skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: The TWD40-2 protein and the AP2 complex cooperate in the clathrin-mediated endocytosis of cellulose synthase to regulate cellulose biosynthesis

Abstract

Here, cellulose biosynthesis is performed exclusively by plasma membrane-localized cellulose synthases (CESAs). Therefore, the trafficking of CESAs to and from the plasma membrane is an important mechanism for regulating cellulose biosynthesis. CESAs were recently identified as cargo proteins of the classic adaptor protein 2 (AP2) complex of the clathrin-mediated endocytosis (CME) pathway. The AP2 complex of the CME pathway is conserved in yeast, animals, and plants, and has been well-characterized in many systems. In contrast, the recently discovered TPLATE complex (TPC), which is proposed to function as a CME adaptor complex, is only conserved in plants and a few other eukaryotes. In this study, we discovered that the TWD40-2 protein, a putative member of the TPC, is also important for the endocytosis of CESAs. Genetic analysis between TWD40-2 and AP2M of the AP2 complex revealed that the roles of TWD40-2 in CME are both distinct from and cooperative with the AP2 complex. Loss of efficient CME in twd40-2-3 resulted in the unregulated overaccumulation of CESAs at the plasma membrane. In seedlings of twd40-2-3 and other CME-deficient mutants, a direct correlation was revealed between endocytic deficiency and cellulose content deficiency, highlighting the importance of controlled CESA endocytosis in regulating cellulose biosynthesis.

Authors:
 [1];  [1];  [1];  [1]
  1. Pennsylvania State Univ., University Park, PA (United States)
Publication Date:
Research Org.:
Pennsylvania State Univ., University Park, PA (United States); Energy Frontier Research Centers (EFRC) (United States). Center for Lignocellulose Structure and Formation (CLSF)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1235133
Alternate Identifier(s):
OSTI ID: 1347980
Grant/Contract Number:  
SC0001090
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 112; Journal Issue: 41; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; cellulose synthase; endocytosis; clathrin; plasma membrane; trafficking

Citation Formats

Bashline, Logan, Li, Shundai, Zhu, Xiaoyu, and Gu, Ying. The TWD40-2 protein and the AP2 complex cooperate in the clathrin-mediated endocytosis of cellulose synthase to regulate cellulose biosynthesis. United States: N. p., 2015. Web. doi:10.1073/pnas.1509292112.
Bashline, Logan, Li, Shundai, Zhu, Xiaoyu, & Gu, Ying. The TWD40-2 protein and the AP2 complex cooperate in the clathrin-mediated endocytosis of cellulose synthase to regulate cellulose biosynthesis. United States. doi:10.1073/pnas.1509292112.
Bashline, Logan, Li, Shundai, Zhu, Xiaoyu, and Gu, Ying. Mon . "The TWD40-2 protein and the AP2 complex cooperate in the clathrin-mediated endocytosis of cellulose synthase to regulate cellulose biosynthesis". United States. doi:10.1073/pnas.1509292112.
@article{osti_1235133,
title = {The TWD40-2 protein and the AP2 complex cooperate in the clathrin-mediated endocytosis of cellulose synthase to regulate cellulose biosynthesis},
author = {Bashline, Logan and Li, Shundai and Zhu, Xiaoyu and Gu, Ying},
abstractNote = {Here, cellulose biosynthesis is performed exclusively by plasma membrane-localized cellulose synthases (CESAs). Therefore, the trafficking of CESAs to and from the plasma membrane is an important mechanism for regulating cellulose biosynthesis. CESAs were recently identified as cargo proteins of the classic adaptor protein 2 (AP2) complex of the clathrin-mediated endocytosis (CME) pathway. The AP2 complex of the CME pathway is conserved in yeast, animals, and plants, and has been well-characterized in many systems. In contrast, the recently discovered TPLATE complex (TPC), which is proposed to function as a CME adaptor complex, is only conserved in plants and a few other eukaryotes. In this study, we discovered that the TWD40-2 protein, a putative member of the TPC, is also important for the endocytosis of CESAs. Genetic analysis between TWD40-2 and AP2M of the AP2 complex revealed that the roles of TWD40-2 in CME are both distinct from and cooperative with the AP2 complex. Loss of efficient CME in twd40-2-3 resulted in the unregulated overaccumulation of CESAs at the plasma membrane. In seedlings of twd40-2-3 and other CME-deficient mutants, a direct correlation was revealed between endocytic deficiency and cellulose content deficiency, highlighting the importance of controlled CESA endocytosis in regulating cellulose biosynthesis.},
doi = {10.1073/pnas.1509292112},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 41,
volume = 112,
place = {United States},
year = {2015},
month = {9}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1073/pnas.1509292112

Citation Metrics:
Cited by: 10 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Advances in Analysis of Low Signal-to-Noise Images Link Dynamin and AP2 to the Functions of an Endocytic Checkpoint
journal, August 2013


Roles of AP-2 in Clathrin-Mediated Endocytosis
journal, May 2010


Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments
journal, June 2009

  • Gutierrez, Ryan; Lindeboom, Jelmer J.; Paredez, Alex R.
  • Nature Cell Biology, Vol. 11, Issue 7
  • DOI: 10.1038/ncb1886

Molecular mechanism and physiological functions of clathrin-mediated endocytosis
journal, July 2011

  • McMahon, Harvey T.; Boucrot, Emmanuel
  • Nature Reviews Molecular Cell Biology, Vol. 12, Issue 8
  • DOI: 10.1038/nrm3151

Adaptor Protein Complex 2–Mediated Endocytosis Is Crucial for Male Reproductive Organ Development in Arabidopsis
journal, August 2013


Growth of the plant cell wall
journal, November 2005

  • Cosgrove, Daniel J.
  • Nature Reviews Molecular Cell Biology, Vol. 6, Issue 11, p. 850-861
  • DOI: 10.1038/nrm1746

Identification and Dynamics of Arabidopsis Adaptor Protein-2 Complex and Its Involvement in Floral Organ Development
journal, August 2013

  • Yamaoka, Shohei; Shimono, Yuki; Shirakawa, Makoto
  • The Plant Cell, Vol. 25, Issue 8
  • DOI: 10.1105/tpc.113.114082

Cellulose synthase interactive protein 1 (CSI1) links microtubules and cellulose synthase complexes
journal, December 2011

  • Li, S.; Lei, L.; Somerville, C. R.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 1
  • DOI: 10.1073/pnas.1118560109

Characterization of TSET, an ancient and widespread membrane trafficking complex
journal, May 2014

  • Hirst, Jennifer; Schlacht, Alexander; Norcott, John P.
  • eLife, Vol. 3
  • DOI: 10.7554/eLife.02866

Pausing of Golgi Bodies on Microtubules Regulates Secretion of Cellulose Synthase Complexes in Arabidopsis
journal, April 2009

  • Crowell, E. F.; Bischoff, V.; Desprez, T.
  • The Plant Cell, Vol. 21, Issue 4, p. 1141-1154
  • DOI: 10.1105/tpc.108.065334

The trafficking of the cellulose synthase complex in higher plants
journal, March 2014

  • Bashline, Logan; Li, Shundai; Gu, Ying
  • Annals of Botany, Vol. 114, Issue 6
  • DOI: 10.1093/aob/mcu040

The Endocytosis of Cellulose Synthase in Arabidopsis Is Dependent on μ2, a Clathrin-Mediated Endocytosis Adaptin
journal, July 2013

  • Bashline, Logan; Li, Shundai; Anderson, Charles T.
  • Plant Physiology, Vol. 163, Issue 1
  • DOI: 10.1104/pp.113.221234

GATEWAY™ vectors for Agrobacterium-mediated plant transformation
journal, May 2002


Cellulose Synthesis and Its Regulation
journal, January 2014

  • Li, Shundai; Bashline, Logan; Lei, Lei
  • The Arabidopsis Book, Vol. 12
  • DOI: 10.1199/tab.0169

FM-dyes as experimental probes for dissecting vesicle trafficking in living plant cells
journal, May 2004


Dynamic behavior of clathrin in Arabidopsis thaliana unveiled by live imaging
journal, October 2011


The First Five Seconds in the Life of a Clathrin-Coated Pit
journal, August 2012


Cargo and Dynamin Regulate Clathrin-Coated Pit Maturation
journal, March 2009


Cellulose Synthesis in Higher Plants
journal, November 2006


The TPLATE Adaptor Complex Drives Clathrin-Mediated Endocytosis in Plants
journal, February 2014


The Clathrin Adaptor Complex AP-2 Mediates Endocytosis of BRASSINOSTEROID INSENSITIVE1 in Arabidopsis
journal, August 2013

  • Di Rubbo, Simone; Irani, Niloufer G.; Kim, Soo Youn
  • The Plant Cell, Vol. 25, Issue 8
  • DOI: 10.1105/tpc.113.114058

Semimicro determination of cellulose inbiological materials
journal, December 1969


Dynamics of Arabidopsis Dynamin-Related Protein 1C and a Clathrin Light Chain at the Plasma Membrane
journal, May 2008

  • Konopka, Catherine A.; Backues, Steven K.; Bednarek, Sebastian Y.
  • The Plant Cell, Vol. 20, Issue 5
  • DOI: 10.1105/tpc.108.059428

Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
journal, December 2001


Identification of a cellulose synthase-associated protein required for cellulose biosynthesis
journal, July 2010

  • Gu, Y.; Kaplinsky, N.; Bringmann, M.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 29
  • DOI: 10.1073/pnas.1007092107

Clathrin Mediates Endocytosis and Polar Distribution of PIN Auxin Transporters in Arabidopsis
journal, May 2011

  • Kitakura, Saeko; Vanneste, Steffen; Robert, Stéphanie
  • The Plant Cell, Vol. 23, Issue 5
  • DOI: 10.1105/tpc.111.083030