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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Veröffentlicht in:The Plant journal : for cell and molecular biology 2024-07, Vol.119 (2), p.942-959
Hauptverfasser: Min, Ji‐Hee, Park, Cho‐Rong, Gong, Ying, Chung, Moon‐Soo, Nam, Seung‐Hee, Yun, Hye Sup, Kim, Cheol Soo
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container_title The Plant journal : for cell and molecular biology
container_volume 119
creator Min, Ji‐Hee
Park, Cho‐Rong
Gong, Ying
Chung, Moon‐Soo
Nam, Seung‐Hee
Yun, Hye Sup
Kim, Cheol Soo
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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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 &amp; Sons Ltd.</rights><rights>2024 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley &amp; 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 &amp; 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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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