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The Microtubule Plus-End Tracking Protein ARMADILLO-REPEAT KINESIN1 Promotes Microtubule Catastrophe in Arabidopsis
Microtubule dynamics are critically important for plant cell development. Here, we show that Arabidopsis thaliana ARMADILLOREPEAT KINESIN1 (ARK1) plays a key role in root hair tip growth by promoting microtubule catastrophe events. This destabilizing activity appears to maintain adequate free tubuli...
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Published in: | The Plant cell 2014-08, Vol.26 (8), p.3372-3386 |
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description | Microtubule dynamics are critically important for plant cell development. Here, we show that Arabidopsis thaliana ARMADILLOREPEAT KINESIN1 (ARK1) plays a key role in root hair tip growth by promoting microtubule catastrophe events. This destabilizing activity appears to maintain adequate free tubulin concentrations in order to permit rapid microtubule growth, which in turn is correlated with uniform tip growth. Microtubules in ark1-1 root hairs exhibited reduced catastrophe frequency and slower growth velocities, both of which were restored by low concentrations of the microtubule-destabilizing drug oryzalin. An ARK1-GFP (green fluorescent protein) fusion protein expressed under its endogenous promoter localized to growing microtubule plus ends and rescued the ark1-1 root hair phenotype. Transient overexpression of ARK1-RFP (red fluorescent protein) increased microtubule catastrophe frequency. ARK1-fusion protein constructs lacking the N-terminal motor domain still labeled microtubules, suggesting the existence of a second microtubule binding domain at the C terminus of ARK1. ARK1-GFP was broadly expressed in seedlings, but mutant phenotypes were restricted to root hairs, indicating that ARK1's function is redundant in cells other than those forming root hairs. |
doi_str_mv | 10.1105/tpc.114.126789 |
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Here, we show that Arabidopsis thaliana ARMADILLOREPEAT KINESIN1 (ARK1) plays a key role in root hair tip growth by promoting microtubule catastrophe events. This destabilizing activity appears to maintain adequate free tubulin concentrations in order to permit rapid microtubule growth, which in turn is correlated with uniform tip growth. Microtubules in ark1-1 root hairs exhibited reduced catastrophe frequency and slower growth velocities, both of which were restored by low concentrations of the microtubule-destabilizing drug oryzalin. An ARK1-GFP (green fluorescent protein) fusion protein expressed under its endogenous promoter localized to growing microtubule plus ends and rescued the ark1-1 root hair phenotype. Transient overexpression of ARK1-RFP (red fluorescent protein) increased microtubule catastrophe frequency. ARK1-fusion protein constructs lacking the N-terminal motor domain still labeled microtubules, suggesting the existence of a second microtubule binding domain at the C terminus of ARK1. ARK1-GFP was broadly expressed in seedlings, but mutant phenotypes were restricted to root hairs, indicating that ARK1's function is redundant in cells other than those forming root hairs.</description><identifier>ISSN: 1040-4651</identifier><identifier>EISSN: 1532-298X</identifier><identifier>DOI: 10.1105/tpc.114.126789</identifier><identifier>PMID: 25159991</identifier><language>eng</language><publisher>United States: American Society of Plant Biologists</publisher><subject>Arabidopsis - growth & development ; Arabidopsis - metabolism ; Arabidopsis - ultrastructure ; Arabidopsis Proteins - analysis ; Arabidopsis Proteins - metabolism ; Arabidopsis Proteins - physiology ; Binding Sites ; Cell growth ; Dinitrobenzenes - pharmacology ; Disasters ; Epidermal cells ; Fluorescence ; Kinesin - analysis ; Kinesin - metabolism ; Kinesin - physiology ; Microtubules ; Microtubules - metabolism ; Microtubules - ultrastructure ; Phenotypes ; Plant cells ; Plant Roots - growth & development ; Plant Roots - metabolism ; Plant Roots - ultrastructure ; Plants ; Protein Structure, Tertiary ; Proteins ; Root hairs ; Sulfanilamides - pharmacology</subject><ispartof>The Plant cell, 2014-08, Vol.26 (8), p.3372-3386</ispartof><rights>2014 American Society of Plant Biologists</rights><rights>2014 American Society of Plant Biologists. All rights reserved.</rights><rights>2014 American Society of Plant Biologists. All rights reserved. 2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c478t-427cb9d5378ef0dc63fa74dd6436c6dfa4eda181996294e85dab5a9ac1bdde823</citedby><orcidid>0000-0002-8746-7994</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/43190536$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/43190536$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,780,784,885,27924,27925,58238,58471</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25159991$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Eng, Ryan Christopher</creatorcontrib><creatorcontrib>Wasteneys, Geoffrey O.</creatorcontrib><title>The Microtubule Plus-End Tracking Protein ARMADILLO-REPEAT KINESIN1 Promotes Microtubule Catastrophe in Arabidopsis</title><title>The Plant cell</title><addtitle>Plant Cell</addtitle><description>Microtubule dynamics are critically important for plant cell development. Here, we show that Arabidopsis thaliana ARMADILLOREPEAT KINESIN1 (ARK1) plays a key role in root hair tip growth by promoting microtubule catastrophe events. This destabilizing activity appears to maintain adequate free tubulin concentrations in order to permit rapid microtubule growth, which in turn is correlated with uniform tip growth. Microtubules in ark1-1 root hairs exhibited reduced catastrophe frequency and slower growth velocities, both of which were restored by low concentrations of the microtubule-destabilizing drug oryzalin. An ARK1-GFP (green fluorescent protein) fusion protein expressed under its endogenous promoter localized to growing microtubule plus ends and rescued the ark1-1 root hair phenotype. Transient overexpression of ARK1-RFP (red fluorescent protein) increased microtubule catastrophe frequency. ARK1-fusion protein constructs lacking the N-terminal motor domain still labeled microtubules, suggesting the existence of a second microtubule binding domain at the C terminus of ARK1. ARK1-GFP was broadly expressed in seedlings, but mutant phenotypes were restricted to root hairs, indicating that ARK1's function is redundant in cells other than those forming root hairs.</description><subject>Arabidopsis - growth & development</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis - ultrastructure</subject><subject>Arabidopsis Proteins - analysis</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Arabidopsis Proteins - physiology</subject><subject>Binding Sites</subject><subject>Cell growth</subject><subject>Dinitrobenzenes - pharmacology</subject><subject>Disasters</subject><subject>Epidermal cells</subject><subject>Fluorescence</subject><subject>Kinesin - analysis</subject><subject>Kinesin - metabolism</subject><subject>Kinesin - physiology</subject><subject>Microtubules</subject><subject>Microtubules - metabolism</subject><subject>Microtubules - ultrastructure</subject><subject>Phenotypes</subject><subject>Plant cells</subject><subject>Plant Roots - growth & development</subject><subject>Plant Roots - metabolism</subject><subject>Plant Roots - ultrastructure</subject><subject>Plants</subject><subject>Protein Structure, Tertiary</subject><subject>Proteins</subject><subject>Root hairs</subject><subject>Sulfanilamides - pharmacology</subject><issn>1040-4651</issn><issn>1532-298X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><recordid>eNpVkUFP4zAQha0VaAssV26gHPeS4klsJ74gVSXLVhSooEjcLMd2wJAmwU6Q-PfrqqVaTn7S--bNyA-hE8BjAEzP-04FQcaQsCznP9AB0DSJE54_7QWNCY4JozBCh96_YowhA_4TjRIKlHMOB8gvX0x0Y5Vr-6EcahMt6sHHRaOjpZPqzTbP0SJ4xjbR5P5mcjmbz-_i-2JRTJbR9ey2eJjdwppYBcZ_C5rKXvretV1YsJ52srS67bz1v9B-JWtvjrfvEXr8Uyynf-P53dVsOpnHimR5H5MkUyXXNM1yU2GtWFrJjGjNSMoU05UkRkvIgXOWcGJyqmVJJZcKSq1NnqRH6GKT2w3lymhlmt7JWnTOrqT7FK204rvT2Bfx3H4IAhkjBIeA39sA174PxvdiZb0ydS0b0w5eAGUMcIY5D-h4g4YP8N6ZarcGsFg3JUJTQRCxaSoMnP1_3A7_qiYApxvg1fet2_kkBY5pytJ_evaaYg</recordid><startdate>20140801</startdate><enddate>20140801</enddate><creator>Eng, Ryan Christopher</creator><creator>Wasteneys, Geoffrey O.</creator><general>American Society of Plant Biologists</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>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-8746-7994</orcidid></search><sort><creationdate>20140801</creationdate><title>The Microtubule Plus-End Tracking Protein ARMADILLO-REPEAT KINESIN1 Promotes Microtubule Catastrophe in Arabidopsis</title><author>Eng, Ryan Christopher ; Wasteneys, Geoffrey O.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c478t-427cb9d5378ef0dc63fa74dd6436c6dfa4eda181996294e85dab5a9ac1bdde823</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Arabidopsis - growth & development</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis - ultrastructure</topic><topic>Arabidopsis Proteins - analysis</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Arabidopsis Proteins - physiology</topic><topic>Binding Sites</topic><topic>Cell growth</topic><topic>Dinitrobenzenes - pharmacology</topic><topic>Disasters</topic><topic>Epidermal cells</topic><topic>Fluorescence</topic><topic>Kinesin - analysis</topic><topic>Kinesin - metabolism</topic><topic>Kinesin - physiology</topic><topic>Microtubules</topic><topic>Microtubules - metabolism</topic><topic>Microtubules - ultrastructure</topic><topic>Phenotypes</topic><topic>Plant cells</topic><topic>Plant Roots - growth & development</topic><topic>Plant Roots - metabolism</topic><topic>Plant Roots - ultrastructure</topic><topic>Plants</topic><topic>Protein Structure, Tertiary</topic><topic>Proteins</topic><topic>Root hairs</topic><topic>Sulfanilamides - pharmacology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Eng, Ryan Christopher</creatorcontrib><creatorcontrib>Wasteneys, Geoffrey O.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Plant cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Eng, Ryan Christopher</au><au>Wasteneys, Geoffrey O.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The Microtubule Plus-End Tracking Protein ARMADILLO-REPEAT KINESIN1 Promotes Microtubule Catastrophe in Arabidopsis</atitle><jtitle>The Plant cell</jtitle><addtitle>Plant Cell</addtitle><date>2014-08-01</date><risdate>2014</risdate><volume>26</volume><issue>8</issue><spage>3372</spage><epage>3386</epage><pages>3372-3386</pages><issn>1040-4651</issn><eissn>1532-298X</eissn><abstract>Microtubule dynamics are critically important for plant cell development. Here, we show that Arabidopsis thaliana ARMADILLOREPEAT KINESIN1 (ARK1) plays a key role in root hair tip growth by promoting microtubule catastrophe events. This destabilizing activity appears to maintain adequate free tubulin concentrations in order to permit rapid microtubule growth, which in turn is correlated with uniform tip growth. Microtubules in ark1-1 root hairs exhibited reduced catastrophe frequency and slower growth velocities, both of which were restored by low concentrations of the microtubule-destabilizing drug oryzalin. An ARK1-GFP (green fluorescent protein) fusion protein expressed under its endogenous promoter localized to growing microtubule plus ends and rescued the ark1-1 root hair phenotype. Transient overexpression of ARK1-RFP (red fluorescent protein) increased microtubule catastrophe frequency. ARK1-fusion protein constructs lacking the N-terminal motor domain still labeled microtubules, suggesting the existence of a second microtubule binding domain at the C terminus of ARK1. ARK1-GFP was broadly expressed in seedlings, but mutant phenotypes were restricted to root hairs, indicating that ARK1's function is redundant in cells other than those forming root hairs.</abstract><cop>United States</cop><pub>American Society of Plant Biologists</pub><pmid>25159991</pmid><doi>10.1105/tpc.114.126789</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0002-8746-7994</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Arabidopsis - growth & development Arabidopsis - metabolism Arabidopsis - ultrastructure Arabidopsis Proteins - analysis Arabidopsis Proteins - metabolism Arabidopsis Proteins - physiology Binding Sites Cell growth Dinitrobenzenes - pharmacology Disasters Epidermal cells Fluorescence Kinesin - analysis Kinesin - metabolism Kinesin - physiology Microtubules Microtubules - metabolism Microtubules - ultrastructure Phenotypes Plant cells Plant Roots - growth & development Plant Roots - metabolism Plant Roots - ultrastructure Plants Protein Structure, Tertiary Proteins Root hairs Sulfanilamides - pharmacology |
title | The Microtubule Plus-End Tracking Protein ARMADILLO-REPEAT KINESIN1 Promotes Microtubule Catastrophe in Arabidopsis |
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