Excessive UDPG resulting from the mutation of UAP1 causes programmed cell death by triggering reactive oxygen species accumulation and caspase-like activity in rice
Lesion mimic mutants are valuable to unravel the mechanisms governing the programmed cell death (PCD) process. Uridine 5′-diphosphoglucose-glucose (UDPG) functions as a signaling molecule activating multiple pathways in animals, but little is known about its function in plants. Two novel allelic mut...
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description | Lesion mimic mutants are valuable to unravel the mechanisms governing the programmed cell death (PCD) process. Uridine 5′-diphosphoglucose-glucose (UDPG) functions as a signaling molecule activating multiple pathways in animals, but little is known about its function in plants.
Two novel allelic mutants of spl29 with typical PCD characters and reduced pollen viability were obtained by ethane methyl sulfonate mutagenesis in rice cv Kitaake.
The enzymatic analyses showed that UDP-N-acetylglucosamine pyrophosphorylase 1 (UAP1) irreversibly catalyzed the decomposition of UDPG. Its activity was severely destroyed and caused excessive UDPG accumulation, with the lesion occurrence associated with the enhanced caspase-like activities in spl29-2. At the transcriptional level, several key genes involved in endoplasmic reticulum stress and the unfolded protein response were abnormally expressed. Moreover, exogenous UDPG could aggravate lesion initiation and development in spl29-2. Importantly, exogenous UDPG and its derivative UDP-N-acetylglucosamine could induce reactive oxygen species (ROS) accumulation and lesion mimics in Kitaake seedlings.
These results suggest that the excessive accumulation of UDPG, caused by the mutation of UAP1, was a key biochemical event resulting in the lesion mimics in spl29-2. Thus, our findings revealed that UDPG might be an important component involved in ROS accumulation, PCD execution and lesion mimicking in rice, which also provided new clues for investigating the connection between sugar metabolism and PCD process. |
doi_str_mv | 10.1111/nph.14818 |
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Two novel allelic mutants of spl29 with typical PCD characters and reduced pollen viability were obtained by ethane methyl sulfonate mutagenesis in rice cv Kitaake.
The enzymatic analyses showed that UDP-N-acetylglucosamine pyrophosphorylase 1 (UAP1) irreversibly catalyzed the decomposition of UDPG. Its activity was severely destroyed and caused excessive UDPG accumulation, with the lesion occurrence associated with the enhanced caspase-like activities in spl29-2. At the transcriptional level, several key genes involved in endoplasmic reticulum stress and the unfolded protein response were abnormally expressed. Moreover, exogenous UDPG could aggravate lesion initiation and development in spl29-2. Importantly, exogenous UDPG and its derivative UDP-N-acetylglucosamine could induce reactive oxygen species (ROS) accumulation and lesion mimics in Kitaake seedlings.
These results suggest that the excessive accumulation of UDPG, caused by the mutation of UAP1, was a key biochemical event resulting in the lesion mimics in spl29-2. Thus, our findings revealed that UDPG might be an important component involved in ROS accumulation, PCD execution and lesion mimicking in rice, which also provided new clues for investigating the connection between sugar metabolism and PCD process.</description><identifier>ISSN: 0028-646X</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.14818</identifier><identifier>PMID: 28967675</identifier><language>eng</language><publisher>England: New Phytologist Trust</publisher><subject>Accumulation ; Apoptosis ; Caspase ; caspase‐like activity ; Cell death ; Endoplasmic reticulum ; Ethane ; Genes ; lesion ; Lesions ; Metabolism ; Mimicry ; Mutagenesis ; Mutants ; Mutation ; N-Acetylglucosamine ; Oryza ; Oxygen ; Plants (botany) ; Pollen ; programmed cell death (PCD) ; Protein folding ; Proteins ; Reactive oxygen species ; reactive oxygen species (ROS) ; rice (Oryza sativa) ; Saccharides ; Seedlings ; Signaling ; Species ; Sugar ; Transcription ; UDP-N-acetylglucosamine pyrophosphorylase ; UDP‐N‐acetylglucosamine pyrophosphorylase 1 (UAP1) ; Uridine ; uridine 5′‐diphosphoglucoseglucose (UDPG) ; Viability</subject><ispartof>The New phytologist, 2018-01, Vol.217 (1), p.332-343</ispartof><rights>Copyright © 2017 New Phytologist Trust</rights><rights>2017 The Authors. New Phytologist © 2017 New Phytologist Trust</rights><rights>2017 The Authors. New Phytologist © 2017 New Phytologist Trust.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4768-92b694d45ef33f1f25c97ffd62211896eb8b1556998fabc0d0cd9690e56b8c443</citedby><cites>FETCH-LOGICAL-c4768-92b694d45ef33f1f25c97ffd62211896eb8b1556998fabc0d0cd9690e56b8c443</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/90016370$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/90016370$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>314,780,784,803,1417,1433,27924,27925,45574,45575,46409,46833,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28967675$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Xiao, Guiqing</creatorcontrib><creatorcontrib>Zhou, Jiahao</creatorcontrib><creatorcontrib>Lu, Xiangyang</creatorcontrib><creatorcontrib>Huang, Rongfeng</creatorcontrib><creatorcontrib>Zhang, Haiwen</creatorcontrib><title>Excessive UDPG resulting from the mutation of UAP1 causes programmed cell death by triggering reactive oxygen species accumulation and caspase-like activity in rice</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>Lesion mimic mutants are valuable to unravel the mechanisms governing the programmed cell death (PCD) process. Uridine 5′-diphosphoglucose-glucose (UDPG) functions as a signaling molecule activating multiple pathways in animals, but little is known about its function in plants.
Two novel allelic mutants of spl29 with typical PCD characters and reduced pollen viability were obtained by ethane methyl sulfonate mutagenesis in rice cv Kitaake.
The enzymatic analyses showed that UDP-N-acetylglucosamine pyrophosphorylase 1 (UAP1) irreversibly catalyzed the decomposition of UDPG. Its activity was severely destroyed and caused excessive UDPG accumulation, with the lesion occurrence associated with the enhanced caspase-like activities in spl29-2. At the transcriptional level, several key genes involved in endoplasmic reticulum stress and the unfolded protein response were abnormally expressed. Moreover, exogenous UDPG could aggravate lesion initiation and development in spl29-2. Importantly, exogenous UDPG and its derivative UDP-N-acetylglucosamine could induce reactive oxygen species (ROS) accumulation and lesion mimics in Kitaake seedlings.
These results suggest that the excessive accumulation of UDPG, caused by the mutation of UAP1, was a key biochemical event resulting in the lesion mimics in spl29-2. Thus, our findings revealed that UDPG might be an important component involved in ROS accumulation, PCD execution and lesion mimicking in rice, which also provided new clues for investigating the connection between sugar metabolism and PCD process.</description><subject>Accumulation</subject><subject>Apoptosis</subject><subject>Caspase</subject><subject>caspase‐like activity</subject><subject>Cell death</subject><subject>Endoplasmic reticulum</subject><subject>Ethane</subject><subject>Genes</subject><subject>lesion</subject><subject>Lesions</subject><subject>Metabolism</subject><subject>Mimicry</subject><subject>Mutagenesis</subject><subject>Mutants</subject><subject>Mutation</subject><subject>N-Acetylglucosamine</subject><subject>Oryza</subject><subject>Oxygen</subject><subject>Plants (botany)</subject><subject>Pollen</subject><subject>programmed cell death (PCD)</subject><subject>Protein folding</subject><subject>Proteins</subject><subject>Reactive oxygen species</subject><subject>reactive oxygen species (ROS)</subject><subject>rice (Oryza sativa)</subject><subject>Saccharides</subject><subject>Seedlings</subject><subject>Signaling</subject><subject>Species</subject><subject>Sugar</subject><subject>Transcription</subject><subject>UDP-N-acetylglucosamine pyrophosphorylase</subject><subject>UDP‐N‐acetylglucosamine pyrophosphorylase 1 (UAP1)</subject><subject>Uridine</subject><subject>uridine 5′‐diphosphoglucoseglucose (UDPG)</subject><subject>Viability</subject><issn>0028-646X</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><recordid>eNp1kctu1DAUhi0EokNhwQOAjsSKRVo7F8deVqW0SBXMgpHYRY5znPGQG7YDzfvwoHiatjvOxpvv_46Of0LeMnrG4pwP0_6M5YKJZ2TDci4TwbLyOdlQmoqE5_zHCXnl_YFSKgueviQnqZC85GWxIX-v7jR6b38j7D5tr8Ghn7tghxaMG3sIe4R-DirYcYDRwO5iy0Cr2aOHyY2tU32PDWjsOmhQhT3UCwRn2xbdUeJQ6XCUj3dLiwP4CbWNWaX13M_d6lVDNCg_KY9JZ38i3GdsWMAO4KzG1-SFUZ3HNw_vKdl9vvp-eZPcfrv-cnlxm-i85CKRac1l3uQFmiwzzKSFlqUxDU9TxuLFWIuaFQWXUhhVa9pQ3UguKRa8FjrPs1PyYfXG037N6EN1GGc3xJUVk1zIIpMii9THldJu9N6hqSZne-WWitHq2EcV-6ju-4js-wfjXMePeiIfC4jA-Qr8sR0u_zdVX7c3j8p3a-Lgw-ieEpJSxrOSZv8AoLOhDg</recordid><startdate>201801</startdate><enddate>201801</enddate><creator>Xiao, Guiqing</creator><creator>Zhou, Jiahao</creator><creator>Lu, Xiangyang</creator><creator>Huang, Rongfeng</creator><creator>Zhang, Haiwen</creator><general>New Phytologist Trust</general><general>Wiley Subscription Services, Inc</general><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></search><sort><creationdate>201801</creationdate><title>Excessive UDPG resulting from the mutation of UAP1 causes programmed cell death by triggering reactive oxygen species accumulation and caspase-like activity in rice</title><author>Xiao, Guiqing ; Zhou, Jiahao ; Lu, Xiangyang ; Huang, Rongfeng ; Zhang, Haiwen</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4768-92b694d45ef33f1f25c97ffd62211896eb8b1556998fabc0d0cd9690e56b8c443</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Accumulation</topic><topic>Apoptosis</topic><topic>Caspase</topic><topic>caspase‐like activity</topic><topic>Cell death</topic><topic>Endoplasmic reticulum</topic><topic>Ethane</topic><topic>Genes</topic><topic>lesion</topic><topic>Lesions</topic><topic>Metabolism</topic><topic>Mimicry</topic><topic>Mutagenesis</topic><topic>Mutants</topic><topic>Mutation</topic><topic>N-Acetylglucosamine</topic><topic>Oryza</topic><topic>Oxygen</topic><topic>Plants (botany)</topic><topic>Pollen</topic><topic>programmed cell death (PCD)</topic><topic>Protein folding</topic><topic>Proteins</topic><topic>Reactive oxygen species</topic><topic>reactive oxygen species (ROS)</topic><topic>rice (Oryza sativa)</topic><topic>Saccharides</topic><topic>Seedlings</topic><topic>Signaling</topic><topic>Species</topic><topic>Sugar</topic><topic>Transcription</topic><topic>UDP-N-acetylglucosamine pyrophosphorylase</topic><topic>UDP‐N‐acetylglucosamine pyrophosphorylase 1 (UAP1)</topic><topic>Uridine</topic><topic>uridine 5′‐diphosphoglucoseglucose (UDPG)</topic><topic>Viability</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Xiao, Guiqing</creatorcontrib><creatorcontrib>Zhou, Jiahao</creatorcontrib><creatorcontrib>Lu, Xiangyang</creatorcontrib><creatorcontrib>Huang, Rongfeng</creatorcontrib><creatorcontrib>Zhang, Haiwen</creatorcontrib><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 & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><jtitle>The New phytologist</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Xiao, Guiqing</au><au>Zhou, Jiahao</au><au>Lu, Xiangyang</au><au>Huang, Rongfeng</au><au>Zhang, Haiwen</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Excessive UDPG resulting from the mutation of UAP1 causes programmed cell death by triggering reactive oxygen species accumulation and caspase-like activity in rice</atitle><jtitle>The New phytologist</jtitle><addtitle>New Phytol</addtitle><date>2018-01</date><risdate>2018</risdate><volume>217</volume><issue>1</issue><spage>332</spage><epage>343</epage><pages>332-343</pages><issn>0028-646X</issn><eissn>1469-8137</eissn><abstract>Lesion mimic mutants are valuable to unravel the mechanisms governing the programmed cell death (PCD) process. Uridine 5′-diphosphoglucose-glucose (UDPG) functions as a signaling molecule activating multiple pathways in animals, but little is known about its function in plants.
Two novel allelic mutants of spl29 with typical PCD characters and reduced pollen viability were obtained by ethane methyl sulfonate mutagenesis in rice cv Kitaake.
The enzymatic analyses showed that UDP-N-acetylglucosamine pyrophosphorylase 1 (UAP1) irreversibly catalyzed the decomposition of UDPG. Its activity was severely destroyed and caused excessive UDPG accumulation, with the lesion occurrence associated with the enhanced caspase-like activities in spl29-2. At the transcriptional level, several key genes involved in endoplasmic reticulum stress and the unfolded protein response were abnormally expressed. Moreover, exogenous UDPG could aggravate lesion initiation and development in spl29-2. Importantly, exogenous UDPG and its derivative UDP-N-acetylglucosamine could induce reactive oxygen species (ROS) accumulation and lesion mimics in Kitaake seedlings.
These results suggest that the excessive accumulation of UDPG, caused by the mutation of UAP1, was a key biochemical event resulting in the lesion mimics in spl29-2. Thus, our findings revealed that UDPG might be an important component involved in ROS accumulation, PCD execution and lesion mimicking in rice, which also provided new clues for investigating the connection between sugar metabolism and PCD process.</abstract><cop>England</cop><pub>New Phytologist Trust</pub><pmid>28967675</pmid><doi>10.1111/nph.14818</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Accumulation Apoptosis Caspase caspase‐like activity Cell death Endoplasmic reticulum Ethane Genes lesion Lesions Metabolism Mimicry Mutagenesis Mutants Mutation N-Acetylglucosamine Oryza Oxygen Plants (botany) Pollen programmed cell death (PCD) Protein folding Proteins Reactive oxygen species reactive oxygen species (ROS) rice (Oryza sativa) Saccharides Seedlings Signaling Species Sugar Transcription UDP-N-acetylglucosamine pyrophosphorylase UDP‐N‐acetylglucosamine pyrophosphorylase 1 (UAP1) Uridine uridine 5′‐diphosphoglucoseglucose (UDPG) Viability |
title | Excessive UDPG resulting from the mutation of UAP1 causes programmed cell death by triggering reactive oxygen species accumulation and caspase-like activity in rice |
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