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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Veröffentlicht in:Plant science (Limerick) 2025-01, Vol.350, p.112320, Article 112320
Hauptverfasser: Xin, Cuihua, Wang, Junjie, Chi, Junling, Xu, Yang, Liang, Ruiping, Jian, Lei, Wang, Liangming, Guo, Jiangbo
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container_title Plant science (Limerick)
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Wang, Junjie
Chi, Junling
Xu, Yang
Liang, Ruiping
Jian, Lei
Wang, Liangming
Guo, Jiangbo
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.
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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><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. 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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 ; 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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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identifier ISSN: 0168-9452
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source MEDLINE; Elsevier ScienceDirect Journals
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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