Rapid chromosome evolution in recently formed polyploids in Tragopogon (Asteraceae)

Polyploidy, frequently termed "whole genome duplication", is a major force in the evolution of many eukaryotes. Indeed, most angiosperm species have undergone at least one round of polyploidy in their evolutionary history. Despite enormous progress in our understanding of many aspects of p...

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Hauptverfasser: Lim, K Yoong, Soltis, Douglas E, Soltis, Pamela S, Tate, Jennifer, Matyasek, Roman, Srubarova, Hana, Kovarik, Ales, Pires, J Chris, Xiong, Zhiyong, Leitch, Andrew R
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container_start_page e3353
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creator Lim, K Yoong
Soltis, Douglas E
Soltis, Pamela S
Tate, Jennifer
Matyasek, Roman
Srubarova, Hana
Kovarik, Ales
Pires, J Chris
Xiong, Zhiyong
Leitch, Andrew R
description Polyploidy, frequently termed "whole genome duplication", is a major force in the evolution of many eukaryotes. Indeed, most angiosperm species have undergone at least one round of polyploidy in their evolutionary history. Despite enormous progress in our understanding of many aspects of polyploidy, we essentially have no information about the role of chromosome divergence in the establishment of young polyploid populations. Here we investigate synthetic lines and natural populations of two recently and recurrently formed allotetraploids Tragopogon mirus and T. miscellus (formed within the past 80 years) to assess the role of aberrant meiosis in generating chromosomal/genomic diversity. That diversity is likely important in the formation, establishment and survival of polyploid populations and species. Applications of fluorescence in situ hybridisation (FISH) to natural populations of T. mirus and T. miscellus suggest that chromosomal rearrangements and other chromosomal changes are common in both allotetraploids. We detected extensive chromosomal polymorphism between individuals and populations, including (i) plants monosomic and trisomic for particular chromosomes (perhaps indicating compensatory trisomy), (ii) intergenomic translocations and (iii) variable sizes and expression patterns of individual ribosomal DNA (rDNA) loci. We even observed karyotypic variation among sibling plants. Significantly, translocations, chromosome loss, and meiotic irregularities, including quadrivalent formation, were observed in synthetic (S(0) and S(1) generations) polyploid lines. Our results not only provide a mechanism for chromosomal variation in natural populations, but also indicate that chromosomal changes occur rapidly following polyploidisation. These data shed new light on previous analyses of genome and transcriptome structures in de novo and establishing polyploid species. Crucially our results highlight the necessity of studying karyotypes in young (
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Indeed, most angiosperm species have undergone at least one round of polyploidy in their evolutionary history. Despite enormous progress in our understanding of many aspects of polyploidy, we essentially have no information about the role of chromosome divergence in the establishment of young polyploid populations. Here we investigate synthetic lines and natural populations of two recently and recurrently formed allotetraploids Tragopogon mirus and T. miscellus (formed within the past 80 years) to assess the role of aberrant meiosis in generating chromosomal/genomic diversity. That diversity is likely important in the formation, establishment and survival of polyploid populations and species. Applications of fluorescence in situ hybridisation (FISH) to natural populations of T. mirus and T. miscellus suggest that chromosomal rearrangements and other chromosomal changes are common in both allotetraploids. 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Crucially our results highlight the necessity of studying karyotypes in young (&lt;150 years old) polyploid species and synthetic polyploids that resemble natural species. The data also provide insight into the mechanisms that perturb inheritance patterns of genetic markers in synthetic polyploids and populations of young natural polyploid species.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0003353</identifier><identifier>PMID: 18843372</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Aberration ; Analysis ; Asteraceae ; Barley ; Biological evolution ; Biology ; Biophysics ; Chromosome rearrangements ; Chromosome translocations ; Chromosomes ; Chromosomes, Plant ; Cytogenetics ; Deoxyribonucleic acid ; Diploidy ; Divergence ; DNA ; DNA methylation ; DNA, Ribosomal - genetics ; Epigenetics ; Eukaryotes ; Evolution ; Evolution, Molecular ; Evolutionary genetics ; Fish populations ; Fluorescence ; Fluorescence in situ hybridization ; Gene expression ; Genetic markers ; Genetic polymorphisms ; Genetic research ; Genetics ; Genetics and Genomics/Genomics ; Genetics and Genomics/Plant Genomes and Evolution ; Genetics and Genomics/Population Genetics ; Genome, Plant ; Genomes ; Genomics ; Heredity ; Hybridization ; In Situ Hybridization, Fluorescence ; Karyotypes ; Karyotyping ; Life sciences ; Meiosis ; Meiosis - physiology ; Mitosis - physiology ; Mutation ; Natural populations ; Polymorphism ; Polyploidy ; Populations ; Rape plants ; Species ; Tragopogon - anatomy &amp; histology ; Tragopogon - genetics ; Tragopogon dubius ; Tragopogon mirus ; Tragopogon miscellus ; Tragopogon porrifolius ; Trisomy</subject><ispartof>PloS one, 2008-10, Vol.3 (10), p.e3353-e3353</ispartof><rights>COPYRIGHT 2008 Public Library of Science</rights><rights>2008 Lim et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Lim et al. 2008</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c728t-2ffd01ec1783ca1bccbc194376faaeb836fcc1334343028b0cbcb2433b12debd3</citedby><cites>FETCH-LOGICAL-c728t-2ffd01ec1783ca1bccbc194376faaeb836fcc1334343028b0cbcb2433b12debd3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2556386/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2556386/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/18843372$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lim, K Yoong</creatorcontrib><creatorcontrib>Soltis, Douglas E</creatorcontrib><creatorcontrib>Soltis, Pamela S</creatorcontrib><creatorcontrib>Tate, Jennifer</creatorcontrib><creatorcontrib>Matyasek, Roman</creatorcontrib><creatorcontrib>Srubarova, Hana</creatorcontrib><creatorcontrib>Kovarik, Ales</creatorcontrib><creatorcontrib>Pires, J Chris</creatorcontrib><creatorcontrib>Xiong, Zhiyong</creatorcontrib><creatorcontrib>Leitch, Andrew R</creatorcontrib><title>Rapid chromosome evolution in recently formed polyploids in Tragopogon (Asteraceae)</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Polyploidy, frequently termed "whole genome duplication", is a major force in the evolution of many eukaryotes. Indeed, most angiosperm species have undergone at least one round of polyploidy in their evolutionary history. Despite enormous progress in our understanding of many aspects of polyploidy, we essentially have no information about the role of chromosome divergence in the establishment of young polyploid populations. Here we investigate synthetic lines and natural populations of two recently and recurrently formed allotetraploids Tragopogon mirus and T. miscellus (formed within the past 80 years) to assess the role of aberrant meiosis in generating chromosomal/genomic diversity. That diversity is likely important in the formation, establishment and survival of polyploid populations and species. Applications of fluorescence in situ hybridisation (FISH) to natural populations of T. mirus and T. miscellus suggest that chromosomal rearrangements and other chromosomal changes are common in both allotetraploids. 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Crucially our results highlight the necessity of studying karyotypes in young (&lt;150 years old) polyploid species and synthetic polyploids that resemble natural species. The data also provide insight into the mechanisms that perturb inheritance patterns of genetic markers in synthetic polyploids and populations of young natural polyploid species.</description><subject>Aberration</subject><subject>Analysis</subject><subject>Asteraceae</subject><subject>Barley</subject><subject>Biological evolution</subject><subject>Biology</subject><subject>Biophysics</subject><subject>Chromosome rearrangements</subject><subject>Chromosome translocations</subject><subject>Chromosomes</subject><subject>Chromosomes, Plant</subject><subject>Cytogenetics</subject><subject>Deoxyribonucleic acid</subject><subject>Diploidy</subject><subject>Divergence</subject><subject>DNA</subject><subject>DNA methylation</subject><subject>DNA, Ribosomal - genetics</subject><subject>Epigenetics</subject><subject>Eukaryotes</subject><subject>Evolution</subject><subject>Evolution, Molecular</subject><subject>Evolutionary genetics</subject><subject>Fish populations</subject><subject>Fluorescence</subject><subject>Fluorescence in situ hybridization</subject><subject>Gene expression</subject><subject>Genetic markers</subject><subject>Genetic polymorphisms</subject><subject>Genetic research</subject><subject>Genetics</subject><subject>Genetics and Genomics/Genomics</subject><subject>Genetics and Genomics/Plant Genomes and Evolution</subject><subject>Genetics and Genomics/Population Genetics</subject><subject>Genome, Plant</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Heredity</subject><subject>Hybridization</subject><subject>In Situ Hybridization, Fluorescence</subject><subject>Karyotypes</subject><subject>Karyotyping</subject><subject>Life sciences</subject><subject>Meiosis</subject><subject>Meiosis - physiology</subject><subject>Mitosis - physiology</subject><subject>Mutation</subject><subject>Natural populations</subject><subject>Polymorphism</subject><subject>Polyploidy</subject><subject>Populations</subject><subject>Rape plants</subject><subject>Species</subject><subject>Tragopogon - anatomy &amp; histology</subject><subject>Tragopogon - genetics</subject><subject>Tragopogon dubius</subject><subject>Tragopogon mirus</subject><subject>Tragopogon miscellus</subject><subject>Tragopogon porrifolius</subject><subject>Trisomy</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2008</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNkl9v0zAUxSMEYmPwDRBEQprYQ4v_pE7yglRNAypNmrQNXi3HuU5dOXGwk4l-e27XAC3iAfnBlu_vHl8fnSR5Tcmc8px-2PgxdMrNe9_BnBDC-YI_SU5pydlMMMKfHpxPkhcxbghZ8EKI58kJLYqM85ydJne3qrd1qtfBtz76FlJ48G4crO9S26UBNHSD26bGhxbqtPdu2ztv67ir3gfV-N43yL5fxgGC0qDg4mXyzCgX4dW0nyVfP13dX36ZXd98Xl0ur2c6Z8UwY8bUhIKmecG1opXWlaZlxnNhlIKq4MJoTTnPcBFWVATrFcO5K8pqqGp-lrzd6-JEUU5-REk5RaqkgiOx2hO1VxvZB9uqsJVeWfl44UMjVRisdiC5ELUqjVgQ0BnDmSDXNSkEVaLUphSo9XF6bazQip0vQbkj0eNKZ9ey8Q-SLRYCfUeB80kg-O8jxEG2NmpwTnXgxyhFKbKSkhLBd3-B__7bfE81Cse3nfH4qsZVQ2s1hsJYvF9mOROU0bLAhoujBmQG-DE0aoxRru5u_5-9-XbMnh-wa1BuWMcpQ_EYzPagDj7GAOa3eZTIXaZ__VPuMi2nTGPbm0Pj_zRNIeY_AZbw81M</recordid><startdate>20081009</startdate><enddate>20081009</enddate><creator>Lim, K Yoong</creator><creator>Soltis, Douglas E</creator><creator>Soltis, Pamela S</creator><creator>Tate, Jennifer</creator><creator>Matyasek, Roman</creator><creator>Srubarova, Hana</creator><creator>Kovarik, Ales</creator><creator>Pires, J Chris</creator><creator>Xiong, Zhiyong</creator><creator>Leitch, Andrew R</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>AEUYN</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>20081009</creationdate><title>Rapid chromosome evolution in recently formed polyploids in Tragopogon (Asteraceae)</title><author>Lim, K Yoong ; Soltis, Douglas E ; Soltis, Pamela S ; Tate, Jennifer ; Matyasek, Roman ; Srubarova, Hana ; Kovarik, Ales ; Pires, J Chris ; Xiong, Zhiyong ; Leitch, Andrew R</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c728t-2ffd01ec1783ca1bccbc194376faaeb836fcc1334343028b0cbcb2433b12debd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2008</creationdate><topic>Aberration</topic><topic>Analysis</topic><topic>Asteraceae</topic><topic>Barley</topic><topic>Biological evolution</topic><topic>Biology</topic><topic>Biophysics</topic><topic>Chromosome rearrangements</topic><topic>Chromosome translocations</topic><topic>Chromosomes</topic><topic>Chromosomes, Plant</topic><topic>Cytogenetics</topic><topic>Deoxyribonucleic acid</topic><topic>Diploidy</topic><topic>Divergence</topic><topic>DNA</topic><topic>DNA methylation</topic><topic>DNA, Ribosomal - genetics</topic><topic>Epigenetics</topic><topic>Eukaryotes</topic><topic>Evolution</topic><topic>Evolution, Molecular</topic><topic>Evolutionary genetics</topic><topic>Fish populations</topic><topic>Fluorescence</topic><topic>Fluorescence in situ hybridization</topic><topic>Gene expression</topic><topic>Genetic markers</topic><topic>Genetic polymorphisms</topic><topic>Genetic research</topic><topic>Genetics</topic><topic>Genetics and Genomics/Genomics</topic><topic>Genetics and Genomics/Plant Genomes and Evolution</topic><topic>Genetics and Genomics/Population Genetics</topic><topic>Genome, Plant</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Heredity</topic><topic>Hybridization</topic><topic>In Situ Hybridization, Fluorescence</topic><topic>Karyotypes</topic><topic>Karyotyping</topic><topic>Life sciences</topic><topic>Meiosis</topic><topic>Meiosis - physiology</topic><topic>Mitosis - physiology</topic><topic>Mutation</topic><topic>Natural populations</topic><topic>Polymorphism</topic><topic>Polyploidy</topic><topic>Populations</topic><topic>Rape plants</topic><topic>Species</topic><topic>Tragopogon - anatomy &amp; histology</topic><topic>Tragopogon - genetics</topic><topic>Tragopogon dubius</topic><topic>Tragopogon mirus</topic><topic>Tragopogon miscellus</topic><topic>Tragopogon porrifolius</topic><topic>Trisomy</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lim, K Yoong</creatorcontrib><creatorcontrib>Soltis, Douglas E</creatorcontrib><creatorcontrib>Soltis, Pamela S</creatorcontrib><creatorcontrib>Tate, Jennifer</creatorcontrib><creatorcontrib>Matyasek, Roman</creatorcontrib><creatorcontrib>Srubarova, Hana</creatorcontrib><creatorcontrib>Kovarik, Ales</creatorcontrib><creatorcontrib>Pires, J Chris</creatorcontrib><creatorcontrib>Xiong, Zhiyong</creatorcontrib><creatorcontrib>Leitch, Andrew R</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing &amp; 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Indeed, most angiosperm species have undergone at least one round of polyploidy in their evolutionary history. Despite enormous progress in our understanding of many aspects of polyploidy, we essentially have no information about the role of chromosome divergence in the establishment of young polyploid populations. Here we investigate synthetic lines and natural populations of two recently and recurrently formed allotetraploids Tragopogon mirus and T. miscellus (formed within the past 80 years) to assess the role of aberrant meiosis in generating chromosomal/genomic diversity. That diversity is likely important in the formation, establishment and survival of polyploid populations and species. Applications of fluorescence in situ hybridisation (FISH) to natural populations of T. mirus and T. miscellus suggest that chromosomal rearrangements and other chromosomal changes are common in both allotetraploids. We detected extensive chromosomal polymorphism between individuals and populations, including (i) plants monosomic and trisomic for particular chromosomes (perhaps indicating compensatory trisomy), (ii) intergenomic translocations and (iii) variable sizes and expression patterns of individual ribosomal DNA (rDNA) loci. We even observed karyotypic variation among sibling plants. Significantly, translocations, chromosome loss, and meiotic irregularities, including quadrivalent formation, were observed in synthetic (S(0) and S(1) generations) polyploid lines. Our results not only provide a mechanism for chromosomal variation in natural populations, but also indicate that chromosomal changes occur rapidly following polyploidisation. These data shed new light on previous analyses of genome and transcriptome structures in de novo and establishing polyploid species. Crucially our results highlight the necessity of studying karyotypes in young (&lt;150 years old) polyploid species and synthetic polyploids that resemble natural species. The data also provide insight into the mechanisms that perturb inheritance patterns of genetic markers in synthetic polyploids and populations of young natural polyploid species.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>18843372</pmid><doi>10.1371/journal.pone.0003353</doi><tpages>e3353</tpages><oa>free_for_read</oa></addata></record>
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identifier ISSN: 1932-6203
ispartof PloS one, 2008-10, Vol.3 (10), p.e3353-e3353
issn 1932-6203
1932-6203
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source Public Library of Science (PLoS) Journals Open Access; MEDLINE; DOAJ Directory of Open Access Journals; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry
subjects Aberration
Analysis
Asteraceae
Barley
Biological evolution
Biology
Biophysics
Chromosome rearrangements
Chromosome translocations
Chromosomes
Chromosomes, Plant
Cytogenetics
Deoxyribonucleic acid
Diploidy
Divergence
DNA
DNA methylation
DNA, Ribosomal - genetics
Epigenetics
Eukaryotes
Evolution
Evolution, Molecular
Evolutionary genetics
Fish populations
Fluorescence
Fluorescence in situ hybridization
Gene expression
Genetic markers
Genetic polymorphisms
Genetic research
Genetics
Genetics and Genomics/Genomics
Genetics and Genomics/Plant Genomes and Evolution
Genetics and Genomics/Population Genetics
Genome, Plant
Genomes
Genomics
Heredity
Hybridization
In Situ Hybridization, Fluorescence
Karyotypes
Karyotyping
Life sciences
Meiosis
Meiosis - physiology
Mitosis - physiology
Mutation
Natural populations
Polymorphism
Polyploidy
Populations
Rape plants
Species
Tragopogon - anatomy & histology
Tragopogon - genetics
Tragopogon dubius
Tragopogon mirus
Tragopogon miscellus
Tragopogon porrifolius
Trisomy
title Rapid chromosome evolution in recently formed polyploids in Tragopogon (Asteraceae)
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