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

Plant Physiology

Volumn 167, Issue 2, 2015, Pages 381-393

  Worden, Natasha ^a   Wilkop, Thomas E ^a   Esteve, Victor Esteva ^a   Jeannotte, Richard ^a   Lathe, Rahul ^b   Vernhettes, Samantha ^c   Weimer, Bart ^a   Hicks, Glenn ^d   Alonso, Jose ^e   Labavitch, John ^a   Persson, Staffan ^b,f   Ehrhardt, David ^g   Drakakaki, Georgia ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^c CEMAGREF   (France)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e NORTH CAROLINA STATE UNIVERSITY   (United States)

^f UNIVERSITY OF MELBOURNE   (Australia)

^g GEOPHYSICAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; BENZAMIDE DERIVATIVE; CARRIER PROTEIN; CELLULASE; CELLULOSE; CELLULOSE SYNTHASE; CSI1 PROTEIN, ARABIDOPSIS; ENZYME INHIBITOR; GLUCOSE; GLUCOSYLTRANSFERASE; GREEN FLUORESCENT PROTEIN; ISOXABEN; KOR1 PROTEIN, ARABIDOPSIS; MEMBRANE PROTEIN; MULTIPROTEIN COMPLEX; NITROBENZENE DERIVATIVE; ORYZALIN; SULFANILAMIDE DERIVATIVE;

ANISOTROPY; ARABIDOPSIS; CELL COMPARTMENTALIZATION; CELL MEMBRANE; CYTOLOGY; DRUG EFFECTS; ENZYMOLOGY; GROWTH, DEVELOPMENT AND AGING; HYPOCOTYL; METABOLISM; MICROTUBULE; PROTEIN TRANSPORT;

ANISOTROPY; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BENZAMIDES; CARRIER PROTEINS; CELL COMPARTMENTATION; CELL MEMBRANE; CELLULASE; CELLULOSE; DINITROBENZENES; ENZYME INHIBITORS; GLUCOSE; GLUCOSYLTRANSFERASES; GREEN FLUORESCENT PROTEINS; HYPOCOTYL; MEMBRANE PROTEINS; MICROTUBULES; MULTIPROTEIN COMPLEXES; PROTEIN TRANSPORT; SULFANILAMIDES;

EID: 84921975777     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.249003     Document Type: Article

References (85)

1. Atmodjo MA, Hao Z, Mohnen D (2013) Evolving views of pectin biosynthesis. Annu Rev Plant Biol 64: 747-779
2. Bashline L, Li S, Gu Y (2014) The trafficking of the cellulose synthase complex in higher plants. Ann Bot (Lond) 114: 1059-1067
3. Baskin TI (2001) On the alignment of cellulose microfibrils by cortical microtubules: a review and a model. Protoplasma 215: 150-171
4. Baskin TI (2005) Anisotropic expansion of the plant cell wall. Annu Rev Cell Dev Biol 21: 203-222
5. Baskin TI, Beemster GT, Judy-March JE, Marga F (2004) Disorganization of cortical microtubules stimulates tangential expansion and reduces the uniformity of cellulose microfibril alignment among cells in the root of Arabidopsis. Plant Physiol 135: 2279-2290
6. Bichet A, Desnos T, Turner S, Grandjean O, Höfte H (2001) BOTERO1 is required for normal orientation of cortical microtubules and anisotropic cell expansion in Arabidopsis. Plant J 25: 137-148
7. Bischoff V, Cookson SJ, Wu S, Scheible WR (2009) Thaxtomin A affects CESA-complex density, expression of cell wall genes, cell wall composition, and causes ectopic lignification in Arabidopsis thaliana seedlings. J Exp Bot 60: 955-965
8. Bischoff V, Desprez T, Mouille G, Vernhettes S, Gonneau M, Höfte H (2011) Phytochrome regulation of cellulose synthesis in Arabidopsis. Curr Biol 21: 1822-1827
9. Brabham C, Debolt S (2012) Chemical genetics to examine cellulose biosynthesis. Front Plant Sci 3: 309
10. Brabham C, Lei L, Gu Y, Stork J, Barrett M, DeBolt S (2014) Indaziflam herbicidal action: a potent cellulose biosynthesis inhibitor. Plant Physiol 166: 1177-1185
11. Bringmann M, Li E, Sampathkumar A, Kocabek T, Hauser MT, Persson S (2012) POM-POM2/cellulose synthase interacting1 is essential for the functional association of cellulose synthase and microtubules in Arabidopsis. Plant Cell 24: 163-177
12. Chan J, Calder GM, Doonan JH, Lloyd CW (2003) EB1 reveals mobile microtubule nucleation sites in Arabidopsis. Nat Cell Biol 5: 967-971
13. Chen S, Ehrhardt DW, Somerville CR (2010) Mutations of cellulose synthase (CESA1) phosphorylation sites modulate anisotropic cell expansion and bidirectional mobility of cellulose synthase. Proc Natl Acad Sci USA 107: 17188-17193
14. Costes SV, Daelemans D, Cho EH, Dobbin Z, Pavlakis G, Lockett S (2004) Automatic and quantitative measurement of protein-protein colocalization in live cells. Biophys J 86: 3993-4003
15. Crowell EF, Bischoff V, Desprez T, Rolland A, Stierhof YD, Schumacher K, Gonneau M, Höfte H, Vernhettes S (2009) Pausing of Golgi bodies on microtubules regulates secretion of cellulose synthase complexes in Arabidopsis. Plant Cell 21: 1141-1154
16. DeBolt S, Gutierrez R, Ehrhardt DW, Melo CV, Ross L, Cutler SR, Somerville C, Bonetta D (2007a) Morlin, an inhibitor of cortical microtubule dynamics and cellulose synthase movement. Proc Natl Acad Sci USA 104: 5854-5859
17. DeBolt S, Gutierrez R, Ehrhardt DW, Somerville C (2007b) Nonmotile cellulose synthase subunits repeatedly accumulate within localized regions at the plasma membrane in Arabidopsis hypocotyl cells following 2,6-dichlorobenzonitrile treatment. Plant Physiol 145: 334-338
18. Desprez T, Juraniec M, Crowell EF, Jouy H, Pochylova Z, Parcy F, Höfte H, Gonneau M, Vernhettes S (2007) Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 104: 15572-15577
19. +-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18: 715-730
20. Dische Z (1962) Color reaction of carbohydrates. In R Whistler, M Wolfrom, eds, Methods in Carbohydrate Biochemistry. Academic Press, New York, pp 475-514
21. Dixit R, Chang E, Cyr R (2006) Establishment of polarity during organization of the acentrosomal plant cortical microtubule array. Mol Biol Cell 17: 1298-1305
22. Drakakaki G, Robert S, Raikhel NV, Hicks GR (2009) Chemical dissection of endosomal pathways. Plant Signal Behav 4: 57-62
23. Drakakaki G, Robert S, Szatmari AM, Brown MQ, Nagawa S, Van Damme D, Leonard M, Yang Z, Girke T, Schmid SL, et al (2011) Clusters of bioactive compounds target dynamic endomembrane networks in vivo. Proc Natl Acad Sci USA 108: 17850-17855
24. Drakakaki G, van de Ven W, Pan S, Miao Y, Wang J, Keinath NF, Weatherly B, Jiang L, Schumacher K, Hicks G, et al (2012) Isolation and proteomic analysis of the SYP61 compartment reveal its role in exocytic trafficking in Arabidopsis. Cell Res 22: 413-424
25. Dunkley TP, Hester S, Shadforth IP, Runions J, Weimar T, Hanton SL, Griffin JL, Bessant C, Brandizzi F, Hawes C, et al (2006) Mapping the Arabidopsis organelle proteome. Proc Natl Acad Sci USA 103: 6518- 6523
26. Fagard M, Desnos T, Desprez T, Goubet F, Refregier G, Mouille G, McCann M, Rayon C, Vernhettes S, Höfte H (2000) PROCUSTE1 encodes a cellulose synthase required for normal cell elongation specifically in roots and dark-grown hypocotyls of Arabidopsis. Plant Cell 12: 2409-2424
27. Fernandes AN, Thomas LH, Altaner CM, Callow P, Forsyth VT, Apperley DC, Kennedy CJ, Jarvis MC (2011) Nanostructure of cellulose microfibrils in spruce wood. Proc Natl Acad Sci USA 108: E1195-E1203
28. Gardiner JC, Taylor NG, Turner SR (2003) Control of cellulose synthase complex localization in developing xylem. Plant Cell 15: 1740-1748
29. Geldner N, Dénervaud-Tendon V, Hyman DL, Mayer U, Stierhof YD, Chory J (2009) Rapid, combinatorial analysis of membrane compartments in intact plants with a multicolor marker set. Plant J 59: 169-178
30. Green PB (1962) Mechanism for plant cellular morphogenesis. Science 138: 1404-1405
31. 13C]glucose tracer and gas chromatography-mass spectrometry. Plant Physiol 97: 1456-1461
32. Groen AJ, Sancho-Andrés G, Breckels LM, Gatto L, Aniento F, Lilley KS (2014) Identification of trans-Golgi network proteins in Arabidopsis thaliana root tissue. J Proteome Res 13: 763-776
33. Gu Y, Kaplinsky N, Bringmann M, Cobb A, Carroll A, Sampathkumar A, Baskin TI, Persson S, Somerville CR (2010) Identification of a cellulose synthase-associated protein required for cellulose biosynthesis. Proc Natl Acad Sci USA 107: 12866-12871
34. Günl M, Gille S, Pauly M (2010) OLIgo Mass Profiling (OLIMP) of extracellular polysaccharides. J Vis Exp 40: 2046
35. Gutierrez R, Lindeboom JJ, Paredez AR, Emons AM, Ehrhardt DW (2009) Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nat Cell Biol 11: 797-806
36. Haigler CH, Brown RM (1986) Transport of rosettes from the Golgi apparatus to the plasma membrane in isolated mesophyll cells of Zinnia elegans during differentiation to tracheary elements in suspension culture. Protoplasma 134: 111-120
37. Harris DM, Corbin K, Wang T, Gutierrez R, Bertolo AL, Petti C, Smilgies DM, Estevez JM, Bonetta D, Urbanowicz BR, et al (2012) Cellulose microfibril crystallinity is reduced by mutating C-terminal transmembrane region residues CESA1A903V and CESA3T942I of cellulose synthase. Proc Natl Acad Sci USA 109: 4098-4103
38. Heim DR, Roberts JL, Pike PD, Larrinua IM (1989) Mutation of a locus of Arabidopsis thaliana confers resistance to the herbicide isoxaben. Plant Physiol 90: 146-150
39. Hématy K, Sado PE, Van Tuinen A, Rochange S, Desnos T, Balzergue S, Pelletier S, Renou JP, Höfte H (2007) A receptor-like kinase mediates the response of Arabidopsis cells to the inhibition of cellulose synthesis. Curr Biol 17: 922-931
40. Herth W (1987) Effects of 2,6-DCB on plasma membrane rosettes of wheat root cells. Naturwissenschaften 74: 556-557
41. Hunter PR, Craddock CP, Di Benedetto S, Roberts LM, Frigerio L (2007) Fluorescent reporter proteins for the tonoplast and the vacuolar lumen identify a single vacuolar compartment in Arabidopsis cells. Plant Physiol 145: 1371-1382
42. Huysamer M, Greve LC, Labavitch JM (1997) Cell wall metabolism in ripening fruit: IX. Synthesis of pectic and hemicellulosic cell wall polymers in the outer pericarp of mature green tomatoes (cv XMT-22). Plant Physiol 114: 1523-1531
43. Jarvis MC (2013) Cellulose biosynthesis: counting the chains. Plant Physiol 163: 1485-1486
44. Konopka CA, Backues SK, Bednarek SY (2008) Dynamics of Arabidopsis dynamin-related protein 1C and a clathrin light chain at the plasma membrane. Plant Cell 20: 1363-1380
45. Landrein B, Lathe R, Bringmann M, Vouillot C, Ivakov A, Boudaoud A, Persson S, Hamant O (2013) Impaired cellulose synthase guidance leads to stem torsion and twists phyllotactic patterns in Arabidopsis. Curr Biol 23: 895-900
46. Lane DR, Wiedemeier A, Peng L, Höfte H, Vernhettes S, Desprez T, Hocart CH, Birch RJ, Baskin TI, Burn JE, et al (2001) Temperaturesensitive alleles of RSW2 link the KORRIGAN endo-1,4-β-glucanase to cellulose synthesis and cytokinesis in Arabidopsis. Plant Physiol 126: 278-288
47. Ledbetter MC, Porter KR (1963) A "microtubule" in plant cell fine structure. J Cell Biol 19: 239-250
48. Lee JC, Timasheff SN (1977) In vitro reconstitution of calf brain microtubules: effects of solution variables. Biochemistry 16: 1754-1764
49. Lei L, Li S, Bashline L, Gu Y (2014a) Dissecting the molecular mechanism underlying the intimate relationship between cellulose microfibrils and cortical microtubules. Front Plant Sci 5: 90
50. Lei L, Zhang T, Strasser R, Lee CM, Gonneau M, Mach L, Vernhettes S, Kim SH, Cosgrove D, Li S, et al (2014b) 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 26: 2601-2616
51. Li S, Lei L, Somerville CR, Gu Y (2012) Cellulose synthase interactive protein 1 (CSI1) links microtubules and cellulose synthase complexes. Proc Natl Acad Sci USA 109: 185-190
52. Mathur J, Spielhofer P, Kost B, Chua N (1999) The actin cytoskeleton is required to elaborate and maintain spatial patterning during trichome cell morphogenesis in Arabidopsis thaliana. Development 126: 5559- 5568
53. McFarlane HE, Döring A, Persson S (2014) The cell biology of cellulose synthesis. Annu Rev Plant Biol 65: 69-94
54. Mei Y, Gao HB, Yuan M, Xue HW (2012) The Arabidopsis ARCP protein, CSI1, which is required for microtubule stability, is necessary for root and anther development. Plant Cell 24: 1066-1080
55. Morejohn LC, Bureau TE, Molè-Bajer J, Bajer AS, Fosket DE (1987) Oryzalin, a dinitroaniline herbicide, binds to plant tubulin and inhibits microtubule polymerization in vitro. Planta 172: 252-264
56. Mutwil M, Debolt S, Persson S (2008) Cellulose synthesis: a complex complex. Curr Opin Plant Biol 11: 252-257
57. Nakamura M, Naoi K, Shoji T, Hashimoto T (2004) Low concentrations of propyzamide and oryzalin alter microtubule dynamics in Arabidopsis epidermal cells. Plant Cell Physiol 45: 1330-1334
58. Nebenführ A, Gallagher LA, Dunahay TG, Frohlick JA, Mazurkiewicz AM, Meehl JB, Staehelin LA (1999) Stop-and-go movements of plant Golgi stacks are mediated by the acto-myosin system. Plant Physiol 121: 1127-1142
59. Nelson BK, Cai X, Nebenführ A (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J 51: 1126-1136
60. Newman RH, Hill SJ, Harris PJ (2013) Wide-angle x-ray scattering and solid-state nuclear magnetic resonance data combined to test models for cellulose microfibrils in mung bean cell walls. Plant Physiol 163: 1558-1567
61. Nikolovski N, Rubtsov D, Segura MP, Miles GP, Stevens TJ, Dunkley TP, Munro S, Lilley KS, Dupree P (2012) Putative glycosyltransferases and other plant Golgi apparatus proteins are revealed by LOPIT proteomics. Plant Physiol 160: 1037-1051
62. Paredez AR, Persson S, Ehrhardt DW, Somerville CR (2008) Genetic evidence that cellulose synthase activity influences microtubule cortical array organization. Plant Physiol 147: 1723-1734
63. Paredez AR, Somerville CR, Ehrhardt DW (2006) Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312: 1491-1495
64. Parsons HT, Christiansen K, Knierim B, Carroll A, Ito J, Batth TS, Smith- Moritz AM, Morrison S, McInerney P, Hadi MZ, et al (2012) Isolation and proteomic characterization of the Arabidopsis Golgi defines functional and novel components involved in plant cell wall biosynthesis. Plant Physiol 159: 12-26
65. Persson S, Paredez A, Carroll A, Palsdottir H, Doblin M, Poindexter P, Khitrov N, Auer M, Somerville CR (2007) Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis. Proc Natl Acad Sci USA 104: 15566-15571
66. Robert S, Bichet A, Grandjean O, Kierzkowski D, Satiat-Jeunemaître B, Pelletier S, Hauser MT, Höfte H, Vernhettes S (2005) An Arabidopsis endo-1,4-β-D-glucanase involved in cellulose synthesis undergoes regulated intracellular cycling. Plant Cell 17: 3378-3389
67. Robert S, Chary SN, Drakakaki G, Li S, Yang Z, Raikhel NV, Hicks GR (2008) Endosidin1 defines a compartment involved in endocytosis of the brassinosteroid receptor BRI1 and the auxin transporters PIN2 and AUX1. Proc Natl Acad Sci USA 105: 8464-8469
68. Roudier F, Fernandez AG, Fujita M, Himmelspach R, Borner GH, Schindelman G, Song S, Baskin TI, Dupree P, Wasteneys GO, et al (2005) COBRA, an Arabidopsis extracellular glycosyl-phosphatidyl inositol-anchored protein, specifically controls highly anisotropic expansion through its involvement in cellulose microfibril orientation. Plant Cell 17: 1749-1763
69. Sampathkumar A, Gutierrez R, McFarlane HE, Bringmann M, Lindeboom J, Emons AM, Samuels L, Ketelaar T, Ehrhardt DW, Persson S (2013) Patterning and lifetime of plasma membrane-localized cellulose synthase is dependent on actin organization in Arabidopsis interphase cells. Plant Physiol 162: 675-688
70. Scheible WR, Eshed R, Richmond T, Delmer D, Somerville C (2001) Modifications of cellulose synthase confer resistance to isoxaben and thiazolidinone herbicides in Arabidopsis Ixr1 mutants. Proc Natl Acad Sci USA 98: 10079-10084
71. Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61: 263-289
72. Shaw SL, Kamyar R, Ehrhardt DW (2003) Sustained microtubule treadmilling in Arabidopsis cortical arrays. Science 300: 1715-1718
73. Shelanski ML, Gaskin F, Cantor CR (1973) Microtubule assembly in the absence of added nucleotides. Proc Natl Acad Sci USA 70: 765-768
74. Smertenko AP, Chang HY, Sonobe S, Fenyk SI, Weingartner M, Bögre L, Hussey PJ (2006) Control of the AtMAP65-1 interaction with microtubules through the cell cycle. J Cell Sci 119: 3227-3237
75. Smertenko AP, Kaloriti D, Chang HY, Fiserova J, Opatrny Z, Hussey PJ (2008) The C-terminal variable region specifies the dynamic properties of Arabidopsis microtubule-associated proteinMAP65 isotypes. Plant Cell 20: 3346-3358
76. Somerville C (2006) Cellulose synthesis in higher plants. Annu Rev Cell Dev Biol 22: 53-78
77. Sugimoto K, Himmelspach R, Williamson RE, Wasteneys GO (2003) Mutation or drug-dependent microtubule disruption causes radial swelling without altering parallel cellulose microfibril deposition in Arabidopsis root cells. Plant Cell 15: 1414-1429
78. Thomas LH, Forsyth VT, Sturcová A, Kennedy CJ, May RP, Altaner CM, Apperley DC, Wess TJ, Jarvis MC (2013) Structure of cellulose microfibrils in primary cell walls from collenchyma. Plant Physiol 161: 465- 476
79. Updegraff DM (1969) Semimicro determination of cellulose in biological materials. Anal Biochem 32: 420-424
80. Vain T, Crowell EF, Timpano H, Biot E, Desprez T, Mansoori N, Trindade LM, Pagant S, Robert S, Höfte H, et al (2014) The cellulase KORRIGAN is part of the cellulose synthase complex. Plant Physiol 165: 1521-1532
81. Wasteneys GO, Fujita M (2006) Establishing and maintaining axial growth: wall mechanical properties and the cytoskeleton. J Plant Res 119: 5-10
82. Yoneda A, Higaki T, Kutsuna N, Kondo Y, Osada H, Hasezawa S, Matsui M (2007) Chemical genetic screening identifies a novel inhibitor of parallel alignment of cortical microtubules and cellulose microfibrils. Plant Cell Physiol 48: 1393-1403
83. Yoneda A, Ito T, Higaki T, Kutsuna N, Saito T, Ishimizu T, Osada H, Hasezawa S, Matsui M, Demura T (2010) Cobtorin target analysis reveals that pectin functions in the deposition of cellulose microfibrils in parallel with cortical microtubules. Plant J 64: 657-667
84. Zhou R, Benavente LM, Stepanova AN, Alonso JM (2011) A recombineering-based gene tagging system for Arabidopsis. Plant J 66: 712-723
85. Zheng H, Kunst L, Hawes C, Moore I (2004) A GFP-based assay reveals a role for RHD3 in transport between the endoplasmic reticulum and Golgi apparatus. Plant J 37: 398-414