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...
Gespeichert in:
Veröffentlicht in: | Genome biology and evolution 2024-09, Vol.16 (9) |
---|---|
Hauptverfasser: | , , , , , , , |
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 & 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 |