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Orchestration of microtubules and the actin cytoskeleton in trichome cell shape determination by a plant-unique kinesin

Microtubules (MTs) and actin filaments (F-actin) function cooperatively to regulate plant cell morphogenesis. However, the mechanisms underlying the crosstalk between these two cytoskeletal systems, particularly in cell shape control, remain largely unknown. In this study, we show that introduction...

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Autores principales: Tian, Juan, Han, Libo, Feng, Zhidi, Wang, Guangda, Liu, Weiwei, Ma, Yinping, Yu, Yanjun, Kong, Zhaosheng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4574192/
https://www.ncbi.nlm.nih.gov/pubmed/26287478
http://dx.doi.org/10.7554/eLife.09351
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author Tian, Juan
Han, Libo
Feng, Zhidi
Wang, Guangda
Liu, Weiwei
Ma, Yinping
Yu, Yanjun
Kong, Zhaosheng
author_facet Tian, Juan
Han, Libo
Feng, Zhidi
Wang, Guangda
Liu, Weiwei
Ma, Yinping
Yu, Yanjun
Kong, Zhaosheng
author_sort Tian, Juan
collection PubMed
description Microtubules (MTs) and actin filaments (F-actin) function cooperatively to regulate plant cell morphogenesis. However, the mechanisms underlying the crosstalk between these two cytoskeletal systems, particularly in cell shape control, remain largely unknown. In this study, we show that introduction of the MyTH4-FERM tandem into KCBP (kinesin-like calmodulin-binding protein) during evolution conferred novel functions. The MyTH4 domain and the FERM domain in the N-terminal tail of KCBP physically bind to MTs and F-actin, respectively. During trichome morphogenesis, KCBP distributes in a specific cortical gradient and concentrates at the branching sites and the apexes of elongating branches, which lack MTs but have cortical F-actin. Further, live-cell imaging and genetic analyses revealed that KCBP acts as a hub integrating MTs and actin filaments to assemble the required cytoskeletal configuration for the unique, polarized diffuse growth pattern during trichome cell morphogenesis. Our findings provide significant insights into the mechanisms underlying cytoskeletal regulation of cell shape determination. DOI: http://dx.doi.org/10.7554/eLife.09351.001
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spelling pubmed-45741922015-09-21 Orchestration of microtubules and the actin cytoskeleton in trichome cell shape determination by a plant-unique kinesin Tian, Juan Han, Libo Feng, Zhidi Wang, Guangda Liu, Weiwei Ma, Yinping Yu, Yanjun Kong, Zhaosheng eLife Cell Biology Microtubules (MTs) and actin filaments (F-actin) function cooperatively to regulate plant cell morphogenesis. However, the mechanisms underlying the crosstalk between these two cytoskeletal systems, particularly in cell shape control, remain largely unknown. In this study, we show that introduction of the MyTH4-FERM tandem into KCBP (kinesin-like calmodulin-binding protein) during evolution conferred novel functions. The MyTH4 domain and the FERM domain in the N-terminal tail of KCBP physically bind to MTs and F-actin, respectively. During trichome morphogenesis, KCBP distributes in a specific cortical gradient and concentrates at the branching sites and the apexes of elongating branches, which lack MTs but have cortical F-actin. Further, live-cell imaging and genetic analyses revealed that KCBP acts as a hub integrating MTs and actin filaments to assemble the required cytoskeletal configuration for the unique, polarized diffuse growth pattern during trichome cell morphogenesis. Our findings provide significant insights into the mechanisms underlying cytoskeletal regulation of cell shape determination. DOI: http://dx.doi.org/10.7554/eLife.09351.001 eLife Sciences Publications, Ltd 2015-08-19 /pmc/articles/PMC4574192/ /pubmed/26287478 http://dx.doi.org/10.7554/eLife.09351 Text en © 2015, Tian et al http://creativecommons.org/licenses/by/4.0/ This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
Tian, Juan
Han, Libo
Feng, Zhidi
Wang, Guangda
Liu, Weiwei
Ma, Yinping
Yu, Yanjun
Kong, Zhaosheng
Orchestration of microtubules and the actin cytoskeleton in trichome cell shape determination by a plant-unique kinesin
title Orchestration of microtubules and the actin cytoskeleton in trichome cell shape determination by a plant-unique kinesin
title_full Orchestration of microtubules and the actin cytoskeleton in trichome cell shape determination by a plant-unique kinesin
title_fullStr Orchestration of microtubules and the actin cytoskeleton in trichome cell shape determination by a plant-unique kinesin
title_full_unstemmed Orchestration of microtubules and the actin cytoskeleton in trichome cell shape determination by a plant-unique kinesin
title_short Orchestration of microtubules and the actin cytoskeleton in trichome cell shape determination by a plant-unique kinesin
title_sort orchestration of microtubules and the actin cytoskeleton in trichome cell shape determination by a plant-unique kinesin
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4574192/
https://www.ncbi.nlm.nih.gov/pubmed/26287478
http://dx.doi.org/10.7554/eLife.09351
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