Lipid metabolism during seed germination of Pistacia chinensis and its response to gibberellic acid
Lipid metabolism may play a critical role in fueling seed germination, but the knowledge of lipid metabolism during germination is still ambiguous. Here, we hypothesize that gibberellic acid (GA) promotes germination by means of enhancing lipid mobilization in Chinese pistachio (Pistacia chinensis B...
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description | Lipid metabolism may play a critical role in fueling seed germination, but the knowledge of lipid metabolism during germination is still ambiguous. Here, we hypothesize that gibberellic acid (GA) promotes germination by means of enhancing lipid mobilization in Chinese pistachio (Pistacia chinensis Bunge), a species belonging to Anacardiaceae with high oil content in its seeds. A multi-omics approach has been applied to measure lipid mobilization during seed germination, and to identify the key regulators involved in GA-mediated lipid metabolism. The results indicated that GA contents increased, while IAA, ABA and JA contents decreased during seed germination. GA3 increased significantly in the two germination stages (i.e. imbibition and radicle protrusion), and it was more abundant than GA1 and GA4. In addition, the relative content of most lipids decreased during germination, and the differentially changed metabolites were significantly enriched in lipid metabolic pathways based on KEGG analysis. WGCNA indicated that GA3 was correlated with more genes in lipid metabolic pathways. Transcriptomic analysis further revealed that differentially expressed genes (DEGs) related to fatty acid biosynthesis, glycerolipid metabolism, glycerophospholipid metabolism and starch and sucrose metabolism were upregulated under GA3 application, such as the acetyl-CoA carboxylase biotin carboxyl carrier protein (ACCB), fatty acyl-ACP thioesterase B (FATB), diacylglycerol acyltransferase (DGAT) and DEFECTIVE IN ANTHER DEHISCENCE 1 (DAD1). Therefore, our study supports the hypothesis that GA promotes seed germination in P. chinensis by enhancing lipid mobilization. This study proposes a novel mechanism of lipid responses to exogenous GA, which contributes to a deep understanding of germination of oleaginous seeds.
•GA contents increased, while IAA, ABA and JA contents decreased during seed germination.•The differentially changed metabolites and differentially expressed genes were significantly enriched in lipid metabolic pathways, and most lipids decreased during germination.•GA promotes seed germination in Pistacia chinensis by enhancing lipid mobilization. |
doi_str_mv | 10.1016/j.plaphy.2024.109371 |
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•GA contents increased, while IAA, ABA and JA contents decreased during seed germination.•The differentially changed metabolites and differentially expressed genes were significantly enriched in lipid metabolic pathways, and most lipids decreased during germination.•GA promotes seed germination in Pistacia chinensis by enhancing lipid mobilization.</description><identifier>ISSN: 0981-9428</identifier><identifier>ISSN: 1873-2690</identifier><identifier>EISSN: 1873-2690</identifier><identifier>DOI: 10.1016/j.plaphy.2024.109371</identifier><identifier>PMID: 39667083</identifier><language>eng</language><publisher>France: Elsevier Masson SAS</publisher><subject>acetyl-CoA carboxylase ; Anacardiaceae ; biosynthesis ; biotin ; dehiscence ; diacylglycerol acyltransferase ; fatty acids ; gene expression regulation ; Gibberellic acid ; glycerophospholipids ; imbibition ; lipid content ; Lipid metabolism ; metabolites ; multiomics ; pistachios ; Pistacia chinensis ; Pistacia chinensis Bunge ; Seed dormancy ; Seed germination ; species ; starch ; sucrose ; transcriptomics</subject><ispartof>Plant physiology and biochemistry, 2025-02, Vol.219, p.109371, Article 109371</ispartof><rights>2024 Elsevier Masson SAS</rights><rights>Copyright © 2024 Elsevier Masson SAS. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c274t-d8315629b43963d08501abbe595c69950ed2cad6062a9644b0d54a56e35ebcf23</cites><orcidid>0000-0002-6958-0205</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0981942824010398$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3536,27903,27904,65309</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39667083$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Guo, Huanhuan</creatorcontrib><creatorcontrib>Li, Jinjin</creatorcontrib><creatorcontrib>Liu, Yong</creatorcontrib><creatorcontrib>Fernández-Pascual, Eduardo</creatorcontrib><title>Lipid metabolism during seed germination of Pistacia chinensis and its response to gibberellic acid</title><title>Plant physiology and biochemistry</title><addtitle>Plant Physiol Biochem</addtitle><description>Lipid metabolism may play a critical role in fueling seed germination, but the knowledge of lipid metabolism during germination is still ambiguous. Here, we hypothesize that gibberellic acid (GA) promotes germination by means of enhancing lipid mobilization in Chinese pistachio (Pistacia chinensis Bunge), a species belonging to Anacardiaceae with high oil content in its seeds. A multi-omics approach has been applied to measure lipid mobilization during seed germination, and to identify the key regulators involved in GA-mediated lipid metabolism. The results indicated that GA contents increased, while IAA, ABA and JA contents decreased during seed germination. GA3 increased significantly in the two germination stages (i.e. imbibition and radicle protrusion), and it was more abundant than GA1 and GA4. In addition, the relative content of most lipids decreased during germination, and the differentially changed metabolites were significantly enriched in lipid metabolic pathways based on KEGG analysis. WGCNA indicated that GA3 was correlated with more genes in lipid metabolic pathways. Transcriptomic analysis further revealed that differentially expressed genes (DEGs) related to fatty acid biosynthesis, glycerolipid metabolism, glycerophospholipid metabolism and starch and sucrose metabolism were upregulated under GA3 application, such as the acetyl-CoA carboxylase biotin carboxyl carrier protein (ACCB), fatty acyl-ACP thioesterase B (FATB), diacylglycerol acyltransferase (DGAT) and DEFECTIVE IN ANTHER DEHISCENCE 1 (DAD1). Therefore, our study supports the hypothesis that GA promotes seed germination in P. chinensis by enhancing lipid mobilization. This study proposes a novel mechanism of lipid responses to exogenous GA, which contributes to a deep understanding of germination of oleaginous seeds.
•GA contents increased, while IAA, ABA and JA contents decreased during seed germination.•The differentially changed metabolites and differentially expressed genes were significantly enriched in lipid metabolic pathways, and most lipids decreased during germination.•GA promotes seed germination in Pistacia chinensis by enhancing lipid mobilization.</description><subject>acetyl-CoA carboxylase</subject><subject>Anacardiaceae</subject><subject>biosynthesis</subject><subject>biotin</subject><subject>dehiscence</subject><subject>diacylglycerol acyltransferase</subject><subject>fatty acids</subject><subject>gene expression regulation</subject><subject>Gibberellic acid</subject><subject>glycerophospholipids</subject><subject>imbibition</subject><subject>lipid content</subject><subject>Lipid metabolism</subject><subject>metabolites</subject><subject>multiomics</subject><subject>pistachios</subject><subject>Pistacia chinensis</subject><subject>Pistacia chinensis Bunge</subject><subject>Seed dormancy</subject><subject>Seed germination</subject><subject>species</subject><subject>starch</subject><subject>sucrose</subject><subject>transcriptomics</subject><issn>0981-9428</issn><issn>1873-2690</issn><issn>1873-2690</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2025</creationdate><recordtype>article</recordtype><recordid>eNqNkc2LFDEQxYMo7rj6H4jk6KXHfHfnIsiyfsCAHvQc0knNbA3dSZv0CPvfm6VXj-KpoPjVe496hLzmbM8ZN-_O-2Xyy939XjCh2srKnj8hOz70shPGsqdkx-zAO6vEcEVe1HpmrJG9fE6upDWmZ4PckXDABSOdYfVjnrDONF4KphOtAJGeoMyY_Io50Xyk37CuPqCn4Q4TpIqV-hQprpUWqEtOFeia6QnHEQpMEwba8PiSPDv6qcKrx3lNfny8_X7zuTt8_fTl5sOhC6JXaxcHybURdlQtnoxs0Iz7pqStDsZazSCK4KNhRnhrlBpZ1MprA1LDGI5CXpO3m-5S8s8L1NXNWEPL4RPkS3VNXgmluOL_gSpjjJRWN1RtaCi51gJHtxScfbl3nLmHJtzZbU24hybc1kQ7e_PocBlniH-P_ry-Ae83ANpLfiEUVwNCChCxQFhdzPhvh996MJvN</recordid><startdate>20250201</startdate><enddate>20250201</enddate><creator>Guo, Huanhuan</creator><creator>Li, Jinjin</creator><creator>Liu, Yong</creator><creator>Fernández-Pascual, Eduardo</creator><general>Elsevier Masson SAS</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0002-6958-0205</orcidid></search><sort><creationdate>20250201</creationdate><title>Lipid metabolism during seed germination of Pistacia chinensis and its response to gibberellic acid</title><author>Guo, Huanhuan ; Li, Jinjin ; Liu, Yong ; Fernández-Pascual, Eduardo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c274t-d8315629b43963d08501abbe595c69950ed2cad6062a9644b0d54a56e35ebcf23</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2025</creationdate><topic>acetyl-CoA carboxylase</topic><topic>Anacardiaceae</topic><topic>biosynthesis</topic><topic>biotin</topic><topic>dehiscence</topic><topic>diacylglycerol acyltransferase</topic><topic>fatty acids</topic><topic>gene expression regulation</topic><topic>Gibberellic acid</topic><topic>glycerophospholipids</topic><topic>imbibition</topic><topic>lipid content</topic><topic>Lipid metabolism</topic><topic>metabolites</topic><topic>multiomics</topic><topic>pistachios</topic><topic>Pistacia chinensis</topic><topic>Pistacia chinensis Bunge</topic><topic>Seed dormancy</topic><topic>Seed germination</topic><topic>species</topic><topic>starch</topic><topic>sucrose</topic><topic>transcriptomics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Guo, Huanhuan</creatorcontrib><creatorcontrib>Li, Jinjin</creatorcontrib><creatorcontrib>Liu, Yong</creatorcontrib><creatorcontrib>Fernández-Pascual, Eduardo</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Plant physiology and biochemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Guo, Huanhuan</au><au>Li, Jinjin</au><au>Liu, Yong</au><au>Fernández-Pascual, Eduardo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Lipid metabolism during seed germination of Pistacia chinensis and its response to gibberellic acid</atitle><jtitle>Plant physiology and biochemistry</jtitle><addtitle>Plant Physiol Biochem</addtitle><date>2025-02-01</date><risdate>2025</risdate><volume>219</volume><spage>109371</spage><pages>109371-</pages><artnum>109371</artnum><issn>0981-9428</issn><issn>1873-2690</issn><eissn>1873-2690</eissn><abstract>Lipid metabolism may play a critical role in fueling seed germination, but the knowledge of lipid metabolism during germination is still ambiguous. Here, we hypothesize that gibberellic acid (GA) promotes germination by means of enhancing lipid mobilization in Chinese pistachio (Pistacia chinensis Bunge), a species belonging to Anacardiaceae with high oil content in its seeds. A multi-omics approach has been applied to measure lipid mobilization during seed germination, and to identify the key regulators involved in GA-mediated lipid metabolism. The results indicated that GA contents increased, while IAA, ABA and JA contents decreased during seed germination. GA3 increased significantly in the two germination stages (i.e. imbibition and radicle protrusion), and it was more abundant than GA1 and GA4. In addition, the relative content of most lipids decreased during germination, and the differentially changed metabolites were significantly enriched in lipid metabolic pathways based on KEGG analysis. WGCNA indicated that GA3 was correlated with more genes in lipid metabolic pathways. Transcriptomic analysis further revealed that differentially expressed genes (DEGs) related to fatty acid biosynthesis, glycerolipid metabolism, glycerophospholipid metabolism and starch and sucrose metabolism were upregulated under GA3 application, such as the acetyl-CoA carboxylase biotin carboxyl carrier protein (ACCB), fatty acyl-ACP thioesterase B (FATB), diacylglycerol acyltransferase (DGAT) and DEFECTIVE IN ANTHER DEHISCENCE 1 (DAD1). Therefore, our study supports the hypothesis that GA promotes seed germination in P. chinensis by enhancing lipid mobilization. This study proposes a novel mechanism of lipid responses to exogenous GA, which contributes to a deep understanding of germination of oleaginous seeds.
•GA contents increased, while IAA, ABA and JA contents decreased during seed germination.•The differentially changed metabolites and differentially expressed genes were significantly enriched in lipid metabolic pathways, and most lipids decreased during germination.•GA promotes seed germination in Pistacia chinensis by enhancing lipid mobilization.</abstract><cop>France</cop><pub>Elsevier Masson SAS</pub><pmid>39667083</pmid><doi>10.1016/j.plaphy.2024.109371</doi><orcidid>https://orcid.org/0000-0002-6958-0205</orcidid></addata></record> |
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subjects | acetyl-CoA carboxylase Anacardiaceae biosynthesis biotin dehiscence diacylglycerol acyltransferase fatty acids gene expression regulation Gibberellic acid glycerophospholipids imbibition lipid content Lipid metabolism metabolites multiomics pistachios Pistacia chinensis Pistacia chinensis Bunge Seed dormancy Seed germination species starch sucrose transcriptomics |
title | Lipid metabolism during seed germination of Pistacia chinensis and its response to gibberellic acid |
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