Rhamnogalacturonan lyase 1 (RGL1), as a suppressor of E3 ubiquitin ligase Arabidopsis thaliana ring zinc finger 1 (AtRZF1), is involved in dehydration response to mediate proline synthesis and pectin rhamnogalacturonan‐I composition
SUMMARY Proline metabolism plays a crucial role in both environmental stress responses and plant growth. However, the specific mechanism by which proline contributes to abiotic stress processes remains to be elucidated. In this study, we utilized atrzf1 (Arabidopsis thaliana ring zinc finger 1) as a...
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description | SUMMARY
Proline metabolism plays a crucial role in both environmental stress responses and plant growth. However, the specific mechanism by which proline contributes to abiotic stress processes remains to be elucidated. In this study, we utilized atrzf1 (Arabidopsis thaliana ring zinc finger 1) as a parental line for T‐DNA tagging mutagenesis and identified a suppressor mutant of atrzf1, designated proline content alterative 31 (pca31). The pca31 mutant suppressed the insensitivity of atrzf1 to dehydration stress during early seedling growth. Using Thermal Asymmetric Interlaced‐PCR, we found that the T‐DNA of pca31 was inserted into the promoter region of the At2g22620 gene, which encodes the cell wall enzyme rhamnogalacturonan lyase 1 (RGL1). Enzymatic assays indicated that RGL1 exhibited rhamnogalacturonan lyase activity, influencing cell wall pectin composition. The decrease in RGL1 gene expression suppressed the transcriptomic perturbation of the atrzf1 mutant. Silencing of the RGL1 gene in atrzf1 resulted in a sensitive phenotype similar to pca31 under osmotic stress conditions. Treatment with mannitol, salt, hydrogen peroxide, and abscisic acid induced RGL1 expression. Furthermore, we uncovered that RGL1 plays a role in modulating root growth and vascular tissue development. Molecular, physiological, and genetic experiments revealed that the positive modulation of RGL1 during abiotic stress was linked to the AtRZF1 pathway. Taken together, these findings establish that pca31 acts as a suppressor of atrzf1 in abiotic stress responses through proline and cell wall metabolisms.
Significance Statement
RGL1 exhibits rhamnogalacturonan lyase activity, which contributes to the modulation of pectin composition, vascular tissue development, and root growth. RGL1, as a suppressor of E3 ubiquitin ligase AtRZF1, functions as a positive modulator in proline synthesis and cell wall metabolism under osmotic stress conditions. |
doi_str_mv | 10.1111/tpj.16808 |
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Proline metabolism plays a crucial role in both environmental stress responses and plant growth. However, the specific mechanism by which proline contributes to abiotic stress processes remains to be elucidated. In this study, we utilized atrzf1 (Arabidopsis thaliana ring zinc finger 1) as a parental line for T‐DNA tagging mutagenesis and identified a suppressor mutant of atrzf1, designated proline content alterative 31 (pca31). The pca31 mutant suppressed the insensitivity of atrzf1 to dehydration stress during early seedling growth. Using Thermal Asymmetric Interlaced‐PCR, we found that the T‐DNA of pca31 was inserted into the promoter region of the At2g22620 gene, which encodes the cell wall enzyme rhamnogalacturonan lyase 1 (RGL1). Enzymatic assays indicated that RGL1 exhibited rhamnogalacturonan lyase activity, influencing cell wall pectin composition. The decrease in RGL1 gene expression suppressed the transcriptomic perturbation of the atrzf1 mutant. Silencing of the RGL1 gene in atrzf1 resulted in a sensitive phenotype similar to pca31 under osmotic stress conditions. Treatment with mannitol, salt, hydrogen peroxide, and abscisic acid induced RGL1 expression. Furthermore, we uncovered that RGL1 plays a role in modulating root growth and vascular tissue development. Molecular, physiological, and genetic experiments revealed that the positive modulation of RGL1 during abiotic stress was linked to the AtRZF1 pathway. Taken together, these findings establish that pca31 acts as a suppressor of atrzf1 in abiotic stress responses through proline and cell wall metabolisms.
Significance Statement
RGL1 exhibits rhamnogalacturonan lyase activity, which contributes to the modulation of pectin composition, vascular tissue development, and root growth. RGL1, as a suppressor of E3 ubiquitin ligase AtRZF1, functions as a positive modulator in proline synthesis and cell wall metabolism under osmotic stress conditions.</description><identifier>ISSN: 0960-7412</identifier><identifier>ISSN: 1365-313X</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/tpj.16808</identifier><identifier>PMID: 38743860</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Abiotic stress ; abiotic stress response ; Abscisic acid ; Arabidopsis - genetics ; Arabidopsis - metabolism ; Arabidopsis - physiology ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Arabidopsis thaliana ; AtRZF1 ; Cell Wall - metabolism ; Cell walls ; Cellular stress response ; Composition ; Dehydration ; Deoxyribonucleic acid ; DNA ; Environmental stress ; Gene expression ; Gene Expression Regulation, Plant ; genes ; Hydrogen peroxide ; Mannitol ; metabolism ; Mutagenesis ; mutants ; Osmotic stress ; Pectin ; pectin content ; pectins ; Pectins - metabolism ; phenotype ; Phenotypes ; Plant growth ; Plant tissues ; Plants, Genetically Modified ; Polysaccharide-Lyases - genetics ; Polysaccharide-Lyases - metabolism ; Proline ; Proline - metabolism ; promoter regions ; Rhamnogalacturonan ; rhamnogalacturonan lyase ; root growth ; seedling growth ; Seedlings ; Stress, Physiological ; suppressor ; Suppressor mutant ; Transcriptomics ; Ubiquitin-protein ligase ; Ubiquitin-Protein Ligases - genetics ; Ubiquitin-Protein Ligases - metabolism ; vascular bundle ; Vascular tissue ; Zinc ; zinc finger motif ; Zinc finger proteins</subject><ispartof>The Plant journal : for cell and molecular biology, 2024-07, Vol.119 (2), p.942-959</ispartof><rights>2024 The Authors. published by Society for Experimental Biology and John Wiley & Sons Ltd.</rights><rights>2024 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.</rights><rights>2024. This article is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c3818-f8cbf60ee75e88c99a09927959a97aad21b10966bf4372a30a4c7ff93f276663</cites><orcidid>0000-0001-6017-4166</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Ftpj.16808$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Ftpj.16808$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38743860$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Min, Ji‐Hee</creatorcontrib><creatorcontrib>Park, Cho‐Rong</creatorcontrib><creatorcontrib>Gong, Ying</creatorcontrib><creatorcontrib>Chung, Moon‐Soo</creatorcontrib><creatorcontrib>Nam, Seung‐Hee</creatorcontrib><creatorcontrib>Yun, Hye Sup</creatorcontrib><creatorcontrib>Kim, Cheol Soo</creatorcontrib><title>Rhamnogalacturonan lyase 1 (RGL1), as a suppressor of E3 ubiquitin ligase Arabidopsis thaliana ring zinc finger 1 (AtRZF1), is involved in dehydration response to mediate proline synthesis and pectin rhamnogalacturonan‐I composition</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>SUMMARY
Proline metabolism plays a crucial role in both environmental stress responses and plant growth. However, the specific mechanism by which proline contributes to abiotic stress processes remains to be elucidated. In this study, we utilized atrzf1 (Arabidopsis thaliana ring zinc finger 1) as a parental line for T‐DNA tagging mutagenesis and identified a suppressor mutant of atrzf1, designated proline content alterative 31 (pca31). The pca31 mutant suppressed the insensitivity of atrzf1 to dehydration stress during early seedling growth. Using Thermal Asymmetric Interlaced‐PCR, we found that the T‐DNA of pca31 was inserted into the promoter region of the At2g22620 gene, which encodes the cell wall enzyme rhamnogalacturonan lyase 1 (RGL1). Enzymatic assays indicated that RGL1 exhibited rhamnogalacturonan lyase activity, influencing cell wall pectin composition. The decrease in RGL1 gene expression suppressed the transcriptomic perturbation of the atrzf1 mutant. Silencing of the RGL1 gene in atrzf1 resulted in a sensitive phenotype similar to pca31 under osmotic stress conditions. Treatment with mannitol, salt, hydrogen peroxide, and abscisic acid induced RGL1 expression. Furthermore, we uncovered that RGL1 plays a role in modulating root growth and vascular tissue development. Molecular, physiological, and genetic experiments revealed that the positive modulation of RGL1 during abiotic stress was linked to the AtRZF1 pathway. Taken together, these findings establish that pca31 acts as a suppressor of atrzf1 in abiotic stress responses through proline and cell wall metabolisms.
Significance Statement
RGL1 exhibits rhamnogalacturonan lyase activity, which contributes to the modulation of pectin composition, vascular tissue development, and root growth. RGL1, as a suppressor of E3 ubiquitin ligase AtRZF1, functions as a positive modulator in proline synthesis and cell wall metabolism under osmotic stress conditions.</description><subject>Abiotic stress</subject><subject>abiotic stress response</subject><subject>Abscisic acid</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis - physiology</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Arabidopsis thaliana</subject><subject>AtRZF1</subject><subject>Cell Wall - metabolism</subject><subject>Cell walls</subject><subject>Cellular stress response</subject><subject>Composition</subject><subject>Dehydration</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>Environmental stress</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant</subject><subject>genes</subject><subject>Hydrogen peroxide</subject><subject>Mannitol</subject><subject>metabolism</subject><subject>Mutagenesis</subject><subject>mutants</subject><subject>Osmotic stress</subject><subject>Pectin</subject><subject>pectin content</subject><subject>pectins</subject><subject>Pectins - metabolism</subject><subject>phenotype</subject><subject>Phenotypes</subject><subject>Plant growth</subject><subject>Plant tissues</subject><subject>Plants, Genetically Modified</subject><subject>Polysaccharide-Lyases - genetics</subject><subject>Polysaccharide-Lyases - metabolism</subject><subject>Proline</subject><subject>Proline - metabolism</subject><subject>promoter regions</subject><subject>Rhamnogalacturonan</subject><subject>rhamnogalacturonan lyase</subject><subject>root growth</subject><subject>seedling growth</subject><subject>Seedlings</subject><subject>Stress, Physiological</subject><subject>suppressor</subject><subject>Suppressor mutant</subject><subject>Transcriptomics</subject><subject>Ubiquitin-protein ligase</subject><subject>Ubiquitin-Protein Ligases - genetics</subject><subject>Ubiquitin-Protein Ligases - metabolism</subject><subject>vascular bundle</subject><subject>Vascular tissue</subject><subject>Zinc</subject><subject>zinc finger motif</subject><subject>Zinc finger proteins</subject><issn>0960-7412</issn><issn>1365-313X</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><recordid>eNqFkk1u1DAUgCMEokNhwQWQJTatRFo7ju14OaraUjQSaDQLxCZ6SewZjxI7tZNWYcUROCNLToHDFBYghBf2W3z-3o9ekrwk-IzEcz70-zPCC1w8ShaEcpZSQj8-ThZYcpyKnGRHybMQ9hgTQXn-NDmihchpwfEi-b7eQWfdFlqoh9E7Cxa1EwSFCDpZX6_I6RsEAQEKY997FYLzyGl0SdFYmdvRDCbyZjt_WHqoTOP6YAIadtAasIC8sVv02dga6RgpP2uXw_rT1SyOoLF3rr1TTQxQo3ZT42EwzqKYqnc2WgeHOtUYGBTqvWuNVShMdtipOQ3YBvWqnovwf_Xx7cvXG1S7rnfBzM7nyRMNbVAvHt7jZHN1ubl4m67eX99cLFdpTQtSpLqoK82xUoKpoqilBCxlJiSTIAVAk5GKxMHySudUZEAx5LXQWlKdCc45PU5ODtpY7u2owlB2JtSqbcEqN4aSEkY5j1f-fxQzljPCJI7o6z_QvRu9jX1ESshYXcZYpE4PVO1dCF7psvemAz-VBJfzqpRxVcqfqxLZVw_GsYoT_k3-2o0InB-Ae9Oq6d-mcvPh3UH5A9qxzDg</recordid><startdate>202407</startdate><enddate>202407</enddate><creator>Min, Ji‐Hee</creator><creator>Park, Cho‐Rong</creator><creator>Gong, Ying</creator><creator>Chung, Moon‐Soo</creator><creator>Nam, Seung‐Hee</creator><creator>Yun, Hye Sup</creator><creator>Kim, Cheol Soo</creator><general>Blackwell Publishing Ltd</general><scope>24P</scope><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>7QO</scope><scope>7QP</scope><scope>7QR</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0001-6017-4166</orcidid></search><sort><creationdate>202407</creationdate><title>Rhamnogalacturonan lyase 1 (RGL1), as a suppressor of E3 ubiquitin ligase Arabidopsis thaliana ring zinc finger 1 (AtRZF1), is involved in dehydration response to mediate proline synthesis and pectin rhamnogalacturonan‐I composition</title><author>Min, Ji‐Hee ; Park, Cho‐Rong ; Gong, Ying ; Chung, Moon‐Soo ; Nam, Seung‐Hee ; Yun, Hye Sup ; Kim, Cheol Soo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3818-f8cbf60ee75e88c99a09927959a97aad21b10966bf4372a30a4c7ff93f276663</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Abiotic stress</topic><topic>abiotic stress response</topic><topic>Abscisic acid</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis - physiology</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Arabidopsis thaliana</topic><topic>AtRZF1</topic><topic>Cell Wall - metabolism</topic><topic>Cell walls</topic><topic>Cellular stress response</topic><topic>Composition</topic><topic>Dehydration</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>Environmental stress</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Plant</topic><topic>genes</topic><topic>Hydrogen peroxide</topic><topic>Mannitol</topic><topic>metabolism</topic><topic>Mutagenesis</topic><topic>mutants</topic><topic>Osmotic stress</topic><topic>Pectin</topic><topic>pectin content</topic><topic>pectins</topic><topic>Pectins - metabolism</topic><topic>phenotype</topic><topic>Phenotypes</topic><topic>Plant growth</topic><topic>Plant tissues</topic><topic>Plants, Genetically Modified</topic><topic>Polysaccharide-Lyases - genetics</topic><topic>Polysaccharide-Lyases - metabolism</topic><topic>Proline</topic><topic>Proline - metabolism</topic><topic>promoter regions</topic><topic>Rhamnogalacturonan</topic><topic>rhamnogalacturonan lyase</topic><topic>root growth</topic><topic>seedling growth</topic><topic>Seedlings</topic><topic>Stress, Physiological</topic><topic>suppressor</topic><topic>Suppressor mutant</topic><topic>Transcriptomics</topic><topic>Ubiquitin-protein ligase</topic><topic>Ubiquitin-Protein Ligases - genetics</topic><topic>Ubiquitin-Protein Ligases - metabolism</topic><topic>vascular bundle</topic><topic>Vascular tissue</topic><topic>Zinc</topic><topic>zinc finger motif</topic><topic>Zinc finger proteins</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Min, Ji‐Hee</creatorcontrib><creatorcontrib>Park, Cho‐Rong</creatorcontrib><creatorcontrib>Gong, Ying</creatorcontrib><creatorcontrib>Chung, Moon‐Soo</creatorcontrib><creatorcontrib>Nam, Seung‐Hee</creatorcontrib><creatorcontrib>Yun, Hye Sup</creatorcontrib><creatorcontrib>Kim, Cheol Soo</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>The Plant journal : for cell and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Min, Ji‐Hee</au><au>Park, Cho‐Rong</au><au>Gong, Ying</au><au>Chung, Moon‐Soo</au><au>Nam, Seung‐Hee</au><au>Yun, Hye Sup</au><au>Kim, Cheol Soo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Rhamnogalacturonan lyase 1 (RGL1), as a suppressor of E3 ubiquitin ligase Arabidopsis thaliana ring zinc finger 1 (AtRZF1), is involved in dehydration response to mediate proline synthesis and pectin rhamnogalacturonan‐I composition</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2024-07</date><risdate>2024</risdate><volume>119</volume><issue>2</issue><spage>942</spage><epage>959</epage><pages>942-959</pages><issn>0960-7412</issn><issn>1365-313X</issn><eissn>1365-313X</eissn><abstract>SUMMARY
Proline metabolism plays a crucial role in both environmental stress responses and plant growth. However, the specific mechanism by which proline contributes to abiotic stress processes remains to be elucidated. In this study, we utilized atrzf1 (Arabidopsis thaliana ring zinc finger 1) as a parental line for T‐DNA tagging mutagenesis and identified a suppressor mutant of atrzf1, designated proline content alterative 31 (pca31). The pca31 mutant suppressed the insensitivity of atrzf1 to dehydration stress during early seedling growth. Using Thermal Asymmetric Interlaced‐PCR, we found that the T‐DNA of pca31 was inserted into the promoter region of the At2g22620 gene, which encodes the cell wall enzyme rhamnogalacturonan lyase 1 (RGL1). Enzymatic assays indicated that RGL1 exhibited rhamnogalacturonan lyase activity, influencing cell wall pectin composition. The decrease in RGL1 gene expression suppressed the transcriptomic perturbation of the atrzf1 mutant. Silencing of the RGL1 gene in atrzf1 resulted in a sensitive phenotype similar to pca31 under osmotic stress conditions. Treatment with mannitol, salt, hydrogen peroxide, and abscisic acid induced RGL1 expression. Furthermore, we uncovered that RGL1 plays a role in modulating root growth and vascular tissue development. Molecular, physiological, and genetic experiments revealed that the positive modulation of RGL1 during abiotic stress was linked to the AtRZF1 pathway. Taken together, these findings establish that pca31 acts as a suppressor of atrzf1 in abiotic stress responses through proline and cell wall metabolisms.
Significance Statement
RGL1 exhibits rhamnogalacturonan lyase activity, which contributes to the modulation of pectin composition, vascular tissue development, and root growth. RGL1, as a suppressor of E3 ubiquitin ligase AtRZF1, functions as a positive modulator in proline synthesis and cell wall metabolism under osmotic stress conditions.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>38743860</pmid><doi>10.1111/tpj.16808</doi><tpages>18</tpages><orcidid>https://orcid.org/0000-0001-6017-4166</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Abiotic stress abiotic stress response Abscisic acid Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis - physiology Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Arabidopsis thaliana AtRZF1 Cell Wall - metabolism Cell walls Cellular stress response Composition Dehydration Deoxyribonucleic acid DNA Environmental stress Gene expression Gene Expression Regulation, Plant genes Hydrogen peroxide Mannitol metabolism Mutagenesis mutants Osmotic stress Pectin pectin content pectins Pectins - metabolism phenotype Phenotypes Plant growth Plant tissues Plants, Genetically Modified Polysaccharide-Lyases - genetics Polysaccharide-Lyases - metabolism Proline Proline - metabolism promoter regions Rhamnogalacturonan rhamnogalacturonan lyase root growth seedling growth Seedlings Stress, Physiological suppressor Suppressor mutant Transcriptomics Ubiquitin-protein ligase Ubiquitin-Protein Ligases - genetics Ubiquitin-Protein Ligases - metabolism vascular bundle Vascular tissue Zinc zinc finger motif Zinc finger proteins |
title | Rhamnogalacturonan lyase 1 (RGL1), as a suppressor of E3 ubiquitin ligase Arabidopsis thaliana ring zinc finger 1 (AtRZF1), is involved in dehydration response to mediate proline synthesis and pectin rhamnogalacturonan‐I composition |
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