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Genome-wide analysis of tobacco NtTOM1/TOM3 gene family and identification of NtTOM1a/ NtTOM3a response to tobacco mosaic virus
TOBAMOVIRUS MULTIPLICATION 1 (TOM1) and its homolog TOBAMOVIRUS MULTIPLICATION 3 (TOM3) play a prominent role in the multiplication of tobacco mosaic virus (TMV) in higher plants. Although homologs of NtTOM1/TOM3 genes have been identified in several plant species, little is known about the characte...
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Published in: | BMC plant biology 2024-10, Vol.24 (1), p.942-942, Article 942 |
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description | TOBAMOVIRUS MULTIPLICATION 1 (TOM1) and its homolog TOBAMOVIRUS MULTIPLICATION 3 (TOM3) play a prominent role in the multiplication of tobacco mosaic virus (TMV) in higher plants. Although homologs of NtTOM1/TOM3 genes have been identified in several plant species, little is known about the characteristics and functions of NtTOM1/TOM3 at the genome-wide level in tobacco (Nicotiana tabacum L.).
In this study, we performed genome-wide identification and expression pattern analysis of the tobacco NtTOM1/TOM3 gene family. Twelve NtTOM1/TOM3 genes were identified and classified into four groups based on phylogenetic analysis. Sequence and conserved domain analyses showed that all these genes contained a specific DUF1084 domain. Expression pattern analysis showed that NtTOM1a, NtTOM1b, NtTOM1d, NtTOM3a, NtTOM3b, and NtTOM3d were induced by TMV at 1-, 3-, and 9 dpi, whereas the expression of other genes was not responsive to TMV at the early infection stage. TMV virion accumulation showed no obvious difference in either nttom1a or nttom3a mutants compared with the wild type. However, the virus propagation was significantly, but not completely, inhibited in the nttom1atom3a double mutant, indicating that other gene family members may function redundantly, such as NtTOM1b and NtTOM1d. In addition, overexpression of NtTOM1a or NtTOM3a also inhibited the TMV replication to some extent.
The present study performed genome-wide analysis of the NtTOM1/TOM3 gene family in tobacco, and identified NtTOM1a and NtTOM3a as important genes involved in TMV multiplication based on functional analysis. These results provide a theoretical basis for further improving TMV resistance in tobacco. |
doi_str_mv | 10.1186/s12870-024-05632-1 |
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In this study, we performed genome-wide identification and expression pattern analysis of the tobacco NtTOM1/TOM3 gene family. Twelve NtTOM1/TOM3 genes were identified and classified into four groups based on phylogenetic analysis. Sequence and conserved domain analyses showed that all these genes contained a specific DUF1084 domain. Expression pattern analysis showed that NtTOM1a, NtTOM1b, NtTOM1d, NtTOM3a, NtTOM3b, and NtTOM3d were induced by TMV at 1-, 3-, and 9 dpi, whereas the expression of other genes was not responsive to TMV at the early infection stage. TMV virion accumulation showed no obvious difference in either nttom1a or nttom3a mutants compared with the wild type. However, the virus propagation was significantly, but not completely, inhibited in the nttom1atom3a double mutant, indicating that other gene family members may function redundantly, such as NtTOM1b and NtTOM1d. In addition, overexpression of NtTOM1a or NtTOM3a also inhibited the TMV replication to some extent.
The present study performed genome-wide analysis of the NtTOM1/TOM3 gene family in tobacco, and identified NtTOM1a and NtTOM3a as important genes involved in TMV multiplication based on functional analysis. These results provide a theoretical basis for further improving TMV resistance in tobacco.</description><identifier>ISSN: 1471-2229</identifier><identifier>EISSN: 1471-2229</identifier><identifier>DOI: 10.1186/s12870-024-05632-1</identifier><identifier>PMID: 39385089</identifier><language>eng</language><publisher>England: BioMed Central Ltd</publisher><subject>Analysis ; Chloroplasts ; Chromosomes ; Conserved sequence ; Control ; CRISPR ; Diseases and pests ; domain ; Domains ; family ; Functional analysis ; Gene Expression Regulation, Plant ; Genes ; Genes, Plant ; Genetic aspects ; Genome, Plant ; Genome-Wide Association Study ; Genomes ; Genomic analysis ; Growth ; Identification and classification ; Infections ; Multigene Family ; Multiplication ; Mutants ; Mutation ; Nicotiana - genetics ; Nicotiana - virology ; Nicotiana tabacum ; Nucleotide sequence ; Pattern analysis ; Phylogenetics ; Phylogeny ; Plant Diseases - genetics ; Plant Diseases - virology ; Plant layout ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plant species ; Plant virus diseases ; Plant viruses ; Propagation ; Proteins ; species ; Tobacco ; Tobacco (Plant) ; Tobacco mosaic virus ; Tobacco Mosaic Virus - physiology ; Tobamovirus ; Tobamovirus multiplication protein ; TOM1 ; TOM3 ; virion ; Virions ; Viruses</subject><ispartof>BMC plant biology, 2024-10, Vol.24 (1), p.942-942, Article 942</ispartof><rights>2024. The Author(s).</rights><rights>COPYRIGHT 2024 BioMed Central Ltd.</rights><rights>2024. This work is licensed under http://creativecommons.org/licenses/by-nc-nd/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) 2024 2024</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c512t-9a9e899b55b1c2cb75ad5685ba057f4c6b1c66ce4f7b639d98c887f20c5229ab3</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/PMC11465672/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/3115126293?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,25731,27901,27902,36989,36990,44566,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39385089$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Xuebo</creatorcontrib><creatorcontrib>Bai, Yalin</creatorcontrib><creatorcontrib>Shen, Zhan</creatorcontrib><creatorcontrib>Zhang, Xinyao</creatorcontrib><creatorcontrib>Cai, Changchun</creatorcontrib><creatorcontrib>Qiao, Chan</creatorcontrib><creatorcontrib>Jiang, Caihong</creatorcontrib><creatorcontrib>Cheng, Lirui</creatorcontrib><creatorcontrib>Liu, Dan</creatorcontrib><creatorcontrib>Yang, Aiguo</creatorcontrib><title>Genome-wide analysis of tobacco NtTOM1/TOM3 gene family and identification of NtTOM1a/ NtTOM3a response to tobacco mosaic virus</title><title>BMC plant biology</title><addtitle>BMC Plant Biol</addtitle><description>TOBAMOVIRUS MULTIPLICATION 1 (TOM1) and its homolog TOBAMOVIRUS MULTIPLICATION 3 (TOM3) play a prominent role in the multiplication of tobacco mosaic virus (TMV) in higher plants. Although homologs of NtTOM1/TOM3 genes have been identified in several plant species, little is known about the characteristics and functions of NtTOM1/TOM3 at the genome-wide level in tobacco (Nicotiana tabacum L.).
In this study, we performed genome-wide identification and expression pattern analysis of the tobacco NtTOM1/TOM3 gene family. Twelve NtTOM1/TOM3 genes were identified and classified into four groups based on phylogenetic analysis. Sequence and conserved domain analyses showed that all these genes contained a specific DUF1084 domain. Expression pattern analysis showed that NtTOM1a, NtTOM1b, NtTOM1d, NtTOM3a, NtTOM3b, and NtTOM3d were induced by TMV at 1-, 3-, and 9 dpi, whereas the expression of other genes was not responsive to TMV at the early infection stage. TMV virion accumulation showed no obvious difference in either nttom1a or nttom3a mutants compared with the wild type. However, the virus propagation was significantly, but not completely, inhibited in the nttom1atom3a double mutant, indicating that other gene family members may function redundantly, such as NtTOM1b and NtTOM1d. In addition, overexpression of NtTOM1a or NtTOM3a also inhibited the TMV replication to some extent.
The present study performed genome-wide analysis of the NtTOM1/TOM3 gene family in tobacco, and identified NtTOM1a and NtTOM3a as important genes involved in TMV multiplication based on functional analysis. These results provide a theoretical basis for further improving TMV resistance in tobacco.</description><subject>Analysis</subject><subject>Chloroplasts</subject><subject>Chromosomes</subject><subject>Conserved sequence</subject><subject>Control</subject><subject>CRISPR</subject><subject>Diseases and pests</subject><subject>domain</subject><subject>Domains</subject><subject>family</subject><subject>Functional analysis</subject><subject>Gene Expression Regulation, Plant</subject><subject>Genes</subject><subject>Genes, Plant</subject><subject>Genetic aspects</subject><subject>Genome, Plant</subject><subject>Genome-Wide Association Study</subject><subject>Genomes</subject><subject>Genomic analysis</subject><subject>Growth</subject><subject>Identification and classification</subject><subject>Infections</subject><subject>Multigene Family</subject><subject>Multiplication</subject><subject>Mutants</subject><subject>Mutation</subject><subject>Nicotiana - genetics</subject><subject>Nicotiana - virology</subject><subject>Nicotiana tabacum</subject><subject>Nucleotide sequence</subject><subject>Pattern analysis</subject><subject>Phylogenetics</subject><subject>Phylogeny</subject><subject>Plant Diseases - genetics</subject><subject>Plant Diseases - virology</subject><subject>Plant layout</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plant species</subject><subject>Plant virus diseases</subject><subject>Plant viruses</subject><subject>Propagation</subject><subject>Proteins</subject><subject>species</subject><subject>Tobacco</subject><subject>Tobacco (Plant)</subject><subject>Tobacco mosaic virus</subject><subject>Tobacco Mosaic Virus - physiology</subject><subject>Tobamovirus</subject><subject>Tobamovirus multiplication protein</subject><subject>TOM1</subject><subject>TOM3</subject><subject>virion</subject><subject>Virions</subject><subject>Viruses</subject><issn>1471-2229</issn><issn>1471-2229</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNqNkktv1DAUhSMEomXgD7BAkdjAIh0_4tcKVRWUkQqVoKytG8cePEriYieFWfHX8TRl6CAWKJJj3Xzn2PfmFMVzjE4wlnyZMJECVYjUFWKckgo_KI5xLXBFCFEP7-2PiicpbRDCQtbqcXFEFZUMSXVc_Dy3Q-ht9d23toQBum3yqQyuHEMDxoTy43h1-QEv80LLtR1s6aD33TazbZk1w-idNzD6MOxUMw3LeUOhjDZdhyHZ7Le37EMCb8obH6f0tHjkoEv22d17UXx59_bq7H11cXm-Oju9qAzDZKwUKCuVahhrsCGmEQxaxiVrADHhasNzmXNjaycaTlWrpJFSOIIMy-1DQxfFavZtA2z0dfQ9xK0O4PVtIcS1hjh601ltVOOIaI0whNZGNmAVSGGt4UTx1pHs9Wb2up6a3rYmDyFCd2B6-GXwX_U63GiMa8642Dm8unOI4dtk06h7n4ztOhhsmJKmmFFZMyXRf6CYIcUkqjP68i90E6aY_-lMYZIboH-oNeRm_eBCvqPZmepTibEQdHf6ojj5B5Wf1vbehME6n-sHgtcHgsyM9se4hiklvfr86ZAlM2tiSClat58dRnoXbT1HW-do69toa5xFL-5PfS_5nWX6CwxB8Z0</recordid><startdate>20241010</startdate><enddate>20241010</enddate><creator>Wang, Xuebo</creator><creator>Bai, Yalin</creator><creator>Shen, Zhan</creator><creator>Zhang, Xinyao</creator><creator>Cai, Changchun</creator><creator>Qiao, Chan</creator><creator>Jiang, Caihong</creator><creator>Cheng, Lirui</creator><creator>Liu, Dan</creator><creator>Yang, Aiguo</creator><general>BioMed Central Ltd</general><general>BioMed Central</general><general>BMC</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>ISR</scope><scope>3V.</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20241010</creationdate><title>Genome-wide analysis of tobacco NtTOM1/TOM3 gene family and identification of NtTOM1a/ NtTOM3a response to tobacco mosaic virus</title><author>Wang, Xuebo ; Bai, Yalin ; Shen, Zhan ; Zhang, Xinyao ; Cai, Changchun ; Qiao, Chan ; Jiang, Caihong ; Cheng, Lirui ; Liu, Dan ; Yang, Aiguo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c512t-9a9e899b55b1c2cb75ad5685ba057f4c6b1c66ce4f7b639d98c887f20c5229ab3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Analysis</topic><topic>Chloroplasts</topic><topic>Chromosomes</topic><topic>Conserved sequence</topic><topic>Control</topic><topic>CRISPR</topic><topic>Diseases and pests</topic><topic>domain</topic><topic>Domains</topic><topic>family</topic><topic>Functional analysis</topic><topic>Gene Expression Regulation, Plant</topic><topic>Genes</topic><topic>Genes, Plant</topic><topic>Genetic aspects</topic><topic>Genome, Plant</topic><topic>Genome-Wide Association Study</topic><topic>Genomes</topic><topic>Genomic analysis</topic><topic>Growth</topic><topic>Identification and classification</topic><topic>Infections</topic><topic>Multigene Family</topic><topic>Multiplication</topic><topic>Mutants</topic><topic>Mutation</topic><topic>Nicotiana - genetics</topic><topic>Nicotiana - virology</topic><topic>Nicotiana tabacum</topic><topic>Nucleotide sequence</topic><topic>Pattern analysis</topic><topic>Phylogenetics</topic><topic>Phylogeny</topic><topic>Plant Diseases - genetics</topic><topic>Plant Diseases - virology</topic><topic>Plant layout</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plant species</topic><topic>Plant virus diseases</topic><topic>Plant viruses</topic><topic>Propagation</topic><topic>Proteins</topic><topic>species</topic><topic>Tobacco</topic><topic>Tobacco (Plant)</topic><topic>Tobacco mosaic virus</topic><topic>Tobacco Mosaic Virus - physiology</topic><topic>Tobamovirus</topic><topic>Tobamovirus multiplication protein</topic><topic>TOM1</topic><topic>TOM3</topic><topic>virion</topic><topic>Virions</topic><topic>Viruses</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wang, Xuebo</creatorcontrib><creatorcontrib>Bai, Yalin</creatorcontrib><creatorcontrib>Shen, Zhan</creatorcontrib><creatorcontrib>Zhang, Xinyao</creatorcontrib><creatorcontrib>Cai, Changchun</creatorcontrib><creatorcontrib>Qiao, Chan</creatorcontrib><creatorcontrib>Jiang, Caihong</creatorcontrib><creatorcontrib>Cheng, Lirui</creatorcontrib><creatorcontrib>Liu, Dan</creatorcontrib><creatorcontrib>Yang, Aiguo</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: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Agricultural Science Collection</collection><collection>ProQuest - 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Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>BMC plant biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Xuebo</au><au>Bai, Yalin</au><au>Shen, Zhan</au><au>Zhang, Xinyao</au><au>Cai, Changchun</au><au>Qiao, Chan</au><au>Jiang, Caihong</au><au>Cheng, Lirui</au><au>Liu, Dan</au><au>Yang, Aiguo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genome-wide analysis of tobacco NtTOM1/TOM3 gene family and identification of NtTOM1a/ NtTOM3a response to tobacco mosaic virus</atitle><jtitle>BMC plant biology</jtitle><addtitle>BMC Plant Biol</addtitle><date>2024-10-10</date><risdate>2024</risdate><volume>24</volume><issue>1</issue><spage>942</spage><epage>942</epage><pages>942-942</pages><artnum>942</artnum><issn>1471-2229</issn><eissn>1471-2229</eissn><abstract>TOBAMOVIRUS MULTIPLICATION 1 (TOM1) and its homolog TOBAMOVIRUS MULTIPLICATION 3 (TOM3) play a prominent role in the multiplication of tobacco mosaic virus (TMV) in higher plants. Although homologs of NtTOM1/TOM3 genes have been identified in several plant species, little is known about the characteristics and functions of NtTOM1/TOM3 at the genome-wide level in tobacco (Nicotiana tabacum L.).
In this study, we performed genome-wide identification and expression pattern analysis of the tobacco NtTOM1/TOM3 gene family. Twelve NtTOM1/TOM3 genes were identified and classified into four groups based on phylogenetic analysis. Sequence and conserved domain analyses showed that all these genes contained a specific DUF1084 domain. Expression pattern analysis showed that NtTOM1a, NtTOM1b, NtTOM1d, NtTOM3a, NtTOM3b, and NtTOM3d were induced by TMV at 1-, 3-, and 9 dpi, whereas the expression of other genes was not responsive to TMV at the early infection stage. TMV virion accumulation showed no obvious difference in either nttom1a or nttom3a mutants compared with the wild type. However, the virus propagation was significantly, but not completely, inhibited in the nttom1atom3a double mutant, indicating that other gene family members may function redundantly, such as NtTOM1b and NtTOM1d. In addition, overexpression of NtTOM1a or NtTOM3a also inhibited the TMV replication to some extent.
The present study performed genome-wide analysis of the NtTOM1/TOM3 gene family in tobacco, and identified NtTOM1a and NtTOM3a as important genes involved in TMV multiplication based on functional analysis. These results provide a theoretical basis for further improving TMV resistance in tobacco.</abstract><cop>England</cop><pub>BioMed Central Ltd</pub><pmid>39385089</pmid><doi>10.1186/s12870-024-05632-1</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Analysis Chloroplasts Chromosomes Conserved sequence Control CRISPR Diseases and pests domain Domains family Functional analysis Gene Expression Regulation, Plant Genes Genes, Plant Genetic aspects Genome, Plant Genome-Wide Association Study Genomes Genomic analysis Growth Identification and classification Infections Multigene Family Multiplication Mutants Mutation Nicotiana - genetics Nicotiana - virology Nicotiana tabacum Nucleotide sequence Pattern analysis Phylogenetics Phylogeny Plant Diseases - genetics Plant Diseases - virology Plant layout Plant Proteins - genetics Plant Proteins - metabolism Plant species Plant virus diseases Plant viruses Propagation Proteins species Tobacco Tobacco (Plant) Tobacco mosaic virus Tobacco Mosaic Virus - physiology Tobamovirus Tobamovirus multiplication protein TOM1 TOM3 virion Virions Viruses |
title | Genome-wide analysis of tobacco NtTOM1/TOM3 gene family and identification of NtTOM1a/ NtTOM3a response to tobacco mosaic virus |
url | http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-01T13%3A43%3A47IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_doaj_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Genome-wide%20analysis%20of%20tobacco%20NtTOM1/TOM3%20gene%20family%20and%20identification%20of%20NtTOM1a/%20NtTOM3a%20response%20to%20tobacco%20mosaic%20virus&rft.jtitle=BMC%20plant%20biology&rft.au=Wang,%20Xuebo&rft.date=2024-10-10&rft.volume=24&rft.issue=1&rft.spage=942&rft.epage=942&rft.pages=942-942&rft.artnum=942&rft.issn=1471-2229&rft.eissn=1471-2229&rft_id=info:doi/10.1186/s12870-024-05632-1&rft_dat=%3Cgale_doaj_%3EA811773315%3C/gale_doaj_%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c512t-9a9e899b55b1c2cb75ad5685ba057f4c6b1c66ce4f7b639d98c887f20c5229ab3%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=3115126293&rft_id=info:pmid/39385089&rft_galeid=A811773315&rfr_iscdi=true |