cortical cytoskeletal network and cell-wall dynamics in the unicellular charophycean green alga Penium margaritaceum
Background and AimsPenium margaritaceum is a unicellular charophycean green alga with a unique bi-directional polar expansion mechanism that occurs at the central isthmus zone prior to cell division. This entails the focused deposition of cell-wall polymers coordinated by the activities of component...
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description | Background and AimsPenium margaritaceum is a unicellular charophycean green alga with a unique bi-directional polar expansion mechanism that occurs at the central isthmus zone prior to cell division. This entails the focused deposition of cell-wall polymers coordinated by the activities of components of the endomembrane system and cytoskeletal networks. The goal of this study was to elucidate the structural organization of the cortical cytoskeletal network during the cell cycle and identify its specific functional roles during key cell-wall developmental events: pre-division expansion and cell division.MethodsMicrotubules and actin filaments were labelled during various cell cycle phases with an anti-tubulin antibody and rhodamine phalloidin, respectively. Chemically induced disruption of the cytoskeleton was used to elucidate specific functional roles of microtubules and actin during cell expansion and division. Correlation of cytoskeletal dynamics with cell-wall development included live cell labelling with wall polymer-specific antibodies and electron microscopy.Key ResultsThe cortical cytoplasm of Penium is highlighted by a band of microtubules found at the cell isthmus, i.e. the site of pre-division wall expansion. This band, along with an associated, transient band of actin filaments, probably acts to direct the deposition of new wall material and to mark the plane of the future cell division. Two additional bands of microtubules, which we identify as satellite bands, arise from the isthmus microtubular band at the onset of expansion and displace toward the poles during expansion, ultimately marking the isthmus of future daughter cells. Treatment with microtubule and actin perturbation agents reversibly stops cell division.ConclusionsThe cortical cytoplasm of Penium contains distinct bands of microtubules and actin filaments that persist through the cell cycle. One of these bands, termed the isthmus microtubule band, or IMB, marks the site of both pre-division wall expansion and the zone where a cross wall will form during cytokinesis. This suggests that prior to the evolution of land plants, a dynamic, cortical cytoskeletal array similar to a pre-prophase band had evolved in the charophytes. However, an interesting variation on the cortical band theme is present in Penium, where two satellite microtubule bands are produced at the onset of cell expansion, each of which is destined to become an IMB in the two daughter cells after cytokinesis. These un |
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This entails the focused deposition of cell-wall polymers coordinated by the activities of components of the endomembrane system and cytoskeletal networks. The goal of this study was to elucidate the structural organization of the cortical cytoskeletal network during the cell cycle and identify its specific functional roles during key cell-wall developmental events: pre-division expansion and cell division.MethodsMicrotubules and actin filaments were labelled during various cell cycle phases with an anti-tubulin antibody and rhodamine phalloidin, respectively. Chemically induced disruption of the cytoskeleton was used to elucidate specific functional roles of microtubules and actin during cell expansion and division. Correlation of cytoskeletal dynamics with cell-wall development included live cell labelling with wall polymer-specific antibodies and electron microscopy.Key ResultsThe cortical cytoplasm of Penium is highlighted by a band of microtubules found at the cell isthmus, i.e. the site of pre-division wall expansion. This band, along with an associated, transient band of actin filaments, probably acts to direct the deposition of new wall material and to mark the plane of the future cell division. Two additional bands of microtubules, which we identify as satellite bands, arise from the isthmus microtubular band at the onset of expansion and displace toward the poles during expansion, ultimately marking the isthmus of future daughter cells. Treatment with microtubule and actin perturbation agents reversibly stops cell division.ConclusionsThe cortical cytoplasm of Penium contains distinct bands of microtubules and actin filaments that persist through the cell cycle. One of these bands, termed the isthmus microtubule band, or IMB, marks the site of both pre-division wall expansion and the zone where a cross wall will form during cytokinesis. This suggests that prior to the evolution of land plants, a dynamic, cortical cytoskeletal array similar to a pre-prophase band had evolved in the charophytes. However, an interesting variation on the cortical band theme is present in Penium, where two satellite microtubule bands are produced at the onset of cell expansion, each of which is destined to become an IMB in the two daughter cells after cytokinesis. These unique cytoskeletal components demonstrate the close temporal control and highly coordinated cytoskeletal dynamics of cellular development in Penium.</description><identifier>ISSN: 0305-7364</identifier><identifier>EISSN: 1095-8290</identifier><identifier>DOI: 10.1093/aob/mcu013</identifier><identifier>PMID: 24603606</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>actin ; Actin Cytoskeleton - metabolism ; Actin Cytoskeleton - ultrastructure ; Actins ; Actins - metabolism ; antibodies ; Cell cycle ; Cell Division ; Cell nucleus ; Cell Wall - metabolism ; Cell Wall - ultrastructure ; Cell walls ; Charophyta ; Cytokinesis ; Cytoskeleton ; Cytoskeleton - metabolism ; Cytoskeleton - ultrastructure ; Daughter cells ; Desmidiales - physiology ; Desmidiales - ultrastructure ; embryophytes ; endomembrane system ; evolution ; Microfilaments ; Microtubules ; Microtubules - metabolism ; Microtubules - ultrastructure ; Mitosis ; Penium ; Plant cells ; polymers</subject><ispartof>Annals of botany, 2014-10, Vol.114 (6), p.1237-1249</ispartof><rights>Annals of Botany Company 2014</rights><rights>The Author 2014. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: journals.permissions@oup.com.</rights><rights>The Author 2014. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: journals.permissions@oup.com 2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c424t-23f8086c3f633a39cb1a0f1e65a1c089c09d4d71109984609f4bd8f7be4f28253</citedby><cites>FETCH-LOGICAL-c424t-23f8086c3f633a39cb1a0f1e65a1c089c09d4d71109984609f4bd8f7be4f28253</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/43579687$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/43579687$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,803,885,27924,27925,53791,53793,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24603606$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ochs, Julie</creatorcontrib><creatorcontrib>LaRue, Therese</creatorcontrib><creatorcontrib>Tinaz, Berke</creatorcontrib><creatorcontrib>Yongue, Camille</creatorcontrib><creatorcontrib>Domozych, David S</creatorcontrib><title>cortical cytoskeletal network and cell-wall dynamics in the unicellular charophycean green alga Penium margaritaceum</title><title>Annals of botany</title><addtitle>Ann Bot</addtitle><description>Background and AimsPenium margaritaceum is a unicellular charophycean green alga with a unique bi-directional polar expansion mechanism that occurs at the central isthmus zone prior to cell division. This entails the focused deposition of cell-wall polymers coordinated by the activities of components of the endomembrane system and cytoskeletal networks. The goal of this study was to elucidate the structural organization of the cortical cytoskeletal network during the cell cycle and identify its specific functional roles during key cell-wall developmental events: pre-division expansion and cell division.MethodsMicrotubules and actin filaments were labelled during various cell cycle phases with an anti-tubulin antibody and rhodamine phalloidin, respectively. Chemically induced disruption of the cytoskeleton was used to elucidate specific functional roles of microtubules and actin during cell expansion and division. Correlation of cytoskeletal dynamics with cell-wall development included live cell labelling with wall polymer-specific antibodies and electron microscopy.Key ResultsThe cortical cytoplasm of Penium is highlighted by a band of microtubules found at the cell isthmus, i.e. the site of pre-division wall expansion. This band, along with an associated, transient band of actin filaments, probably acts to direct the deposition of new wall material and to mark the plane of the future cell division. Two additional bands of microtubules, which we identify as satellite bands, arise from the isthmus microtubular band at the onset of expansion and displace toward the poles during expansion, ultimately marking the isthmus of future daughter cells. Treatment with microtubule and actin perturbation agents reversibly stops cell division.ConclusionsThe cortical cytoplasm of Penium contains distinct bands of microtubules and actin filaments that persist through the cell cycle. One of these bands, termed the isthmus microtubule band, or IMB, marks the site of both pre-division wall expansion and the zone where a cross wall will form during cytokinesis. This suggests that prior to the evolution of land plants, a dynamic, cortical cytoskeletal array similar to a pre-prophase band had evolved in the charophytes. However, an interesting variation on the cortical band theme is present in Penium, where two satellite microtubule bands are produced at the onset of cell expansion, each of which is destined to become an IMB in the two daughter cells after cytokinesis. These unique cytoskeletal components demonstrate the close temporal control and highly coordinated cytoskeletal dynamics of cellular development in Penium.</description><subject>actin</subject><subject>Actin Cytoskeleton - metabolism</subject><subject>Actin Cytoskeleton - ultrastructure</subject><subject>Actins</subject><subject>Actins - metabolism</subject><subject>antibodies</subject><subject>Cell cycle</subject><subject>Cell Division</subject><subject>Cell nucleus</subject><subject>Cell Wall - metabolism</subject><subject>Cell Wall - ultrastructure</subject><subject>Cell walls</subject><subject>Charophyta</subject><subject>Cytokinesis</subject><subject>Cytoskeleton</subject><subject>Cytoskeleton - metabolism</subject><subject>Cytoskeleton - ultrastructure</subject><subject>Daughter cells</subject><subject>Desmidiales - physiology</subject><subject>Desmidiales - ultrastructure</subject><subject>embryophytes</subject><subject>endomembrane system</subject><subject>evolution</subject><subject>Microfilaments</subject><subject>Microtubules</subject><subject>Microtubules - metabolism</subject><subject>Microtubules - ultrastructure</subject><subject>Mitosis</subject><subject>Penium</subject><subject>Plant cells</subject><subject>polymers</subject><issn>0305-7364</issn><issn>1095-8290</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkd1rFDEUxQdR7Fp98V3Nowhj8zWZ5KUgxS8oKGifw51MZjdtJlmTjGX_e7NMXfQp3Jwf597DaZqXBL8nWLELiMPFbBZM2KNmU3-6VlKFHzcbzHDX9kzws-ZZzrcYYyoUedqcUS4wE1hsmmJiKs6AR-ZQYr6z3pY6BFvuY7pDEEZkrPftPXiPxkOA2ZmMXEBlZ9ES3FFcPCRkdpDifncwFgLaJmsDAr8F9N0Gt8xohrSF5AoYu8zPmycT-GxfPLznzc2njz-vvrTX3z5_vfpw3RpOeWkpmySWwrBJMAZMmYEAnogVHRCDpTJYjXzsSY2sZE2kJj6McuoHyycqacfOm8vVd78Msx2NDSWB1_vk6jkHHcHp_5Xgdnobf2tOVNdxWg3ePhik-GuxuejZ5WNkCDYuWRNBKJWy73FF362oSTHnZKfTGoL1sSZda9JrTRV-_e9hJ_RvLxV4tQK3ucR00jnreiVkX_U3qz5B1LBNLuubHxSTrnbc9ZIS9gcm-qTH</recordid><startdate>20141001</startdate><enddate>20141001</enddate><creator>Ochs, Julie</creator><creator>LaRue, Therese</creator><creator>Tinaz, Berke</creator><creator>Yongue, Camille</creator><creator>Domozych, David S</creator><general>Oxford University Press</general><scope>FBQ</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>7X8</scope><scope>5PM</scope></search><sort><creationdate>20141001</creationdate><title>cortical cytoskeletal network and cell-wall dynamics in the unicellular charophycean green alga Penium margaritaceum</title><author>Ochs, Julie ; LaRue, Therese ; Tinaz, Berke ; Yongue, Camille ; Domozych, David S</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c424t-23f8086c3f633a39cb1a0f1e65a1c089c09d4d71109984609f4bd8f7be4f28253</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>actin</topic><topic>Actin Cytoskeleton - metabolism</topic><topic>Actin Cytoskeleton - ultrastructure</topic><topic>Actins</topic><topic>Actins - metabolism</topic><topic>antibodies</topic><topic>Cell cycle</topic><topic>Cell Division</topic><topic>Cell nucleus</topic><topic>Cell Wall - metabolism</topic><topic>Cell Wall - ultrastructure</topic><topic>Cell walls</topic><topic>Charophyta</topic><topic>Cytokinesis</topic><topic>Cytoskeleton</topic><topic>Cytoskeleton - metabolism</topic><topic>Cytoskeleton - ultrastructure</topic><topic>Daughter cells</topic><topic>Desmidiales - physiology</topic><topic>Desmidiales - ultrastructure</topic><topic>embryophytes</topic><topic>endomembrane system</topic><topic>evolution</topic><topic>Microfilaments</topic><topic>Microtubules</topic><topic>Microtubules - metabolism</topic><topic>Microtubules - ultrastructure</topic><topic>Mitosis</topic><topic>Penium</topic><topic>Plant cells</topic><topic>polymers</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ochs, Julie</creatorcontrib><creatorcontrib>LaRue, Therese</creatorcontrib><creatorcontrib>Tinaz, Berke</creatorcontrib><creatorcontrib>Yongue, Camille</creatorcontrib><creatorcontrib>Domozych, David S</creatorcontrib><collection>AGRIS</collection><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>Annals of botany</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ochs, Julie</au><au>LaRue, Therese</au><au>Tinaz, Berke</au><au>Yongue, Camille</au><au>Domozych, David S</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>cortical cytoskeletal network and cell-wall dynamics in the unicellular charophycean green alga Penium margaritaceum</atitle><jtitle>Annals of botany</jtitle><addtitle>Ann Bot</addtitle><date>2014-10-01</date><risdate>2014</risdate><volume>114</volume><issue>6</issue><spage>1237</spage><epage>1249</epage><pages>1237-1249</pages><issn>0305-7364</issn><eissn>1095-8290</eissn><abstract>Background and AimsPenium margaritaceum is a unicellular charophycean green alga with a unique bi-directional polar expansion mechanism that occurs at the central isthmus zone prior to cell division. This entails the focused deposition of cell-wall polymers coordinated by the activities of components of the endomembrane system and cytoskeletal networks. The goal of this study was to elucidate the structural organization of the cortical cytoskeletal network during the cell cycle and identify its specific functional roles during key cell-wall developmental events: pre-division expansion and cell division.MethodsMicrotubules and actin filaments were labelled during various cell cycle phases with an anti-tubulin antibody and rhodamine phalloidin, respectively. Chemically induced disruption of the cytoskeleton was used to elucidate specific functional roles of microtubules and actin during cell expansion and division. Correlation of cytoskeletal dynamics with cell-wall development included live cell labelling with wall polymer-specific antibodies and electron microscopy.Key ResultsThe cortical cytoplasm of Penium is highlighted by a band of microtubules found at the cell isthmus, i.e. the site of pre-division wall expansion. This band, along with an associated, transient band of actin filaments, probably acts to direct the deposition of new wall material and to mark the plane of the future cell division. Two additional bands of microtubules, which we identify as satellite bands, arise from the isthmus microtubular band at the onset of expansion and displace toward the poles during expansion, ultimately marking the isthmus of future daughter cells. Treatment with microtubule and actin perturbation agents reversibly stops cell division.ConclusionsThe cortical cytoplasm of Penium contains distinct bands of microtubules and actin filaments that persist through the cell cycle. One of these bands, termed the isthmus microtubule band, or IMB, marks the site of both pre-division wall expansion and the zone where a cross wall will form during cytokinesis. This suggests that prior to the evolution of land plants, a dynamic, cortical cytoskeletal array similar to a pre-prophase band had evolved in the charophytes. However, an interesting variation on the cortical band theme is present in Penium, where two satellite microtubule bands are produced at the onset of cell expansion, each of which is destined to become an IMB in the two daughter cells after cytokinesis. These unique cytoskeletal components demonstrate the close temporal control and highly coordinated cytoskeletal dynamics of cellular development in Penium.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>24603606</pmid><doi>10.1093/aob/mcu013</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record> |
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subjects | actin Actin Cytoskeleton - metabolism Actin Cytoskeleton - ultrastructure Actins Actins - metabolism antibodies Cell cycle Cell Division Cell nucleus Cell Wall - metabolism Cell Wall - ultrastructure Cell walls Charophyta Cytokinesis Cytoskeleton Cytoskeleton - metabolism Cytoskeleton - ultrastructure Daughter cells Desmidiales - physiology Desmidiales - ultrastructure embryophytes endomembrane system evolution Microfilaments Microtubules Microtubules - metabolism Microtubules - ultrastructure Mitosis Penium Plant cells polymers |
title | cortical cytoskeletal network and cell-wall dynamics in the unicellular charophycean green alga Penium margaritaceum |
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