Microtubule initiation from the nuclear surface controls cortical microtubule growth polarity and orientation in Arabidopsis thaliana

The nuclear envelope in plant cells has long been known to be a microtubule organizing center (MTOC), but its influence on microtubule organization in the cell cortex has been unclear. Here we show that nuclear MTOC activity favors the formation of longitudinal cortical microtubule (CMT) arrays. We...

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Published in:Plant and cell physiology Vol. 55; no. 9; pp. 1636 - 1645
Main Authors: Ambrose, Chris, Wasteneys, Geoffrey O
Format: Journal Article
Language:English
Published: Japan Oxford University Press 01-09-2014
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Abstract The nuclear envelope in plant cells has long been known to be a microtubule organizing center (MTOC), but its influence on microtubule organization in the cell cortex has been unclear. Here we show that nuclear MTOC activity favors the formation of longitudinal cortical microtubule (CMT) arrays. We used green fluorescent protein (GFP)-tagged gamma tubulin-complex protein 2 (GCP2) to identify nuclear MTOC activity and GFP-tagged End-Binding Protein 1b (EB1b) to track microtubule growth directions. We found that microtubules initiate from nuclei and enter the cortex in two directions along the long axis of the cell, creating bipolar longitudinal CMT arrays. Such arrays were observed in all cell types showing nuclear MTOC activity, including root hairs, recently divided cells in root tips, and the leaf epidermis. In order to confirm the causal nature of nuclei in bipolar array formation, we displaced nuclei by centrifugation, which generated a corresponding shift in the bipolarity split point. We also found that bipolar CMT arrays were associated with bidirectional trafficking of vesicular components to cell ends. Together, these findings reveal a conserved function of plant nuclear MTOCs and centrosomes/spindle pole bodies in animals and fungi, wherein all structures serve to establish polarities in microtubule growth.
AbstractList The nuclear envelope in plant cells has long been known to be a microtubule organizing center (MTOC), but its influence on microtubule organization in the cell cortex has been unclear. Here we show that nuclear MTOC activity favors the formation of longitudinal cortical microtubule (CMT) arrays. We used green fluorescent protein (GFP)-tagged gamma tubulin-complex protein 2 (GCP2) to identify nuclear MTOC activity and GFP-tagged End-Binding Protein 1b (EB1b) to track microtubule growth directions. We found that microtubules initiate from nuclei and enter the cortex in two directions along the long axis of the cell, creating bipolar longitudinal CMT arrays. Such arrays were observed in all cell types showing nuclear MTOC activity, including root hairs, recently divided cells in root tips, and the leaf epidermis. In order to confirm the causal nature of nuclei in bipolar array formation, we displaced nuclei by centrifugation, which generated a corresponding shift in the bipolarity split point. We also found that bipolar CMT arrays were associated with bidirectional trafficking of vesicular components to cell ends. Together, these findings reveal a conserved function of plant nuclear MTOCs and centrosomes/spindle pole bodies in animals and fungi, wherein all structures serve to establish polarities in microtubule growth.
Author Ambrose, Chris
Wasteneys, Geoffrey O
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  surname: Ambrose
  fullname: Ambrose, Chris
  organization: Department of Botany, The University of British Columbia, Vancouver V6T 1Z4, Canada
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  givenname: Geoffrey O
  surname: Wasteneys
  fullname: Wasteneys, Geoffrey O
  email: geoffrey.wasteneys@ubc.ca
  organization: Department of Botany, The University of British Columbia, Vancouver V6T 1Z4, Canada geoffrey.wasteneys@ubc.ca
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Copyright The Author 2014. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: journals.permissions@oup.com.
The Author 2014. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: journals.permissions@oup.com 2014
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Issue 9
Keywords Cytoskeleton
Polarity
Microtubule
Root
Arabidopsis
Root hair
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Snippet The nuclear envelope in plant cells has long been known to be a microtubule organizing center (MTOC), but its influence on microtubule organization in the cell...
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SubjectTerms Arabidopsis - metabolism
Arabidopsis - ultrastructure
Arabidopsis Proteins - metabolism
Cell Nucleus - metabolism
Cell Nucleus - ultrastructure
Cell Polarity
Centrosome - metabolism
Centrosome - ultrastructure
Cytoplasm - metabolism
Cytoplasm - ultrastructure
Genes, Reporter
Microtubule-Associated Proteins - metabolism
Microtubule-Organizing Center - metabolism
Microtubule-Organizing Center - ultrastructure
Microtubules - metabolism
Microtubules - ultrastructure
Plant Epidermis - metabolism
Plant Epidermis - ultrastructure
Plant Leaves - metabolism
Plant Leaves - ultrastructure
Plant Roots - metabolism
Plant Roots - ultrastructure
Recombinant Fusion Proteins
Regular Papers
Spindle Pole Bodies - metabolism
Spindle Pole Bodies - ultrastructure
Tubulin - metabolism
Title Microtubule initiation from the nuclear surface controls cortical microtubule growth polarity and orientation in Arabidopsis thaliana
URI https://www.ncbi.nlm.nih.gov/pubmed/25008974
https://search.proquest.com/docview/1561971559
https://pubmed.ncbi.nlm.nih.gov/PMC4160572
Volume 55
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