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Title: Cellulose synthase complexes display distinct dynamic behaviors during xylem transdifferentiation

Abstract

In plants, plasma membrane-embedded CELLULOSE SYNTHASE (CESA) enzyme complexes deposit cellulose polymers into the developing cell wall. Cellulose synthesis requires two different sets of CESA complexes that are active during cell expansion and secondary cell wall thickening, respectively. Hence, developing xylem cells, which first undergo cell expansion and subsequently deposit thick secondary walls, need to completely reorganize their CESA complexes from primary wall- to secondary wall-specific CESAs. Using live-cell imaging, we analyzed the principles underlying this remodeling. At the onset of secondary wall synthesis, the primary wall CESAs ceased to be delivered to the plasma membrane and were gradually removed from both the plasma membrane and the Golgi. For a brief transition period, both primary wall- and secondary wall-specific CESAs coexisted in banded domains of the plasma membrane where secondary wall synthesis is concentrated. During this transition, primary and secondary wall CESAs displayed discrete dynamic behaviors and sensitivities to the inhibitor isoxaben. As secondary wall-specific CESAs were delivered and inserted into the plasma membrane, the primary wall CESAs became concentrated in prevacuolar compartments and lytic vacuoles. This adjustment in localization between the two CESAs was accompanied by concurrent decreased primary wall CESA and increased secondary wall CESA protein abundance. Ourmore » data reveal distinct and dynamic subcellular trafficking patterns that underpin the remodeling of the cellulose biosynthetic machinery, resulting in the removal and degradation of the primary wall CESA complex with concurrent production and recycling of the secondary wall CESAs.« less

Authors:
 [1];  [2];  [3]; ORCiD logo [3]; ORCiD logo [4];  [5];  [6];  [3]
  1. Univ. of British Columbia, Vancouver, BC (Canada). Dept. of Botany; Univ. of British Columbia, Vancouver, BC (Canada). Dept. of Wood Science
  2. Univ. of Melbourne (Australia). School of Biosciences; Max Planck Inst. for Molecular Plant Physiology, Potsdam (Germany)
  3. Univ. of British Columbia, Vancouver, BC (Canada). Dept. of Wood Science
  4. Pennsylvania State Univ., University Park, PA (United States). Dept. of Biochemistry and Molecular Biology; Michigan State Univ., East Lansing, MI (United States). Dept. of Horticulture
  5. Univ. of British Columbia, Vancouver, BC (Canada). Dept. of Botany
  6. Univ. of Melbourne (Australia). School of Biosciences
Publication Date:
Research Org.:
Energy Frontier Research Centers (EFRC), Washington D.C (United States). Center for Lignocellulose Structure and Formation (CLSF)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1440385
Alternate Identifier(s):
OSTI ID: 1470632
Grant/Contract Number:  
SC0001090; RGPIN-2013-229548
Resource Type:
Journal Article: Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 115; Journal Issue: 27; Related Information: CLSF partners with Pennsylvania State University (lead); North Carolina State University; University of Rhode Island; Virginia Tech University; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
biofuels (including algae and biomass); bio-inspired; membrane; carbon sequestration; materials and chemistry by design; synthesis (self-assembly); cellulose; primary cell wall; secondary cell wall; cellulose biosynthesis; xylem transdifferentiation

Citation Formats

Watanabe, Yoichiro, Schneider, Rene, Barkwill, Sarah, Gonzales-Vigil, Eliana, Hill, Joseph L., Samuels, A. Lacey, Persson, Staffan, and Mansfield, Shawn D. Cellulose synthase complexes display distinct dynamic behaviors during xylem transdifferentiation. United States: N. p., 2018. Web. doi:10.1073/pnas.1802113115.
Watanabe, Yoichiro, Schneider, Rene, Barkwill, Sarah, Gonzales-Vigil, Eliana, Hill, Joseph L., Samuels, A. Lacey, Persson, Staffan, & Mansfield, Shawn D. Cellulose synthase complexes display distinct dynamic behaviors during xylem transdifferentiation. United States. doi:10.1073/pnas.1802113115.
Watanabe, Yoichiro, Schneider, Rene, Barkwill, Sarah, Gonzales-Vigil, Eliana, Hill, Joseph L., Samuels, A. Lacey, Persson, Staffan, and Mansfield, Shawn D. Tue . "Cellulose synthase complexes display distinct dynamic behaviors during xylem transdifferentiation". United States. doi:10.1073/pnas.1802113115.
@article{osti_1440385,
title = {Cellulose synthase complexes display distinct dynamic behaviors during xylem transdifferentiation},
author = {Watanabe, Yoichiro and Schneider, Rene and Barkwill, Sarah and Gonzales-Vigil, Eliana and Hill, Joseph L. and Samuels, A. Lacey and Persson, Staffan and Mansfield, Shawn D.},
abstractNote = {In plants, plasma membrane-embedded CELLULOSE SYNTHASE (CESA) enzyme complexes deposit cellulose polymers into the developing cell wall. Cellulose synthesis requires two different sets of CESA complexes that are active during cell expansion and secondary cell wall thickening, respectively. Hence, developing xylem cells, which first undergo cell expansion and subsequently deposit thick secondary walls, need to completely reorganize their CESA complexes from primary wall- to secondary wall-specific CESAs. Using live-cell imaging, we analyzed the principles underlying this remodeling. At the onset of secondary wall synthesis, the primary wall CESAs ceased to be delivered to the plasma membrane and were gradually removed from both the plasma membrane and the Golgi. For a brief transition period, both primary wall- and secondary wall-specific CESAs coexisted in banded domains of the plasma membrane where secondary wall synthesis is concentrated. During this transition, primary and secondary wall CESAs displayed discrete dynamic behaviors and sensitivities to the inhibitor isoxaben. As secondary wall-specific CESAs were delivered and inserted into the plasma membrane, the primary wall CESAs became concentrated in prevacuolar compartments and lytic vacuoles. This adjustment in localization between the two CESAs was accompanied by concurrent decreased primary wall CESA and increased secondary wall CESA protein abundance. Our data reveal distinct and dynamic subcellular trafficking patterns that underpin the remodeling of the cellulose biosynthetic machinery, resulting in the removal and degradation of the primary wall CESA complex with concurrent production and recycling of the secondary wall CESAs.},
doi = {10.1073/pnas.1802113115},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
issn = {0027-8424},
number = 27,
volume = 115,
place = {United States},
year = {2018},
month = {6}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at 10.1073/pnas.1802113115

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Cited by: 23 works
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