CESA TRAFFICKING INHIBITOR Inhibits Cellulose Deposition and Interferes with the Trafficking of Cellulose Synthase Complexes and Their Associated Proteins KORRIGAN1 and POM2/CELLULOSE SYNTHASE INTERACTIVE PROTEIN1

Overview

Journal Plant Physiol

Specialty Physiology

Date 2014 Dec 24

PMID 25535279

Citations 21

Authors

Natasha Worden

Thomas E Wilkop

Victor Esteva Esteve

Richard Jeannotte

Rahul Lathe

Samantha Vernhettes

Bart Weimer

Glenn Hicks

Jose Alonso

John Labavitch

Staffan Persson

David Ehrhardt

Georgia Drakakaki

Affiliations

Soon will be listed here.

Abstract

Cellulose synthase complexes (CSCs) at the plasma membrane (PM) are aligned with cortical microtubules (MTs) and direct the biosynthesis of cellulose. The mechanism of the interaction between CSCs and MTs, and the cellular determinants that control the delivery of CSCs at the PM, are not yet well understood. We identified a unique small molecule, CESA TRAFFICKING INHIBITOR (CESTRIN), which reduces cellulose content and alters the anisotropic growth of Arabidopsis (Arabidopsis thaliana) hypocotyls. We monitored the distribution and mobility of fluorescently labeled cellulose synthases (CESAs) in live Arabidopsis cells under chemical exposure to characterize their subcellular effects. CESTRIN reduces the velocity of PM CSCs and causes their accumulation in the cell cortex. The CSC-associated proteins KORRIGAN1 (KOR1) and POM2/CELLULOSE SYNTHASE INTERACTIVE PROTEIN1 (CSI1) were differentially affected by CESTRIN treatment, indicating different forms of association with the PM CSCs. KOR1 accumulated in bodies similar to CESA; however, POM2/CSI1 dissociated into the cytoplasm. In addition, MT stability was altered without direct inhibition of MT polymerization, suggesting a feedback mechanism caused by cellulose interference. The selectivity of CESTRIN was assessed using a variety of subcellular markers for which no morphological effect was observed. The association of CESAs with vesicles decorated by the trans-Golgi network-localized protein SYNTAXIN OF PLANTS61 (SYP61) was increased under CESTRIN treatment, implicating SYP61 compartments in CESA trafficking. The properties of CESTRIN compared with known CESA inhibitors afford unique avenues to study and understand the mechanism under which PM-associated CSCs are maintained and interact with MTs and to dissect their trafficking routes in etiolated hypocotyls.

Citing Articles

A high-resolution model of gene expression during Gossypium hirsutum (cotton) fiber development.

Grover C, Jareczek J, Swaminathan S, Lee Y, Howell A, Rani H BMC Genomics. 2025; 26(1):221.

PMID: 40050725 PMC: 11884195. DOI: 10.1186/s12864-025-11360-z.

A cellulose synthesis inhibitor affects cellulose synthase complex secretion and cortical microtubule dynamics.

Renou J, Li D, Lu J, Zhang B, Gineau E, Ye Y Plant Physiol. 2024; 196(1):124-136.

PMID: 38833284 PMC: 11376392. DOI: 10.1093/plphys/kiae232.

Breaking-Down Barriers: Proposal of Using Cellulose Biosynthesis Inhibitors and Cellulase Enzyme as a Novel Treatment Modality for Vision Threatening Pythium Insidiosum Keratitis.

Gurnani B, Natarajan R, Mohan M, Kaur K Clin Ophthalmol. 2024; 18:765-776.

PMID: 38495678 PMC: 10941664. DOI: 10.2147/OPTH.S450665.

Research overview on the genetic mechanism underlying the biosynthesis of polysaccharide in tuber plants.

Xu M, Hu J, Li H, Li K, Xu D PeerJ. 2024; 12:e17052.

PMID: 38464751 PMC: 10924778. DOI: 10.7717/peerj.17052.

Discovery and Characterization of Fluopipamine, a Putative Cellulose Synthase 1 Antagonist within .

Amos B, Pook V, Prates E, Stork J, Shah M, Jacobson D J Agric Food Chem. 2024; 72(6):3171-3179.

PMID: 38291808 PMC: 10870765. DOI: 10.1021/acs.jafc.3c05199.

References

Yoneda A, Higaki T, Kutsuna N, Kondo Y, Osada H, Hasezawa S . Chemical genetic screening identifies a novel inhibitor of parallel alignment of cortical microtubules and cellulose microfibrils. Plant Cell Physiol. 2007; 48(10):1393-403. DOI: 10.1093/pcp/pcm120. View

Shelanski M, Gaskin F, Cantor C . Microtubule assembly in the absence of added nucleotides. Proc Natl Acad Sci U S A. 1973; 70(3):765-8. PMC: 433354. DOI: 10.1073/pnas.70.3.765. View

Gardiner J, Taylor N, Turner S . Control of cellulose synthase complex localization in developing xylem. Plant Cell. 2003; 15(8):1740-8. PMC: 167166. DOI: 10.1105/tpc.012815. View

Crowell E, Bischoff V, Desprez T, Rolland A, Stierhof Y, Schumacher K . Pausing of Golgi bodies on microtubules regulates secretion of cellulose synthase complexes in Arabidopsis. Plant Cell. 2009; 21(4):1141-54. PMC: 2685615. DOI: 10.1105/tpc.108.065334. View

Gunl M, Gille S, Pauly M . OLIgo mass profiling (OLIMP) of extracellular polysaccharides. J Vis Exp. 2010; (40). PMC: 3143487. DOI: 10.3791/2046. View

Morejohn L, Bureau T, Mole-Bajer J, Bajer A, Fosket D . Oryzalin, a dinitroaniline herbicide, binds to plant tubulin and inhibits microtubule polymerization in vitro. Planta. 2013; 172(2):252-64. DOI: 10.1007/BF00394595. View

Persson S, Paredez A, Carroll A, Palsdottir H, Doblin M, Poindexter P . Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis. Proc Natl Acad Sci U S A. 2007; 104(39):15566-71. PMC: 2000526. DOI: 10.1073/pnas.0706592104. View

Chan J, Calder G, Doonan J, Lloyd C . EB1 reveals mobile microtubule nucleation sites in Arabidopsis. Nat Cell Biol. 2003; 5(11):967-71. DOI: 10.1038/ncb1057. View

Groen A, Sancho-Andres G, Breckels L, Gatto L, Aniento F, Lilley K . Identification of trans-golgi network proteins in Arabidopsis thaliana root tissue. J Proteome Res. 2013; 13(2):763-76. PMC: 3929368. DOI: 10.1021/pr4008464. View

10.

Drakakaki G, Robert S, Raikhel N, Hicks G . Chemical dissection of endosomal pathways. Plant Signal Behav. 2009; 4(1):57-62. PMC: 2634075. DOI: 10.4161/psb.4.1.7314. View

11.

Drakakaki G, van de Ven W, Pan S, Miao Y, Wang J, Keinath N . Isolation and proteomic analysis of the SYP61 compartment reveal its role in exocytic trafficking in Arabidopsis. Cell Res. 2011; 22(2):413-24. PMC: 3271593. DOI: 10.1038/cr.2011.129. View

12.

Nelson B, Cai X, Nebenfuhr A . A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 2007; 51(6):1126-36. DOI: 10.1111/j.1365-313X.2007.03212.x. View

13.

Desprez T, Juraniec M, Crowell E, Jouy H, Pochylova Z, Parcy F . Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 2007; 104(39):15572-7. PMC: 2000492. DOI: 10.1073/pnas.0706569104. View

14.

Zhou R, Benavente L, Stepanova A, Alonso J . A recombineering-based gene tagging system for Arabidopsis. Plant J. 2011; 66(4):712-23. DOI: 10.1111/j.1365-313X.2011.04524.x. View

15.

Geldner N, Denervaud-Tendon V, Hyman D, Mayer U, Stierhof Y, Chory J . Rapid, combinatorial analysis of membrane compartments in intact plants with a multicolor marker set. Plant J. 2009; 59(1):169-78. PMC: 4854200. DOI: 10.1111/j.1365-313X.2009.03851.x. View

16.

Dixit R, Chang E, Cyr R . Establishment of polarity during organization of the acentrosomal plant cortical microtubule array. Mol Biol Cell. 2005; 17(3):1298-305. PMC: 1382318. DOI: 10.1091/mbc.e05-09-0864. View

17.

Wasteneys G, Fujita M . Establishing and maintaining axial growth: wall mechanical properties and the cytoskeleton. J Plant Res. 2005; 119(1):5-10. DOI: 10.1007/s10265-005-0233-3. View

18.

Costes S, Daelemans D, Cho E, Dobbin Z, Pavlakis G, Lockett S . Automatic and quantitative measurement of protein-protein colocalization in live cells. Biophys J. 2004; 86(6):3993-4003. PMC: 1304300. DOI: 10.1529/biophysj.103.038422. View

19.

Lei L, Zhang T, Strasser R, Lee C, Gonneau M, Mach L . The jiaoyao1 Mutant Is an Allele of korrigan1 That Abolishes Endoglucanase Activity and Affects the Organization of Both Cellulose Microfibrils and Microtubules in Arabidopsis. Plant Cell. 2014; 26(6):2601-2616. PMC: 4114954. DOI: 10.1105/tpc.114.126193. View

20.

Hematy K, Sado P, van Tuinen A, Rochange S, Desnos T, Balzergue S . A receptor-like kinase mediates the response of Arabidopsis cells to the inhibition of cellulose synthesis. Curr Biol. 2007; 17(11):922-31. DOI: 10.1016/j.cub.2007.05.018. View