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Title: Tubulin perturbation leads to unexpected cell wall modifications and affects stomatal behaviour in Populus

Abstract

Cortical microtubules are integral to plant morphogenesis, cell wall synthesis, and stomatal behaviour, presumably by governing cellulose microfibril orientation. Genetic manipulation of tubulins often leads to abnormal plant development, making it difficult to probe additional roles of cortical microtubules in cell wall biogenesis. Here, it is shown that expressing post-translational C-terminal modification mimics of α-tubulin altered cell wall characteristics and guard cell dynamics in transgenic Populus tremula x alba that otherwise appear normal. 35S promoter-driven transgene expression was high in leaves but unusually low in xylem, suggesting high levels of tubulin transgene expression were not tolerated in wood-forming tissues during regeneration of transformants. Cellulose, hemicellulose, and lignin contents were unaffected in transgenic wood, but expression of cell wall-modifying enzymes, and extractability of lignin-bound pectin and xylan polysaccharides were increased in developing xylem. The results suggest that pectin and xylan polysaccharides deposited early during cell wall biogenesis are more sensitive to subtle tubulin perturbation than cellulose and matrix polysaccharides deposited later. Tubulin perturbation also affected guard cell behaviour, delaying drought-induced stomatal closure as well as light-induced stomatal opening in leaves. Pectins have been shown to confer cell wall flexibility critical for reversible stomatal movement, and results presented here are consistent withmore » microtubule involvement in this process. In conclusion, taken together, the data show the value of growth-compatible tubulin perturbations for discerning microtubule functions, and add to the growing body of evidence for microtubule involvement in non-cellulosic polysaccharide assembly during cell wall biogenesis.« less

Authors:
 [1];  [2];  [2];  [3];  [4];  [2];  [5];  [2];  [2];  [6];  [2];  [3];  [2];  [2]
+ Show Author Affiliations
  1. Univ. of Georgia, Athens, GA (United States); Washington State Univ., Prosser, WA (United States)
  2. Univ. of Georgia, Athens, GA (United States)
  3. Univ. of British Columbia, Vancouver, BC (Canada)
  4. Albert Einstein College of Medicine, Bronx, NY (United States)
  5. Taiwan Forestry Research Institute, Taipei (Taiwan)
  6. Univ. of Florida, Gainesville, FL (United States)
Publication Date:
Research Org.:
Univ. of Georgia, Athens, GA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1343289
Grant/Contract Number:  
SC0008470
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Experimental Botany
Additional Journal Information:
Journal Volume: 66; Journal Issue: 20; Journal ID: ISSN 0022-0957
Publisher:
Oxford University Press
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; cell wall; detyrosination; guard cell; microtubule; polysaccharide; tubulin post translational modification

Citation Formats

Swamy, Prashant S., Hu, Hao, Pattathil, Sivakumar, Maloney, Victoria J., Xiao, Hui, Xue, Liang -Jiao, Chung, Jeng -Der, Johnson, Virgil E., Zhu, Yingying, Peter, Gary F., Hahn, Michael G., Mansfield, Shawn D., Harding, Scott A., and Tsai, Chung -Jui. Tubulin perturbation leads to unexpected cell wall modifications and affects stomatal behaviour in Populus. United States: N. p., 2015. Web. doi:10.1093/jxb/erv383.
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Swamy, Prashant S., Hu, Hao, Pattathil, Sivakumar, Maloney, Victoria J., Xiao, Hui, Xue, Liang -Jiao, Chung, Jeng -Der, Johnson, Virgil E., Zhu, Yingying, Peter, Gary F., Hahn, Michael G., Mansfield, Shawn D., Harding, Scott A., & Tsai, Chung -Jui. Tubulin perturbation leads to unexpected cell wall modifications and affects stomatal behaviour in Populus. United States. https://doi.org/10.1093/jxb/erv383
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Swamy, Prashant S., Hu, Hao, Pattathil, Sivakumar, Maloney, Victoria J., Xiao, Hui, Xue, Liang -Jiao, Chung, Jeng -Der, Johnson, Virgil E., Zhu, Yingying, Peter, Gary F., Hahn, Michael G., Mansfield, Shawn D., Harding, Scott A., and Tsai, Chung -Jui. Wed . "Tubulin perturbation leads to unexpected cell wall modifications and affects stomatal behaviour in Populus". United States. https://doi.org/10.1093/jxb/erv383. https://www.osti.gov/servlets/purl/1343289.
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@article{osti_1343289,
title = {Tubulin perturbation leads to unexpected cell wall modifications and affects stomatal behaviour in Populus},
author = {Swamy, Prashant S. and Hu, Hao and Pattathil, Sivakumar and Maloney, Victoria J. and Xiao, Hui and Xue, Liang -Jiao and Chung, Jeng -Der and Johnson, Virgil E. and Zhu, Yingying and Peter, Gary F. and Hahn, Michael G. and Mansfield, Shawn D. and Harding, Scott A. and Tsai, Chung -Jui},
abstractNote = {Cortical microtubules are integral to plant morphogenesis, cell wall synthesis, and stomatal behaviour, presumably by governing cellulose microfibril orientation. Genetic manipulation of tubulins often leads to abnormal plant development, making it difficult to probe additional roles of cortical microtubules in cell wall biogenesis. Here, it is shown that expressing post-translational C-terminal modification mimics of α-tubulin altered cell wall characteristics and guard cell dynamics in transgenic Populus tremula x alba that otherwise appear normal. 35S promoter-driven transgene expression was high in leaves but unusually low in xylem, suggesting high levels of tubulin transgene expression were not tolerated in wood-forming tissues during regeneration of transformants. Cellulose, hemicellulose, and lignin contents were unaffected in transgenic wood, but expression of cell wall-modifying enzymes, and extractability of lignin-bound pectin and xylan polysaccharides were increased in developing xylem. The results suggest that pectin and xylan polysaccharides deposited early during cell wall biogenesis are more sensitive to subtle tubulin perturbation than cellulose and matrix polysaccharides deposited later. Tubulin perturbation also affected guard cell behaviour, delaying drought-induced stomatal closure as well as light-induced stomatal opening in leaves. Pectins have been shown to confer cell wall flexibility critical for reversible stomatal movement, and results presented here are consistent with microtubule involvement in this process. In conclusion, taken together, the data show the value of growth-compatible tubulin perturbations for discerning microtubule functions, and add to the growing body of evidence for microtubule involvement in non-cellulosic polysaccharide assembly during cell wall biogenesis.},
doi = {10.1093/jxb/erv383},
journal = {Journal of Experimental Botany},
number = 20,
volume = 66,
place = {United States},
year = {Wed Aug 05 00:00:00 EDT 2015},
month = {Wed Aug 05 00:00:00 EDT 2015}
}
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Microtubule Defects and Cell Morphogenesis in the lefty1lefty2 Tubulin Mutant of Arabidopsis thaliana
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Microtubules Are Essential for Guard-Cell Function in Vicia and Arabidopsis
journal, May 2012

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Stress-responsive hydroxycinnamate glycosyltransferase modulates phenylpropanoid metabolism in Populus
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  • Journal of Experimental Botany, Vol. 65, Issue 15
  • DOI: 10.1093/jxb/eru192

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Aspen pectate lyase PtxtPL1-27 mobilizes matrix polysaccharides from woody tissues and improves saccharification yield
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  • Biotechnology for Biofuels, Vol. 7, Issue 1
  • DOI: 10.1186/1754-6834-7-11

Microtubule organization in the green kingdom: chaos or self-order?
journal, April 2002

Guard cell wall: immunocytochemical detection of polysaccharide components
journal, May 2002

Microtubule organization in the green kingdom: chaos or self-order?
journal, April 2002

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    Works referencing / citing this record:

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    • DOI: 10.1093/treephys/tpy026

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    journal, June 2019

    • An, Yuyan; Xiong, Lijun; Hu, Shu
    • Physiologia Plantarum, Vol. 168, Issue 3
    • DOI: 10.1111/ppl.13016
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