Arabidopsis Villins Promote Actin Turnover at Pollen Tube Tips and Facilitate the Construction of Actin Collars
Apical actin filaments are crucial for pollen tube tip growth. However, the specific dynamic changes and regulatory mechanisms associated with actin filaments in the apical region remain largely unknown. Here, we have investigated the quantitative dynamic parameters that underlie actin filament grow...
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| Veröffentlicht in: | The Plant cell 2013-05, Vol.25 (5), p.1803-1817 |
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| creator | Qu, Xiaolu Zhang, Hua Xie, Yurong Wang, Juan Chen, Naizhi Huang, Shanjin |
| description | Apical actin filaments are crucial for pollen tube tip growth. However, the specific dynamic changes and regulatory mechanisms associated with actin filaments in the apical region remain largely unknown. Here, we have investigated the quantitative dynamic parameters that underlie actin filament growth and disappearance in the apical regions of pollen tubes and identified villin as the major player that drives rapid turnover of actin filaments in this region. Downregulation of Arabidopsis thaliana VILLIN2 (VLN2) and VLN5 led to accumulation of actin filaments at the pollen tube apex. Careful analysis of single filament dynamics showed that the severing frequency significantly decreased, and the lifetime significantly increased in vln2 vln5 pollen tubes. These results indicate that villin-mediated severing is critical for turnover and departure of actin filaments originating in the apical region. Consequently, the construction of actin collars was affected in vln2 vln5 pollen tubes. In addition to the decrease in severing frequency, actin filaments also became wavy and buckled in the apical cytoplasm of vln2 vln5 pollen tubes. These results suggest that villin confers rigidity upon actin filaments. Furthermore, an observed decrease in skewness of actin filaments in the subapical region of vln2 vln5 pollen tubes suggests that villin-mediated bundling activity may also play a role in the construction of actin collars. Thus, our data suggest that villins promote actin turnover at pollen tube tips and facilitate the construction of actin collars. |
| doi_str_mv | 10.1105/tpc.113.110940 |
| format | Article |
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However, the specific dynamic changes and regulatory mechanisms associated with actin filaments in the apical region remain largely unknown. Here, we have investigated the quantitative dynamic parameters that underlie actin filament growth and disappearance in the apical regions of pollen tubes and identified villin as the major player that drives rapid turnover of actin filaments in this region. Downregulation of Arabidopsis thaliana VILLIN2 (VLN2) and VLN5 led to accumulation of actin filaments at the pollen tube apex. Careful analysis of single filament dynamics showed that the severing frequency significantly decreased, and the lifetime significantly increased in vln2 vln5 pollen tubes. These results indicate that villin-mediated severing is critical for turnover and departure of actin filaments originating in the apical region. Consequently, the construction of actin collars was affected in vln2 vln5 pollen tubes. In addition to the decrease in severing frequency, actin filaments also became wavy and buckled in the apical cytoplasm of vln2 vln5 pollen tubes. These results suggest that villin confers rigidity upon actin filaments. Furthermore, an observed decrease in skewness of actin filaments in the subapical region of vln2 vln5 pollen tubes suggests that villin-mediated bundling activity may also play a role in the construction of actin collars. Thus, our data suggest that villins promote actin turnover at pollen tube tips and facilitate the construction of actin collars.</description><identifier>ISSN: 1040-4651</identifier><identifier>EISSN: 1532-298X</identifier><identifier>DOI: 10.1105/tpc.113.110940</identifier><identifier>PMID: 23715472</identifier><language>eng</language><publisher>United States: American Society of Plant Biologists</publisher><subject>actin ; Actin Cytoskeleton - genetics ; Actin Cytoskeleton - metabolism ; Actins ; Actins - genetics ; Actins - metabolism ; Arabidopsis ; Arabidopsis - genetics ; Arabidopsis - growth & development ; Arabidopsis - metabolism ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Bundling ; Calcium ; Cell growth ; collars ; Gene Expression Regulation, Plant ; Luminescent Proteins - genetics ; Luminescent Proteins - metabolism ; Microfilament Proteins - genetics ; Microfilament Proteins - metabolism ; Microfilaments ; Microscopy, Confocal ; Microscopy, Fluorescence ; Models, Biological ; Mutation ; Plant cells ; Plant growth regulators ; Plants ; Plants, Genetically Modified ; Pollen ; Pollen Tube - genetics ; Pollen Tube - growth & development ; Pollen Tube - metabolism ; Pollen tubes ; rab GTP-Binding Proteins - genetics ; rab GTP-Binding Proteins - metabolism ; Reverse Transcriptase Polymerase Chain Reaction ; Transport Vesicles - metabolism</subject><ispartof>The Plant cell, 2013-05, Vol.25 (5), p.1803-1817</ispartof><rights>2013 American Society of Plant Biologists</rights><rights>2013 American Society of Plant Biologists. All rights reserved. 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c511t-57cf80e641949d984ae2f6bdb2f6985437b30377bd50ee51b7fb199c2ad2dce3</citedby><orcidid>0000-0001-9517-2515</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/23481919$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/23481919$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,776,780,799,881,27901,27902,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23715472$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Qu, Xiaolu</creatorcontrib><creatorcontrib>Zhang, Hua</creatorcontrib><creatorcontrib>Xie, Yurong</creatorcontrib><creatorcontrib>Wang, Juan</creatorcontrib><creatorcontrib>Chen, Naizhi</creatorcontrib><creatorcontrib>Huang, Shanjin</creatorcontrib><title>Arabidopsis Villins Promote Actin Turnover at Pollen Tube Tips and Facilitate the Construction of Actin Collars</title><title>The Plant cell</title><addtitle>Plant Cell</addtitle><description>Apical actin filaments are crucial for pollen tube tip growth. However, the specific dynamic changes and regulatory mechanisms associated with actin filaments in the apical region remain largely unknown. Here, we have investigated the quantitative dynamic parameters that underlie actin filament growth and disappearance in the apical regions of pollen tubes and identified villin as the major player that drives rapid turnover of actin filaments in this region. Downregulation of Arabidopsis thaliana VILLIN2 (VLN2) and VLN5 led to accumulation of actin filaments at the pollen tube apex. Careful analysis of single filament dynamics showed that the severing frequency significantly decreased, and the lifetime significantly increased in vln2 vln5 pollen tubes. These results indicate that villin-mediated severing is critical for turnover and departure of actin filaments originating in the apical region. Consequently, the construction of actin collars was affected in vln2 vln5 pollen tubes. In addition to the decrease in severing frequency, actin filaments also became wavy and buckled in the apical cytoplasm of vln2 vln5 pollen tubes. These results suggest that villin confers rigidity upon actin filaments. Furthermore, an observed decrease in skewness of actin filaments in the subapical region of vln2 vln5 pollen tubes suggests that villin-mediated bundling activity may also play a role in the construction of actin collars. Thus, our data suggest that villins promote actin turnover at pollen tube tips and facilitate the construction of actin collars.</description><subject>actin</subject><subject>Actin Cytoskeleton - genetics</subject><subject>Actin Cytoskeleton - metabolism</subject><subject>Actins</subject><subject>Actins - genetics</subject><subject>Actins - metabolism</subject><subject>Arabidopsis</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - growth & development</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Bundling</subject><subject>Calcium</subject><subject>Cell growth</subject><subject>collars</subject><subject>Gene Expression Regulation, Plant</subject><subject>Luminescent Proteins - genetics</subject><subject>Luminescent Proteins - metabolism</subject><subject>Microfilament Proteins - genetics</subject><subject>Microfilament Proteins - metabolism</subject><subject>Microfilaments</subject><subject>Microscopy, Confocal</subject><subject>Microscopy, Fluorescence</subject><subject>Models, Biological</subject><subject>Mutation</subject><subject>Plant cells</subject><subject>Plant growth regulators</subject><subject>Plants</subject><subject>Plants, Genetically Modified</subject><subject>Pollen</subject><subject>Pollen Tube - genetics</subject><subject>Pollen Tube - growth & development</subject><subject>Pollen Tube - metabolism</subject><subject>Pollen tubes</subject><subject>rab GTP-Binding Proteins - genetics</subject><subject>rab GTP-Binding Proteins - metabolism</subject><subject>Reverse Transcriptase Polymerase Chain Reaction</subject><subject>Transport Vesicles - metabolism</subject><issn>1040-4651</issn><issn>1532-298X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFUUFrHCEYlZLSpEmuvbV4zGVSv1HH8RJYliQtBJrDUnoTdZzGMKtTdRb67-uy25CeetHn97338PseQh-AXAMQ_rnMtgK6f0hG3qAz4LRtWtn_OKmYMNKwjsMpep_zMyEEBMh36LSlAjgT7RmKq6SNH-Kcfcbf_TT5kPFjittYHF7Z4gPeLCnEnUtYF_wYp8ntS8bhjZ8z1mHAd9r6yRddFeXJ4XUMuaSlamPAcTy6rKtSp3yB3o56yu7yeJ-jzd3tZv2lefh2_3W9emgsBygNF3bsiesYSCYH2TPt2rEzg6mn7DmjwlBChTADJ85xMGI0IKVt9dAO1tFzdHOwnRezdbUSStKTmpPf6vRbRe3Vv53gn9TPuFO0k0wQUQ2ujgYp_lpcLmrrs3V1huDiklW7X2ZXl0j-SwUqKGOEE1ap1weqTTHn5MaXHwFR-zxVzbMCqg55VsGn13O80P8GWAkfD4TnXGJ61Wc9SJD0D4N0pzw</recordid><startdate>20130501</startdate><enddate>20130501</enddate><creator>Qu, Xiaolu</creator><creator>Zhang, Hua</creator><creator>Xie, Yurong</creator><creator>Wang, Juan</creator><creator>Chen, Naizhi</creator><creator>Huang, Shanjin</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>7S9</scope><scope>L.6</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-9517-2515</orcidid></search><sort><creationdate>20130501</creationdate><title>Arabidopsis Villins Promote Actin Turnover at Pollen Tube Tips and Facilitate the Construction of Actin Collars</title><author>Qu, Xiaolu ; Zhang, Hua ; Xie, Yurong ; Wang, Juan ; Chen, Naizhi ; Huang, Shanjin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c511t-57cf80e641949d984ae2f6bdb2f6985437b30377bd50ee51b7fb199c2ad2dce3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>actin</topic><topic>Actin Cytoskeleton - genetics</topic><topic>Actin Cytoskeleton - metabolism</topic><topic>Actins</topic><topic>Actins - genetics</topic><topic>Actins - metabolism</topic><topic>Arabidopsis</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - growth & development</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Bundling</topic><topic>Calcium</topic><topic>Cell growth</topic><topic>collars</topic><topic>Gene Expression Regulation, Plant</topic><topic>Luminescent Proteins - genetics</topic><topic>Luminescent Proteins - metabolism</topic><topic>Microfilament Proteins - genetics</topic><topic>Microfilament Proteins - metabolism</topic><topic>Microfilaments</topic><topic>Microscopy, Confocal</topic><topic>Microscopy, Fluorescence</topic><topic>Models, Biological</topic><topic>Mutation</topic><topic>Plant cells</topic><topic>Plant growth regulators</topic><topic>Plants</topic><topic>Plants, Genetically Modified</topic><topic>Pollen</topic><topic>Pollen Tube - genetics</topic><topic>Pollen Tube - growth & development</topic><topic>Pollen Tube - metabolism</topic><topic>Pollen tubes</topic><topic>rab GTP-Binding Proteins - genetics</topic><topic>rab GTP-Binding Proteins - metabolism</topic><topic>Reverse Transcriptase Polymerase Chain Reaction</topic><topic>Transport Vesicles - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Qu, Xiaolu</creatorcontrib><creatorcontrib>Zhang, Hua</creatorcontrib><creatorcontrib>Xie, Yurong</creatorcontrib><creatorcontrib>Wang, Juan</creatorcontrib><creatorcontrib>Chen, Naizhi</creatorcontrib><creatorcontrib>Huang, Shanjin</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>AGRICOLA</collection><collection>AGRICOLA - 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>Qu, Xiaolu</au><au>Zhang, Hua</au><au>Xie, Yurong</au><au>Wang, Juan</au><au>Chen, Naizhi</au><au>Huang, Shanjin</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Arabidopsis Villins Promote Actin Turnover at Pollen Tube Tips and Facilitate the Construction of Actin Collars</atitle><jtitle>The Plant cell</jtitle><addtitle>Plant Cell</addtitle><date>2013-05-01</date><risdate>2013</risdate><volume>25</volume><issue>5</issue><spage>1803</spage><epage>1817</epage><pages>1803-1817</pages><issn>1040-4651</issn><eissn>1532-298X</eissn><abstract>Apical actin filaments are crucial for pollen tube tip growth. However, the specific dynamic changes and regulatory mechanisms associated with actin filaments in the apical region remain largely unknown. Here, we have investigated the quantitative dynamic parameters that underlie actin filament growth and disappearance in the apical regions of pollen tubes and identified villin as the major player that drives rapid turnover of actin filaments in this region. Downregulation of Arabidopsis thaliana VILLIN2 (VLN2) and VLN5 led to accumulation of actin filaments at the pollen tube apex. Careful analysis of single filament dynamics showed that the severing frequency significantly decreased, and the lifetime significantly increased in vln2 vln5 pollen tubes. These results indicate that villin-mediated severing is critical for turnover and departure of actin filaments originating in the apical region. Consequently, the construction of actin collars was affected in vln2 vln5 pollen tubes. In addition to the decrease in severing frequency, actin filaments also became wavy and buckled in the apical cytoplasm of vln2 vln5 pollen tubes. These results suggest that villin confers rigidity upon actin filaments. Furthermore, an observed decrease in skewness of actin filaments in the subapical region of vln2 vln5 pollen tubes suggests that villin-mediated bundling activity may also play a role in the construction of actin collars. Thus, our data suggest that villins promote actin turnover at pollen tube tips and facilitate the construction of actin collars.</abstract><cop>United States</cop><pub>American Society of Plant Biologists</pub><pmid>23715472</pmid><doi>10.1105/tpc.113.110940</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0001-9517-2515</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | The Plant cell, 2013-05, Vol.25 (5), p.1803-1817 |
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| source | Jstor Complete Legacy; Oxford University Press Journals All Titles (1996-Current); MEDLINE; EZB-FREE-00999 freely available EZB journals |
| subjects | actin Actin Cytoskeleton - genetics Actin Cytoskeleton - metabolism Actins Actins - genetics Actins - metabolism Arabidopsis Arabidopsis - genetics Arabidopsis - growth & development Arabidopsis - metabolism Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Bundling Calcium Cell growth collars Gene Expression Regulation, Plant Luminescent Proteins - genetics Luminescent Proteins - metabolism Microfilament Proteins - genetics Microfilament Proteins - metabolism Microfilaments Microscopy, Confocal Microscopy, Fluorescence Models, Biological Mutation Plant cells Plant growth regulators Plants Plants, Genetically Modified Pollen Pollen Tube - genetics Pollen Tube - growth & development Pollen Tube - metabolism Pollen tubes rab GTP-Binding Proteins - genetics rab GTP-Binding Proteins - metabolism Reverse Transcriptase Polymerase Chain Reaction Transport Vesicles - metabolism |
| title | Arabidopsis Villins Promote Actin Turnover at Pollen Tube Tips and Facilitate the Construction of Actin Collars |
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