Dual transcriptomic and metabolomic analyses provide novel insights into the role of vitamins A and B metabolism in ectomycorrhizal symbiosis between Pinus yunnanensis and Lactarius deliciosus
Ectomycorrhizal (EM) fungi play important roles in nutrient cycling and plant community establishment in forest ecosystems. Effects of EM formation on global alterations of the transcriptome and metabolome during plant‐fungal interaction and the key metabolites involved in EM development are largely...
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description | Ectomycorrhizal (EM) fungi play important roles in nutrient cycling and plant community establishment in forest ecosystems. Effects of EM formation on global alterations of the transcriptome and metabolome during plant‐fungal interaction and the key metabolites involved in EM development are largely unknown. Here, dual RNA‐Seq and untargeted metabolomic analyses were used to reveal stage‐specific and core responses of Pinus yunnanensis and Lactarius deliciosus during mycorrhizal colonization. We found that L. deliciosus colonization in P. yunnanensis roots induced different transcriptional changes across three interaction stages, with a small core of genes consistently regulated at all stages. Concentrations of retinol (vitamin A) and retinoic acid increased while that of B group vitamins decreased during EM formation, which was coordinately regulated by these two plant‐fungus partners, with L. deliciosus possibly playing a dominant role. Exogenous retinol altered the diameter and mantle thickness of P. yunnanensis ‐ L. deliciosus EM tips and affected host plant growth and phosphorus acquisition. In the absence of L. deliciosus, exogenous retinol increased the root diameter and the number of root tips of P. yunnanensis. Furthermore, the concentration of auxin increased, but that of abscisic acid decreased during EM formation, and the genes involved in plant hormone signal transduction were gradually activated, and auxin and cytokinin signal transduction potentially played a positive role in this EM symbiosis. In conclusion, we propose that the interaction of P. yunnanensis and L. deliciosus alters vitamin metabolism, which may further affect plant hormone biosynthesis and signal transduction, modulating root morphology and EM traits. |
doi_str_mv | 10.1111/ppl.14194 |
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Effects of EM formation on global alterations of the transcriptome and metabolome during plant‐fungal interaction and the key metabolites involved in EM development are largely unknown. Here, dual RNA‐Seq and untargeted metabolomic analyses were used to reveal stage‐specific and core responses of Pinus yunnanensis and Lactarius deliciosus during mycorrhizal colonization. We found that L. deliciosus colonization in P. yunnanensis roots induced different transcriptional changes across three interaction stages, with a small core of genes consistently regulated at all stages. Concentrations of retinol (vitamin A) and retinoic acid increased while that of B group vitamins decreased during EM formation, which was coordinately regulated by these two plant‐fungus partners, with L. deliciosus possibly playing a dominant role. Exogenous retinol altered the diameter and mantle thickness of P. yunnanensis ‐ L. deliciosus EM tips and affected host plant growth and phosphorus acquisition. In the absence of L. deliciosus, exogenous retinol increased the root diameter and the number of root tips of P. yunnanensis. Furthermore, the concentration of auxin increased, but that of abscisic acid decreased during EM formation, and the genes involved in plant hormone signal transduction were gradually activated, and auxin and cytokinin signal transduction potentially played a positive role in this EM symbiosis. In conclusion, we propose that the interaction of P. yunnanensis and L. deliciosus alters vitamin metabolism, which may further affect plant hormone biosynthesis and signal transduction, modulating root morphology and EM traits.</description><identifier>ISSN: 0031-9317</identifier><identifier>EISSN: 1399-3054</identifier><identifier>DOI: 10.1111/ppl.14194</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Abscisic acid ; Auxins ; Biosynthesis ; Colonization ; Cytokinins ; Diameters ; ectomycorrhizae ; Ectomycorrhizas ; Forest ecosystems ; forests ; Fungi ; Genes ; Host plants ; Lactarius deliciosus ; Metabolism ; Metabolites ; metabolome ; Metabolomics ; Nutrient cycles ; phosphorus ; Phytohormones ; Pinus yunnanensis ; Plant communities ; Plant growth ; Plant hormones ; Retinoic acid ; sequence analysis ; Signal transduction ; Symbiosis ; Terrestrial ecosystems ; Tips ; transcription (genetics) ; transcriptome ; Transcriptomes ; Transcriptomics ; Vitamin A ; vitamin metabolism ; Vitamins</subject><ispartof>Physiologia plantarum, 2024-01, Vol.176 (1), p.n/a</ispartof><rights>2024 Scandinavian Plant Physiology Society.</rights><rights>2024 Scandinavian Plant Physiology Society</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3304-6d8bad63eb3bc228fab2a8510d374273ebd54bd9a3df3371729da842fc445a93</citedby><cites>FETCH-LOGICAL-c3304-6d8bad63eb3bc228fab2a8510d374273ebd54bd9a3df3371729da842fc445a93</cites><orcidid>0000-0001-6095-8235 ; 0000-0002-4118-2272</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.14194$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fppl.14194$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1416,27915,27916,45565,45566</link.rule.ids></links><search><creatorcontrib>Su, Kai</creatorcontrib><creatorcontrib>Yuan, Jing</creatorcontrib><creatorcontrib>Wang, Ran</creatorcontrib><creatorcontrib>Huang, Lanlan</creatorcontrib><creatorcontrib>Zhan, Jian</creatorcontrib><creatorcontrib>Zhang, Xueqiong</creatorcontrib><creatorcontrib>Wan, Shanping</creatorcontrib><creatorcontrib>He, Xinhua</creatorcontrib><creatorcontrib>Lambers, Hans</creatorcontrib><creatorcontrib>Yu, Fuqiang</creatorcontrib><creatorcontrib>Wang, Yanliang</creatorcontrib><title>Dual transcriptomic and metabolomic analyses provide novel insights into the role of vitamins A and B metabolism in ectomycorrhizal symbiosis between Pinus yunnanensis and Lactarius deliciosus</title><title>Physiologia plantarum</title><description>Ectomycorrhizal (EM) fungi play important roles in nutrient cycling and plant community establishment in forest ecosystems. Effects of EM formation on global alterations of the transcriptome and metabolome during plant‐fungal interaction and the key metabolites involved in EM development are largely unknown. Here, dual RNA‐Seq and untargeted metabolomic analyses were used to reveal stage‐specific and core responses of Pinus yunnanensis and Lactarius deliciosus during mycorrhizal colonization. We found that L. deliciosus colonization in P. yunnanensis roots induced different transcriptional changes across three interaction stages, with a small core of genes consistently regulated at all stages. Concentrations of retinol (vitamin A) and retinoic acid increased while that of B group vitamins decreased during EM formation, which was coordinately regulated by these two plant‐fungus partners, with L. deliciosus possibly playing a dominant role. Exogenous retinol altered the diameter and mantle thickness of P. yunnanensis ‐ L. deliciosus EM tips and affected host plant growth and phosphorus acquisition. In the absence of L. deliciosus, exogenous retinol increased the root diameter and the number of root tips of P. yunnanensis. Furthermore, the concentration of auxin increased, but that of abscisic acid decreased during EM formation, and the genes involved in plant hormone signal transduction were gradually activated, and auxin and cytokinin signal transduction potentially played a positive role in this EM symbiosis. In conclusion, we propose that the interaction of P. yunnanensis and L. deliciosus alters vitamin metabolism, which may further affect plant hormone biosynthesis and signal transduction, modulating root morphology and EM traits.</description><subject>Abscisic acid</subject><subject>Auxins</subject><subject>Biosynthesis</subject><subject>Colonization</subject><subject>Cytokinins</subject><subject>Diameters</subject><subject>ectomycorrhizae</subject><subject>Ectomycorrhizas</subject><subject>Forest ecosystems</subject><subject>forests</subject><subject>Fungi</subject><subject>Genes</subject><subject>Host plants</subject><subject>Lactarius deliciosus</subject><subject>Metabolism</subject><subject>Metabolites</subject><subject>metabolome</subject><subject>Metabolomics</subject><subject>Nutrient cycles</subject><subject>phosphorus</subject><subject>Phytohormones</subject><subject>Pinus yunnanensis</subject><subject>Plant communities</subject><subject>Plant growth</subject><subject>Plant hormones</subject><subject>Retinoic acid</subject><subject>sequence analysis</subject><subject>Signal transduction</subject><subject>Symbiosis</subject><subject>Terrestrial ecosystems</subject><subject>Tips</subject><subject>transcription (genetics)</subject><subject>transcriptome</subject><subject>Transcriptomes</subject><subject>Transcriptomics</subject><subject>Vitamin A</subject><subject>vitamin metabolism</subject><subject>Vitamins</subject><issn>0031-9317</issn><issn>1399-3054</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNp1kc1uEzEUhS0EEqGw4A0ssYHFtP5LZrwsLS1Ikciie8tje4grjz34elINT8ej4SRlg4Q3_rnfPce6B6H3lFzSuq6mKVxSQaV4gVaUS9lwshYv0YoQThvJafsavQF4JIRuNpSt0O_bWQdcso5gsp9KGr3BOlo8uqL7FJ7vOizgAE85Hbx1OKaDC9hH8D_2BeqhJFz2DucUHE4DPviix1rG1yetz3_VPIwVxs5Un8WknPf-V7WHZex9Ag-4d-XJuYh3Ps6AlzlGHV08Vo46W22Kzr5WrAve1JYZ3qJXgw7g3j3vF-jh7svDzddm-_3-2831tjGcE9FsbNdru-Gu571hrBt0z3S3psTyVrC2vtu16K3U3A6ct7Rl0upOsMEIsdaSX6CPZ9k6gp-zg6JGD8aFUP-XZlDVg_CuY5JV9MM_6GOacx0hKFYT4J3kJ-rTmTI5AWQ3qCn7UedFUaKOUaoapTpFWdmrM_vkg1v-D6rdbnvu-APJzKW1</recordid><startdate>202401</startdate><enddate>202401</enddate><creator>Su, Kai</creator><creator>Yuan, Jing</creator><creator>Wang, Ran</creator><creator>Huang, Lanlan</creator><creator>Zhan, Jian</creator><creator>Zhang, Xueqiong</creator><creator>Wan, Shanping</creator><creator>He, Xinhua</creator><creator>Lambers, Hans</creator><creator>Yu, Fuqiang</creator><creator>Wang, Yanliang</creator><general>Blackwell Publishing Ltd</general><general>Wiley Subscription Services, Inc</general><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>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0001-6095-8235</orcidid><orcidid>https://orcid.org/0000-0002-4118-2272</orcidid></search><sort><creationdate>202401</creationdate><title>Dual transcriptomic and metabolomic analyses provide novel insights into the role of vitamins A and B metabolism in ectomycorrhizal symbiosis between Pinus yunnanensis and Lactarius deliciosus</title><author>Su, Kai ; Yuan, Jing ; Wang, Ran ; Huang, Lanlan ; Zhan, Jian ; Zhang, Xueqiong ; Wan, Shanping ; He, Xinhua ; Lambers, Hans ; Yu, Fuqiang ; Wang, Yanliang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3304-6d8bad63eb3bc228fab2a8510d374273ebd54bd9a3df3371729da842fc445a93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Abscisic acid</topic><topic>Auxins</topic><topic>Biosynthesis</topic><topic>Colonization</topic><topic>Cytokinins</topic><topic>Diameters</topic><topic>ectomycorrhizae</topic><topic>Ectomycorrhizas</topic><topic>Forest ecosystems</topic><topic>forests</topic><topic>Fungi</topic><topic>Genes</topic><topic>Host plants</topic><topic>Lactarius deliciosus</topic><topic>Metabolism</topic><topic>Metabolites</topic><topic>metabolome</topic><topic>Metabolomics</topic><topic>Nutrient cycles</topic><topic>phosphorus</topic><topic>Phytohormones</topic><topic>Pinus yunnanensis</topic><topic>Plant communities</topic><topic>Plant growth</topic><topic>Plant hormones</topic><topic>Retinoic acid</topic><topic>sequence analysis</topic><topic>Signal transduction</topic><topic>Symbiosis</topic><topic>Terrestrial ecosystems</topic><topic>Tips</topic><topic>transcription (genetics)</topic><topic>transcriptome</topic><topic>Transcriptomes</topic><topic>Transcriptomics</topic><topic>Vitamin A</topic><topic>vitamin metabolism</topic><topic>Vitamins</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Su, Kai</creatorcontrib><creatorcontrib>Yuan, Jing</creatorcontrib><creatorcontrib>Wang, Ran</creatorcontrib><creatorcontrib>Huang, Lanlan</creatorcontrib><creatorcontrib>Zhan, Jian</creatorcontrib><creatorcontrib>Zhang, Xueqiong</creatorcontrib><creatorcontrib>Wan, Shanping</creatorcontrib><creatorcontrib>He, Xinhua</creatorcontrib><creatorcontrib>Lambers, Hans</creatorcontrib><creatorcontrib>Yu, Fuqiang</creatorcontrib><creatorcontrib>Wang, Yanliang</creatorcontrib><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>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Physiologia plantarum</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Su, Kai</au><au>Yuan, Jing</au><au>Wang, Ran</au><au>Huang, Lanlan</au><au>Zhan, Jian</au><au>Zhang, Xueqiong</au><au>Wan, Shanping</au><au>He, Xinhua</au><au>Lambers, Hans</au><au>Yu, Fuqiang</au><au>Wang, Yanliang</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Dual transcriptomic and metabolomic analyses provide novel insights into the role of vitamins A and B metabolism in ectomycorrhizal symbiosis between Pinus yunnanensis and Lactarius deliciosus</atitle><jtitle>Physiologia plantarum</jtitle><date>2024-01</date><risdate>2024</risdate><volume>176</volume><issue>1</issue><epage>n/a</epage><issn>0031-9317</issn><eissn>1399-3054</eissn><abstract>Ectomycorrhizal (EM) fungi play important roles in nutrient cycling and plant community establishment in forest ecosystems. Effects of EM formation on global alterations of the transcriptome and metabolome during plant‐fungal interaction and the key metabolites involved in EM development are largely unknown. Here, dual RNA‐Seq and untargeted metabolomic analyses were used to reveal stage‐specific and core responses of Pinus yunnanensis and Lactarius deliciosus during mycorrhizal colonization. We found that L. deliciosus colonization in P. yunnanensis roots induced different transcriptional changes across three interaction stages, with a small core of genes consistently regulated at all stages. Concentrations of retinol (vitamin A) and retinoic acid increased while that of B group vitamins decreased during EM formation, which was coordinately regulated by these two plant‐fungus partners, with L. deliciosus possibly playing a dominant role. Exogenous retinol altered the diameter and mantle thickness of P. yunnanensis ‐ L. deliciosus EM tips and affected host plant growth and phosphorus acquisition. In the absence of L. deliciosus, exogenous retinol increased the root diameter and the number of root tips of P. yunnanensis. Furthermore, the concentration of auxin increased, but that of abscisic acid decreased during EM formation, and the genes involved in plant hormone signal transduction were gradually activated, and auxin and cytokinin signal transduction potentially played a positive role in this EM symbiosis. In conclusion, we propose that the interaction of P. yunnanensis and L. deliciosus alters vitamin metabolism, which may further affect plant hormone biosynthesis and signal transduction, modulating root morphology and EM traits.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><doi>10.1111/ppl.14194</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0001-6095-8235</orcidid><orcidid>https://orcid.org/0000-0002-4118-2272</orcidid></addata></record> |
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subjects | Abscisic acid Auxins Biosynthesis Colonization Cytokinins Diameters ectomycorrhizae Ectomycorrhizas Forest ecosystems forests Fungi Genes Host plants Lactarius deliciosus Metabolism Metabolites metabolome Metabolomics Nutrient cycles phosphorus Phytohormones Pinus yunnanensis Plant communities Plant growth Plant hormones Retinoic acid sequence analysis Signal transduction Symbiosis Terrestrial ecosystems Tips transcription (genetics) transcriptome Transcriptomes Transcriptomics Vitamin A vitamin metabolism Vitamins |
title | Dual transcriptomic and metabolomic analyses provide novel insights into the role of vitamins A and B metabolism in ectomycorrhizal symbiosis between Pinus yunnanensis and Lactarius deliciosus |
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