ZmmiR398b negatively regulates maize resistance to sugarcane mosaic virus infection by targeting ZmCSD2/4/9
MicroRNAs (miRNAs) are widely involved in various biological processes of plants and contribute to plant resistance against various pathogens. In this study, upon sugarcane mosaic virus (SCMV) infection, the accumulation of maize (Zea mays) miR398b (ZmmiR398b) was significantly reduced in resistant...
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| Veröffentlicht in: | Molecular plant pathology 2024-05, Vol.25 (5), p.e13462-n/a |
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| creator | Gao, Xinran Du, Zhichao Hao, Kaiqiang Zhang, Sijia Li, Jian Guo, Jinxiu Wang, Zhiping Zhao, Shixue Sang, Lijun An, Mengnan Xia, Zihao Wu, Yuanhua |
| description | MicroRNAs (miRNAs) are widely involved in various biological processes of plants and contribute to plant resistance against various pathogens. In this study, upon sugarcane mosaic virus (SCMV) infection, the accumulation of maize (Zea mays) miR398b (ZmmiR398b) was significantly reduced in resistant inbred line Chang7‐2, while it was increased in susceptible inbred line Mo17. Degradome sequencing analysis coupled with transient co‐expression assays revealed that ZmmiR398b can target Cu/Zn‐superoxidase dismutase2 (ZmCSD2), ZmCSD4, and ZmCSD9 in vivo, of which the expression levels were all upregulated by SCMV infection in Chang7‐2 and Mo17. Moreover, overexpressing ZmmiR398b (OE398b) exhibited increased susceptibility to SCMV infection, probably by increasing reactive oxygen species (ROS) accumulation, which were consistent with ZmCSD2/4/9‐silenced maize plants. By contrast, silencing ZmmiR398b (STTM398b) through short tandem target mimic (STTM) technology enhanced maize resistance to SCMV infection and decreased ROS levels. Interestingly, copper (Cu)‐gradient hydroponic experiments demonstrated that Cu deficiency promoted SCMV infection while Cu sufficiency inhibited SCMV infection by regulating accumulations of ZmmiR398b and ZmCSD2/4/9 in maize. These results revealed that manipulating the ZmmiR398b‐ZmCSD2/4/9‐ROS module provides a prospective strategy for developing SCMV‐tolerant maize varieties.
The ZmmiR398b‐ZmCSD2/4/9‐ROS module regulates maize resistance to sugarcane mosaic virus (SCMV) infection and provides a prospective strategy for developing SCMV‐tolerant maize varieties. |
| doi_str_mv | 10.1111/mpp.13462 |
| format | Article |
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The ZmmiR398b‐ZmCSD2/4/9‐ROS module regulates maize resistance to sugarcane mosaic virus (SCMV) infection and provides a prospective strategy for developing SCMV‐tolerant maize varieties.</description><identifier>ISSN: 1464-6722</identifier><identifier>EISSN: 1364-3703</identifier><identifier>DOI: 10.1111/mpp.13462</identifier><identifier>PMID: 38695630</identifier><language>eng</language><publisher>England: John Wiley & Sons, Inc</publisher><subject>Accumulation ; Barley ; Biological activity ; Copper ; copper deficiency ; Corn ; Disease resistance ; Disease Resistance - genetics ; Gene Expression Regulation, Plant ; Genes ; Homeostasis ; Hydroponics ; inbred lines ; Inbreeding ; Infections ; microRNA ; MicroRNAs - genetics ; MicroRNAs - metabolism ; miRNA ; Original ; Plant diseases ; Plant Diseases - genetics ; Plant Diseases - virology ; plant pathology ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plant resistance ; Plant virus diseases ; Plant viruses ; Potyvirus - pathogenicity ; Potyvirus - physiology ; Reactive oxygen species ; Reactive Oxygen Species - metabolism ; ROS ; SCMV ; Sequence analysis ; Sorghum ; Sugarcane ; Sugarcane mosaic virus ; Zea mays ; Zea mays - genetics ; Zea mays - virology ; ZmCSD2/4/9 ; ZmmiR398b</subject><ispartof>Molecular plant pathology, 2024-05, Vol.25 (5), p.e13462-n/a</ispartof><rights>2024 The Authors. published by British Society for Plant Pathology and John Wiley & Sons Ltd.</rights><rights>2024 The Authors. Molecular Plant Pathology published by British Society for Plant Pathology and John Wiley & Sons Ltd.</rights><rights>2024. This work is published 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><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c4372-98e506f0ff58e0d2bbab1c4cfb3d995692ae1f9958554540a0a51701a78322423</cites><orcidid>0000-0001-7905-106X ; 0000-0002-8599-8679</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/PMC11064800/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11064800/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,1411,11541,27901,27902,45550,45551,46027,46451,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38695630$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Gao, Xinran</creatorcontrib><creatorcontrib>Du, Zhichao</creatorcontrib><creatorcontrib>Hao, Kaiqiang</creatorcontrib><creatorcontrib>Zhang, Sijia</creatorcontrib><creatorcontrib>Li, Jian</creatorcontrib><creatorcontrib>Guo, Jinxiu</creatorcontrib><creatorcontrib>Wang, Zhiping</creatorcontrib><creatorcontrib>Zhao, Shixue</creatorcontrib><creatorcontrib>Sang, Lijun</creatorcontrib><creatorcontrib>An, Mengnan</creatorcontrib><creatorcontrib>Xia, Zihao</creatorcontrib><creatorcontrib>Wu, Yuanhua</creatorcontrib><title>ZmmiR398b negatively regulates maize resistance to sugarcane mosaic virus infection by targeting ZmCSD2/4/9</title><title>Molecular plant pathology</title><addtitle>Mol Plant Pathol</addtitle><description>MicroRNAs (miRNAs) are widely involved in various biological processes of plants and contribute to plant resistance against various pathogens. In this study, upon sugarcane mosaic virus (SCMV) infection, the accumulation of maize (Zea mays) miR398b (ZmmiR398b) was significantly reduced in resistant inbred line Chang7‐2, while it was increased in susceptible inbred line Mo17. Degradome sequencing analysis coupled with transient co‐expression assays revealed that ZmmiR398b can target Cu/Zn‐superoxidase dismutase2 (ZmCSD2), ZmCSD4, and ZmCSD9 in vivo, of which the expression levels were all upregulated by SCMV infection in Chang7‐2 and Mo17. Moreover, overexpressing ZmmiR398b (OE398b) exhibited increased susceptibility to SCMV infection, probably by increasing reactive oxygen species (ROS) accumulation, which were consistent with ZmCSD2/4/9‐silenced maize plants. By contrast, silencing ZmmiR398b (STTM398b) through short tandem target mimic (STTM) technology enhanced maize resistance to SCMV infection and decreased ROS levels. Interestingly, copper (Cu)‐gradient hydroponic experiments demonstrated that Cu deficiency promoted SCMV infection while Cu sufficiency inhibited SCMV infection by regulating accumulations of ZmmiR398b and ZmCSD2/4/9 in maize. These results revealed that manipulating the ZmmiR398b‐ZmCSD2/4/9‐ROS module provides a prospective strategy for developing SCMV‐tolerant maize varieties.
The ZmmiR398b‐ZmCSD2/4/9‐ROS module regulates maize resistance to sugarcane mosaic virus (SCMV) infection and provides a prospective strategy for developing SCMV‐tolerant maize varieties.</description><subject>Accumulation</subject><subject>Barley</subject><subject>Biological activity</subject><subject>Copper</subject><subject>copper deficiency</subject><subject>Corn</subject><subject>Disease resistance</subject><subject>Disease Resistance - genetics</subject><subject>Gene Expression Regulation, Plant</subject><subject>Genes</subject><subject>Homeostasis</subject><subject>Hydroponics</subject><subject>inbred lines</subject><subject>Inbreeding</subject><subject>Infections</subject><subject>microRNA</subject><subject>MicroRNAs - genetics</subject><subject>MicroRNAs - metabolism</subject><subject>miRNA</subject><subject>Original</subject><subject>Plant diseases</subject><subject>Plant Diseases - genetics</subject><subject>Plant Diseases - virology</subject><subject>plant pathology</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plant resistance</subject><subject>Plant virus diseases</subject><subject>Plant viruses</subject><subject>Potyvirus - pathogenicity</subject><subject>Potyvirus - physiology</subject><subject>Reactive oxygen species</subject><subject>Reactive Oxygen Species - metabolism</subject><subject>ROS</subject><subject>SCMV</subject><subject>Sequence analysis</subject><subject>Sorghum</subject><subject>Sugarcane</subject><subject>Sugarcane mosaic virus</subject><subject>Zea mays</subject><subject>Zea mays - genetics</subject><subject>Zea mays - virology</subject><subject>ZmCSD2/4/9</subject><subject>ZmmiR398b</subject><issn>1464-6722</issn><issn>1364-3703</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNp1kU1PVDEYhRsiEUQX_AHTxA0uhunn_VgZMyiSQCB-bNg0vZ33Xou37dj2jhl_PcUBgiZ209P0yel5exA6pOSYljV3q9Ux5aJiO2if8krMeE34s6JF0VXN2B56kdINIbRumXyO9nhTtbLiZB_9uHbOfuZt02EPg852DeMGRximUWdI2Gn7G8o52ZS1N4BzwGkadDTaA3YhaWvw2sYpYet7MNkGj7sNzjoOkK0f8LVbfDlhczFvX6LdXo8JXt3vB-jbxw9fF59m55enZ4v35zMjeM1mbQOSVD3pe9kAWbKu0x01wvQdX7Yldss00L6oRkohBdFES1oTquuGMyYYP0Dvtr6rqXOwNOBz1KNaRet03Kigrfr7xtvvaghrRSmpRENIcTi6d4jh5wQpK2eTgXEsQ4cpKU4ll6Jh9O6xN_-gN2GKvsynOKlI-WkpeKHebikTQ0oR-sc0lKi7DlXpUP3psLCvn8Z_JB9KK8B8C_yyI2z-76Qurq62lrfc7aXQ</recordid><startdate>202405</startdate><enddate>202405</enddate><creator>Gao, Xinran</creator><creator>Du, Zhichao</creator><creator>Hao, Kaiqiang</creator><creator>Zhang, Sijia</creator><creator>Li, Jian</creator><creator>Guo, Jinxiu</creator><creator>Wang, Zhiping</creator><creator>Zhao, Shixue</creator><creator>Sang, Lijun</creator><creator>An, Mengnan</creator><creator>Xia, Zihao</creator><creator>Wu, Yuanhua</creator><general>John Wiley & Sons, Inc</general><general>John Wiley and Sons Inc</general><scope>24P</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>3V.</scope><scope>7QL</scope><scope>7QO</scope><scope>7T7</scope><scope>7U9</scope><scope>7X2</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</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>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>LK8</scope><scope>M0K</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-7905-106X</orcidid><orcidid>https://orcid.org/0000-0002-8599-8679</orcidid></search><sort><creationdate>202405</creationdate><title>ZmmiR398b negatively regulates maize resistance to sugarcane mosaic virus infection by targeting ZmCSD2/4/9</title><author>Gao, Xinran ; Du, Zhichao ; Hao, Kaiqiang ; Zhang, Sijia ; Li, Jian ; Guo, Jinxiu ; Wang, Zhiping ; Zhao, Shixue ; Sang, Lijun ; An, Mengnan ; Xia, Zihao ; Wu, Yuanhua</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4372-98e506f0ff58e0d2bbab1c4cfb3d995692ae1f9958554540a0a51701a78322423</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Accumulation</topic><topic>Barley</topic><topic>Biological activity</topic><topic>Copper</topic><topic>copper deficiency</topic><topic>Corn</topic><topic>Disease resistance</topic><topic>Disease Resistance - genetics</topic><topic>Gene Expression Regulation, Plant</topic><topic>Genes</topic><topic>Homeostasis</topic><topic>Hydroponics</topic><topic>inbred lines</topic><topic>Inbreeding</topic><topic>Infections</topic><topic>microRNA</topic><topic>MicroRNAs - genetics</topic><topic>MicroRNAs - metabolism</topic><topic>miRNA</topic><topic>Original</topic><topic>Plant diseases</topic><topic>Plant Diseases - genetics</topic><topic>Plant Diseases - virology</topic><topic>plant pathology</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plant resistance</topic><topic>Plant virus diseases</topic><topic>Plant viruses</topic><topic>Potyvirus - pathogenicity</topic><topic>Potyvirus - physiology</topic><topic>Reactive oxygen species</topic><topic>Reactive Oxygen Species - metabolism</topic><topic>ROS</topic><topic>SCMV</topic><topic>Sequence analysis</topic><topic>Sorghum</topic><topic>Sugarcane</topic><topic>Sugarcane mosaic virus</topic><topic>Zea mays</topic><topic>Zea mays - genetics</topic><topic>Zea mays - virology</topic><topic>ZmCSD2/4/9</topic><topic>ZmmiR398b</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Gao, Xinran</creatorcontrib><creatorcontrib>Du, Zhichao</creatorcontrib><creatorcontrib>Hao, Kaiqiang</creatorcontrib><creatorcontrib>Zhang, Sijia</creatorcontrib><creatorcontrib>Li, Jian</creatorcontrib><creatorcontrib>Guo, Jinxiu</creatorcontrib><creatorcontrib>Wang, Zhiping</creatorcontrib><creatorcontrib>Zhao, Shixue</creatorcontrib><creatorcontrib>Sang, Lijun</creatorcontrib><creatorcontrib>An, Mengnan</creatorcontrib><creatorcontrib>Xia, Zihao</creatorcontrib><creatorcontrib>Wu, Yuanhua</creatorcontrib><collection>Wiley Online Library Open Access</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 Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science 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>ProQuest Central China</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Molecular plant pathology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Gao, Xinran</au><au>Du, Zhichao</au><au>Hao, Kaiqiang</au><au>Zhang, Sijia</au><au>Li, Jian</au><au>Guo, Jinxiu</au><au>Wang, Zhiping</au><au>Zhao, Shixue</au><au>Sang, Lijun</au><au>An, Mengnan</au><au>Xia, Zihao</au><au>Wu, Yuanhua</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>ZmmiR398b negatively regulates maize resistance to sugarcane mosaic virus infection by targeting ZmCSD2/4/9</atitle><jtitle>Molecular plant pathology</jtitle><addtitle>Mol Plant Pathol</addtitle><date>2024-05</date><risdate>2024</risdate><volume>25</volume><issue>5</issue><spage>e13462</spage><epage>n/a</epage><pages>e13462-n/a</pages><issn>1464-6722</issn><eissn>1364-3703</eissn><abstract>MicroRNAs (miRNAs) are widely involved in various biological processes of plants and contribute to plant resistance against various pathogens. In this study, upon sugarcane mosaic virus (SCMV) infection, the accumulation of maize (Zea mays) miR398b (ZmmiR398b) was significantly reduced in resistant inbred line Chang7‐2, while it was increased in susceptible inbred line Mo17. Degradome sequencing analysis coupled with transient co‐expression assays revealed that ZmmiR398b can target Cu/Zn‐superoxidase dismutase2 (ZmCSD2), ZmCSD4, and ZmCSD9 in vivo, of which the expression levels were all upregulated by SCMV infection in Chang7‐2 and Mo17. Moreover, overexpressing ZmmiR398b (OE398b) exhibited increased susceptibility to SCMV infection, probably by increasing reactive oxygen species (ROS) accumulation, which were consistent with ZmCSD2/4/9‐silenced maize plants. By contrast, silencing ZmmiR398b (STTM398b) through short tandem target mimic (STTM) technology enhanced maize resistance to SCMV infection and decreased ROS levels. Interestingly, copper (Cu)‐gradient hydroponic experiments demonstrated that Cu deficiency promoted SCMV infection while Cu sufficiency inhibited SCMV infection by regulating accumulations of ZmmiR398b and ZmCSD2/4/9 in maize. These results revealed that manipulating the ZmmiR398b‐ZmCSD2/4/9‐ROS module provides a prospective strategy for developing SCMV‐tolerant maize varieties.
The ZmmiR398b‐ZmCSD2/4/9‐ROS module regulates maize resistance to sugarcane mosaic virus (SCMV) infection and provides a prospective strategy for developing SCMV‐tolerant maize varieties.</abstract><cop>England</cop><pub>John Wiley & Sons, Inc</pub><pmid>38695630</pmid><doi>10.1111/mpp.13462</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0001-7905-106X</orcidid><orcidid>https://orcid.org/0000-0002-8599-8679</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | Molecular plant pathology, 2024-05, Vol.25 (5), p.e13462-n/a |
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| source | MEDLINE; Wiley Online Library Open Access; DOAJ Directory of Open Access Journals; Wiley Online Library Journals Frontfile Complete; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central |
| subjects | Accumulation Barley Biological activity Copper copper deficiency Corn Disease resistance Disease Resistance - genetics Gene Expression Regulation, Plant Genes Homeostasis Hydroponics inbred lines Inbreeding Infections microRNA MicroRNAs - genetics MicroRNAs - metabolism miRNA Original Plant diseases Plant Diseases - genetics Plant Diseases - virology plant pathology Plant Proteins - genetics Plant Proteins - metabolism Plant resistance Plant virus diseases Plant viruses Potyvirus - pathogenicity Potyvirus - physiology Reactive oxygen species Reactive Oxygen Species - metabolism ROS SCMV Sequence analysis Sorghum Sugarcane Sugarcane mosaic virus Zea mays Zea mays - genetics Zea mays - virology ZmCSD2/4/9 ZmmiR398b |
| title | ZmmiR398b negatively regulates maize resistance to sugarcane mosaic virus infection by targeting ZmCSD2/4/9 |
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