Identification of transcriptional modules linked to the drought response of Brassica napus during seed development and their mitigation by early biotic stress
In order to capture the drought impacts on seed quality acquisition in Brassica napus and its potential interaction with early biotic stress, seeds of the ‘Express’ genotype of oilseed rape were characterized from late embryogenesis to full maturity from plants submitted to reduced watering (WS) wit...
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creator | Bianchetti, Grégoire Clouet, Vanessa Legeai, Fabrice Baron, Cécile Gazengel, Kévin Vu, Benoit Ly Baud, Sébastien To, Alexandra Manzanares‐Dauleux, Maria J. Buitink, Julia Nesi, Nathalie |
description | In order to capture the drought impacts on seed quality acquisition in Brassica napus and its potential interaction with early biotic stress, seeds of the ‘Express’ genotype of oilseed rape were characterized from late embryogenesis to full maturity from plants submitted to reduced watering (WS) with or without pre‐occurring inoculation by the telluric pathogen Plasmodiophora brassicae (Pb + WS or Pb, respectively), and compared to control conditions (C). Drought as a single constraint led to significantly lower accumulation of lipids, higher protein content and reduced longevity of the WS‐treated seeds. In contrast, when water shortage was preceded by clubroot infection, these phenotypic differences were completely abolished despite the upregulation of the drought sensor RD20. A weighted gene co‐expression network of seed development in oilseed rape was generated using 72 transcriptomes from developing seeds from the four treatments and identified 33 modules. Module 29 was highly enriched in heat shock proteins and chaperones that showed a stronger upregulation in Pb + WS compared to the WS condition, pointing to a possible priming effect by the early P. brassicae infection on seed quality acquisition. Module 13 was enriched with genes encoding 12S and 2S seed storage proteins, with the latter being strongly upregulated under WS conditions. Cis‐element promotor enrichment identified PEI1/TZF6, FUS3 and bZIP68 as putative regulators significantly upregulated upon WS compared to Pb + WS. Our results provide a temporal co‐expression atlas of seed development in oilseed rape and will serve as a resource to characterize the plant response towards combinations of biotic and abiotic stresses. |
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Drought as a single constraint led to significantly lower accumulation of lipids, higher protein content and reduced longevity of the WS‐treated seeds. In contrast, when water shortage was preceded by clubroot infection, these phenotypic differences were completely abolished despite the upregulation of the drought sensor RD20. A weighted gene co‐expression network of seed development in oilseed rape was generated using 72 transcriptomes from developing seeds from the four treatments and identified 33 modules. Module 29 was highly enriched in heat shock proteins and chaperones that showed a stronger upregulation in Pb + WS compared to the WS condition, pointing to a possible priming effect by the early P. brassicae infection on seed quality acquisition. Module 13 was enriched with genes encoding 12S and 2S seed storage proteins, with the latter being strongly upregulated under WS conditions. Cis‐element promotor enrichment identified PEI1/TZF6, FUS3 and bZIP68 as putative regulators significantly upregulated upon WS compared to Pb + WS. Our results provide a temporal co‐expression atlas of seed development in oilseed rape and will serve as a resource to characterize the plant response towards combinations of biotic and abiotic stresses.</description><identifier>ISSN: 0031-9317</identifier><identifier>EISSN: 1399-3054</identifier><identifier>DOI: 10.1111/ppl.14130</identifier><identifier>PMID: 38842416</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Brassica ; Brassica napus ; Brassica napus - genetics ; Brassica napus - physiology ; Clubroot ; Drought ; Droughts ; Embryogenesis ; Embryonic growth stage ; Enrichment ; Environmental impact ; Gene expression ; Gene Expression Regulation, Plant ; Genotypes ; Heat shock proteins ; Inoculation ; Life Sciences ; Lipids ; Modules ; Nutrient content ; Oilseeds ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plasmodiophora brassicae ; Plasmodiophorida - physiology ; Rape plants ; Rapeseed ; Seeds ; Seeds - genetics ; Seeds - growth & development ; Storage proteins ; Stress, Physiological - genetics ; Transcriptome - genetics ; Transcriptomes ; Up-regulation ; Water shortages</subject><ispartof>Physiologia plantarum, 2024-01, Vol.176 (1), p.e14130-n/a</ispartof><rights>2024 The Authors. published by John Wiley & Sons Ltd on behalf of Scandinavian Plant Physiology Society.</rights><rights>2024 The Authors. Physiologia Plantarum published by John Wiley & Sons Ltd on behalf of Scandinavian Plant Physiology Society.</rights><rights>2024. This article 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><rights>Attribution - NonCommercial - NoDerivatives</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c3820-6bdde55aacd45fef5a263036ee03149006ccd96924b48796699c74508cd95eba3</cites><orcidid>0000-0002-6452-0393 ; 0000-0002-2552-472X ; 0000-0003-1192-982X ; 0000-0001-9054-2281 ; 0000-0002-1457-764X ; 0000-0002-5507-327X ; 0000-0002-6472-4839 ; 0000-0002-3713-370X ; 0000-0001-8541-7291 ; 0000-0002-0204-4045</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%2Fppl.14130$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fppl.14130$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,315,781,785,886,1418,4025,27927,27928,27929,45578,45579</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38842416$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-04443649$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Bianchetti, Grégoire</creatorcontrib><creatorcontrib>Clouet, Vanessa</creatorcontrib><creatorcontrib>Legeai, Fabrice</creatorcontrib><creatorcontrib>Baron, Cécile</creatorcontrib><creatorcontrib>Gazengel, Kévin</creatorcontrib><creatorcontrib>Vu, Benoit Ly</creatorcontrib><creatorcontrib>Baud, Sébastien</creatorcontrib><creatorcontrib>To, Alexandra</creatorcontrib><creatorcontrib>Manzanares‐Dauleux, Maria J.</creatorcontrib><creatorcontrib>Buitink, Julia</creatorcontrib><creatorcontrib>Nesi, Nathalie</creatorcontrib><title>Identification of transcriptional modules linked to the drought response of Brassica napus during seed development and their mitigation by early biotic stress</title><title>Physiologia plantarum</title><addtitle>Physiol Plant</addtitle><description>In order to capture the drought impacts on seed quality acquisition in Brassica napus and its potential interaction with early biotic stress, seeds of the ‘Express’ genotype of oilseed rape were characterized from late embryogenesis to full maturity from plants submitted to reduced watering (WS) with or without pre‐occurring inoculation by the telluric pathogen Plasmodiophora brassicae (Pb + WS or Pb, respectively), and compared to control conditions (C). Drought as a single constraint led to significantly lower accumulation of lipids, higher protein content and reduced longevity of the WS‐treated seeds. In contrast, when water shortage was preceded by clubroot infection, these phenotypic differences were completely abolished despite the upregulation of the drought sensor RD20. A weighted gene co‐expression network of seed development in oilseed rape was generated using 72 transcriptomes from developing seeds from the four treatments and identified 33 modules. Module 29 was highly enriched in heat shock proteins and chaperones that showed a stronger upregulation in Pb + WS compared to the WS condition, pointing to a possible priming effect by the early P. brassicae infection on seed quality acquisition. Module 13 was enriched with genes encoding 12S and 2S seed storage proteins, with the latter being strongly upregulated under WS conditions. Cis‐element promotor enrichment identified PEI1/TZF6, FUS3 and bZIP68 as putative regulators significantly upregulated upon WS compared to Pb + WS. Our results provide a temporal co‐expression atlas of seed development in oilseed rape and will serve as a resource to characterize the plant response towards combinations of biotic and abiotic stresses.</description><subject>Brassica</subject><subject>Brassica napus</subject><subject>Brassica napus - genetics</subject><subject>Brassica napus - physiology</subject><subject>Clubroot</subject><subject>Drought</subject><subject>Droughts</subject><subject>Embryogenesis</subject><subject>Embryonic growth stage</subject><subject>Enrichment</subject><subject>Environmental impact</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant</subject><subject>Genotypes</subject><subject>Heat shock proteins</subject><subject>Inoculation</subject><subject>Life Sciences</subject><subject>Lipids</subject><subject>Modules</subject><subject>Nutrient content</subject><subject>Oilseeds</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plasmodiophora brassicae</subject><subject>Plasmodiophorida - physiology</subject><subject>Rape plants</subject><subject>Rapeseed</subject><subject>Seeds</subject><subject>Seeds - genetics</subject><subject>Seeds - growth & development</subject><subject>Storage proteins</subject><subject>Stress, Physiological - genetics</subject><subject>Transcriptome - genetics</subject><subject>Transcriptomes</subject><subject>Up-regulation</subject><subject>Water shortages</subject><issn>0031-9317</issn><issn>1399-3054</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><recordid>eNp1kcFu1DAQhi0EokvhwAsgS1zgkNaOHW98bCuglVaiBzhbjj3ZdXHiYDtF-zI8Kw4pRULCF0ujb74ZzY_Qa0rOaHnn0-TPKKeMPEEbyqSsGGn4U7QhhNFKMro9QS9SuiOECkHr5-iEtS2vORUb9PPGwphd74zOLow49DhHPSYT3bQUtMdDsLOHhL0bv4HFOeB8AGxjmPeHjCOkKYwJls7LqFMqJjzqaU7YztGNe5ygdFm4Bx-moQzDerSLwkU8uOz26-DuiEFHf8SdC9kZnHIxp5foWa99glcP_yn6-vHDl6vravf5083Vxa4yrK1JJTproWm0NpY3PfSNrgUjTACUC3BJiDDGSiFr3vF2K4WQ0mx5Q9pSbaDT7BS9X70H7dUU3aDjUQXt1PXFTi01wjlngst7Wth3KzvF8H2GlNXgkgHv9QhhTooR0dRbVlNe0Lf_oHdhjuWoSdUlF9bKuqV_h5sYUorQP25AiVoCViVg9Tvgwr55MM7dAPaR_JNoAc5X4IfzcPy_Sd3e7lblLxXXsZw</recordid><startdate>202401</startdate><enddate>202401</enddate><creator>Bianchetti, Grégoire</creator><creator>Clouet, Vanessa</creator><creator>Legeai, Fabrice</creator><creator>Baron, Cécile</creator><creator>Gazengel, Kévin</creator><creator>Vu, Benoit Ly</creator><creator>Baud, Sébastien</creator><creator>To, Alexandra</creator><creator>Manzanares‐Dauleux, Maria J.</creator><creator>Buitink, Julia</creator><creator>Nesi, Nathalie</creator><general>Blackwell Publishing Ltd</general><general>Wiley Subscription Services, Inc</general><general>Wiley</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>7SN</scope><scope>7ST</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>SOI</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><orcidid>https://orcid.org/0000-0002-6452-0393</orcidid><orcidid>https://orcid.org/0000-0002-2552-472X</orcidid><orcidid>https://orcid.org/0000-0003-1192-982X</orcidid><orcidid>https://orcid.org/0000-0001-9054-2281</orcidid><orcidid>https://orcid.org/0000-0002-1457-764X</orcidid><orcidid>https://orcid.org/0000-0002-5507-327X</orcidid><orcidid>https://orcid.org/0000-0002-6472-4839</orcidid><orcidid>https://orcid.org/0000-0002-3713-370X</orcidid><orcidid>https://orcid.org/0000-0001-8541-7291</orcidid><orcidid>https://orcid.org/0000-0002-0204-4045</orcidid></search><sort><creationdate>202401</creationdate><title>Identification of transcriptional modules linked to the drought response of Brassica napus during seed development and their mitigation by early biotic stress</title><author>Bianchetti, Grégoire ; Clouet, Vanessa ; Legeai, Fabrice ; Baron, Cécile ; Gazengel, Kévin ; Vu, Benoit Ly ; Baud, Sébastien ; To, Alexandra ; Manzanares‐Dauleux, Maria J. ; Buitink, Julia ; Nesi, Nathalie</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3820-6bdde55aacd45fef5a263036ee03149006ccd96924b48796699c74508cd95eba3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Brassica</topic><topic>Brassica napus</topic><topic>Brassica napus - genetics</topic><topic>Brassica napus - physiology</topic><topic>Clubroot</topic><topic>Drought</topic><topic>Droughts</topic><topic>Embryogenesis</topic><topic>Embryonic growth stage</topic><topic>Enrichment</topic><topic>Environmental impact</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Plant</topic><topic>Genotypes</topic><topic>Heat shock proteins</topic><topic>Inoculation</topic><topic>Life Sciences</topic><topic>Lipids</topic><topic>Modules</topic><topic>Nutrient content</topic><topic>Oilseeds</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plasmodiophora brassicae</topic><topic>Plasmodiophorida - physiology</topic><topic>Rape plants</topic><topic>Rapeseed</topic><topic>Seeds</topic><topic>Seeds - genetics</topic><topic>Seeds - growth & development</topic><topic>Storage proteins</topic><topic>Stress, Physiological - genetics</topic><topic>Transcriptome - genetics</topic><topic>Transcriptomes</topic><topic>Up-regulation</topic><topic>Water shortages</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Bianchetti, Grégoire</creatorcontrib><creatorcontrib>Clouet, Vanessa</creatorcontrib><creatorcontrib>Legeai, Fabrice</creatorcontrib><creatorcontrib>Baron, Cécile</creatorcontrib><creatorcontrib>Gazengel, Kévin</creatorcontrib><creatorcontrib>Vu, Benoit Ly</creatorcontrib><creatorcontrib>Baud, Sébastien</creatorcontrib><creatorcontrib>To, Alexandra</creatorcontrib><creatorcontrib>Manzanares‐Dauleux, Maria J.</creatorcontrib><creatorcontrib>Buitink, Julia</creatorcontrib><creatorcontrib>Nesi, Nathalie</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Wiley Online Library (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>Ecology Abstracts</collection><collection>Environment Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><jtitle>Physiologia plantarum</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Bianchetti, Grégoire</au><au>Clouet, Vanessa</au><au>Legeai, Fabrice</au><au>Baron, Cécile</au><au>Gazengel, Kévin</au><au>Vu, Benoit Ly</au><au>Baud, Sébastien</au><au>To, Alexandra</au><au>Manzanares‐Dauleux, Maria J.</au><au>Buitink, Julia</au><au>Nesi, Nathalie</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Identification of transcriptional modules linked to the drought response of Brassica napus during seed development and their mitigation by early biotic stress</atitle><jtitle>Physiologia plantarum</jtitle><addtitle>Physiol Plant</addtitle><date>2024-01</date><risdate>2024</risdate><volume>176</volume><issue>1</issue><spage>e14130</spage><epage>n/a</epage><pages>e14130-n/a</pages><issn>0031-9317</issn><eissn>1399-3054</eissn><abstract>In order to capture the drought impacts on seed quality acquisition in Brassica napus and its potential interaction with early biotic stress, seeds of the ‘Express’ genotype of oilseed rape were characterized from late embryogenesis to full maturity from plants submitted to reduced watering (WS) with or without pre‐occurring inoculation by the telluric pathogen Plasmodiophora brassicae (Pb + WS or Pb, respectively), and compared to control conditions (C). Drought as a single constraint led to significantly lower accumulation of lipids, higher protein content and reduced longevity of the WS‐treated seeds. In contrast, when water shortage was preceded by clubroot infection, these phenotypic differences were completely abolished despite the upregulation of the drought sensor RD20. A weighted gene co‐expression network of seed development in oilseed rape was generated using 72 transcriptomes from developing seeds from the four treatments and identified 33 modules. Module 29 was highly enriched in heat shock proteins and chaperones that showed a stronger upregulation in Pb + WS compared to the WS condition, pointing to a possible priming effect by the early P. brassicae infection on seed quality acquisition. Module 13 was enriched with genes encoding 12S and 2S seed storage proteins, with the latter being strongly upregulated under WS conditions. Cis‐element promotor enrichment identified PEI1/TZF6, FUS3 and bZIP68 as putative regulators significantly upregulated upon WS compared to Pb + WS. Our results provide a temporal co‐expression atlas of seed development in oilseed rape and will serve as a resource to characterize the plant response towards combinations of biotic and abiotic stresses.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>38842416</pmid><doi>10.1111/ppl.14130</doi><tpages>22</tpages><orcidid>https://orcid.org/0000-0002-6452-0393</orcidid><orcidid>https://orcid.org/0000-0002-2552-472X</orcidid><orcidid>https://orcid.org/0000-0003-1192-982X</orcidid><orcidid>https://orcid.org/0000-0001-9054-2281</orcidid><orcidid>https://orcid.org/0000-0002-1457-764X</orcidid><orcidid>https://orcid.org/0000-0002-5507-327X</orcidid><orcidid>https://orcid.org/0000-0002-6472-4839</orcidid><orcidid>https://orcid.org/0000-0002-3713-370X</orcidid><orcidid>https://orcid.org/0000-0001-8541-7291</orcidid><orcidid>https://orcid.org/0000-0002-0204-4045</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Brassica Brassica napus Brassica napus - genetics Brassica napus - physiology Clubroot Drought Droughts Embryogenesis Embryonic growth stage Enrichment Environmental impact Gene expression Gene Expression Regulation, Plant Genotypes Heat shock proteins Inoculation Life Sciences Lipids Modules Nutrient content Oilseeds Plant Proteins - genetics Plant Proteins - metabolism Plasmodiophora brassicae Plasmodiophorida - physiology Rape plants Rapeseed Seeds Seeds - genetics Seeds - growth & development Storage proteins Stress, Physiological - genetics Transcriptome - genetics Transcriptomes Up-regulation Water shortages |
title | Identification of transcriptional modules linked to the drought response of Brassica napus during seed development and their mitigation by early biotic stress |
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