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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Veröffentlicht in:Plant physiology and biochemistry 2025-02, Vol.219, p.109371, Article 109371
Hauptverfasser: Guo, Huanhuan, Li, Jinjin, Liu, Yong, Fernández-Pascual, Eduardo
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Li, Jinjin
Liu, Yong
Fernández-Pascual, Eduardo
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.
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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><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. 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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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