Intragenic cytosine methylation modification regulates the response of SUCLα1 to lower temperature in Solanaceae
The tricarboxylic acid cycle (TCAC) is a fundamental metabolic process governing matter and energy in plant cells, playing an indispensable role. However, its involvement in responding to low temperature stress in potato remains poorly understood. Previous studies have identified succinyl-CoA ligase...
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description | The tricarboxylic acid cycle (TCAC) is a fundamental metabolic process governing matter and energy in plant cells, playing an indispensable role. However, its involvement in responding to low temperature stress in potato remains poorly understood. Previous studies have identified succinyl-CoA ligase (SUCL), which catalyzes the phosphorylation of TCAC substrates, as a gene associated with lower temperatures. Nevertheless, its function in potato's response to lower temperatures remains unclear. Phylogenetic analysis has revealed that Solanum tuberosum possesses α and β subunits of SUCL, which cluster with those of Solanum lycopersicum, Nicotiana tabacum and Nicotiana benthamiana. Further investigation has shown that StSUCLα1 is predominantly located within mitochondria. Low temperatures induce methylation modification alterations at 11 intragenic cytosine sites and lead to changes in StSUCLα1 expression levels. Correlation analysis suggests that alterations in intragenic cytosine methylation sites of SUCLα1 may be associated with MET1. Knocking down NbSUCLα1, the homologous gene of StSUCLα1 in N. benthamiana, results in increased susceptibility to low temperature stress in plants. In summary, we have confirmed that SUCLα1 is a key gene modulated by intragenic cytosine methylation in response to lower temperatures, providing a novel target for genetic breeding aimed at enhancing potato tolerance to low temperature stress.
•Two of succinyl-CoA ligase (SUCL) subunits encoding genes were identified in potato.•Lower temperature induced alteration of intragenic cytosine sites methylation status in StSUCLα1 sequence.•Correlation analysis revealed MET1 contributed to alteration of intragenic cytosine sites methylation status in StSUCLα1.•SUCLα1 is a key gene in response to lower temperature in plants. |
doi_str_mv | 10.1016/j.plantsci.2024.112320 |
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•Two of succinyl-CoA ligase (SUCL) subunits encoding genes were identified in potato.•Lower temperature induced alteration of intragenic cytosine sites methylation status in StSUCLα1 sequence.•Correlation analysis revealed MET1 contributed to alteration of intragenic cytosine sites methylation status in StSUCLα1.•SUCLα1 is a key gene in response to lower temperature in plants.</description><identifier>ISSN: 0168-9452</identifier><identifier>ISSN: 1873-2259</identifier><identifier>EISSN: 1873-2259</identifier><identifier>DOI: 10.1016/j.plantsci.2024.112320</identifier><identifier>PMID: 39547447</identifier><language>eng</language><publisher>Ireland: Elsevier B.V</publisher><subject>cold stress ; Cold Temperature ; cold tolerance ; cytosine ; Cytosine - metabolism ; Cytosine methylation ; DNA Methylation ; energy ; Gene Expression Regulation, Plant ; genes ; ligases ; Lower temperature ; mitochondria ; Nicotiana - genetics ; Nicotiana benthamiana ; Nicotiana tabacum ; phosphorylation ; Phylogeny ; Plant Proteins - genetics ; Plant Proteins - metabolism ; potatoes ; Solanaceae ; Solanaceae - genetics ; Solanaceae - metabolism ; Solanaceae - physiology ; Solanum lycopersicum ; Solanum tuberosum ; Solanum tuberosum - genetics ; Solanum tuberosum - metabolism ; Succinyl-CoA ligase ; temperature ; tricarboxylic acid cycle</subject><ispartof>Plant science (Limerick), 2025-01, Vol.350, p.112320, Article 112320</ispartof><rights>2024 Elsevier B.V.</rights><rights>Copyright © 2024 Elsevier B.V. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c278t-7b021b48ccb1c22e707fa68be149d1902aa56a203e2ff78d4760f6aebbb906803</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0168945224003479$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39547447$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Xin, Cuihua</creatorcontrib><creatorcontrib>Wang, Junjie</creatorcontrib><creatorcontrib>Chi, Junling</creatorcontrib><creatorcontrib>Xu, Yang</creatorcontrib><creatorcontrib>Liang, Ruiping</creatorcontrib><creatorcontrib>Jian, Lei</creatorcontrib><creatorcontrib>Wang, Liangming</creatorcontrib><creatorcontrib>Guo, Jiangbo</creatorcontrib><title>Intragenic cytosine methylation modification regulates the response of SUCLα1 to lower temperature in Solanaceae</title><title>Plant science (Limerick)</title><addtitle>Plant Sci</addtitle><description>The tricarboxylic acid cycle (TCAC) is a fundamental metabolic process governing matter and energy in plant cells, playing an indispensable role. However, its involvement in responding to low temperature stress in potato remains poorly understood. Previous studies have identified succinyl-CoA ligase (SUCL), which catalyzes the phosphorylation of TCAC substrates, as a gene associated with lower temperatures. Nevertheless, its function in potato's response to lower temperatures remains unclear. Phylogenetic analysis has revealed that Solanum tuberosum possesses α and β subunits of SUCL, which cluster with those of Solanum lycopersicum, Nicotiana tabacum and Nicotiana benthamiana. Further investigation has shown that StSUCLα1 is predominantly located within mitochondria. Low temperatures induce methylation modification alterations at 11 intragenic cytosine sites and lead to changes in StSUCLα1 expression levels. Correlation analysis suggests that alterations in intragenic cytosine methylation sites of SUCLα1 may be associated with MET1. Knocking down NbSUCLα1, the homologous gene of StSUCLα1 in N. benthamiana, results in increased susceptibility to low temperature stress in plants. In summary, we have confirmed that SUCLα1 is a key gene modulated by intragenic cytosine methylation in response to lower temperatures, providing a novel target for genetic breeding aimed at enhancing potato tolerance to low temperature stress.
•Two of succinyl-CoA ligase (SUCL) subunits encoding genes were identified in potato.•Lower temperature induced alteration of intragenic cytosine sites methylation status in StSUCLα1 sequence.•Correlation analysis revealed MET1 contributed to alteration of intragenic cytosine sites methylation status in StSUCLα1.•SUCLα1 is a key gene in response to lower temperature in plants.</description><subject>cold stress</subject><subject>Cold Temperature</subject><subject>cold tolerance</subject><subject>cytosine</subject><subject>Cytosine - metabolism</subject><subject>Cytosine methylation</subject><subject>DNA Methylation</subject><subject>energy</subject><subject>Gene Expression Regulation, Plant</subject><subject>genes</subject><subject>ligases</subject><subject>Lower temperature</subject><subject>mitochondria</subject><subject>Nicotiana - genetics</subject><subject>Nicotiana benthamiana</subject><subject>Nicotiana tabacum</subject><subject>phosphorylation</subject><subject>Phylogeny</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>potatoes</subject><subject>Solanaceae</subject><subject>Solanaceae - genetics</subject><subject>Solanaceae - metabolism</subject><subject>Solanaceae - physiology</subject><subject>Solanum lycopersicum</subject><subject>Solanum tuberosum</subject><subject>Solanum tuberosum - genetics</subject><subject>Solanum tuberosum - metabolism</subject><subject>Succinyl-CoA ligase</subject><subject>temperature</subject><subject>tricarboxylic acid cycle</subject><issn>0168-9452</issn><issn>1873-2259</issn><issn>1873-2259</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2025</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkc1O3DAQgC1UBFvaV0A-9pLFv7Fza7VqC9JKPQBny3Em4FUSB9tptY_Fi_SZahTotT2NZvTNj-ZD6JKSLSW0vjps58FOOTm_ZYSJLaWMM3KCNlQrXjEmm3doU0BdNUKyc_Q-pQMhhEmpztA5b6RQQqgNerqZcrQPMHmH3TGH5CfAI-TH42CzDxMeQ-d779YkwsNS6pBwfoSSpTlMCXDo8e39bv_7meIc8BB-QcQZxhmizUsE7Cd8G8q51oGFD-i0t0OCj6_xAt1_-3q3u672P77f7L7sK8eUzpVqCaOt0M611DEGiqje1roFKpqONoRZK2vLCAfW90p3QtWkry20bduQWhN-gT6tc-cYnhZI2Yw-ORjKHRCWZDiVgtWca_kfKNONapjkBa1X1MWQUoTezNGPNh4NJebFjDmYNzPmxYxZzZTGy9cdSztC97ftTUUBPq8AlKf89BBNGQGTg85HcNl0wf9rxx899KUA</recordid><startdate>20250101</startdate><enddate>20250101</enddate><creator>Xin, Cuihua</creator><creator>Wang, Junjie</creator><creator>Chi, Junling</creator><creator>Xu, Yang</creator><creator>Liang, Ruiping</creator><creator>Jian, Lei</creator><creator>Wang, Liangming</creator><creator>Guo, Jiangbo</creator><general>Elsevier B.V</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>7X8</scope><scope>7S9</scope><scope>L.6</scope></search><sort><creationdate>20250101</creationdate><title>Intragenic cytosine methylation modification regulates the response of SUCLα1 to lower temperature in Solanaceae</title><author>Xin, Cuihua ; Wang, Junjie ; Chi, Junling ; Xu, Yang ; Liang, Ruiping ; Jian, Lei ; Wang, Liangming ; Guo, Jiangbo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c278t-7b021b48ccb1c22e707fa68be149d1902aa56a203e2ff78d4760f6aebbb906803</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2025</creationdate><topic>cold stress</topic><topic>Cold Temperature</topic><topic>cold tolerance</topic><topic>cytosine</topic><topic>Cytosine - metabolism</topic><topic>Cytosine methylation</topic><topic>DNA Methylation</topic><topic>energy</topic><topic>Gene Expression Regulation, Plant</topic><topic>genes</topic><topic>ligases</topic><topic>Lower temperature</topic><topic>mitochondria</topic><topic>Nicotiana - genetics</topic><topic>Nicotiana benthamiana</topic><topic>Nicotiana tabacum</topic><topic>phosphorylation</topic><topic>Phylogeny</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>potatoes</topic><topic>Solanaceae</topic><topic>Solanaceae - genetics</topic><topic>Solanaceae - metabolism</topic><topic>Solanaceae - physiology</topic><topic>Solanum lycopersicum</topic><topic>Solanum tuberosum</topic><topic>Solanum tuberosum - genetics</topic><topic>Solanum tuberosum - metabolism</topic><topic>Succinyl-CoA ligase</topic><topic>temperature</topic><topic>tricarboxylic acid cycle</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Xin, Cuihua</creatorcontrib><creatorcontrib>Wang, Junjie</creatorcontrib><creatorcontrib>Chi, Junling</creatorcontrib><creatorcontrib>Xu, Yang</creatorcontrib><creatorcontrib>Liang, Ruiping</creatorcontrib><creatorcontrib>Jian, Lei</creatorcontrib><creatorcontrib>Wang, Liangming</creatorcontrib><creatorcontrib>Guo, Jiangbo</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Plant science (Limerick)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Xin, Cuihua</au><au>Wang, Junjie</au><au>Chi, Junling</au><au>Xu, Yang</au><au>Liang, Ruiping</au><au>Jian, Lei</au><au>Wang, Liangming</au><au>Guo, Jiangbo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Intragenic cytosine methylation modification regulates the response of SUCLα1 to lower temperature in Solanaceae</atitle><jtitle>Plant science (Limerick)</jtitle><addtitle>Plant Sci</addtitle><date>2025-01-01</date><risdate>2025</risdate><volume>350</volume><spage>112320</spage><pages>112320-</pages><artnum>112320</artnum><issn>0168-9452</issn><issn>1873-2259</issn><eissn>1873-2259</eissn><abstract>The tricarboxylic acid cycle (TCAC) is a fundamental metabolic process governing matter and energy in plant cells, playing an indispensable role. However, its involvement in responding to low temperature stress in potato remains poorly understood. Previous studies have identified succinyl-CoA ligase (SUCL), which catalyzes the phosphorylation of TCAC substrates, as a gene associated with lower temperatures. Nevertheless, its function in potato's response to lower temperatures remains unclear. Phylogenetic analysis has revealed that Solanum tuberosum possesses α and β subunits of SUCL, which cluster with those of Solanum lycopersicum, Nicotiana tabacum and Nicotiana benthamiana. Further investigation has shown that StSUCLα1 is predominantly located within mitochondria. Low temperatures induce methylation modification alterations at 11 intragenic cytosine sites and lead to changes in StSUCLα1 expression levels. Correlation analysis suggests that alterations in intragenic cytosine methylation sites of SUCLα1 may be associated with MET1. Knocking down NbSUCLα1, the homologous gene of StSUCLα1 in N. benthamiana, results in increased susceptibility to low temperature stress in plants. In summary, we have confirmed that SUCLα1 is a key gene modulated by intragenic cytosine methylation in response to lower temperatures, providing a novel target for genetic breeding aimed at enhancing potato tolerance to low temperature stress.
•Two of succinyl-CoA ligase (SUCL) subunits encoding genes were identified in potato.•Lower temperature induced alteration of intragenic cytosine sites methylation status in StSUCLα1 sequence.•Correlation analysis revealed MET1 contributed to alteration of intragenic cytosine sites methylation status in StSUCLα1.•SUCLα1 is a key gene in response to lower temperature in plants.</abstract><cop>Ireland</cop><pub>Elsevier B.V</pub><pmid>39547447</pmid><doi>10.1016/j.plantsci.2024.112320</doi></addata></record> |
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subjects | cold stress Cold Temperature cold tolerance cytosine Cytosine - metabolism Cytosine methylation DNA Methylation energy Gene Expression Regulation, Plant genes ligases Lower temperature mitochondria Nicotiana - genetics Nicotiana benthamiana Nicotiana tabacum phosphorylation Phylogeny Plant Proteins - genetics Plant Proteins - metabolism potatoes Solanaceae Solanaceae - genetics Solanaceae - metabolism Solanaceae - physiology Solanum lycopersicum Solanum tuberosum Solanum tuberosum - genetics Solanum tuberosum - metabolism Succinyl-CoA ligase temperature tricarboxylic acid cycle |
title | Intragenic cytosine methylation modification regulates the response of SUCLα1 to lower temperature in Solanaceae |
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