Putrescine Depletion Affects Arabidopsis Root Meristem Size by Modulating Auxin and Cytokinin Signaling and ROS Accumulation
Polyamines (PAs) dramatically affect root architecture and development, mainly by unknown mechanisms; however, accumulating evidence points to hormone signaling and reactive oxygen species (ROS) as candidate mechanisms. To test this hypothesis, PA levels were modified by progressively reducing ADC1/...
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| Veröffentlicht in: | International journal of molecular sciences 2021-04, Vol.22 (8), p.4094, Article 4094 |
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| description | Polyamines (PAs) dramatically affect root architecture and development, mainly by unknown mechanisms; however, accumulating evidence points to hormone signaling and reactive oxygen species (ROS) as candidate mechanisms. To test this hypothesis, PA levels were modified by progressively reducing ADC1/2 activity and Put levels, and then changes in root meristematic zone (MZ) size, ROS, and auxin and cytokinin (CK) signaling were investigated. Decreasing putrescine resulted in an interesting inverted-U-trend in primary root growth and a similar trend in MZ size, and differential changes in putrescine (Put), spermidine (Spd), and combined spermine (Spm) plus thermospermine (Tspm) levels. At low Put concentrations, ROS accumulation increased coincidently with decreasing MZ size, and treatment with ROS scavenger KI partially rescued this phenotype. Analysis of double AtrbohD/F loss-of-function mutants indicated that NADPH oxidases were not involved in H2O2 accumulation and that elevated ROS levels were due to changes in PA back-conversion, terminal catabolism, PA ROS scavenging, or another pathway. Decreasing Put resulted in a non-linear trend in auxin signaling, whereas CK signaling decreased, re-balancing auxin and CK signaling. Different levels of Put modulated the expression of PIN1 and PIN2 auxin transporters, indicating changes to auxin distribution. These data strongly suggest that PAs modulate MZ size through both hormone signaling and ROS accumulation in Arabidopsis. |
| doi_str_mv | 10.3390/ijms22084094 |
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To test this hypothesis, PA levels were modified by progressively reducing ADC1/2 activity and Put levels, and then changes in root meristematic zone (MZ) size, ROS, and auxin and cytokinin (CK) signaling were investigated. Decreasing putrescine resulted in an interesting inverted-U-trend in primary root growth and a similar trend in MZ size, and differential changes in putrescine (Put), spermidine (Spd), and combined spermine (Spm) plus thermospermine (Tspm) levels. At low Put concentrations, ROS accumulation increased coincidently with decreasing MZ size, and treatment with ROS scavenger KI partially rescued this phenotype. Analysis of double AtrbohD/F loss-of-function mutants indicated that NADPH oxidases were not involved in H2O2 accumulation and that elevated ROS levels were due to changes in PA back-conversion, terminal catabolism, PA ROS scavenging, or another pathway. Decreasing Put resulted in a non-linear trend in auxin signaling, whereas CK signaling decreased, re-balancing auxin and CK signaling. Different levels of Put modulated the expression of PIN1 and PIN2 auxin transporters, indicating changes to auxin distribution. These data strongly suggest that PAs modulate MZ size through both hormone signaling and ROS accumulation in Arabidopsis.</description><identifier>ISSN: 1422-0067</identifier><identifier>ISSN: 1661-6596</identifier><identifier>EISSN: 1422-0067</identifier><identifier>DOI: 10.3390/ijms22084094</identifier><identifier>PMID: 33920993</identifier><language>eng</language><publisher>BASEL: Mdpi</publisher><subject><![CDATA[Accumulation ; Arabidopsis ; Arabidopsis - anatomy & histology ; Arabidopsis - drug effects ; Arabidopsis - genetics ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Arginine - pharmacology ; auxin response ; Biochemistry & Molecular Biology ; Biosynthesis ; Catabolism ; Cell division ; Chemistry ; Chemistry, Multidisciplinary ; Competition ; Cytokinins ; Cytokinins - metabolism ; Depletion ; Enzymes ; Genes ; Genotype & phenotype ; Homeostasis ; hormone signaling ; Hydrogen peroxide ; Hydrogen Peroxide - metabolism ; Indoleacetic Acids - metabolism ; Life Sciences & Biomedicine ; Meristem - anatomy & histology ; Meristem - drug effects ; Meristems ; Models, Biological ; Mutation - genetics ; NAD(P)H oxidase ; NADPH Oxidases - metabolism ; Organ Size - drug effects ; Phenotype ; Phenotypes ; Physical Sciences ; Physiology ; PIN transporter ; Pin1 protein ; polyamine ; Polyamines ; Potassium Iodide - pharmacology ; Putrescine ; Putrescine - metabolism ; Reactive Oxygen Species - metabolism ; root meristem ; ROS ; Scavenging ; Science & Technology ; Signal Transduction - drug effects ; Spermidine ; Spermine]]></subject><ispartof>International journal of molecular sciences, 2021-04, Vol.22 (8), p.4094, Article 4094</ispartof><rights>2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2021 by the authors. 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>true</woscitedreferencessubscribed><woscitedreferencescount>27</woscitedreferencescount><woscitedreferencesoriginalsourcerecordid>wos000644323100001</woscitedreferencesoriginalsourcerecordid><citedby>FETCH-LOGICAL-c544t-b79d0b1f0d1b42961b7b7963e09aa5a800aceeaee4a7c86aad2c83503426dd453</citedby><cites>FETCH-LOGICAL-c544t-b79d0b1f0d1b42961b7b7963e09aa5a800aceeaee4a7c86aad2c83503426dd453</cites><orcidid>0000-0002-6464-4580 ; 0000-0001-8264-2450 ; 0000-0001-6524-7264 ; 0009-0003-1226-9242</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8071467/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8071467/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,729,782,786,887,27931,27932,39265,53798,53800</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33920993$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hashem, Ahmed M.</creatorcontrib><creatorcontrib>Moore, Simon</creatorcontrib><creatorcontrib>Chen, Shangjian</creatorcontrib><creatorcontrib>Hu, Chenchen</creatorcontrib><creatorcontrib>Zhao, Qing</creatorcontrib><creatorcontrib>Elesawi, Ibrahim Eid</creatorcontrib><creatorcontrib>Feng, Yanni</creatorcontrib><creatorcontrib>Topping, Jennifer F.</creatorcontrib><creatorcontrib>Liu, Junli</creatorcontrib><creatorcontrib>Lindsey, Keith</creatorcontrib><creatorcontrib>Chen, Chunli</creatorcontrib><title>Putrescine Depletion Affects Arabidopsis Root Meristem Size by Modulating Auxin and Cytokinin Signaling and ROS Accumulation</title><title>International journal of molecular sciences</title><addtitle>INT J MOL SCI</addtitle><addtitle>Int J Mol Sci</addtitle><description>Polyamines (PAs) dramatically affect root architecture and development, mainly by unknown mechanisms; however, accumulating evidence points to hormone signaling and reactive oxygen species (ROS) as candidate mechanisms. To test this hypothesis, PA levels were modified by progressively reducing ADC1/2 activity and Put levels, and then changes in root meristematic zone (MZ) size, ROS, and auxin and cytokinin (CK) signaling were investigated. Decreasing putrescine resulted in an interesting inverted-U-trend in primary root growth and a similar trend in MZ size, and differential changes in putrescine (Put), spermidine (Spd), and combined spermine (Spm) plus thermospermine (Tspm) levels. At low Put concentrations, ROS accumulation increased coincidently with decreasing MZ size, and treatment with ROS scavenger KI partially rescued this phenotype. Analysis of double AtrbohD/F loss-of-function mutants indicated that NADPH oxidases were not involved in H2O2 accumulation and that elevated ROS levels were due to changes in PA back-conversion, terminal catabolism, PA ROS scavenging, or another pathway. Decreasing Put resulted in a non-linear trend in auxin signaling, whereas CK signaling decreased, re-balancing auxin and CK signaling. Different levels of Put modulated the expression of PIN1 and PIN2 auxin transporters, indicating changes to auxin distribution. These data strongly suggest that PAs modulate MZ size through both hormone signaling and ROS accumulation in Arabidopsis.</description><subject>Accumulation</subject><subject>Arabidopsis</subject><subject>Arabidopsis - anatomy & histology</subject><subject>Arabidopsis - drug effects</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Arginine - pharmacology</subject><subject>auxin response</subject><subject>Biochemistry & Molecular Biology</subject><subject>Biosynthesis</subject><subject>Catabolism</subject><subject>Cell division</subject><subject>Chemistry</subject><subject>Chemistry, Multidisciplinary</subject><subject>Competition</subject><subject>Cytokinins</subject><subject>Cytokinins - metabolism</subject><subject>Depletion</subject><subject>Enzymes</subject><subject>Genes</subject><subject>Genotype & phenotype</subject><subject>Homeostasis</subject><subject>hormone signaling</subject><subject>Hydrogen peroxide</subject><subject>Hydrogen Peroxide - metabolism</subject><subject>Indoleacetic Acids - metabolism</subject><subject>Life Sciences & Biomedicine</subject><subject>Meristem - anatomy & histology</subject><subject>Meristem - drug effects</subject><subject>Meristems</subject><subject>Models, Biological</subject><subject>Mutation - genetics</subject><subject>NAD(P)H oxidase</subject><subject>NADPH Oxidases - metabolism</subject><subject>Organ Size - drug effects</subject><subject>Phenotype</subject><subject>Phenotypes</subject><subject>Physical Sciences</subject><subject>Physiology</subject><subject>PIN transporter</subject><subject>Pin1 protein</subject><subject>polyamine</subject><subject>Polyamines</subject><subject>Potassium Iodide - pharmacology</subject><subject>Putrescine</subject><subject>Putrescine - metabolism</subject><subject>Reactive Oxygen Species - metabolism</subject><subject>root meristem</subject><subject>ROS</subject><subject>Scavenging</subject><subject>Science & Technology</subject><subject>Signal Transduction - drug effects</subject><subject>Spermidine</subject><subject>Spermine</subject><issn>1422-0067</issn><issn>1661-6596</issn><issn>1422-0067</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>HGBXW</sourceid><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><sourceid>DOA</sourceid><recordid>eNqNks1vEzEQxVcIREvhxhlZ4ggpXtv7dUGKwkcrtSpq4GyN7dngsLGD7QWC-ONxkhKlN04ev_nNs-Xnonhe0nPOO_rGLleRMdoK2okHxWkpGJtQWjcPj-qT4kmMS0oZZ1X3uDjJg4x2HT8t_nwaU8CorUPyDtcDJusdmfY96hTJNICyxq-jjeTW-0SuMdiYcEXm9jcStSHX3owDJOsWZDr-so6AM2S2Sf6bdXk3twsHw7a71W9v5mSq9bjajXj3tHjUwxDx2d16Vnz58P7z7GJydfPxcja9muhKiDRRTWeoKntqSiVYV5eqyVLNkXYAFbSUgkYERAGNbmsAw3TLK8oFq40RFT8rLve-xsNSroNdQdhID1buBB8WEkKyekDJy8rUvTJ1thalAcCGamgEBdGqvlLZ6-3eaz2qFRqNLgUY7pne7zj7VS78D9nSphR1kw1e3hkE_33EmOTSjyG_UpSsEm0tqo7xTL3eUzr4GAP2hxNKKre5y-PcM_7i-FYH-F_QGXi1B36i8n3OG53GA0bzJxGCM17mipaZbv-fntm0S3PmR5f4X-FkzNI</recordid><startdate>20210415</startdate><enddate>20210415</enddate><creator>Hashem, Ahmed M.</creator><creator>Moore, Simon</creator><creator>Chen, Shangjian</creator><creator>Hu, Chenchen</creator><creator>Zhao, Qing</creator><creator>Elesawi, Ibrahim Eid</creator><creator>Feng, Yanni</creator><creator>Topping, Jennifer F.</creator><creator>Liu, Junli</creator><creator>Lindsey, Keith</creator><creator>Chen, Chunli</creator><general>Mdpi</general><general>MDPI AG</general><general>MDPI</general><scope>BLEPL</scope><scope>DTL</scope><scope>HGBXW</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>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>K9.</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>MBDVC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-6464-4580</orcidid><orcidid>https://orcid.org/0000-0001-8264-2450</orcidid><orcidid>https://orcid.org/0000-0001-6524-7264</orcidid><orcidid>https://orcid.org/0009-0003-1226-9242</orcidid></search><sort><creationdate>20210415</creationdate><title>Putrescine Depletion Affects Arabidopsis Root Meristem Size by Modulating Auxin and Cytokinin Signaling and ROS Accumulation</title><author>Hashem, Ahmed M. ; Moore, Simon ; Chen, Shangjian ; Hu, Chenchen ; Zhao, Qing ; Elesawi, Ibrahim Eid ; Feng, Yanni ; Topping, Jennifer F. ; Liu, Junli ; Lindsey, Keith ; Chen, Chunli</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c544t-b79d0b1f0d1b42961b7b7963e09aa5a800aceeaee4a7c86aad2c83503426dd453</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Accumulation</topic><topic>Arabidopsis</topic><topic>Arabidopsis - anatomy & histology</topic><topic>Arabidopsis - drug effects</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Arginine - pharmacology</topic><topic>auxin response</topic><topic>Biochemistry & Molecular Biology</topic><topic>Biosynthesis</topic><topic>Catabolism</topic><topic>Cell division</topic><topic>Chemistry</topic><topic>Chemistry, Multidisciplinary</topic><topic>Competition</topic><topic>Cytokinins</topic><topic>Cytokinins - metabolism</topic><topic>Depletion</topic><topic>Enzymes</topic><topic>Genes</topic><topic>Genotype & phenotype</topic><topic>Homeostasis</topic><topic>hormone signaling</topic><topic>Hydrogen peroxide</topic><topic>Hydrogen Peroxide - metabolism</topic><topic>Indoleacetic Acids - metabolism</topic><topic>Life Sciences & Biomedicine</topic><topic>Meristem - anatomy & histology</topic><topic>Meristem - drug effects</topic><topic>Meristems</topic><topic>Models, Biological</topic><topic>Mutation - 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To test this hypothesis, PA levels were modified by progressively reducing ADC1/2 activity and Put levels, and then changes in root meristematic zone (MZ) size, ROS, and auxin and cytokinin (CK) signaling were investigated. Decreasing putrescine resulted in an interesting inverted-U-trend in primary root growth and a similar trend in MZ size, and differential changes in putrescine (Put), spermidine (Spd), and combined spermine (Spm) plus thermospermine (Tspm) levels. At low Put concentrations, ROS accumulation increased coincidently with decreasing MZ size, and treatment with ROS scavenger KI partially rescued this phenotype. Analysis of double AtrbohD/F loss-of-function mutants indicated that NADPH oxidases were not involved in H2O2 accumulation and that elevated ROS levels were due to changes in PA back-conversion, terminal catabolism, PA ROS scavenging, or another pathway. Decreasing Put resulted in a non-linear trend in auxin signaling, whereas CK signaling decreased, re-balancing auxin and CK signaling. Different levels of Put modulated the expression of PIN1 and PIN2 auxin transporters, indicating changes to auxin distribution. These data strongly suggest that PAs modulate MZ size through both hormone signaling and ROS accumulation in Arabidopsis.</abstract><cop>BASEL</cop><pub>Mdpi</pub><pmid>33920993</pmid><doi>10.3390/ijms22084094</doi><tpages>18</tpages><orcidid>https://orcid.org/0000-0002-6464-4580</orcidid><orcidid>https://orcid.org/0000-0001-8264-2450</orcidid><orcidid>https://orcid.org/0000-0001-6524-7264</orcidid><orcidid>https://orcid.org/0009-0003-1226-9242</orcidid><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; MDPI - Multidisciplinary Digital Publishing Institute; Web of Science - Science Citation Index Expanded - 2021<img src="https://exlibris-pub.s3.amazonaws.com/fromwos-v2.jpg" />; PubMed Central |
| subjects | Accumulation Arabidopsis Arabidopsis - anatomy & histology Arabidopsis - drug effects Arabidopsis - genetics Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Arginine - pharmacology auxin response Biochemistry & Molecular Biology Biosynthesis Catabolism Cell division Chemistry Chemistry, Multidisciplinary Competition Cytokinins Cytokinins - metabolism Depletion Enzymes Genes Genotype & phenotype Homeostasis hormone signaling Hydrogen peroxide Hydrogen Peroxide - metabolism Indoleacetic Acids - metabolism Life Sciences & Biomedicine Meristem - anatomy & histology Meristem - drug effects Meristems Models, Biological Mutation - genetics NAD(P)H oxidase NADPH Oxidases - metabolism Organ Size - drug effects Phenotype Phenotypes Physical Sciences Physiology PIN transporter Pin1 protein polyamine Polyamines Potassium Iodide - pharmacology Putrescine Putrescine - metabolism Reactive Oxygen Species - metabolism root meristem ROS Scavenging Science & Technology Signal Transduction - drug effects Spermidine Spermine |
| title | Putrescine Depletion Affects Arabidopsis Root Meristem Size by Modulating Auxin and Cytokinin Signaling and ROS Accumulation |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-04T08%3A49%3A28IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Putrescine%20Depletion%20Affects%20Arabidopsis%20Root%20Meristem%20Size%20by%20Modulating%20Auxin%20and%20Cytokinin%20Signaling%20and%20ROS%20Accumulation&rft.jtitle=International%20journal%20of%20molecular%20sciences&rft.au=Hashem,%20Ahmed%20M.&rft.date=2021-04-15&rft.volume=22&rft.issue=8&rft.spage=4094&rft.pages=4094-&rft.artnum=4094&rft.issn=1422-0067&rft.eissn=1422-0067&rft_id=info:doi/10.3390/ijms22084094&rft_dat=%3Cproquest_cross%3E2548645923%3C/proquest_cross%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2548645923&rft_id=info:pmid/33920993&rft_doaj_id=oai_doaj_org_article_315d6fbd69aa41daae70ca740a48bf5b&rfr_iscdi=true |