Correlation Between Subgenome-biased DNA Loss and DNA Transposon Activation Following Hybridization in the Allotetraploid Xenopus Frogs

Abstract In certain tetraploid species resulting from interspecific hybridization, one parent's subgenome is known to selectively undergo DNA loss. The molecular mechanisms behind this remain unclear. In our study, we compared the genomes of a standard diploid species with two allotetraploid sp...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Genome biology and evolution 2024-09, Vol.16 (9)
Hauptverfasser: Suda, Kosuke, Suzuki, Takahiro, Hayashi, Shun, Okuyama, Honoka, Tsukamoto, Daisuke, Matsuo, Takuya, Tamura, Kei, Ito, Michihiko
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page
container_issue 9
container_start_page
container_title Genome biology and evolution
container_volume 16
creator Suda, Kosuke
Suzuki, Takahiro
Hayashi, Shun
Okuyama, Honoka
Tsukamoto, Daisuke
Matsuo, Takuya
Tamura, Kei
Ito, Michihiko
description Abstract In certain tetraploid species resulting from interspecific hybridization, one parent's subgenome is known to selectively undergo DNA loss. The molecular mechanisms behind this remain unclear. In our study, we compared the genomes of a standard diploid species with two allotetraploid species from the Xenopus genus, both possessing L (longer) and S (shorter) homoeologous subgenomes. We observed substantial gene losses and intergenic DNA deletions in both the S and L subgenomes of the tetraploid species. Gene losses were around 1,000 to 3,000 for L and 4,000 to 6,000 for S, with especially prominent losses in the S subgenome. Many of these losses likely occurred shortly after interspecific hybridization in both L/S subgenomes. We also deduced frequent large inversions in the S subgenome. Upon reassessing transposon dynamics using updated genome databases, we reaffirmed heightened DNA transposon activity during the hybridization, as previously reported. We next investigated whether S subgenome-biased DNA loss could be correlated with the activation of DNA transposons following hybridization. Notably, distinct patterns were observed in the dynamics of DNA transposons between the L and S subgenomes. Several DNA transposon subfamilies correlated positively with DNA deletions in the S subgenome and negatively in the L subgenome. Based on these results, we propose a model that, upon and after hybridization between two related diploid Xenopus species, the mixture of their genomes resulted in the derepression of DNA transposons, especially in the S subgenome, leading to selective DNA loss in the S subgenome.
doi_str_mv 10.1093/gbe/evae179
format Article
fullrecord <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_11415220</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><oup_id>10.1093/gbe/evae179</oup_id><sourcerecordid>3113482880</sourcerecordid><originalsourceid>FETCH-LOGICAL-c292t-54719923878e52b0f858bbfa27a73918ac2fe0506c6a1f7b40f5cc9d8d609e983</originalsourceid><addsrcrecordid>eNp9kUtv1DAUhS0EoqWwYo8sISEkFOpHHvYKDQNDkUawoEjsLNu5SV1l7NROpip_gL-NqwxVYcHKj_vd43N9EHpOyVtKJD_tDZzCXgNt5AN0TJtKFnVd8Yf39kfoSUqXhNR1WfPH6IhLTkoq5DH6tQ4xwqAnFzx-D9M1gMffZtODDzsojNMJWvzhywpvQ0pY--VwHrVPY0i5aWUnt1_6N2EYwrXzPT67MdG17udy7zyeLgCvcnWCKepxCK7FP_IT45zwJoY-PUWPOj0keHZYT9D3zcfz9Vmx_frp83q1LSyTbCqqsqFSMi4aARUzpBOVMKbTrNENl1RoyzogFaltrWnXmJJ0lbWyFW1NJEjBT9C7RXeczQ5aCz77GdQY3U7HGxW0U39XvLtQfdgrSktaMUaywuuDQgxXM6RJ7VyyMAzaQ5iT4pQ02QCVPKMv_0Evwxx9ni9TlJeCCXEr-GahbMxfHKG7c0OJuk1Y5YTVIeFMv7g_wB37J9IMvFqAMI__VfoNCLCx4Q</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>3113482880</pqid></control><display><type>article</type><title>Correlation Between Subgenome-biased DNA Loss and DNA Transposon Activation Following Hybridization in the Allotetraploid Xenopus Frogs</title><source>Oxford Journals Open Access Collection</source><source>MEDLINE</source><source>DOAJ Directory of Open Access Journals</source><source>EZB-FREE-00999 freely available EZB journals</source><source>PubMed Central</source><creator>Suda, Kosuke ; Suzuki, Takahiro ; Hayashi, Shun ; Okuyama, Honoka ; Tsukamoto, Daisuke ; Matsuo, Takuya ; Tamura, Kei ; Ito, Michihiko</creator><creatorcontrib>Suda, Kosuke ; Suzuki, Takahiro ; Hayashi, Shun ; Okuyama, Honoka ; Tsukamoto, Daisuke ; Matsuo, Takuya ; Tamura, Kei ; Ito, Michihiko</creatorcontrib><description>Abstract In certain tetraploid species resulting from interspecific hybridization, one parent's subgenome is known to selectively undergo DNA loss. The molecular mechanisms behind this remain unclear. In our study, we compared the genomes of a standard diploid species with two allotetraploid species from the Xenopus genus, both possessing L (longer) and S (shorter) homoeologous subgenomes. We observed substantial gene losses and intergenic DNA deletions in both the S and L subgenomes of the tetraploid species. Gene losses were around 1,000 to 3,000 for L and 4,000 to 6,000 for S, with especially prominent losses in the S subgenome. Many of these losses likely occurred shortly after interspecific hybridization in both L/S subgenomes. We also deduced frequent large inversions in the S subgenome. Upon reassessing transposon dynamics using updated genome databases, we reaffirmed heightened DNA transposon activity during the hybridization, as previously reported. We next investigated whether S subgenome-biased DNA loss could be correlated with the activation of DNA transposons following hybridization. Notably, distinct patterns were observed in the dynamics of DNA transposons between the L and S subgenomes. Several DNA transposon subfamilies correlated positively with DNA deletions in the S subgenome and negatively in the L subgenome. Based on these results, we propose a model that, upon and after hybridization between two related diploid Xenopus species, the mixture of their genomes resulted in the derepression of DNA transposons, especially in the S subgenome, leading to selective DNA loss in the S subgenome.</description><identifier>ISSN: 1759-6653</identifier><identifier>EISSN: 1759-6653</identifier><identifier>DOI: 10.1093/gbe/evae179</identifier><identifier>PMID: 39304189</identifier><language>eng</language><publisher>UK: Oxford University Press</publisher><subject>Animals ; Deoxyribonucleic acid ; Derepression ; Diploids ; DNA ; DNA Transposable Elements ; Evolution, Molecular ; Genome ; Genomes ; Hybridization ; Hybridization, Genetic ; Interspecific hybridization ; Molecular modelling ; Species ; Tetraploidy ; Transposons ; Xenopus ; Xenopus - genetics</subject><ispartof>Genome biology and evolution, 2024-09, Vol.16 (9)</ispartof><rights>The Author(s) 2024. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution. 2024</rights><rights>The Author(s) 2024. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.</rights><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c292t-54719923878e52b0f858bbfa27a73918ac2fe0506c6a1f7b40f5cc9d8d609e983</cites><orcidid>0000-0002-8030-2361 ; 0000-0001-6195-5984 ; 0000-0003-1881-6916 ; 0009-0000-5792-6064 ; 0009-0005-4508-6498 ; 0000-0001-8960-4975 ; 0009-0000-4772-344X ; 0009-0002-4795-4293</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/PMC11415220/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11415220/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,1598,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39304189$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Suda, Kosuke</creatorcontrib><creatorcontrib>Suzuki, Takahiro</creatorcontrib><creatorcontrib>Hayashi, Shun</creatorcontrib><creatorcontrib>Okuyama, Honoka</creatorcontrib><creatorcontrib>Tsukamoto, Daisuke</creatorcontrib><creatorcontrib>Matsuo, Takuya</creatorcontrib><creatorcontrib>Tamura, Kei</creatorcontrib><creatorcontrib>Ito, Michihiko</creatorcontrib><title>Correlation Between Subgenome-biased DNA Loss and DNA Transposon Activation Following Hybridization in the Allotetraploid Xenopus Frogs</title><title>Genome biology and evolution</title><addtitle>Genome Biol Evol</addtitle><description>Abstract In certain tetraploid species resulting from interspecific hybridization, one parent's subgenome is known to selectively undergo DNA loss. The molecular mechanisms behind this remain unclear. In our study, we compared the genomes of a standard diploid species with two allotetraploid species from the Xenopus genus, both possessing L (longer) and S (shorter) homoeologous subgenomes. We observed substantial gene losses and intergenic DNA deletions in both the S and L subgenomes of the tetraploid species. Gene losses were around 1,000 to 3,000 for L and 4,000 to 6,000 for S, with especially prominent losses in the S subgenome. Many of these losses likely occurred shortly after interspecific hybridization in both L/S subgenomes. We also deduced frequent large inversions in the S subgenome. Upon reassessing transposon dynamics using updated genome databases, we reaffirmed heightened DNA transposon activity during the hybridization, as previously reported. We next investigated whether S subgenome-biased DNA loss could be correlated with the activation of DNA transposons following hybridization. Notably, distinct patterns were observed in the dynamics of DNA transposons between the L and S subgenomes. Several DNA transposon subfamilies correlated positively with DNA deletions in the S subgenome and negatively in the L subgenome. Based on these results, we propose a model that, upon and after hybridization between two related diploid Xenopus species, the mixture of their genomes resulted in the derepression of DNA transposons, especially in the S subgenome, leading to selective DNA loss in the S subgenome.</description><subject>Animals</subject><subject>Deoxyribonucleic acid</subject><subject>Derepression</subject><subject>Diploids</subject><subject>DNA</subject><subject>DNA Transposable Elements</subject><subject>Evolution, Molecular</subject><subject>Genome</subject><subject>Genomes</subject><subject>Hybridization</subject><subject>Hybridization, Genetic</subject><subject>Interspecific hybridization</subject><subject>Molecular modelling</subject><subject>Species</subject><subject>Tetraploidy</subject><subject>Transposons</subject><subject>Xenopus</subject><subject>Xenopus - genetics</subject><issn>1759-6653</issn><issn>1759-6653</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><sourceid>EIF</sourceid><recordid>eNp9kUtv1DAUhS0EoqWwYo8sISEkFOpHHvYKDQNDkUawoEjsLNu5SV1l7NROpip_gL-NqwxVYcHKj_vd43N9EHpOyVtKJD_tDZzCXgNt5AN0TJtKFnVd8Yf39kfoSUqXhNR1WfPH6IhLTkoq5DH6tQ4xwqAnFzx-D9M1gMffZtODDzsojNMJWvzhywpvQ0pY--VwHrVPY0i5aWUnt1_6N2EYwrXzPT67MdG17udy7zyeLgCvcnWCKepxCK7FP_IT45zwJoY-PUWPOj0keHZYT9D3zcfz9Vmx_frp83q1LSyTbCqqsqFSMi4aARUzpBOVMKbTrNENl1RoyzogFaltrWnXmJJ0lbWyFW1NJEjBT9C7RXeczQ5aCz77GdQY3U7HGxW0U39XvLtQfdgrSktaMUaywuuDQgxXM6RJ7VyyMAzaQ5iT4pQ02QCVPKMv_0Evwxx9ni9TlJeCCXEr-GahbMxfHKG7c0OJuk1Y5YTVIeFMv7g_wB37J9IMvFqAMI__VfoNCLCx4Q</recordid><startdate>20240903</startdate><enddate>20240903</enddate><creator>Suda, Kosuke</creator><creator>Suzuki, Takahiro</creator><creator>Hayashi, Shun</creator><creator>Okuyama, Honoka</creator><creator>Tsukamoto, Daisuke</creator><creator>Matsuo, Takuya</creator><creator>Tamura, Kei</creator><creator>Ito, Michihiko</creator><general>Oxford University Press</general><scope>TOX</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>K9.</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-8030-2361</orcidid><orcidid>https://orcid.org/0000-0001-6195-5984</orcidid><orcidid>https://orcid.org/0000-0003-1881-6916</orcidid><orcidid>https://orcid.org/0009-0000-5792-6064</orcidid><orcidid>https://orcid.org/0009-0005-4508-6498</orcidid><orcidid>https://orcid.org/0000-0001-8960-4975</orcidid><orcidid>https://orcid.org/0009-0000-4772-344X</orcidid><orcidid>https://orcid.org/0009-0002-4795-4293</orcidid></search><sort><creationdate>20240903</creationdate><title>Correlation Between Subgenome-biased DNA Loss and DNA Transposon Activation Following Hybridization in the Allotetraploid Xenopus Frogs</title><author>Suda, Kosuke ; Suzuki, Takahiro ; Hayashi, Shun ; Okuyama, Honoka ; Tsukamoto, Daisuke ; Matsuo, Takuya ; Tamura, Kei ; Ito, Michihiko</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c292t-54719923878e52b0f858bbfa27a73918ac2fe0506c6a1f7b40f5cc9d8d609e983</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Animals</topic><topic>Deoxyribonucleic acid</topic><topic>Derepression</topic><topic>Diploids</topic><topic>DNA</topic><topic>DNA Transposable Elements</topic><topic>Evolution, Molecular</topic><topic>Genome</topic><topic>Genomes</topic><topic>Hybridization</topic><topic>Hybridization, Genetic</topic><topic>Interspecific hybridization</topic><topic>Molecular modelling</topic><topic>Species</topic><topic>Tetraploidy</topic><topic>Transposons</topic><topic>Xenopus</topic><topic>Xenopus - genetics</topic><toplevel>online_resources</toplevel><creatorcontrib>Suda, Kosuke</creatorcontrib><creatorcontrib>Suzuki, Takahiro</creatorcontrib><creatorcontrib>Hayashi, Shun</creatorcontrib><creatorcontrib>Okuyama, Honoka</creatorcontrib><creatorcontrib>Tsukamoto, Daisuke</creatorcontrib><creatorcontrib>Matsuo, Takuya</creatorcontrib><creatorcontrib>Tamura, Kei</creatorcontrib><creatorcontrib>Ito, Michihiko</creatorcontrib><collection>Oxford Journals Open Access Collection</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Genome biology and evolution</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Suda, Kosuke</au><au>Suzuki, Takahiro</au><au>Hayashi, Shun</au><au>Okuyama, Honoka</au><au>Tsukamoto, Daisuke</au><au>Matsuo, Takuya</au><au>Tamura, Kei</au><au>Ito, Michihiko</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Correlation Between Subgenome-biased DNA Loss and DNA Transposon Activation Following Hybridization in the Allotetraploid Xenopus Frogs</atitle><jtitle>Genome biology and evolution</jtitle><addtitle>Genome Biol Evol</addtitle><date>2024-09-03</date><risdate>2024</risdate><volume>16</volume><issue>9</issue><issn>1759-6653</issn><eissn>1759-6653</eissn><abstract>Abstract In certain tetraploid species resulting from interspecific hybridization, one parent's subgenome is known to selectively undergo DNA loss. The molecular mechanisms behind this remain unclear. In our study, we compared the genomes of a standard diploid species with two allotetraploid species from the Xenopus genus, both possessing L (longer) and S (shorter) homoeologous subgenomes. We observed substantial gene losses and intergenic DNA deletions in both the S and L subgenomes of the tetraploid species. Gene losses were around 1,000 to 3,000 for L and 4,000 to 6,000 for S, with especially prominent losses in the S subgenome. Many of these losses likely occurred shortly after interspecific hybridization in both L/S subgenomes. We also deduced frequent large inversions in the S subgenome. Upon reassessing transposon dynamics using updated genome databases, we reaffirmed heightened DNA transposon activity during the hybridization, as previously reported. We next investigated whether S subgenome-biased DNA loss could be correlated with the activation of DNA transposons following hybridization. Notably, distinct patterns were observed in the dynamics of DNA transposons between the L and S subgenomes. Several DNA transposon subfamilies correlated positively with DNA deletions in the S subgenome and negatively in the L subgenome. Based on these results, we propose a model that, upon and after hybridization between two related diploid Xenopus species, the mixture of their genomes resulted in the derepression of DNA transposons, especially in the S subgenome, leading to selective DNA loss in the S subgenome.</abstract><cop>UK</cop><pub>Oxford University Press</pub><pmid>39304189</pmid><doi>10.1093/gbe/evae179</doi><orcidid>https://orcid.org/0000-0002-8030-2361</orcidid><orcidid>https://orcid.org/0000-0001-6195-5984</orcidid><orcidid>https://orcid.org/0000-0003-1881-6916</orcidid><orcidid>https://orcid.org/0009-0000-5792-6064</orcidid><orcidid>https://orcid.org/0009-0005-4508-6498</orcidid><orcidid>https://orcid.org/0000-0001-8960-4975</orcidid><orcidid>https://orcid.org/0009-0000-4772-344X</orcidid><orcidid>https://orcid.org/0009-0002-4795-4293</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 1759-6653
ispartof Genome biology and evolution, 2024-09, Vol.16 (9)
issn 1759-6653
1759-6653
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_11415220
source Oxford Journals Open Access Collection; MEDLINE; DOAJ Directory of Open Access Journals; EZB-FREE-00999 freely available EZB journals; PubMed Central
subjects Animals
Deoxyribonucleic acid
Derepression
Diploids
DNA
DNA Transposable Elements
Evolution, Molecular
Genome
Genomes
Hybridization
Hybridization, Genetic
Interspecific hybridization
Molecular modelling
Species
Tetraploidy
Transposons
Xenopus
Xenopus - genetics
title Correlation Between Subgenome-biased DNA Loss and DNA Transposon Activation Following Hybridization in the Allotetraploid Xenopus Frogs
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-05T15%3A01%3A40IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Correlation%20Between%20Subgenome-biased%20DNA%20Loss%20and%20DNA%20Transposon%20Activation%20Following%20Hybridization%20in%20the%20Allotetraploid%20Xenopus%20Frogs&rft.jtitle=Genome%20biology%20and%20evolution&rft.au=Suda,%20Kosuke&rft.date=2024-09-03&rft.volume=16&rft.issue=9&rft.issn=1759-6653&rft.eissn=1759-6653&rft_id=info:doi/10.1093/gbe/evae179&rft_dat=%3Cproquest_pubme%3E3113482880%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=3113482880&rft_id=info:pmid/39304189&rft_oup_id=10.1093/gbe/evae179&rfr_iscdi=true