The plastid‐localized lipoamide dehydrogenase 1 is crucial for redox homeostasis, tolerance to arsenic stress and fatty acid biosynthesis in rice

Summary Soil contamination with arsenic (As) can cause phytotoxicity and reduce crop yield. The mechanisms of As toxicity and tolerance are not fully understood. In this study, we used a forward genetics approach to isolate a rice mutant, ahs1, that exhibits hypersensitivity to both arsenate and ars...

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Veröffentlicht in:The New phytologist 2024-06, Vol.242 (6), p.2604-2619
Hauptverfasser: Chen, Ting‐Ting, Zhao, Peng, Wang, Yuan, Wang, Han‐Qing, Tang, Zhu, Hu, Han, Liu, Yu, Xu, Ji‐Ming, Mao, Chuan‐Zao, Zhao, Fang‐Jie, Wu, Zhong‐Chang
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container_issue 6
container_start_page 2604
container_title The New phytologist
container_volume 242
creator Chen, Ting‐Ting
Zhao, Peng
Wang, Yuan
Wang, Han‐Qing
Tang, Zhu
Hu, Han
Liu, Yu
Xu, Ji‐Ming
Mao, Chuan‐Zao
Zhao, Fang‐Jie
Wu, Zhong‐Chang
description Summary Soil contamination with arsenic (As) can cause phytotoxicity and reduce crop yield. The mechanisms of As toxicity and tolerance are not fully understood. In this study, we used a forward genetics approach to isolate a rice mutant, ahs1, that exhibits hypersensitivity to both arsenate and arsenite. Through genomic resequencing and complementation tests, we identified OsLPD1 as the causal gene, which encodes a putative lipoamide dehydrogenase. OsLPD1 was expressed in the outer cell layer of roots, root meristem cells, and in the mesophyll and vascular tissues of leaves. Subcellular localization and immunoblot analysis demonstrated that OsLPD1 is localized in the stroma of plastids. In vitro assays showed that OsLPD1 exhibited lipoamide dehydrogenase (LPD) activity, which was strongly inhibited by arsenite, but not by arsenate. The ahs1 and OsLPD1 knockout mutants exhibited significantly reduced NADH/NAD+ and GSH/GSSG ratios, along with increased levels of reactive oxygen species and greater oxidative stress in the roots compared with wild‐type (WT) plants under As treatment. Additionally, loss‐of‐function of OsLPD1 also resulted in decreased fatty acid concentrations in rice grain. Taken together, our finding reveals that OsLPD1 plays an important role for maintaining redox homeostasis, conferring tolerance to arsenic stress, and regulating fatty acid biosynthesis in rice.
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The mechanisms of As toxicity and tolerance are not fully understood. In this study, we used a forward genetics approach to isolate a rice mutant, ahs1, that exhibits hypersensitivity to both arsenate and arsenite. Through genomic resequencing and complementation tests, we identified OsLPD1 as the causal gene, which encodes a putative lipoamide dehydrogenase. OsLPD1 was expressed in the outer cell layer of roots, root meristem cells, and in the mesophyll and vascular tissues of leaves. Subcellular localization and immunoblot analysis demonstrated that OsLPD1 is localized in the stroma of plastids. In vitro assays showed that OsLPD1 exhibited lipoamide dehydrogenase (LPD) activity, which was strongly inhibited by arsenite, but not by arsenate. The ahs1 and OsLPD1 knockout mutants exhibited significantly reduced NADH/NAD+ and GSH/GSSG ratios, along with increased levels of reactive oxygen species and greater oxidative stress in the roots compared with wild‐type (WT) plants under As treatment. Additionally, loss‐of‐function of OsLPD1 also resulted in decreased fatty acid concentrations in rice grain. Taken together, our finding reveals that OsLPD1 plays an important role for maintaining redox homeostasis, conferring tolerance to arsenic stress, and regulating fatty acid biosynthesis in rice.</description><identifier>ISSN: 0028-646X</identifier><identifier>ISSN: 1469-8137</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.19727</identifier><identifier>PMID: 38563391</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Acidic soils ; Adaptation, Physiological - drug effects ; Adaptation, Physiological - genetics ; Arsenates ; Arsenic ; Arsenic - toxicity ; Arsenite ; arsenites ; Arsenites - toxicity ; Biological stress ; Biosynthesis ; Complementation ; Contamination ; Crop yield ; Dehydrogenase ; Dehydrogenases ; Dihydrolipoamide Dehydrogenase - genetics ; Dihydrolipoamide Dehydrogenase - metabolism ; Fatty acids ; Fatty Acids - biosynthesis ; Gene Expression Regulation, Plant - drug effects ; genes ; Genetics ; genomics ; Homeostasis ; Hypersensitivity ; Localization ; loss-of-function mutation ; LPD1 ; Meristems ; Mesophyll ; Mutants ; Mutation - genetics ; NADH ; Nicotinamide adenine dinucleotide ; Oryza - drug effects ; Oryza - genetics ; Oryza - metabolism ; Oxidation-Reduction - drug effects ; Oxidative stress ; Oxidative Stress - drug effects ; oxidoreductases ; Phytotoxicity ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plant Roots - drug effects ; Plant Roots - metabolism ; Plant tissues ; Plastids ; Plastids - drug effects ; Plastids - metabolism ; Reactive oxygen species ; Reactive Oxygen Species - metabolism ; Redox ; Rice ; root meristems ; Roots ; ROS ; Soil contamination ; Soil pollution ; Stress, Physiological - drug effects ; Stress, Physiological - genetics ; Stroma ; Toxicity ; Toxicity tolerance ; Vascular tissue</subject><ispartof>The New phytologist, 2024-06, Vol.242 (6), p.2604-2619</ispartof><rights>2024 The Authors © 2024 New Phytologist Foundation</rights><rights>2024 The Authors New Phytologist © 2024 New Phytologist Foundation.</rights><rights>Copyright © 2024 New Phytologist Trust</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c3467-9f62351ee5d02eef9b37c22ba45be55a4b7779e1ecf3b997265edc82ed1c5b1b3</cites><orcidid>0000-0001-6383-3817 ; 0000-0001-5126-2180 ; 0000-0002-0164-169X</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%2Fnph.19727$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fnph.19727$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38563391$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chen, Ting‐Ting</creatorcontrib><creatorcontrib>Zhao, Peng</creatorcontrib><creatorcontrib>Wang, Yuan</creatorcontrib><creatorcontrib>Wang, Han‐Qing</creatorcontrib><creatorcontrib>Tang, Zhu</creatorcontrib><creatorcontrib>Hu, Han</creatorcontrib><creatorcontrib>Liu, Yu</creatorcontrib><creatorcontrib>Xu, Ji‐Ming</creatorcontrib><creatorcontrib>Mao, Chuan‐Zao</creatorcontrib><creatorcontrib>Zhao, Fang‐Jie</creatorcontrib><creatorcontrib>Wu, Zhong‐Chang</creatorcontrib><title>The plastid‐localized lipoamide dehydrogenase 1 is crucial for redox homeostasis, tolerance to arsenic stress and fatty acid biosynthesis in rice</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>Summary Soil contamination with arsenic (As) can cause phytotoxicity and reduce crop yield. The mechanisms of As toxicity and tolerance are not fully understood. In this study, we used a forward genetics approach to isolate a rice mutant, ahs1, that exhibits hypersensitivity to both arsenate and arsenite. Through genomic resequencing and complementation tests, we identified OsLPD1 as the causal gene, which encodes a putative lipoamide dehydrogenase. OsLPD1 was expressed in the outer cell layer of roots, root meristem cells, and in the mesophyll and vascular tissues of leaves. Subcellular localization and immunoblot analysis demonstrated that OsLPD1 is localized in the stroma of plastids. In vitro assays showed that OsLPD1 exhibited lipoamide dehydrogenase (LPD) activity, which was strongly inhibited by arsenite, but not by arsenate. The ahs1 and OsLPD1 knockout mutants exhibited significantly reduced NADH/NAD+ and GSH/GSSG ratios, along with increased levels of reactive oxygen species and greater oxidative stress in the roots compared with wild‐type (WT) plants under As treatment. Additionally, loss‐of‐function of OsLPD1 also resulted in decreased fatty acid concentrations in rice grain. Taken together, our finding reveals that OsLPD1 plays an important role for maintaining redox homeostasis, conferring tolerance to arsenic stress, and regulating fatty acid biosynthesis in rice.</description><subject>Acidic soils</subject><subject>Adaptation, Physiological - drug effects</subject><subject>Adaptation, Physiological - genetics</subject><subject>Arsenates</subject><subject>Arsenic</subject><subject>Arsenic - toxicity</subject><subject>Arsenite</subject><subject>arsenites</subject><subject>Arsenites - toxicity</subject><subject>Biological stress</subject><subject>Biosynthesis</subject><subject>Complementation</subject><subject>Contamination</subject><subject>Crop yield</subject><subject>Dehydrogenase</subject><subject>Dehydrogenases</subject><subject>Dihydrolipoamide Dehydrogenase - genetics</subject><subject>Dihydrolipoamide Dehydrogenase - metabolism</subject><subject>Fatty acids</subject><subject>Fatty Acids - biosynthesis</subject><subject>Gene Expression Regulation, Plant - drug effects</subject><subject>genes</subject><subject>Genetics</subject><subject>genomics</subject><subject>Homeostasis</subject><subject>Hypersensitivity</subject><subject>Localization</subject><subject>loss-of-function mutation</subject><subject>LPD1</subject><subject>Meristems</subject><subject>Mesophyll</subject><subject>Mutants</subject><subject>Mutation - genetics</subject><subject>NADH</subject><subject>Nicotinamide adenine dinucleotide</subject><subject>Oryza - drug effects</subject><subject>Oryza - genetics</subject><subject>Oryza - metabolism</subject><subject>Oxidation-Reduction - drug effects</subject><subject>Oxidative stress</subject><subject>Oxidative Stress - drug effects</subject><subject>oxidoreductases</subject><subject>Phytotoxicity</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plant Roots - drug effects</subject><subject>Plant Roots - metabolism</subject><subject>Plant tissues</subject><subject>Plastids</subject><subject>Plastids - drug effects</subject><subject>Plastids - metabolism</subject><subject>Reactive oxygen species</subject><subject>Reactive Oxygen Species - metabolism</subject><subject>Redox</subject><subject>Rice</subject><subject>root meristems</subject><subject>Roots</subject><subject>ROS</subject><subject>Soil contamination</subject><subject>Soil pollution</subject><subject>Stress, Physiological - drug effects</subject><subject>Stress, Physiological - genetics</subject><subject>Stroma</subject><subject>Toxicity</subject><subject>Toxicity tolerance</subject><subject>Vascular tissue</subject><issn>0028-646X</issn><issn>1469-8137</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqF0UFr1jAYB_AginudHvwCEvAyYd2Spknaowx1wlAPE7yVNHlqM9Km5mlx9eRHEPyGfpJF3-lBEHN5cvjlD0_-hDzm7ITnczrNwwlvdKnvkB2vVFPUXOi7ZMdYWReqUh8OyAPEK8ZYI1V5nxyIWiohGr4j3y8HoHMwuHj34-u3EK0J_gs4GvwczegdUAfD5lL8CJNBoJx6pDat1ptA-5hoAhev6RBHiLgY9HhMlxggmclCvlGTECZvKS4JEKmZHO3NsmzUWO9o5yNu0zJAfkj9RJO38JDc601AeHQ7D8n7ly8uz86Li7evXp89vyisqJQuml6VQnIA6VgJ0Ded0LYsO1PJDqQ0Vae1boCD7UXX5O9REpytS3Dcyo534pAc7XPnFD-tgEs7erQQgpkgrtgKLoWsdMPU_ykTnAvJmMz06V_0Kq5pyotkJWtRC1GyrJ7tlU0RMUHfzsmPJm0tZ-3PUttcavur1Gyf3Cau3Qjuj_zdYgane_DZB9j-ndS-eXe-j7wBq7uuzA</recordid><startdate>202406</startdate><enddate>202406</enddate><creator>Chen, Ting‐Ting</creator><creator>Zhao, Peng</creator><creator>Wang, Yuan</creator><creator>Wang, Han‐Qing</creator><creator>Tang, Zhu</creator><creator>Hu, Han</creator><creator>Liu, Yu</creator><creator>Xu, Ji‐Ming</creator><creator>Mao, Chuan‐Zao</creator><creator>Zhao, Fang‐Jie</creator><creator>Wu, Zhong‐Chang</creator><general>Wiley Subscription Services, Inc</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>7QO</scope><scope>7SN</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H95</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0001-6383-3817</orcidid><orcidid>https://orcid.org/0000-0001-5126-2180</orcidid><orcidid>https://orcid.org/0000-0002-0164-169X</orcidid></search><sort><creationdate>202406</creationdate><title>The plastid‐localized lipoamide dehydrogenase 1 is crucial for redox homeostasis, tolerance to arsenic stress and fatty acid biosynthesis in rice</title><author>Chen, Ting‐Ting ; Zhao, Peng ; Wang, Yuan ; Wang, Han‐Qing ; Tang, Zhu ; Hu, Han ; Liu, Yu ; Xu, Ji‐Ming ; Mao, Chuan‐Zao ; Zhao, Fang‐Jie ; Wu, Zhong‐Chang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3467-9f62351ee5d02eef9b37c22ba45be55a4b7779e1ecf3b997265edc82ed1c5b1b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Acidic soils</topic><topic>Adaptation, Physiological - drug effects</topic><topic>Adaptation, Physiological - genetics</topic><topic>Arsenates</topic><topic>Arsenic</topic><topic>Arsenic - toxicity</topic><topic>Arsenite</topic><topic>arsenites</topic><topic>Arsenites - toxicity</topic><topic>Biological stress</topic><topic>Biosynthesis</topic><topic>Complementation</topic><topic>Contamination</topic><topic>Crop yield</topic><topic>Dehydrogenase</topic><topic>Dehydrogenases</topic><topic>Dihydrolipoamide Dehydrogenase - genetics</topic><topic>Dihydrolipoamide Dehydrogenase - metabolism</topic><topic>Fatty acids</topic><topic>Fatty Acids - biosynthesis</topic><topic>Gene Expression Regulation, Plant - drug effects</topic><topic>genes</topic><topic>Genetics</topic><topic>genomics</topic><topic>Homeostasis</topic><topic>Hypersensitivity</topic><topic>Localization</topic><topic>loss-of-function mutation</topic><topic>LPD1</topic><topic>Meristems</topic><topic>Mesophyll</topic><topic>Mutants</topic><topic>Mutation - genetics</topic><topic>NADH</topic><topic>Nicotinamide adenine dinucleotide</topic><topic>Oryza - drug effects</topic><topic>Oryza - genetics</topic><topic>Oryza - metabolism</topic><topic>Oxidation-Reduction - drug effects</topic><topic>Oxidative stress</topic><topic>Oxidative Stress - drug effects</topic><topic>oxidoreductases</topic><topic>Phytotoxicity</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plant Roots - drug effects</topic><topic>Plant Roots - metabolism</topic><topic>Plant tissues</topic><topic>Plastids</topic><topic>Plastids - drug effects</topic><topic>Plastids - metabolism</topic><topic>Reactive oxygen species</topic><topic>Reactive Oxygen Species - metabolism</topic><topic>Redox</topic><topic>Rice</topic><topic>root meristems</topic><topic>Roots</topic><topic>ROS</topic><topic>Soil contamination</topic><topic>Soil pollution</topic><topic>Stress, Physiological - drug effects</topic><topic>Stress, Physiological - genetics</topic><topic>Stroma</topic><topic>Toxicity</topic><topic>Toxicity tolerance</topic><topic>Vascular tissue</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Chen, Ting‐Ting</creatorcontrib><creatorcontrib>Zhao, Peng</creatorcontrib><creatorcontrib>Wang, Yuan</creatorcontrib><creatorcontrib>Wang, Han‐Qing</creatorcontrib><creatorcontrib>Tang, Zhu</creatorcontrib><creatorcontrib>Hu, Han</creatorcontrib><creatorcontrib>Liu, Yu</creatorcontrib><creatorcontrib>Xu, Ji‐Ming</creatorcontrib><creatorcontrib>Mao, Chuan‐Zao</creatorcontrib><creatorcontrib>Zhao, Fang‐Jie</creatorcontrib><creatorcontrib>Wu, Zhong‐Chang</creatorcontrib><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>Ecology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Aquatic Science &amp; 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The mechanisms of As toxicity and tolerance are not fully understood. In this study, we used a forward genetics approach to isolate a rice mutant, ahs1, that exhibits hypersensitivity to both arsenate and arsenite. Through genomic resequencing and complementation tests, we identified OsLPD1 as the causal gene, which encodes a putative lipoamide dehydrogenase. OsLPD1 was expressed in the outer cell layer of roots, root meristem cells, and in the mesophyll and vascular tissues of leaves. Subcellular localization and immunoblot analysis demonstrated that OsLPD1 is localized in the stroma of plastids. In vitro assays showed that OsLPD1 exhibited lipoamide dehydrogenase (LPD) activity, which was strongly inhibited by arsenite, but not by arsenate. The ahs1 and OsLPD1 knockout mutants exhibited significantly reduced NADH/NAD+ and GSH/GSSG ratios, along with increased levels of reactive oxygen species and greater oxidative stress in the roots compared with wild‐type (WT) plants under As treatment. Additionally, loss‐of‐function of OsLPD1 also resulted in decreased fatty acid concentrations in rice grain. Taken together, our finding reveals that OsLPD1 plays an important role for maintaining redox homeostasis, conferring tolerance to arsenic stress, and regulating fatty acid biosynthesis in rice.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>38563391</pmid><doi>10.1111/nph.19727</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0001-6383-3817</orcidid><orcidid>https://orcid.org/0000-0001-5126-2180</orcidid><orcidid>https://orcid.org/0000-0002-0164-169X</orcidid></addata></record>
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subjects Acidic soils
Adaptation, Physiological - drug effects
Adaptation, Physiological - genetics
Arsenates
Arsenic
Arsenic - toxicity
Arsenite
arsenites
Arsenites - toxicity
Biological stress
Biosynthesis
Complementation
Contamination
Crop yield
Dehydrogenase
Dehydrogenases
Dihydrolipoamide Dehydrogenase - genetics
Dihydrolipoamide Dehydrogenase - metabolism
Fatty acids
Fatty Acids - biosynthesis
Gene Expression Regulation, Plant - drug effects
genes
Genetics
genomics
Homeostasis
Hypersensitivity
Localization
loss-of-function mutation
LPD1
Meristems
Mesophyll
Mutants
Mutation - genetics
NADH
Nicotinamide adenine dinucleotide
Oryza - drug effects
Oryza - genetics
Oryza - metabolism
Oxidation-Reduction - drug effects
Oxidative stress
Oxidative Stress - drug effects
oxidoreductases
Phytotoxicity
Plant Proteins - genetics
Plant Proteins - metabolism
Plant Roots - drug effects
Plant Roots - metabolism
Plant tissues
Plastids
Plastids - drug effects
Plastids - metabolism
Reactive oxygen species
Reactive Oxygen Species - metabolism
Redox
Rice
root meristems
Roots
ROS
Soil contamination
Soil pollution
Stress, Physiological - drug effects
Stress, Physiological - genetics
Stroma
Toxicity
Toxicity tolerance
Vascular tissue
title The plastid‐localized lipoamide dehydrogenase 1 is crucial for redox homeostasis, tolerance to arsenic stress and fatty acid biosynthesis in rice
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