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Phosphoethanolamine N-methyltransferase 1 contributes to maintenance of root apical meristem by affecting ROS and auxin-regulated cell differentiation in Arabidopsis
The continuous growth of roots requires the balance between cell division and differentiation. Reactive oxygen species (ROS) and auxin are important regulators of root development by affecting cell division and differentiation. The mechanism controlling the coordination of cell division and differen...
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Published in: | The New phytologist 2019-10, Vol.224 (1), p.258-273 |
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description | The continuous growth of roots requires the balance between cell division and differentiation. Reactive oxygen species (ROS) and auxin are important regulators of root development by affecting cell division and differentiation. The mechanism controlling the coordination of cell division and differentiation is not well understood.
Using a forward genetic screen, we isolated a mutant, defective primary root 2 (dpr2), defective in root apical meristem (RAM) maintenance. The DPR2 gene encodes phosphoethanolamine N-methyltransferase 1 (PEAMT1) that catalyzes phosphocholine biosynthesis in Arabidopsis. We characterized the primary root phenotypes of dpr2 using various marker lines, using histochemical and pharmacological analysis to probe early root development.
Loss-of-function of DPR2/PEAMT1 resulted in RAM consumption by affecting root stem cell niche, division zone, elongation and differentiation zone (EDZ). PIN-FORMED (PIN) protein abundance, PIN2 polar distribution and general endocytosis were impaired in the root tip of dpr2. Excess hydrogen peroxide and auxin accumulate in the EDZ of dpr2, leading to RAM consumption by accelerating cell differentiation. Suppression of ROS over-accumulation or inhibition of auxin signalling partially prevent RAM differentiation in dpr2 after choline starvation.
Taken together, we conclude that the EDZ of the root tip is most sensitive to choline shortage, leading to RAM consumption through an ROS–auxin regulation module. |
doi_str_mv | 10.1111/nph.16028 |
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Using a forward genetic screen, we isolated a mutant, defective primary root 2 (dpr2), defective in root apical meristem (RAM) maintenance. The DPR2 gene encodes phosphoethanolamine N-methyltransferase 1 (PEAMT1) that catalyzes phosphocholine biosynthesis in Arabidopsis. We characterized the primary root phenotypes of dpr2 using various marker lines, using histochemical and pharmacological analysis to probe early root development.
Loss-of-function of DPR2/PEAMT1 resulted in RAM consumption by affecting root stem cell niche, division zone, elongation and differentiation zone (EDZ). PIN-FORMED (PIN) protein abundance, PIN2 polar distribution and general endocytosis were impaired in the root tip of dpr2. Excess hydrogen peroxide and auxin accumulate in the EDZ of dpr2, leading to RAM consumption by accelerating cell differentiation. Suppression of ROS over-accumulation or inhibition of auxin signalling partially prevent RAM differentiation in dpr2 after choline starvation.
Taken together, we conclude that the EDZ of the root tip is most sensitive to choline shortage, leading to RAM consumption through an ROS–auxin regulation module.</description><identifier>ISSN: 0028-646X</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.16028</identifier><identifier>PMID: 31246280</identifier><language>eng</language><publisher>England: Wiley</publisher><subject>Arabidopsis ; Arabidopsis - cytology ; Arabidopsis - drug effects ; Arabidopsis - enzymology ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Arabidopsis thaliana ; auxin ; Auxins ; Biosynthesis ; Cell differentiation ; Cell Differentiation - drug effects ; Cell division ; Cell Division - drug effects ; Choline ; Choline - pharmacology ; Consumption ; Differentiation (biology) ; Elongation ; Endocytosis ; Endocytosis - drug effects ; Ethanolamines - metabolism ; Genetic screening ; Hydrogen peroxide ; Indoleacetic Acids - pharmacology ; Meristem - cytology ; Meristem - drug effects ; Meristems ; Methyltransferase ; Methyltransferases - metabolism ; Microtubules - drug effects ; Microtubules - metabolism ; Mutation - genetics ; Niches ; Onium Compounds - pharmacology ; Phenotype ; Phenotypes ; Phosphocholine ; phosphoethanolamine N‐methyltransferase (PEAMT) ; Reactive oxygen species ; reactive oxygen species (ROS) ; Reactive Oxygen Species - metabolism ; Regulators ; root apical meristem (RAM) ; Root development ; Starvation ; Stem cells ; Stem Cells - drug effects ; Stem Cells - metabolism</subject><ispartof>The New phytologist, 2019-10, Vol.224 (1), p.258-273</ispartof><rights>2019 The Authors © 2019 New Phytologist Trust</rights><rights>2019 The Authors. New Phytologist © 2019 New Phytologist Trust</rights><rights>2019 The Authors. New Phytologist © 2019 New Phytologist Trust.</rights><rights>Copyright © 2019 New Phytologist Trust</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4108-23780c01e99856d68533c2c8af61e2f1ca369c09620cd949279122792e9ecfc63</citedby><cites>FETCH-LOGICAL-c4108-23780c01e99856d68533c2c8af61e2f1ca369c09620cd949279122792e9ecfc63</cites><orcidid>0000-0003-4640-1793</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26779772$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26779772$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>314,780,784,27924,27925,58238,58471</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31246280$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zou, Yi</creatorcontrib><creatorcontrib>Zhang, Xiaojing</creatorcontrib><creatorcontrib>Tan, Yunyi</creatorcontrib><creatorcontrib>Huang, Jia-Bao</creatorcontrib><creatorcontrib>Zheng, Zhiqiong</creatorcontrib><creatorcontrib>Tao, Li-Zhen</creatorcontrib><title>Phosphoethanolamine N-methyltransferase 1 contributes to maintenance of root apical meristem by affecting ROS and auxin-regulated cell differentiation in Arabidopsis</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>The continuous growth of roots requires the balance between cell division and differentiation. Reactive oxygen species (ROS) and auxin are important regulators of root development by affecting cell division and differentiation. The mechanism controlling the coordination of cell division and differentiation is not well understood.
Using a forward genetic screen, we isolated a mutant, defective primary root 2 (dpr2), defective in root apical meristem (RAM) maintenance. The DPR2 gene encodes phosphoethanolamine N-methyltransferase 1 (PEAMT1) that catalyzes phosphocholine biosynthesis in Arabidopsis. We characterized the primary root phenotypes of dpr2 using various marker lines, using histochemical and pharmacological analysis to probe early root development.
Loss-of-function of DPR2/PEAMT1 resulted in RAM consumption by affecting root stem cell niche, division zone, elongation and differentiation zone (EDZ). PIN-FORMED (PIN) protein abundance, PIN2 polar distribution and general endocytosis were impaired in the root tip of dpr2. Excess hydrogen peroxide and auxin accumulate in the EDZ of dpr2, leading to RAM consumption by accelerating cell differentiation. Suppression of ROS over-accumulation or inhibition of auxin signalling partially prevent RAM differentiation in dpr2 after choline starvation.
Taken together, we conclude that the EDZ of the root tip is most sensitive to choline shortage, leading to RAM consumption through an ROS–auxin regulation module.</description><subject>Arabidopsis</subject><subject>Arabidopsis - cytology</subject><subject>Arabidopsis - drug effects</subject><subject>Arabidopsis - enzymology</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Arabidopsis thaliana</subject><subject>auxin</subject><subject>Auxins</subject><subject>Biosynthesis</subject><subject>Cell differentiation</subject><subject>Cell Differentiation - drug effects</subject><subject>Cell division</subject><subject>Cell Division - drug effects</subject><subject>Choline</subject><subject>Choline - pharmacology</subject><subject>Consumption</subject><subject>Differentiation (biology)</subject><subject>Elongation</subject><subject>Endocytosis</subject><subject>Endocytosis - drug effects</subject><subject>Ethanolamines - metabolism</subject><subject>Genetic screening</subject><subject>Hydrogen peroxide</subject><subject>Indoleacetic Acids - pharmacology</subject><subject>Meristem - cytology</subject><subject>Meristem - drug effects</subject><subject>Meristems</subject><subject>Methyltransferase</subject><subject>Methyltransferases - metabolism</subject><subject>Microtubules - drug effects</subject><subject>Microtubules - metabolism</subject><subject>Mutation - genetics</subject><subject>Niches</subject><subject>Onium Compounds - pharmacology</subject><subject>Phenotype</subject><subject>Phenotypes</subject><subject>Phosphocholine</subject><subject>phosphoethanolamine N‐methyltransferase (PEAMT)</subject><subject>Reactive oxygen species</subject><subject>reactive oxygen species (ROS)</subject><subject>Reactive Oxygen Species - metabolism</subject><subject>Regulators</subject><subject>root apical meristem (RAM)</subject><subject>Root development</subject><subject>Starvation</subject><subject>Stem cells</subject><subject>Stem Cells - drug effects</subject><subject>Stem Cells - metabolism</subject><issn>0028-646X</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><recordid>eNp1kU1r3DAQhkVpaTbbHvoDWgS9pAcn-vDK0jGEtCmEJPQDejOz8jirxZZcSSbdH9T_WaWb5FCoDiNmeOZl4CHkDWfHvLwTP22OuWJCPyMLXitTaS6b52TByqhStfpxQA5T2jLGzEqJl-RAclErodmC_L7ZhDRtAuYN-DDA6DzSq2os_W7IEXzqMUJCyqkNPke3njMmmgMdwfmMHrxFGnoaQ8gUJmdhoCNGlzKOdL2j0Pdos_O39Mv1Vwq-ozD_cr6KeDsPkLGjFoeBdq5wEX12kF3w1Hl6GmHtujAll16RFz0MCV8__Evy_eP5t7OL6vL60-ez08vK1pzpSshGM8s4GqNXqlN6JaUVVkOvOIqeW5DKWGaUYLYztRGN4aIUgQZtb5VckqN97hTDzxlTbkeX7u8Dj2FOrRC1lrrWJXhJ3v-DbsMcfbmuUJpJWRToQn3YUzaGlCL27RTdCHHXctbeu2uLu_avu8K-e0ic1yN2T-SjrAKc7IE7N-Du_0nt1c3FY-Tb_cY25RCfNoRqGtM0Qv4BFj6vLA</recordid><startdate>201910</startdate><enddate>201910</enddate><creator>Zou, Yi</creator><creator>Zhang, Xiaojing</creator><creator>Tan, Yunyi</creator><creator>Huang, Jia-Bao</creator><creator>Zheng, Zhiqiong</creator><creator>Tao, Li-Zhen</creator><general>Wiley</general><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><orcidid>https://orcid.org/0000-0003-4640-1793</orcidid></search><sort><creationdate>201910</creationdate><title>Phosphoethanolamine N-methyltransferase 1 contributes to maintenance of root apical meristem by affecting ROS and auxin-regulated cell differentiation in Arabidopsis</title><author>Zou, Yi ; Zhang, Xiaojing ; Tan, Yunyi ; Huang, Jia-Bao ; Zheng, Zhiqiong ; Tao, Li-Zhen</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4108-23780c01e99856d68533c2c8af61e2f1ca369c09620cd949279122792e9ecfc63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Arabidopsis</topic><topic>Arabidopsis - cytology</topic><topic>Arabidopsis - drug effects</topic><topic>Arabidopsis - enzymology</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Arabidopsis thaliana</topic><topic>auxin</topic><topic>Auxins</topic><topic>Biosynthesis</topic><topic>Cell differentiation</topic><topic>Cell Differentiation - drug effects</topic><topic>Cell division</topic><topic>Cell Division - drug effects</topic><topic>Choline</topic><topic>Choline - pharmacology</topic><topic>Consumption</topic><topic>Differentiation (biology)</topic><topic>Elongation</topic><topic>Endocytosis</topic><topic>Endocytosis - drug effects</topic><topic>Ethanolamines - metabolism</topic><topic>Genetic screening</topic><topic>Hydrogen peroxide</topic><topic>Indoleacetic Acids - pharmacology</topic><topic>Meristem - cytology</topic><topic>Meristem - drug effects</topic><topic>Meristems</topic><topic>Methyltransferase</topic><topic>Methyltransferases - metabolism</topic><topic>Microtubules - drug effects</topic><topic>Microtubules - metabolism</topic><topic>Mutation - genetics</topic><topic>Niches</topic><topic>Onium Compounds - pharmacology</topic><topic>Phenotype</topic><topic>Phenotypes</topic><topic>Phosphocholine</topic><topic>phosphoethanolamine N‐methyltransferase (PEAMT)</topic><topic>Reactive oxygen species</topic><topic>reactive oxygen species (ROS)</topic><topic>Reactive Oxygen Species - metabolism</topic><topic>Regulators</topic><topic>root apical meristem (RAM)</topic><topic>Root development</topic><topic>Starvation</topic><topic>Stem cells</topic><topic>Stem Cells - drug effects</topic><topic>Stem Cells - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zou, Yi</creatorcontrib><creatorcontrib>Zhang, Xiaojing</creatorcontrib><creatorcontrib>Tan, Yunyi</creatorcontrib><creatorcontrib>Huang, Jia-Bao</creatorcontrib><creatorcontrib>Zheng, Zhiqiong</creatorcontrib><creatorcontrib>Tao, Li-Zhen</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 & 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><collection>MEDLINE - Academic</collection><jtitle>The New phytologist</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zou, Yi</au><au>Zhang, Xiaojing</au><au>Tan, Yunyi</au><au>Huang, Jia-Bao</au><au>Zheng, Zhiqiong</au><au>Tao, Li-Zhen</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Phosphoethanolamine N-methyltransferase 1 contributes to maintenance of root apical meristem by affecting ROS and auxin-regulated cell differentiation in Arabidopsis</atitle><jtitle>The New phytologist</jtitle><addtitle>New Phytol</addtitle><date>2019-10</date><risdate>2019</risdate><volume>224</volume><issue>1</issue><spage>258</spage><epage>273</epage><pages>258-273</pages><issn>0028-646X</issn><eissn>1469-8137</eissn><abstract>The continuous growth of roots requires the balance between cell division and differentiation. Reactive oxygen species (ROS) and auxin are important regulators of root development by affecting cell division and differentiation. The mechanism controlling the coordination of cell division and differentiation is not well understood.
Using a forward genetic screen, we isolated a mutant, defective primary root 2 (dpr2), defective in root apical meristem (RAM) maintenance. The DPR2 gene encodes phosphoethanolamine N-methyltransferase 1 (PEAMT1) that catalyzes phosphocholine biosynthesis in Arabidopsis. We characterized the primary root phenotypes of dpr2 using various marker lines, using histochemical and pharmacological analysis to probe early root development.
Loss-of-function of DPR2/PEAMT1 resulted in RAM consumption by affecting root stem cell niche, division zone, elongation and differentiation zone (EDZ). PIN-FORMED (PIN) protein abundance, PIN2 polar distribution and general endocytosis were impaired in the root tip of dpr2. Excess hydrogen peroxide and auxin accumulate in the EDZ of dpr2, leading to RAM consumption by accelerating cell differentiation. Suppression of ROS over-accumulation or inhibition of auxin signalling partially prevent RAM differentiation in dpr2 after choline starvation.
Taken together, we conclude that the EDZ of the root tip is most sensitive to choline shortage, leading to RAM consumption through an ROS–auxin regulation module.</abstract><cop>England</cop><pub>Wiley</pub><pmid>31246280</pmid><doi>10.1111/nph.16028</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0003-4640-1793</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Arabidopsis Arabidopsis - cytology Arabidopsis - drug effects Arabidopsis - enzymology Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Arabidopsis thaliana auxin Auxins Biosynthesis Cell differentiation Cell Differentiation - drug effects Cell division Cell Division - drug effects Choline Choline - pharmacology Consumption Differentiation (biology) Elongation Endocytosis Endocytosis - drug effects Ethanolamines - metabolism Genetic screening Hydrogen peroxide Indoleacetic Acids - pharmacology Meristem - cytology Meristem - drug effects Meristems Methyltransferase Methyltransferases - metabolism Microtubules - drug effects Microtubules - metabolism Mutation - genetics Niches Onium Compounds - pharmacology Phenotype Phenotypes Phosphocholine phosphoethanolamine N‐methyltransferase (PEAMT) Reactive oxygen species reactive oxygen species (ROS) Reactive Oxygen Species - metabolism Regulators root apical meristem (RAM) Root development Starvation Stem cells Stem Cells - drug effects Stem Cells - metabolism |
title | Phosphoethanolamine N-methyltransferase 1 contributes to maintenance of root apical meristem by affecting ROS and auxin-regulated cell differentiation in Arabidopsis |
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