Combined Analysis of the Metabolome and Transcriptome to Explore Heat Stress Responses and Adaptation Mechanisms in Celery ( Apium graveolens L.)
Celery is an important leafy vegetable that can grow during the cool season and does not tolerate high temperatures. Heat stress is widely acknowledged as one of the main abiotic stresses affecting the growth and yield of celery. The morphological and physiological indices of celery were investigate...
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| Veröffentlicht in: | International journal of molecular sciences 2022-03, Vol.23 (6), p.3367 |
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| creator | Li, Mengyao Li, Jie Zhang, Ran Lin, Yuanxiu Xiong, Aisheng Tan, Guofei Luo, Ya Zhang, Yong Chen, Qing Wang, Yan Zhang, Yunting Wang, Xiaorong Tang, Haoru |
| description | Celery is an important leafy vegetable that can grow during the cool season and does not tolerate high temperatures. Heat stress is widely acknowledged as one of the main abiotic stresses affecting the growth and yield of celery. The morphological and physiological indices of celery were investigated in the present study to explore the physiological mechanisms in response to high temperatures. Results showed that the antioxidant enzyme activity, proline, relative conductivity, and malondialdehyde were increased, while chlorophyll and the water content of leaves decreased under high-temperature conditions. Short-term heat treatment increased the stomatal conductance to cool off the leaves by transpiration; however, long-term heat treatment led to stomatal closure to prevent leaf dehydration. In addition, high temperature caused a disordered arrangement of palisade tissue and a loose arrangement of spongy tissue in celery leaves. Combined metabolomic and transcriptomic analyses were further used to reveal the regulatory mechanisms in response to heat stress at the molecular level in celery. A total of 1003 differential metabolites were identified and significantly enriched in amino acid metabolism and the tricarboxilic acid (TCA) cycle. Transcriptome sequencing detected 24,264 different genes, including multiple transcription factor families such as HSF, WRKY, MYB, AP2, bZIP, and bHLH family members that were significantly upregulated in response to heat stress, suggesting that these genes were involved in the response to heat stress. In addition, transcriptional and metabolic pathway analyses showed that heat stress inhibited the glycolysis pathway and delayed the TCA cycle but increased the expression of most amino acid synthesis pathways such as proline, arginine, and serine, consistent with the results of physiological indicators. qRT-PCR further showed that the expression pattern was similar to the expression abundance in the transcriptome. The important metabolites and genes in celery that significantly contributed to the response to high temperatures were identified in the present study, which provided the theoretical basis for breeding heat-resistant celery. |
| doi_str_mv | 10.3390/ijms23063367 |
| format | Article |
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Heat stress is widely acknowledged as one of the main abiotic stresses affecting the growth and yield of celery. The morphological and physiological indices of celery were investigated in the present study to explore the physiological mechanisms in response to high temperatures. Results showed that the antioxidant enzyme activity, proline, relative conductivity, and malondialdehyde were increased, while chlorophyll and the water content of leaves decreased under high-temperature conditions. Short-term heat treatment increased the stomatal conductance to cool off the leaves by transpiration; however, long-term heat treatment led to stomatal closure to prevent leaf dehydration. In addition, high temperature caused a disordered arrangement of palisade tissue and a loose arrangement of spongy tissue in celery leaves. Combined metabolomic and transcriptomic analyses were further used to reveal the regulatory mechanisms in response to heat stress at the molecular level in celery. A total of 1003 differential metabolites were identified and significantly enriched in amino acid metabolism and the tricarboxilic acid (TCA) cycle. Transcriptome sequencing detected 24,264 different genes, including multiple transcription factor families such as HSF, WRKY, MYB, AP2, bZIP, and bHLH family members that were significantly upregulated in response to heat stress, suggesting that these genes were involved in the response to heat stress. In addition, transcriptional and metabolic pathway analyses showed that heat stress inhibited the glycolysis pathway and delayed the TCA cycle but increased the expression of most amino acid synthesis pathways such as proline, arginine, and serine, consistent with the results of physiological indicators. qRT-PCR further showed that the expression pattern was similar to the expression abundance in the transcriptome. The important metabolites and genes in celery that significantly contributed to the response to high temperatures were identified in the present study, which provided the theoretical basis for breeding heat-resistant celery.</description><identifier>ISSN: 1422-0067</identifier><identifier>ISSN: 1661-6596</identifier><identifier>EISSN: 1422-0067</identifier><identifier>DOI: 10.3390/ijms23063367</identifier><identifier>PMID: 35328788</identifier><language>eng</language><publisher>Switzerland: MDPI AG</publisher><subject>Adaptation ; Amino Acids - metabolism ; Antioxidants ; Apium ; Celery ; Chlorophyll ; Climate change ; Cool season ; Dehydration ; Enzymatic activity ; Enzyme activity ; Enzymes ; Gene Expression Regulation, Plant ; Genes ; Genotype & phenotype ; Glycolysis ; Heat ; Heat resistance ; Heat shock proteins ; Heat stress ; Heat treatment ; Heat treatments ; Heat-Shock Response - genetics ; High temperature ; Homeostasis ; Leaves ; Malondialdehyde ; Metabolic pathways ; Metabolism ; Metabolites ; Metabolome ; Metabolomics ; Moisture content ; Physiology ; Plant Breeding ; Plant Leaves - metabolism ; Proline ; Proline - metabolism ; Quality control ; Signal transduction ; Stomata ; Stress response ; Stress, Physiological - genetics ; Transcription factors ; Transcriptome ; Transcriptomes ; Transcriptomics ; Transpiration ; Tricarboxylic acid cycle ; Vegetables - metabolism ; Water content</subject><ispartof>International journal of molecular sciences, 2022-03, Vol.23 (6), p.3367</ispartof><rights>2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2022 by the authors. 2022</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c412t-c571822effabc88ab60ee7d10541f2bfc34fe0e45b61a8cc295cbc6965f791473</citedby><cites>FETCH-LOGICAL-c412t-c571822effabc88ab60ee7d10541f2bfc34fe0e45b61a8cc295cbc6965f791473</cites><orcidid>0000-0002-2281-4481 ; 0000-0002-3199-9465 ; 0000-0001-6008-2747 ; 0000-0002-9332-9571 ; 0000-0002-6542-7836 ; 0000-0002-7900-5001 ; 0000-0002-2460-7697</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/PMC8950972/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8950972/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35328788$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Li, Mengyao</creatorcontrib><creatorcontrib>Li, Jie</creatorcontrib><creatorcontrib>Zhang, Ran</creatorcontrib><creatorcontrib>Lin, Yuanxiu</creatorcontrib><creatorcontrib>Xiong, Aisheng</creatorcontrib><creatorcontrib>Tan, Guofei</creatorcontrib><creatorcontrib>Luo, Ya</creatorcontrib><creatorcontrib>Zhang, Yong</creatorcontrib><creatorcontrib>Chen, Qing</creatorcontrib><creatorcontrib>Wang, Yan</creatorcontrib><creatorcontrib>Zhang, Yunting</creatorcontrib><creatorcontrib>Wang, Xiaorong</creatorcontrib><creatorcontrib>Tang, Haoru</creatorcontrib><title>Combined Analysis of the Metabolome and Transcriptome to Explore Heat Stress Responses and Adaptation Mechanisms in Celery ( Apium graveolens L.)</title><title>International journal of molecular sciences</title><addtitle>Int J Mol Sci</addtitle><description>Celery is an important leafy vegetable that can grow during the cool season and does not tolerate high temperatures. Heat stress is widely acknowledged as one of the main abiotic stresses affecting the growth and yield of celery. The morphological and physiological indices of celery were investigated in the present study to explore the physiological mechanisms in response to high temperatures. Results showed that the antioxidant enzyme activity, proline, relative conductivity, and malondialdehyde were increased, while chlorophyll and the water content of leaves decreased under high-temperature conditions. Short-term heat treatment increased the stomatal conductance to cool off the leaves by transpiration; however, long-term heat treatment led to stomatal closure to prevent leaf dehydration. In addition, high temperature caused a disordered arrangement of palisade tissue and a loose arrangement of spongy tissue in celery leaves. Combined metabolomic and transcriptomic analyses were further used to reveal the regulatory mechanisms in response to heat stress at the molecular level in celery. A total of 1003 differential metabolites were identified and significantly enriched in amino acid metabolism and the tricarboxilic acid (TCA) cycle. Transcriptome sequencing detected 24,264 different genes, including multiple transcription factor families such as HSF, WRKY, MYB, AP2, bZIP, and bHLH family members that were significantly upregulated in response to heat stress, suggesting that these genes were involved in the response to heat stress. In addition, transcriptional and metabolic pathway analyses showed that heat stress inhibited the glycolysis pathway and delayed the TCA cycle but increased the expression of most amino acid synthesis pathways such as proline, arginine, and serine, consistent with the results of physiological indicators. qRT-PCR further showed that the expression pattern was similar to the expression abundance in the transcriptome. The important metabolites and genes in celery that significantly contributed to the response to high temperatures were identified in the present study, which provided the theoretical basis for breeding heat-resistant celery.</description><subject>Adaptation</subject><subject>Amino Acids - metabolism</subject><subject>Antioxidants</subject><subject>Apium</subject><subject>Celery</subject><subject>Chlorophyll</subject><subject>Climate change</subject><subject>Cool season</subject><subject>Dehydration</subject><subject>Enzymatic activity</subject><subject>Enzyme activity</subject><subject>Enzymes</subject><subject>Gene Expression Regulation, Plant</subject><subject>Genes</subject><subject>Genotype & phenotype</subject><subject>Glycolysis</subject><subject>Heat</subject><subject>Heat resistance</subject><subject>Heat shock proteins</subject><subject>Heat stress</subject><subject>Heat treatment</subject><subject>Heat treatments</subject><subject>Heat-Shock Response - genetics</subject><subject>High temperature</subject><subject>Homeostasis</subject><subject>Leaves</subject><subject>Malondialdehyde</subject><subject>Metabolic pathways</subject><subject>Metabolism</subject><subject>Metabolites</subject><subject>Metabolome</subject><subject>Metabolomics</subject><subject>Moisture content</subject><subject>Physiology</subject><subject>Plant Breeding</subject><subject>Plant Leaves - metabolism</subject><subject>Proline</subject><subject>Proline - metabolism</subject><subject>Quality control</subject><subject>Signal transduction</subject><subject>Stomata</subject><subject>Stress response</subject><subject>Stress, Physiological - genetics</subject><subject>Transcription factors</subject><subject>Transcriptome</subject><subject>Transcriptomes</subject><subject>Transcriptomics</subject><subject>Transpiration</subject><subject>Tricarboxylic acid cycle</subject><subject>Vegetables - metabolism</subject><subject>Water content</subject><issn>1422-0067</issn><issn>1661-6596</issn><issn>1422-0067</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>BENPR</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNpdkU1v1DAQhiNERUvhxhlZ4lIktjj-SOxLpdWq0EqLkKCcLceZdL1K7OBxKvZn8I9JP7XlNKOZZ17NzFsU70p6yrmmn_12QMZpxXlVvyiOSsHYgtKqfrmXHxavEbeUMs6kflUccsmZqpU6Kv6u4tD4AC1ZBtvv0COJHckbIN8g2yb2cQBiQ0uukg3okh_zbSVHcv5n7GMCcgE2k585ASL5ATjGgIB3I8vWjtlmH8Ms5jY2eByQ-EBW0EPakROyHP00kOtkbyD2EJCsTz--KQ462yO8fYjHxa8v51eri8X6-9fL1XK9cKJkeeFkXSrGoOts45SyTUUB6rakUpQdazrHRQcUhGyq0irnmJaucZWuZFfrUtT8uDi71x2nZoDWQcjJ9mZMfrBpZ6L15nkn-I25jjdGaUl1zWaBkweBFH9PgNkMHh30vQ0QJzSsEoJSrpic0Q__ods4pfnhdxQTWmqtZurTPeVSREzQPS1TUnPrtdn3esbf7x_wBD-ay_8Bv0Cnow</recordid><startdate>20220320</startdate><enddate>20220320</enddate><creator>Li, Mengyao</creator><creator>Li, Jie</creator><creator>Zhang, Ran</creator><creator>Lin, Yuanxiu</creator><creator>Xiong, Aisheng</creator><creator>Tan, Guofei</creator><creator>Luo, Ya</creator><creator>Zhang, Yong</creator><creator>Chen, Qing</creator><creator>Wang, Yan</creator><creator>Zhang, Yunting</creator><creator>Wang, Xiaorong</creator><creator>Tang, Haoru</creator><general>MDPI AG</general><general>MDPI</general><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>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>K9.</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>MBDVC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-2281-4481</orcidid><orcidid>https://orcid.org/0000-0002-3199-9465</orcidid><orcidid>https://orcid.org/0000-0001-6008-2747</orcidid><orcidid>https://orcid.org/0000-0002-9332-9571</orcidid><orcidid>https://orcid.org/0000-0002-6542-7836</orcidid><orcidid>https://orcid.org/0000-0002-7900-5001</orcidid><orcidid>https://orcid.org/0000-0002-2460-7697</orcidid></search><sort><creationdate>20220320</creationdate><title>Combined Analysis of the Metabolome and Transcriptome to Explore Heat Stress Responses and Adaptation Mechanisms in Celery ( Apium graveolens L.)</title><author>Li, Mengyao ; Li, Jie ; Zhang, Ran ; Lin, Yuanxiu ; Xiong, Aisheng ; Tan, Guofei ; Luo, Ya ; Zhang, Yong ; Chen, Qing ; Wang, Yan ; Zhang, Yunting ; Wang, Xiaorong ; Tang, Haoru</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c412t-c571822effabc88ab60ee7d10541f2bfc34fe0e45b61a8cc295cbc6965f791473</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Adaptation</topic><topic>Amino Acids - metabolism</topic><topic>Antioxidants</topic><topic>Apium</topic><topic>Celery</topic><topic>Chlorophyll</topic><topic>Climate change</topic><topic>Cool season</topic><topic>Dehydration</topic><topic>Enzymatic activity</topic><topic>Enzyme activity</topic><topic>Enzymes</topic><topic>Gene Expression Regulation, Plant</topic><topic>Genes</topic><topic>Genotype & phenotype</topic><topic>Glycolysis</topic><topic>Heat</topic><topic>Heat resistance</topic><topic>Heat shock proteins</topic><topic>Heat stress</topic><topic>Heat treatment</topic><topic>Heat treatments</topic><topic>Heat-Shock Response - genetics</topic><topic>High temperature</topic><topic>Homeostasis</topic><topic>Leaves</topic><topic>Malondialdehyde</topic><topic>Metabolic pathways</topic><topic>Metabolism</topic><topic>Metabolites</topic><topic>Metabolome</topic><topic>Metabolomics</topic><topic>Moisture content</topic><topic>Physiology</topic><topic>Plant Breeding</topic><topic>Plant Leaves - metabolism</topic><topic>Proline</topic><topic>Proline - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>International journal of molecular sciences</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Li, Mengyao</au><au>Li, Jie</au><au>Zhang, Ran</au><au>Lin, Yuanxiu</au><au>Xiong, Aisheng</au><au>Tan, Guofei</au><au>Luo, Ya</au><au>Zhang, Yong</au><au>Chen, Qing</au><au>Wang, Yan</au><au>Zhang, Yunting</au><au>Wang, Xiaorong</au><au>Tang, Haoru</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Combined Analysis of the Metabolome and Transcriptome to Explore Heat Stress Responses and Adaptation Mechanisms in Celery ( Apium graveolens L.)</atitle><jtitle>International journal of molecular sciences</jtitle><addtitle>Int J Mol Sci</addtitle><date>2022-03-20</date><risdate>2022</risdate><volume>23</volume><issue>6</issue><spage>3367</spage><pages>3367-</pages><issn>1422-0067</issn><issn>1661-6596</issn><eissn>1422-0067</eissn><abstract>Celery is an important leafy vegetable that can grow during the cool season and does not tolerate high temperatures. Heat stress is widely acknowledged as one of the main abiotic stresses affecting the growth and yield of celery. The morphological and physiological indices of celery were investigated in the present study to explore the physiological mechanisms in response to high temperatures. Results showed that the antioxidant enzyme activity, proline, relative conductivity, and malondialdehyde were increased, while chlorophyll and the water content of leaves decreased under high-temperature conditions. Short-term heat treatment increased the stomatal conductance to cool off the leaves by transpiration; however, long-term heat treatment led to stomatal closure to prevent leaf dehydration. In addition, high temperature caused a disordered arrangement of palisade tissue and a loose arrangement of spongy tissue in celery leaves. Combined metabolomic and transcriptomic analyses were further used to reveal the regulatory mechanisms in response to heat stress at the molecular level in celery. A total of 1003 differential metabolites were identified and significantly enriched in amino acid metabolism and the tricarboxilic acid (TCA) cycle. Transcriptome sequencing detected 24,264 different genes, including multiple transcription factor families such as HSF, WRKY, MYB, AP2, bZIP, and bHLH family members that were significantly upregulated in response to heat stress, suggesting that these genes were involved in the response to heat stress. In addition, transcriptional and metabolic pathway analyses showed that heat stress inhibited the glycolysis pathway and delayed the TCA cycle but increased the expression of most amino acid synthesis pathways such as proline, arginine, and serine, consistent with the results of physiological indicators. qRT-PCR further showed that the expression pattern was similar to the expression abundance in the transcriptome. The important metabolites and genes in celery that significantly contributed to the response to high temperatures were identified in the present study, which provided the theoretical basis for breeding heat-resistant celery.</abstract><cop>Switzerland</cop><pub>MDPI AG</pub><pmid>35328788</pmid><doi>10.3390/ijms23063367</doi><orcidid>https://orcid.org/0000-0002-2281-4481</orcidid><orcidid>https://orcid.org/0000-0002-3199-9465</orcidid><orcidid>https://orcid.org/0000-0001-6008-2747</orcidid><orcidid>https://orcid.org/0000-0002-9332-9571</orcidid><orcidid>https://orcid.org/0000-0002-6542-7836</orcidid><orcidid>https://orcid.org/0000-0002-7900-5001</orcidid><orcidid>https://orcid.org/0000-0002-2460-7697</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1422-0067 |
| ispartof | International journal of molecular sciences, 2022-03, Vol.23 (6), p.3367 |
| issn | 1422-0067 1661-6596 1422-0067 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_8950972 |
| source | MDPI - Multidisciplinary Digital Publishing Institute; MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central |
| subjects | Adaptation Amino Acids - metabolism Antioxidants Apium Celery Chlorophyll Climate change Cool season Dehydration Enzymatic activity Enzyme activity Enzymes Gene Expression Regulation, Plant Genes Genotype & phenotype Glycolysis Heat Heat resistance Heat shock proteins Heat stress Heat treatment Heat treatments Heat-Shock Response - genetics High temperature Homeostasis Leaves Malondialdehyde Metabolic pathways Metabolism Metabolites Metabolome Metabolomics Moisture content Physiology Plant Breeding Plant Leaves - metabolism Proline Proline - metabolism Quality control Signal transduction Stomata Stress response Stress, Physiological - genetics Transcription factors Transcriptome Transcriptomes Transcriptomics Transpiration Tricarboxylic acid cycle Vegetables - metabolism Water content |
| title | Combined Analysis of the Metabolome and Transcriptome to Explore Heat Stress Responses and Adaptation Mechanisms in Celery ( Apium graveolens L.) |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-14T12%3A35%3A34IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Combined%20Analysis%20of%20the%20Metabolome%20and%20Transcriptome%20to%20Explore%20Heat%20Stress%20Responses%20and%20Adaptation%20Mechanisms%20in%20Celery%20(%20Apium%20graveolens%20L.)&rft.jtitle=International%20journal%20of%20molecular%20sciences&rft.au=Li,%20Mengyao&rft.date=2022-03-20&rft.volume=23&rft.issue=6&rft.spage=3367&rft.pages=3367-&rft.issn=1422-0067&rft.eissn=1422-0067&rft_id=info:doi/10.3390/ijms23063367&rft_dat=%3Cproquest_pubme%3E2642495998%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2642495998&rft_id=info:pmid/35328788&rfr_iscdi=true |