Chromosome‐scale genome assembly‐assisted identification of Mi‐9 gene in Solanum arcanum accession LA2157, conferring heat‐stable resistance to Meloidogyne incognita
Summary Root‐knot nematodes (RKNs) are infamous plant pathogens in tomato production, causing considerable losses in agriculture worldwide. Mi‐1 is the only commercially available RKN‐resistance gene; however, the resistance is inactivated when the soil temperature is over 28 °C. Mi‐9 in wild tomato...
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| Veröffentlicht in: | Plant biotechnology journal 2023-07, Vol.21 (7), p.1496-1509 |
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| creator | Jiang, Lijun Ling, Jian Zhao, Jianlong Yang, Yu Yang, Yuhong Li, Yan Jiao, Yang Mao, Zhenchuan Wang, Yunsheng Xie, Bingyan |
| description | Summary
Root‐knot nematodes (RKNs) are infamous plant pathogens in tomato production, causing considerable losses in agriculture worldwide. Mi‐1 is the only commercially available RKN‐resistance gene; however, the resistance is inactivated when the soil temperature is over 28 °C. Mi‐9 in wild tomato (Solanum arcanum LA2157) has stable resistance to RKNs under high temperature but has not been cloned and applied. In this study, a chromosome‐scale genome assembly of S. arcanum LA2157 was constructed through Nanopore and Hi‐C sequencing. Based on molecular markers of Mi‐9 and comparative genomic analysis, the localization region and candidate Mi‐9 genes cluster consisting of seven nucleotide‐binding sites and leucine‐rich repeat (NBS‐LRR) genes were located. Transcriptional expression profiles confirmed that five of the seven candidate genes were expressed in root tissue. Moreover, virus‐induced gene silencing of the Sarc_034200 gene resulted in increased susceptibility of S. arcanum LA2157 to Meloidogyne incognita, and genetic transformation of the Sarc_034200 gene in susceptible Solanum pimpinellifolium conferred significant resistance to M. incognita at 25 °C and 30 °C and showed hypersensitive responses at nematode infection sites. This suggested that Sarc_034200 is the Mi‐9 gene. In summary, we cloned, confirmed and applied the heat‐stable RKN‐resistance gene Mi‐9, which is of great significance to tomato breeding for nematode resistance. |
| doi_str_mv | 10.1111/pbi.14055 |
| format | Article |
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Root‐knot nematodes (RKNs) are infamous plant pathogens in tomato production, causing considerable losses in agriculture worldwide. Mi‐1 is the only commercially available RKN‐resistance gene; however, the resistance is inactivated when the soil temperature is over 28 °C. Mi‐9 in wild tomato (Solanum arcanum LA2157) has stable resistance to RKNs under high temperature but has not been cloned and applied. In this study, a chromosome‐scale genome assembly of S. arcanum LA2157 was constructed through Nanopore and Hi‐C sequencing. Based on molecular markers of Mi‐9 and comparative genomic analysis, the localization region and candidate Mi‐9 genes cluster consisting of seven nucleotide‐binding sites and leucine‐rich repeat (NBS‐LRR) genes were located. Transcriptional expression profiles confirmed that five of the seven candidate genes were expressed in root tissue. Moreover, virus‐induced gene silencing of the Sarc_034200 gene resulted in increased susceptibility of S. arcanum LA2157 to Meloidogyne incognita, and genetic transformation of the Sarc_034200 gene in susceptible Solanum pimpinellifolium conferred significant resistance to M. incognita at 25 °C and 30 °C and showed hypersensitive responses at nematode infection sites. This suggested that Sarc_034200 is the Mi‐9 gene. In summary, we cloned, confirmed and applied the heat‐stable RKN‐resistance gene Mi‐9, which is of great significance to tomato breeding for nematode resistance.</description><identifier>ISSN: 1467-7644</identifier><identifier>EISSN: 1467-7652</identifier><identifier>DOI: 10.1111/pbi.14055</identifier><identifier>PMID: 37074757</identifier><language>eng</language><publisher>England: John Wiley & Sons, Inc</publisher><subject>Agricultural production ; Animals ; Artificial chromosomes ; Assembly ; Binding sites ; Chromosomes ; Chromosomes - metabolism ; Cloning ; Flowers & plants ; Gene expression ; Gene silencing ; Genes ; genome assembly ; Genomes ; Genomic analysis ; Genomics ; Heat ; Heat resistance ; High temperature ; Hi‐C ; Hot Temperature ; Leucine ; Localization ; Meloidogyne incognita ; Mi‐9 ; NBS-LRR gene ; Nematodes ; Nucleotides ; Pest resistance ; Plant Breeding ; Plant Diseases - genetics ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plant Roots - genetics ; Plant tissues ; Soil temperature ; Solanum - genetics ; Solanum arcanum ; Solanum arcanum LA2157 ; Solanum lycopersicum - genetics ; Thermal stability ; tomato genetic transformation ; Tomatoes ; Tylenchoidea ; VIGS</subject><ispartof>Plant biotechnology journal, 2023-07, Vol.21 (7), p.1496-1509</ispartof><rights>2023 The Authors. published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.</rights><rights>2023 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.</rights><rights>2023. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4445-4d417ac965bcc14dbb803471fba2194b9b0d3d8aa0afbc37b88c3e7262b171083</citedby><cites>FETCH-LOGICAL-c4445-4d417ac965bcc14dbb803471fba2194b9b0d3d8aa0afbc37b88c3e7262b171083</cites><orcidid>0000-0002-1035-7711 ; 0000-0002-6667-1179 ; 0000-0001-5003-4434 ; 0000-0002-8831-6020 ; 0000-0001-9640-8956 ; 0000-0002-4841-9543 ; 0000-0002-5311-8809 ; 0000-0002-8179-6885 ; 0000-0002-7605-5732</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fpbi.14055$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fpbi.14055$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,780,784,864,885,1417,11562,27924,27925,45574,45575,46052,46476</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37074757$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Jiang, Lijun</creatorcontrib><creatorcontrib>Ling, Jian</creatorcontrib><creatorcontrib>Zhao, Jianlong</creatorcontrib><creatorcontrib>Yang, Yu</creatorcontrib><creatorcontrib>Yang, Yuhong</creatorcontrib><creatorcontrib>Li, Yan</creatorcontrib><creatorcontrib>Jiao, Yang</creatorcontrib><creatorcontrib>Mao, Zhenchuan</creatorcontrib><creatorcontrib>Wang, Yunsheng</creatorcontrib><creatorcontrib>Xie, Bingyan</creatorcontrib><title>Chromosome‐scale genome assembly‐assisted identification of Mi‐9 gene in Solanum arcanum accession LA2157, conferring heat‐stable resistance to Meloidogyne incognita</title><title>Plant biotechnology journal</title><addtitle>Plant Biotechnol J</addtitle><description>Summary
Root‐knot nematodes (RKNs) are infamous plant pathogens in tomato production, causing considerable losses in agriculture worldwide. Mi‐1 is the only commercially available RKN‐resistance gene; however, the resistance is inactivated when the soil temperature is over 28 °C. Mi‐9 in wild tomato (Solanum arcanum LA2157) has stable resistance to RKNs under high temperature but has not been cloned and applied. In this study, a chromosome‐scale genome assembly of S. arcanum LA2157 was constructed through Nanopore and Hi‐C sequencing. Based on molecular markers of Mi‐9 and comparative genomic analysis, the localization region and candidate Mi‐9 genes cluster consisting of seven nucleotide‐binding sites and leucine‐rich repeat (NBS‐LRR) genes were located. Transcriptional expression profiles confirmed that five of the seven candidate genes were expressed in root tissue. Moreover, virus‐induced gene silencing of the Sarc_034200 gene resulted in increased susceptibility of S. arcanum LA2157 to Meloidogyne incognita, and genetic transformation of the Sarc_034200 gene in susceptible Solanum pimpinellifolium conferred significant resistance to M. incognita at 25 °C and 30 °C and showed hypersensitive responses at nematode infection sites. This suggested that Sarc_034200 is the Mi‐9 gene. In summary, we cloned, confirmed and applied the heat‐stable RKN‐resistance gene Mi‐9, which is of great significance to tomato breeding for nematode resistance.</description><subject>Agricultural production</subject><subject>Animals</subject><subject>Artificial chromosomes</subject><subject>Assembly</subject><subject>Binding sites</subject><subject>Chromosomes</subject><subject>Chromosomes - metabolism</subject><subject>Cloning</subject><subject>Flowers & plants</subject><subject>Gene expression</subject><subject>Gene silencing</subject><subject>Genes</subject><subject>genome assembly</subject><subject>Genomes</subject><subject>Genomic analysis</subject><subject>Genomics</subject><subject>Heat</subject><subject>Heat resistance</subject><subject>High temperature</subject><subject>Hi‐C</subject><subject>Hot Temperature</subject><subject>Leucine</subject><subject>Localization</subject><subject>Meloidogyne incognita</subject><subject>Mi‐9</subject><subject>NBS-LRR gene</subject><subject>Nematodes</subject><subject>Nucleotides</subject><subject>Pest resistance</subject><subject>Plant Breeding</subject><subject>Plant Diseases - genetics</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plant Roots - genetics</subject><subject>Plant tissues</subject><subject>Soil temperature</subject><subject>Solanum - genetics</subject><subject>Solanum arcanum</subject><subject>Solanum arcanum LA2157</subject><subject>Solanum lycopersicum - genetics</subject><subject>Thermal stability</subject><subject>tomato genetic transformation</subject><subject>Tomatoes</subject><subject>Tylenchoidea</subject><subject>VIGS</subject><issn>1467-7644</issn><issn>1467-7652</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp1ks1u1DAQxy0EoqVw4AWQJS5UYlt_JU5OqKz4qLQVSMDZsp1J1lVib-2Eam88Ai_CS_EkeDdlBUj4MrbnN_-ZsQehp5Sc0bzON8adUUGK4h46pqKUC1kW7P5hL8QRepTSNSGMlkX5EB1xSaSQhTxGP5brGIaQwgA_v31PVveAO_D5iHVKMJh-m-_z1qURGuwa8KNrndWjCx6HFl-57K93MYCdx59Cr_00YB3tbK2FHJzZ1QWjhXyJbfAtxOh8h9egx13WUZucNsIuifYW8BjwFfTBNaHb7nVt6Lwb9WP0oNV9gid39gR9efvm8_L9YvXh3eXyYrWwQohiIRpBpbZ1WRhrqWiMqQgXkrZGM1oLUxvS8KbSmujWWC5NVVkOkpXMUElJxU_Qq1l3M5kBGpubjrpXm-gGHbcqaKf-9ni3Vl34qihhFS33Ci_uFGK4mSCNanDJQp9fB8KUFMsVcU5ZLTL6_B_0OkzR5_4yxaSkJa-LTJ3OlI0hpQjtoRpK1G4KVJ4CtZ-CzD77s_wD-fvbM3A-A7euh-3_ldTH15ez5C9O58OX</recordid><startdate>202307</startdate><enddate>202307</enddate><creator>Jiang, Lijun</creator><creator>Ling, Jian</creator><creator>Zhao, Jianlong</creator><creator>Yang, Yu</creator><creator>Yang, Yuhong</creator><creator>Li, Yan</creator><creator>Jiao, Yang</creator><creator>Mao, Zhenchuan</creator><creator>Wang, Yunsheng</creator><creator>Xie, Bingyan</creator><general>John Wiley & Sons, Inc</general><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>WIN</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>7QO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>L6V</scope><scope>LK8</scope><scope>M7P</scope><scope>M7S</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PTHSS</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-1035-7711</orcidid><orcidid>https://orcid.org/0000-0002-6667-1179</orcidid><orcidid>https://orcid.org/0000-0001-5003-4434</orcidid><orcidid>https://orcid.org/0000-0002-8831-6020</orcidid><orcidid>https://orcid.org/0000-0001-9640-8956</orcidid><orcidid>https://orcid.org/0000-0002-4841-9543</orcidid><orcidid>https://orcid.org/0000-0002-5311-8809</orcidid><orcidid>https://orcid.org/0000-0002-8179-6885</orcidid><orcidid>https://orcid.org/0000-0002-7605-5732</orcidid></search><sort><creationdate>202307</creationdate><title>Chromosome‐scale genome assembly‐assisted identification of Mi‐9 gene in Solanum arcanum accession LA2157, conferring heat‐stable resistance to Meloidogyne incognita</title><author>Jiang, Lijun ; Ling, Jian ; Zhao, Jianlong ; Yang, Yu ; Yang, Yuhong ; Li, Yan ; Jiao, Yang ; Mao, Zhenchuan ; Wang, Yunsheng ; Xie, Bingyan</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4445-4d417ac965bcc14dbb803471fba2194b9b0d3d8aa0afbc37b88c3e7262b171083</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Agricultural production</topic><topic>Animals</topic><topic>Artificial chromosomes</topic><topic>Assembly</topic><topic>Binding sites</topic><topic>Chromosomes</topic><topic>Chromosomes - metabolism</topic><topic>Cloning</topic><topic>Flowers & plants</topic><topic>Gene expression</topic><topic>Gene silencing</topic><topic>Genes</topic><topic>genome assembly</topic><topic>Genomes</topic><topic>Genomic analysis</topic><topic>Genomics</topic><topic>Heat</topic><topic>Heat resistance</topic><topic>High temperature</topic><topic>Hi‐C</topic><topic>Hot Temperature</topic><topic>Leucine</topic><topic>Localization</topic><topic>Meloidogyne incognita</topic><topic>Mi‐9</topic><topic>NBS-LRR gene</topic><topic>Nematodes</topic><topic>Nucleotides</topic><topic>Pest resistance</topic><topic>Plant Breeding</topic><topic>Plant Diseases - genetics</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plant Roots - genetics</topic><topic>Plant tissues</topic><topic>Soil temperature</topic><topic>Solanum - genetics</topic><topic>Solanum arcanum</topic><topic>Solanum arcanum LA2157</topic><topic>Solanum lycopersicum - genetics</topic><topic>Thermal stability</topic><topic>tomato genetic transformation</topic><topic>Tomatoes</topic><topic>Tylenchoidea</topic><topic>VIGS</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Jiang, Lijun</creatorcontrib><creatorcontrib>Ling, Jian</creatorcontrib><creatorcontrib>Zhao, Jianlong</creatorcontrib><creatorcontrib>Yang, Yu</creatorcontrib><creatorcontrib>Yang, Yuhong</creatorcontrib><creatorcontrib>Li, Yan</creatorcontrib><creatorcontrib>Jiao, Yang</creatorcontrib><creatorcontrib>Mao, Zhenchuan</creatorcontrib><creatorcontrib>Wang, Yunsheng</creatorcontrib><creatorcontrib>Xie, Bingyan</creatorcontrib><collection>Wiley-Blackwell Open Access Titles</collection><collection>Wiley Free Content</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Engineering Collection</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Plant biotechnology journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Jiang, Lijun</au><au>Ling, Jian</au><au>Zhao, Jianlong</au><au>Yang, Yu</au><au>Yang, Yuhong</au><au>Li, Yan</au><au>Jiao, Yang</au><au>Mao, Zhenchuan</au><au>Wang, Yunsheng</au><au>Xie, Bingyan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Chromosome‐scale genome assembly‐assisted identification of Mi‐9 gene in Solanum arcanum accession LA2157, conferring heat‐stable resistance to Meloidogyne incognita</atitle><jtitle>Plant biotechnology journal</jtitle><addtitle>Plant Biotechnol J</addtitle><date>2023-07</date><risdate>2023</risdate><volume>21</volume><issue>7</issue><spage>1496</spage><epage>1509</epage><pages>1496-1509</pages><issn>1467-7644</issn><eissn>1467-7652</eissn><abstract>Summary
Root‐knot nematodes (RKNs) are infamous plant pathogens in tomato production, causing considerable losses in agriculture worldwide. Mi‐1 is the only commercially available RKN‐resistance gene; however, the resistance is inactivated when the soil temperature is over 28 °C. Mi‐9 in wild tomato (Solanum arcanum LA2157) has stable resistance to RKNs under high temperature but has not been cloned and applied. In this study, a chromosome‐scale genome assembly of S. arcanum LA2157 was constructed through Nanopore and Hi‐C sequencing. Based on molecular markers of Mi‐9 and comparative genomic analysis, the localization region and candidate Mi‐9 genes cluster consisting of seven nucleotide‐binding sites and leucine‐rich repeat (NBS‐LRR) genes were located. Transcriptional expression profiles confirmed that five of the seven candidate genes were expressed in root tissue. Moreover, virus‐induced gene silencing of the Sarc_034200 gene resulted in increased susceptibility of S. arcanum LA2157 to Meloidogyne incognita, and genetic transformation of the Sarc_034200 gene in susceptible Solanum pimpinellifolium conferred significant resistance to M. incognita at 25 °C and 30 °C and showed hypersensitive responses at nematode infection sites. This suggested that Sarc_034200 is the Mi‐9 gene. In summary, we cloned, confirmed and applied the heat‐stable RKN‐resistance gene Mi‐9, which is of great significance to tomato breeding for nematode resistance.</abstract><cop>England</cop><pub>John Wiley & Sons, Inc</pub><pmid>37074757</pmid><doi>10.1111/pbi.14055</doi><tpages>1509</tpages><orcidid>https://orcid.org/0000-0002-1035-7711</orcidid><orcidid>https://orcid.org/0000-0002-6667-1179</orcidid><orcidid>https://orcid.org/0000-0001-5003-4434</orcidid><orcidid>https://orcid.org/0000-0002-8831-6020</orcidid><orcidid>https://orcid.org/0000-0001-9640-8956</orcidid><orcidid>https://orcid.org/0000-0002-4841-9543</orcidid><orcidid>https://orcid.org/0000-0002-5311-8809</orcidid><orcidid>https://orcid.org/0000-0002-8179-6885</orcidid><orcidid>https://orcid.org/0000-0002-7605-5732</orcidid><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Wiley-Blackwell Open Access Titles; Wiley Online Library All Journals |
| subjects | Agricultural production Animals Artificial chromosomes Assembly Binding sites Chromosomes Chromosomes - metabolism Cloning Flowers & plants Gene expression Gene silencing Genes genome assembly Genomes Genomic analysis Genomics Heat Heat resistance High temperature Hi‐C Hot Temperature Leucine Localization Meloidogyne incognita Mi‐9 NBS-LRR gene Nematodes Nucleotides Pest resistance Plant Breeding Plant Diseases - genetics Plant Proteins - genetics Plant Proteins - metabolism Plant Roots - genetics Plant tissues Soil temperature Solanum - genetics Solanum arcanum Solanum arcanum LA2157 Solanum lycopersicum - genetics Thermal stability tomato genetic transformation Tomatoes Tylenchoidea VIGS |
| title | Chromosome‐scale genome assembly‐assisted identification of Mi‐9 gene in Solanum arcanum accession LA2157, conferring heat‐stable resistance to Meloidogyne incognita |
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