Differential induction of defense genes in hexaploid wheat roots by the plant-parasitic nematodes Pratylenchus neglectus and P. thornei
Pratylenchus neglectus and P. thornei are among the most destructive root lesion nematodes of wheat in the Pacific Northwest, United States of America and throughout the world. The aim of this study was to determine whether both nematode species were similar in their ability to induce defense genes...
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| description | Pratylenchus neglectus and P. thornei are among the most destructive root lesion nematodes of wheat in the Pacific Northwest, United States of America and throughout the world. The aim of this study was to determine whether both nematode species were similar in their ability to induce defense genes in roots of wheat genotype Scarlet, and whether a combination of both species induced a different pattern of gene induction than each species alone. The long-term aspect of the research was to identify nematode-inducible promoters for deploying defense genes in roots in breeding programs. The root transcriptomes of genotype Scarlet were obtained after a one-week infection period with each nematode species separately, or both species combined. Root defense gene expression was induced for all three treatments relative to the no-nematode control, but P. thornei affected expression to a greater extent compared to P. neglectus. The species combination induced the highest number of defense genes. This result was not predicted from nematode enumeration studies, in which P. thornei colonization was substantially lower than that of P. neglectus, and the nematode combination did not show a significant difference. Quantitative real time polymerase chain reaction (qRT-PCR) assays for Dehydrin2, Glucan endo-1,3-beta-glucosidase, 1-cys-Peroxiredoxin, Pathogenesis-related protein 1 and Late embryogenesis-abundant proteins 76 and group 3 authenticated the induction observed in the transcriptome data. In addition, a near-isogenic line of Scarlet harboring genetic resistance to fungal soilborne pathogens, called Scarlet-Rz1, showed similar or higher levels of defense gene expression compared to fungus-susceptible Scarlet in qRT-PCR assays. Finally, transcriptome expression patterns revealed nematode-inducible promoters that are responsive to both P. neglectus and P. thornei. |
| doi_str_mv | 10.1371/journal.pone.0306533 |
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The aim of this study was to determine whether both nematode species were similar in their ability to induce defense genes in roots of wheat genotype Scarlet, and whether a combination of both species induced a different pattern of gene induction than each species alone. The long-term aspect of the research was to identify nematode-inducible promoters for deploying defense genes in roots in breeding programs. The root transcriptomes of genotype Scarlet were obtained after a one-week infection period with each nematode species separately, or both species combined. Root defense gene expression was induced for all three treatments relative to the no-nematode control, but P. thornei affected expression to a greater extent compared to P. neglectus. The species combination induced the highest number of defense genes. This result was not predicted from nematode enumeration studies, in which P. thornei colonization was substantially lower than that of P. neglectus, and the nematode combination did not show a significant difference. Quantitative real time polymerase chain reaction (qRT-PCR) assays for Dehydrin2, Glucan endo-1,3-beta-glucosidase, 1-cys-Peroxiredoxin, Pathogenesis-related protein 1 and Late embryogenesis-abundant proteins 76 and group 3 authenticated the induction observed in the transcriptome data. In addition, a near-isogenic line of Scarlet harboring genetic resistance to fungal soilborne pathogens, called Scarlet-Rz1, showed similar or higher levels of defense gene expression compared to fungus-susceptible Scarlet in qRT-PCR assays. Finally, transcriptome expression patterns revealed nematode-inducible promoters that are responsive to both P. neglectus and P. thornei.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0306533</identifier><identifier>PMID: 39208324</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis ; Animals ; Biology and Life Sciences ; Breeding ; Cold ; Crop rotation ; Cultivars ; Defense ; Diseases and pests ; Drug resistance in microorganisms ; Embryogenesis ; Embryonic growth stage ; Enumeration ; Experiments ; Gene expression ; Gene Expression Regulation, Plant ; Genes ; Genetic aspects ; Genotypes ; Glucan ; Glucan 1,3-b-glucosidase ; Glucosidase ; Growth ; Host-Parasite Interactions - genetics ; Kinases ; Medicine and Health Sciences ; Nematodes ; Pathogenesis ; Pathogens ; People and places ; Peroxiredoxin ; Plant Diseases - genetics ; Plant Diseases - parasitology ; Plant Roots - genetics ; Plant Roots - parasitology ; Polymerase chain reaction ; Polyploidy ; Pratylenchus neglectus ; Prevention ; Promoters ; Proteins ; Risk factors ; Roots ; Roundworm infections ; Salinity ; Species ; Transcriptome ; Transcriptomes ; Triticum - genetics ; Triticum - parasitology ; Tylenchoidea - physiology ; Variance analysis ; Wheat</subject><ispartof>PloS one, 2024-08, Vol.19 (8), p.e0306533</ispartof><rights>Copyright: This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. 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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-c572t-4d3cdbffd5cd598c5d256339cb4f85c39cd9d70f91a3b7eb27ffbd5bbe44ec6f3</cites><orcidid>0000-0002-4252-6911 ; 0000-0002-8513-4862</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/PMC11361681/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11361681/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,728,781,785,865,886,2103,2929,23870,27928,27929,53795,53797</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39208324$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Shokoohi, Ebrahim</contributor><creatorcontrib>Okubara, Patricia A</creatorcontrib><creatorcontrib>Sharpe, Richard M</creatorcontrib><creatorcontrib>Peetz, Amy B</creatorcontrib><creatorcontrib>Li, Xianran</creatorcontrib><creatorcontrib>Zasada, Inga A</creatorcontrib><title>Differential induction of defense genes in hexaploid wheat roots by the plant-parasitic nematodes Pratylenchus neglectus and P. thornei</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Pratylenchus neglectus and P. thornei are among the most destructive root lesion nematodes of wheat in the Pacific Northwest, United States of America and throughout the world. The aim of this study was to determine whether both nematode species were similar in their ability to induce defense genes in roots of wheat genotype Scarlet, and whether a combination of both species induced a different pattern of gene induction than each species alone. The long-term aspect of the research was to identify nematode-inducible promoters for deploying defense genes in roots in breeding programs. The root transcriptomes of genotype Scarlet were obtained after a one-week infection period with each nematode species separately, or both species combined. Root defense gene expression was induced for all three treatments relative to the no-nematode control, but P. thornei affected expression to a greater extent compared to P. neglectus. The species combination induced the highest number of defense genes. 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induction of defense genes in hexaploid wheat roots by the plant-parasitic nematodes Pratylenchus neglectus and P. thornei</title><author>Okubara, Patricia A ; Sharpe, Richard M ; Peetz, Amy B ; Li, Xianran ; Zasada, Inga A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c572t-4d3cdbffd5cd598c5d256339cb4f85c39cd9d70f91a3b7eb27ffbd5bbe44ec6f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Analysis</topic><topic>Animals</topic><topic>Biology and Life Sciences</topic><topic>Breeding</topic><topic>Cold</topic><topic>Crop rotation</topic><topic>Cultivars</topic><topic>Defense</topic><topic>Diseases and pests</topic><topic>Drug resistance in microorganisms</topic><topic>Embryogenesis</topic><topic>Embryonic growth stage</topic><topic>Enumeration</topic><topic>Experiments</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, 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Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Okubara, Patricia A</au><au>Sharpe, Richard M</au><au>Peetz, Amy B</au><au>Li, Xianran</au><au>Zasada, Inga A</au><au>Shokoohi, Ebrahim</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Differential induction of defense genes in hexaploid wheat roots by the plant-parasitic nematodes Pratylenchus neglectus and P. thornei</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2024-08-29</date><risdate>2024</risdate><volume>19</volume><issue>8</issue><spage>e0306533</spage><pages>e0306533-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Pratylenchus neglectus and P. thornei are among the most destructive root lesion nematodes of wheat in the Pacific Northwest, United States of America and throughout the world. The aim of this study was to determine whether both nematode species were similar in their ability to induce defense genes in roots of wheat genotype Scarlet, and whether a combination of both species induced a different pattern of gene induction than each species alone. The long-term aspect of the research was to identify nematode-inducible promoters for deploying defense genes in roots in breeding programs. The root transcriptomes of genotype Scarlet were obtained after a one-week infection period with each nematode species separately, or both species combined. Root defense gene expression was induced for all three treatments relative to the no-nematode control, but P. thornei affected expression to a greater extent compared to P. neglectus. The species combination induced the highest number of defense genes. This result was not predicted from nematode enumeration studies, in which P. thornei colonization was substantially lower than that of P. neglectus, and the nematode combination did not show a significant difference. Quantitative real time polymerase chain reaction (qRT-PCR) assays for Dehydrin2, Glucan endo-1,3-beta-glucosidase, 1-cys-Peroxiredoxin, Pathogenesis-related protein 1 and Late embryogenesis-abundant proteins 76 and group 3 authenticated the induction observed in the transcriptome data. In addition, a near-isogenic line of Scarlet harboring genetic resistance to fungal soilborne pathogens, called Scarlet-Rz1, showed similar or higher levels of defense gene expression compared to fungus-susceptible Scarlet in qRT-PCR assays. Finally, transcriptome expression patterns revealed nematode-inducible promoters that are responsive to both P. neglectus and P. thornei.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>39208324</pmid><doi>10.1371/journal.pone.0306533</doi><tpages>e0306533</tpages><orcidid>https://orcid.org/0000-0002-4252-6911</orcidid><orcidid>https://orcid.org/0000-0002-8513-4862</orcidid><oa>free_for_read</oa></addata></record> |
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| language | eng |
| recordid | cdi_plos_journals_3098716097 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Analysis Animals Biology and Life Sciences Breeding Cold Crop rotation Cultivars Defense Diseases and pests Drug resistance in microorganisms Embryogenesis Embryonic growth stage Enumeration Experiments Gene expression Gene Expression Regulation, Plant Genes Genetic aspects Genotypes Glucan Glucan 1,3-b-glucosidase Glucosidase Growth Host-Parasite Interactions - genetics Kinases Medicine and Health Sciences Nematodes Pathogenesis Pathogens People and places Peroxiredoxin Plant Diseases - genetics Plant Diseases - parasitology Plant Roots - genetics Plant Roots - parasitology Polymerase chain reaction Polyploidy Pratylenchus neglectus Prevention Promoters Proteins Risk factors Roots Roundworm infections Salinity Species Transcriptome Transcriptomes Triticum - genetics Triticum - parasitology Tylenchoidea - physiology Variance analysis Wheat |
| title | Differential induction of defense genes in hexaploid wheat roots by the plant-parasitic nematodes Pratylenchus neglectus and P. thornei |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-17T11%3A46%3A21IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Differential%20induction%20of%20defense%20genes%20in%20hexaploid%20wheat%20roots%20by%20the%20plant-parasitic%20nematodes%20Pratylenchus%20neglectus%20and%20P.%20thornei&rft.jtitle=PloS%20one&rft.au=Okubara,%20Patricia%20A&rft.date=2024-08-29&rft.volume=19&rft.issue=8&rft.spage=e0306533&rft.pages=e0306533-&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0306533&rft_dat=%3Cgale_plos_%3EA806591337%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=3098716097&rft_id=info:pmid/39208324&rft_galeid=A806591337&rft_doaj_id=oai_doaj_org_article_39b0f61961e84945b9ec95e51c504953&rfr_iscdi=true |