SHOU4 Proteins Regulate Trafficking of Cellulose Synthase Complexes to the Plasma Membrane

Polko, Joanna K.; Barnes, William J.; Voiniciuc, Cătălin; Doctor, Stephanie; Steinwand, Blaire; Hill, Jr., Joseph L.; Tien, Ming; Pauly, Markus; Anderson, Charles T.; Kieber, Joseph J.

doi:10.1016/j.cub.2018.07.076

SHOU4 Proteins Regulate Trafficking of Cellulose Synthase Complexes to the Plasma Membrane

Journal Article · Thu Sep 20 00:00:00 EDT 2018 · Current Biology

DOI:https://doi.org/10.1016/j.cub.2018.07.076· OSTI ID:1634833

Polko, Joanna K. ^[1]; Barnes, William J. ^[2]; Voiniciuc, Cătălin ^[3]; Doctor, Stephanie ^[4]; Steinwand, Blaire ^[4]; Hill, Jr., Joseph L. ^[5]; Tien, Ming ^[2]; Pauly, Markus ^[3]; Anderson, Charles T. ^[2]; Kieber, Joseph J. ^[4]

Univ. of North Carolina, Chapel Hill, NC (United States); University of North Carolina, Chapel Hill
Pennsylvania State Univ., University Park, PA (United States)
Heinrich-Heine Univ. Düsseldorf (Germany)
Univ. of North Carolina, Chapel Hill, NC (United States)
Michigan State Univ., East Lansing, MI (United States); Pennsylvania State Univ., University Park, PA (United States)

Cell walls play critical roles in plants, regulating tissue mechanics, defining the extent and orientation of cell expansion, and providing a physical barrier against pathogen attack. Cellulose microfibrils, which are synthesized by plasma membrane-localized cellulose synthase (CESA) complexes, are the primary load-bearing elements of plant cell walls. Cell walls are dynamic structures that are regulated in part by cell wall integrity (CWI)-monitoring systems that feed back to modulate wall properties and the synthesis of new wall components. Several receptor-like kinases have been implicated as sensors of CWI, including the FEI1/FEI2 receptor-like kinases. Here, we characterize two genes encoding novel plant-specific plasma membrane proteins (SHOU4 and SHOU4L) that were identified in a suppressor screen of the cellulose-deficient fei1 fei2 mutant. shou4 shou4l double mutants display phenotypes consistent with elevated levels of cellulose, and elevated levels of non-crystalline cellulose are present in this mutant. Disruption of SHOU4 and SHOU4L increases the abundance of CESA proteins at the plasma membrane as a result of enhanced exocytosis. In conclusion, the SHOU4/4L N-terminal cytosolic domains directly interact with CESAs. Our results suggest that the SHOU4 proteins regulate cellulose synthesis in plants by influencing the trafficking of CESA complexes to the cell surface.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of North Carolina, Chapel Hill, NC (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: SC0001090

OSTI ID:: 1634833

Journal Information:: Current Biology, Journal Name: Current Biology Journal Issue: 19 Vol. 28; ISSN 0960-9822

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (56)

A universal and rapid protocol for protein extraction from recalcitrant plant tissues for proteomic analysis Wang, Wei; Vignani, Rita; Scali, Monica ELECTROPHORESIS, Vol. 27, Issue 13 https://doi.org/10.1002/elps.200500722	journal	July 2006
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method Livak, Kenneth J.; Schmittgen, Thomas D. Methods, Vol. 25, Issue 4 https://doi.org/10.1006/meth.2001.1262	journal	December 2001
Membrane?wall attachments in plasmolysed plant cells Lang, I.; Barton, D. A.; Overall, R. L. Protoplasma, Vol. 224, Issue 3-4 https://doi.org/10.1007/s00709-004-0062-6	journal	December 2004
Longevity in vivo of primary cell wall cellulose synthases Hill, Joseph Lee; Josephs, Cooper; Barnes, William J. Plant Molecular Biology, Vol. 96, Issue 3 https://doi.org/10.1007/s11103-017-0695-4	journal	January 2018
Semimicro determination of cellulose inbiological materials Updegraff, David M. Analytical Biochemistry, Vol. 32, Issue 3 https://doi.org/10.1016/S0003-2697(69)80009-6	journal	December 1969
Local, Efflux-Dependent Auxin Gradients as a Common Module for Plant Organ Formation Benková, Eva; Michniewicz, Marta; Sauer, Michael Cell, Vol. 115, Issue 5 https://doi.org/10.1016/S0092-8674(03)00924-3	journal	November 2003
Regulation of cellulose synthesis in response to stress Kesten, Christopher; Menna, Alexandra; Sánchez-Rodríguez, Clara Current Opinion in Plant Biology, Vol. 40 https://doi.org/10.1016/j.pbi.2017.08.010	journal	December 2017
Crystalline and amorphous cellulose in the secondary walls of Arabidopsis Ruel, Katia; Nishiyama, Yoshiharu; Joseleau, Jean-Paul Plant Science, Vol. 193-194 https://doi.org/10.1016/j.plantsci.2012.05.008	journal	September 2012
Specificity and Affinity of Substrate Binding by a Family 17 Carbohydrate-Binding Module from Clostridium cellulovorans Cellulase 5A ^† Boraston, Alisdair B.; Chiu, Patrick; Warren, R. Antony J. Biochemistry, Vol. 39, Issue 36 https://doi.org/10.1021/bi0007728	journal	September 2000
Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments Gutierrez, Ryan; Lindeboom, Jelmer J.; Paredez, Alex R. Nature Cell Biology, Vol. 11, Issue 7 https://doi.org/10.1038/ncb1886	journal	June 2009
Golgi-localized STELLO proteins regulate the assembly and trafficking of cellulose synthase complexes in Arabidopsis Zhang, Yi; Nikolovski, Nino; Sorieul, Mathias Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11656	journal	June 2016
Fiji: an open-source platform for biological-image analysis Schindelin, Johannes; Arganda-Carreras, Ignacio; Frise, Erwin Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2019	journal	June 2012
V-ATPase activity in the TGN/EE is required for exocytosis and recycling in Arabidopsis Luo, Yu; Scholl, Stefan; Doering, Anett Nature Plants, Vol. 1, Issue 7 https://doi.org/10.1038/nplants.2015.94	journal	July 2015
High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method Gietz, R. Daniel; Schiestl, Robert H. Nature Protocols, Vol. 2, Issue 1 https://doi.org/10.1038/nprot.2007.13	journal	January 2007
Plant cell wall signalling and receptor-like kinases Wolf, Sebastian Biochemical Journal, Vol. 474, Issue 4 https://doi.org/10.1042/BCJ20160238	journal	February 2017
dCAPS, a simple technique for the genetic analysis of single nucleotide polymorphisms: experimental applications in Arabidopsis thaliana genetics Neff, Michael M.; Neff, Joseph D.; Chory, Joanne The Plant Journal, Vol. 14, Issue 3 https://doi.org/10.1046/j.1365-313X.1998.00124.x	journal	May 1998
The Arabidopsis thaliana MERISTEM LAYER 1 promoter specifies epidermal expression in meristems and young primordia: Epidermal expression of transgenes in meristems Sessions, Allen; Weigel, Detlef; Yanofsky, Martin F. The Plant Journal, Vol. 20, Issue 2 https://doi.org/10.1046/j.1365-313x.1999.00594.x	journal	October 1999
In vivo analysis of plant promoters and transcription factors by agroinfiltration of tobacco leaves Yang, Yinong; Li, Rugang; Qi, Min The Plant Journal, Vol. 22, Issue 6 https://doi.org/10.1046/j.1365-313x.2000.00760.x	journal	June 2000
The TWD40-2 protein and the AP2 complex cooperate in the clathrin-mediated endocytosis of cellulose synthase to regulate cellulose biosynthesis Bashline, Logan; Li, Shundai; Zhu, Xiaoyu Proceedings of the National Academy of Sciences, Vol. 112, Issue 41 https://doi.org/10.1073/pnas.1509292112	journal	September 2015
CSI1, PATROL1, and exocyst complex cooperate in delivery of cellulose synthase complexes to the plasma membrane Zhu, Xiaoyu; Li, Shundai; Pan, Songqin Proceedings of the National Academy of Sciences, Vol. 115, Issue 15 https://doi.org/10.1073/pnas.1800182115	journal	March 2018
Understanding the Biological Rationale for the Diversity of Cellulose-directed Carbohydrate-binding Modules in Prokaryotic Enzymes Blake, Anthony W.; McCartney, Lesley; Flint, James E. Journal of Biological Chemistry, Vol. 281, Issue 39 https://doi.org/10.1074/jbc.M605903200	journal	July 2006
easyFRAP: an interactive, easy-to-use tool for qualitative and quantitative analysis of FRAP data Rapsomaniki, Maria Anna; Kotsantis, Panagiotis; Symeonidou, Ioanna-Eleni Bioinformatics, Vol. 28, Issue 13 https://doi.org/10.1093/bioinformatics/bts241	journal	April 2012
Protter: interactive protein feature visualization and integration with experimental proteomic data Omasits, Ulrich; Ahrens, Christian H.; Müller, Sebastian Bioinformatics, Vol. 30, Issue 6 https://doi.org/10.1093/bioinformatics/btt607	journal	October 2013
A plasma membrane-bound putative endo-1,4-beta -D-glucanase is required for normal wall assembly and cell elongation in Arabidopsis Nicol, F. The EMBO Journal, Vol. 17, Issue 19 https://doi.org/10.1093/emboj/17.19.5563	journal	October 1998
MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0 Tamura, Koichiro; Stecher, Glen; Peterson, Daniel Molecular Biology and Evolution, Vol. 30, Issue 12 https://doi.org/10.1093/molbev/mst197	journal	October 2013
COBRA encodes a putative GPI-anchored protein, which is polarly localized and necessary for oriented cell expansion in Arabidopsis Schindelman, G. Genes & Development, Vol. 15, Issue 9 https://doi.org/10.1101/gad.879101	journal	May 2001
Colony Lift Colorimetric Assay for β-Galactosidase Activity Fuxman Bass, Juan I.; Reece-Hoyes, John S.; Walhout, Albertha J. M. Cold Spring Harbor Protocols, Vol. 2016, Issue 12 https://doi.org/10.1101/pdb.prot088963	journal	December 2016
Real-Time Imaging of Cellulose Reorientation during Cell Wall Expansion in Arabidopsis Roots Anderson, Charles T.; Carroll, Andrew; Akhmetova, Laila Plant Physiology, Vol. 152, Issue 2 https://doi.org/10.1104/pp.109.150128	journal	December 2009
Patterning and Lifetime of Plasma Membrane-Localized Cellulose Synthase Is Dependent on Actin Organization in Arabidopsis Interphase Cells Sampathkumar, Arun; Gutierrez, Ryan; McFarlane, Heather E. Plant Physiology, Vol. 162, Issue 2 https://doi.org/10.1104/pp.113.215277	journal	April 2013
The Endocytosis of Cellulose Synthase in Arabidopsis Is Dependent on μ2, a Clathrin-Mediated Endocytosis Adaptin Bashline, Logan; Li, Shundai; Anderson, Charles T. Plant Physiology, Vol. 163, Issue 1 https://doi.org/10.1104/pp.113.221234	journal	July 2013
COBRA-LIKE2, a Member of the Glycosylphosphatidylinositol-Anchored COBRA-LIKE Family, Plays a Role in Cellulose Deposition in Arabidopsis Seed Coat Mucilage Secretory Cells , Ben-Tov, Daniela; Abraham, Yael; Stav, Shira Plant Physiology, Vol. 167, Issue 3 https://doi.org/10.1104/pp.114.240671	journal	January 2015
MUCILAGE-RELATED10 Produces Galactoglucomannan That Maintains Pectin and Cellulose Architecture in Arabidopsis Seed Mucilage Voiniciuc, Cătălin; Schmidt, Maximilian Heinrich-Wilhelm; Berger, Adeline Plant Physiology, Vol. 169, Issue 1 https://doi.org/10.1104/pp.15.00851	journal	July 2015
A Second Locus, Ixr B1 in Arabidopsis thaliana, that Confers Resistance to the Herbicide Isoxaben Heim, Dale R.; Roberts, Jean L.; Pike, Philip D. Plant Physiology, Vol. 92, Issue 3 https://doi.org/10.1104/pp.92.3.858	journal	March 1990
Regulation of Root Hair Initiation and Expansin Gene Expression in Arabidopsis Cho, Hyung-Taeg; Cosgrove, Daniel J. The Plant Cell, Vol. 14, Issue 12 https://doi.org/10.1105/tpc.006437	journal	November 2002
The Arabidopsis SOS5 Locus Encodes a Putative Cell Surface Adhesion Protein and Is Required for Normal Cell Expansion Shi, Huazhong; Kim, YongSig; Guo, Yan The Plant Cell, Vol. 15, Issue 1 https://doi.org/10.1105/tpc.007872	journal	December 2002
Two Leucine-Rich Repeat Receptor Kinases Mediate Signaling, Linking Cell Wall Biosynthesis and ACC Synthase in Arabidopsis Xu, Shou-Ling; Rahman, Abidur; Baskin, Tobias I. The Plant Cell, Vol. 20, Issue 11 https://doi.org/10.1105/tpc.108.063354	journal	November 2008
Pausing of Golgi Bodies on Microtubules Regulates Secretion of Cellulose Synthase Complexes in Arabidopsis Crowell, E. F.; Bischoff, V.; Desprez, T. The Plant Cell, Vol. 21, Issue 4, p. 1141-1154 https://doi.org/10.1105/tpc.108.065334	journal	April 2009
The Arabidopsis Cellulose Synthase Complex: A Proposed Hexamer of CESA Trimers in an Equimolar Stoichiometry Hill, Joseph L.; Hammudi, Mustafa B.; Tien, Ming The Plant Cell, Vol. 26, Issue 12 https://doi.org/10.1105/tpc.114.131193	journal	December 2014
PROCUSTE1 Encodes a Cellulose Synthase Required for Normal Cell Elongation Specifically in Roots and Dark-Grown Hypocotyls of Arabidopsis Fagard, Mathilde; Desnos, Thierry; Desprez, Thierry The Plant Cell, Vol. 12, Issue 12 https://doi.org/10.1105/tpc.12.12.2409	journal	December 2000
Gateway-compatible vectors for plant functional genomics and proteomics Earley, Keith W.; Haag, Jeremy R.; Pontes, Olga The Plant Journal, Vol. 45, Issue 4 https://doi.org/10.1111/j.1365-313X.2005.02617.x	journal	February 2006
Next-generation mapping of Arabidopsis genes: Next-generation mapping of Arabidopsis genes Austin, Ryan S.; Vidaurre, Danielle; Stamatiou, George The Plant Journal, Vol. 67, Issue 4 https://doi.org/10.1111/j.1365-313X.2011.04619.x	journal	July 2011
Cellulose synthesis via the FEI2 RLK/SOS5 pathway and CELLULOSE SYNTHASE 5 is required for the structure of seed coat mucilage in Arabidopsis: Synthesis of cellulose in seed mucilage Harpaz-Saad, Smadar; McFarlane, Heather E.; Xu, Shouling The Plant Journal, Vol. 68, Issue 6 https://doi.org/10.1111/j.1365-313X.2011.04760.x	journal	October 2011
Analysis of protein interactions within the cytokinin-signaling pathway of Arabidopsis thaliana: Protein interactions in cytokinin signaling Dortay, Hakan; Mehnert, Nijuscha; Bürkle, Lukas FEBS Journal, Vol. 273, Issue 20 https://doi.org/10.1111/j.1742-4658.2006.05467.x	journal	September 2006
Role of BASIC PENTACYSTEINE transcription factors in a subset of cytokinin signaling responses Shanks, Carly M.; Hecker, Andreas; Cheng, Chia-Yi The Plant Journal, Vol. 95, Issue 3 https://doi.org/10.1111/tpj.13962	journal	June 2018
Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana Alonso, J. M.; Stepanova, Anna N.; Leisse, Thomas J. Science, Vol. 301, Issue 5633, p. 653-657 https://doi.org/10.1126/science.1086391	journal	August 2003
Visualization of Cellulose Synthase Demonstrates Functional Association with Microtubules Paredez, A. R. Science, Vol. 312, Issue 5779 https://doi.org/10.1126/science.1126551	journal	June 2006
The Cell Biology of Cellulose Synthesis McFarlane, Heather E.; Döring, Anett; Persson, Staffan Annual Review of Plant Biology, Vol. 65, Issue 1 https://doi.org/10.1146/annurev-arplant-050213-040240	journal	April 2014
Accurate multiple sequence alignment of transmembrane proteins with PSI-Coffee Chang, Jia-Ming; Di Tommaso, Paolo; Taly, Jean-Francois BMC Bioinformatics, Vol. 13, Issue Suppl 4 https://doi.org/10.1186/1471-2105-13-S4-S1	journal	January 2012
Insight into the early steps of root hair formation revealed by the procuste1 cellulose synthase mutant of Arabidopsis thaliana Singh, Sunil K.; Fischer, Urs; Singh, Manoj BMC Plant Biology, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2229-8-57	journal	January 2008
Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation Nakagawa, Tsuyoshi; Kurose, Takayuki; Hino, Takeshi Journal of Bioscience and Bioengineering, Vol. 104, Issue 1 https://doi.org/10.1263/jbb.104.34	journal	July 2007
Molecular Modeling and Imaging of Initial Stages of Cellulose Fibril Assembly: Evidence for a Disordered Intermediate Stage Haigler, Candace H.; Grimson, Mark J.; Gervais, Julien PLoS ONE, Vol. 9, Issue 4 https://doi.org/10.1371/journal.pone.0093981	journal	April 2014
Alterations in Auxin Homeostasis Suppress Defects in Cell Wall Function Steinwand, Blaire J.; Xu, Shouling; Polko, Joanna K. PLoS ONE, Vol. 9, Issue 5 https://doi.org/10.1371/journal.pone.0098193	journal	May 2014
Staining of Callose Depositions in Root and Leaf Tissues Schenk, Sebastian; Schikora, Adam BIO-PROTOCOL, Vol. 5, Issue 6 https://doi.org/10.21769/BioProtoc.1429	journal	January 2015
FRAP Analysis of LET-23::GFP in the Vulval Epithelial Cells of Living Caenorhabditis elegans Larvae Walser, Michael; Hajnal, Alex; Escobar-Restrepo, Juan BIO-PROTOCOL, Vol. 5, Issue 11 https://doi.org/10.21769/BioProtoc.1489	journal	January 2015
Starting to Gel: How Arabidopsis Seed Coat Epidermal Cells Produce Specialized Secondary Cell Walls Voiniciuc, Cătălin; Yang, Bo; Schmidt, Maximilian International Journal of Molecular Sciences, Vol. 16, Issue 2 https://doi.org/10.3390/ijms16023452	journal	February 2015
Partial inhibition of Cdk1 in G ₂ phase overrides the SAC and decouples mitotic events McCloy, Rachael A.; Rogers, Samuel; Caldon, C. Elizabeth Cell Cycle, Vol. 13, Issue 9 https://doi.org/10.4161/cc.28401	journal	March 2014

Cited By (3)

Poplar carbohydrate‐active enzymes: whole‐genome annotation and functional analyses based on RNA expression data Kumar, Vikash; Hainaut, Matthieu; Delhomme, Nicolas The Plant Journal, Vol. 99, Issue 4 https://doi.org/10.1111/tpj.14417	journal	July 2019
Spaceflight induces novel regulatory responses in Arabidopsis seedling as revealed by combined proteomic and transcriptomic analyses Kruse, Colin P. S.; Meyers, Alexander D.; Basu, Proma BMC Plant Biology, Vol. 20, Issue 1 https://doi.org/10.1186/s12870-020-02392-6	journal	May 2020
Spatio-temporal control of post-Golgi exocytic trafficking in plants Elliott, Liam; Moore, Ian; Kirchhelle, Charlotte Journal of Cell Science, Vol. 133, Issue 4 https://doi.org/10.1242/jcs.237065	journal	February 2020