; Deoxyribonucleic acid ; Dimorphism ; Dimorphism (Biology) ; DNA ; Extinction (Biology) ; Fluorescence ; Head & neck cancer ; Homology ; In Situ Hybridization ; Laboratories ; Malignancy ; Marsupialia - genetics ; Marsupials ; Medical research ; Mitochondrial DNA ; Molecular biology ; Oogenesis ; Sarcophilus harrisii ; Sex chromosomes ; Sex Chromosomes - genetics ; Species extinction ; Spermatogenesis ; Telomerase ; Telomere - genetics ; Telomere Homeostasis - genetics ; Telomeres ; Tumors ; Veterinary Science ; Y Chromosomes</subject><ispartof>PloS one, 2012-09, Vol.7 (9), p.e46195-e46195</ispartof><rights>COPYRIGHT 2012 Public Library of Science</rights><rights>Bender et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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Telomere dynamics in the Tasmanian devil (Sarcophilus harrisii) are of particular interest in light of the emergence of devil facial tumour disease (DFTD), a transmissible malignancy that causes rapid mortality and threatens the species with extinction. We used fluorescent in situ hybridisation to investigate telomere length in DFTD cells, in healthy Tasmanian devils and in four closely related marsupial species. Here we report that animals in the Order Dasyuromorphia have chromosomes characterised by striking telomere length dimorphism between homologues. Findings in sex chromosomes suggest that telomere length dimorphism may be regulated by events in the parental germlines. Long telomeres on the Y chromosome imply that telomere lengthening occurs during spermatogenesis, whereas telomere diminution occurs during oogenesis. 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Comparative studies in five distantly related marsupials and a monotreme indicate that telomere dimorphism evolved at least 50 million years ago.</description><subject>Animals</subject><subject>Biological evolution</subject><subject>Biology</subject><subject>Cancer</subject><subject>Cell cycle</subject><subject>Cell division</subject><subject>Chromosomes</subject><subject>Comparative studies</subject><subject>Deoxyribonucleic acid</subject><subject>Dimorphism</subject><subject>Dimorphism (Biology)</subject><subject>DNA</subject><subject>Extinction (Biology)</subject><subject>Fluorescence</subject><subject>Head & neck cancer</subject><subject>Homology</subject><subject>In Situ Hybridization</subject><subject>Laboratories</subject><subject>Malignancy</subject><subject>Marsupialia - genetics</subject><subject>Marsupials</subject><subject>Medical research</subject><subject>Mitochondrial DNA</subject><subject>Molecular biology</subject><subject>Oogenesis</subject><subject>Sarcophilus harrisii</subject><subject>Sex chromosomes</subject><subject>Sex Chromosomes - genetics</subject><subject>Species extinction</subject><subject>Spermatogenesis</subject><subject>Telomerase</subject><subject>Telomere - genetics</subject><subject>Telomere Homeostasis - genetics</subject><subject>Telomeres</subject><subject>Tumors</subject><subject>Veterinary Science</subject><subject>Y Chromosomes</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk0Fv1DAQhSMEoqXwDxBYQkJw2MWO7Ti5IFVVgUqVKkHhas0mk6xXjr21naoc-O946bbarXpAOSRyvvfG80ZTFK8ZnTOu2KeVn4IDO197h3NKRcUa-aQ4ZA0vZ1VJ-dOd74PiRYwrSiWvq-p5cVByKppGqcPiz-lNCjgiSWj9iAGJRTekJenM6MN6aeJIjCNpieQS4gjOgCMdXhtLwHUkoIWEHRkhxGltwEYSp2HAmCJZQ0CXwJLWuxS8Jb5_WOVl8azPGny1fR8VP7-cXp58m51ffD07OT6ftVVTpllXim5BpaoWspS8XTTdoqt6rKRqSgF9wwFqyiRULXQM-xJk23DVqr5ZUIS65UfF21vftfVRb5OLmvGykkKJSmXi7JboPKz0Opjc0W_tweh_Bz4MGkIyrUVd5QKKKSml6EUtFQhQpex5dtpkWmevz9tq02LErs0pBLB7pvt_nFnqwV9rLmRNKcsGH7YGwV9NOUw9mtiiteDQT_netJE1KwXboO8eoI93t6UGyA0Y1_tct92Y6mPR1KVkSpWZmj9C5afD0eQhYm_y-Z7g455gM2i8SQNMMeqzH9__n734tc--32GXCDYto7dTMt7FfVDcgm3wMQbs70NmVG-25C4NvdkSvd2SLHuzO6B70d1a8L_Tsg7Q</recordid><startdate>20120925</startdate><enddate>20120925</enddate><creator>Bender, Hannah S</creator><creator>Murchison, Elizabeth P</creator><creator>Pickett, Hilda A</creator><creator>Deakin, Janine E</creator><creator>Strong, Margaret A</creator><creator>Conlan, Carly</creator><creator>McMillan, Daniel A</creator><creator>Neumann, Axel A</creator><creator>Greider, Carol W</creator><creator>Hannon, Gregory J</creator><creator>Reddel, Roger R</creator><creator>Graves, Jennifer A Marshall</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><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>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20120925</creationdate><title>Extreme telomere length dimorphism in the Tasmanian devil and related marsupials suggests parental control of telomere length</title><author>Bender, Hannah S ; Murchison, Elizabeth P ; Pickett, Hilda A ; Deakin, Janine E ; Strong, Margaret A ; Conlan, Carly ; McMillan, Daniel A ; Neumann, Axel A ; Greider, Carol W ; Hannon, Gregory J ; Reddel, Roger R ; Graves, Jennifer A Marshall</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-d24db0576b5253cb9dbd6fe657924af93aa8015a6cad1ef2a5c937c7f9b0ea8c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Animals</topic><topic>Biological evolution</topic><topic>Biology</topic><topic>Cancer</topic><topic>Cell cycle</topic><topic>Cell division</topic><topic>Chromosomes</topic><topic>Comparative studies</topic><topic>Deoxyribonucleic acid</topic><topic>Dimorphism</topic><topic>Dimorphism (Biology)</topic><topic>DNA</topic><topic>Extinction (Biology)</topic><topic>Fluorescence</topic><topic>Head & neck cancer</topic><topic>Homology</topic><topic>In Situ Hybridization</topic><topic>Laboratories</topic><topic>Malignancy</topic><topic>Marsupialia - 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Telomere dynamics in the Tasmanian devil (Sarcophilus harrisii) are of particular interest in light of the emergence of devil facial tumour disease (DFTD), a transmissible malignancy that causes rapid mortality and threatens the species with extinction. We used fluorescent in situ hybridisation to investigate telomere length in DFTD cells, in healthy Tasmanian devils and in four closely related marsupial species. Here we report that animals in the Order Dasyuromorphia have chromosomes characterised by striking telomere length dimorphism between homologues. Findings in sex chromosomes suggest that telomere length dimorphism may be regulated by events in the parental germlines. Long telomeres on the Y chromosome imply that telomere lengthening occurs during spermatogenesis, whereas telomere diminution occurs during oogenesis. Although found in several somatic cell tissue types, telomere length dimorphism was not found in DFTD cancer cells, which are characterised by uniformly short telomeres. This is, to our knowledge, the first report of naturally occurring telomere length dimorphism in any species and suggests a novel strategy of telomere length control. Comparative studies in five distantly related marsupials and a monotreme indicate that telomere dimorphism evolved at least 50 million years ago.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23049977</pmid><doi>10.1371/journal.pone.0046195</doi><tpages>e46195</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Biological evolution Biology Cancer Cell cycle Cell division Chromosomes Comparative studies Deoxyribonucleic acid Dimorphism Dimorphism (Biology) DNA Extinction (Biology) Fluorescence Head & neck cancer Homology In Situ Hybridization Laboratories Malignancy Marsupialia - genetics Marsupials Medical research Mitochondrial DNA Molecular biology Oogenesis Sarcophilus harrisii Sex chromosomes Sex Chromosomes - genetics Species extinction Spermatogenesis Telomerase Telomere - genetics Telomere Homeostasis - genetics Telomeres Tumors Veterinary Science Y Chromosomes |
title | Extreme telomere length dimorphism in the Tasmanian devil and related marsupials suggests parental control of telomere length |
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