The trafficking and behavior of cellulose synthase and a glimpse of potential cellulose synthesis regulators

Abstract

Cellulose biosynthesis is a topic of intensive research not only due to the significance of cellulose in the integrity of plant cell walls, but also due to the potential of using cellulose, a natural carbon source, in the production of biofuels. Characterization of the composition, regulation, and trafficking of cellulose synthase complexes (CSCs) is critical to an understanding of cellulose biosynthesis as well as the characterization of additional proteins that contribute to the production of cellulose either through direct interactions with CSCs or through indirect mechanisms. In this review, a highlight of a few proteins that appear to affect cellulose biosynthesis, which includes: KORRIGAN (KOR), Cellulose Synthase-Interactive Protein 1 (CSI1), and the poplar microtubule-associated protein, PttMAP20, will accompany a description of cellulose synthase (CESA) behavior and a discussion of CESA trafficking compartments that might act in the regulation of cellulose biosynthesis.

Keywords

cellulose synthesis / cellulose synthase complex (CSC) / dynamics / trafficking

References

[1] Arioli T, Peng L, Betzner A S, Burn J, Wittke W, Herth W, Camilleri C, Höfte H, Plazinski J, Birch R, Cork A, Glover J, Redmond J, Williamson R E (1998). Molecular analysis of cellulose biosynthesis in Arabidopsis. Science, 279(5351): 717-720

[2] Benes C H, Wu N, Elia A E H, Dharia T, Cantley L C, Soltoff S P (2005). The C2 domain of PKCδ is a phosphotyrosine binding domain. Cell, 121(2): 271-280

[3] Bowling A J, Brown R M Jr (2008). The cytoplasmic domain of the cellulose-synthesizing complex in vascular plants. Protoplasma, 233(1-2): 115-127

[4] Carroll A, Specht C D (2011). Understanding plant cellulose synthases through a comprehensive investigation of the cellulose synthase family sequences. Front Plant Genet Genomics,

[5] Collings D A, Gebbie L K, Howles P A, Hurley U A, Birch R J, Cork A H, Hocart C H, Arioli T, Williamson R E (2008). Arabidopsis dynamin-like protein DRP1A: a null mutant with widespread defects in endocytosis, cellulose synthesis, cytokinesis, and cell expansion. J Exp Bot, 59(2): 361-376

[6] Crowell E F, Bischoff V, Desprez T, Rolland A, Stierhof Y D, 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(4): 1141-1154

[7] Crowell E F, Gonneau M, Stierhof Y D, Höfte H, Vernhettes S (2010). Regulated trafficking of cellulose synthases. Curr Opin Plant Biol, 13(6): 700-705

[8] Davletov B A, Südhof T C (1993). A single C2 domain from synaptotagmin I is sufficient for high affinity Ca²⁺/phospholipid binding. J Biol Chem, 268(35): 26386-26390

[9] DeBolt S, Gutierrez R, Ehrhardt D W, Somerville C (2007). 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(2): 334-338

[10] Delmer D P (1999). Cellulose biosynthesis: Exciting times for a difficult field of study. Annu Rev Plant Physiol Plant Mol Biol, 50(1): 245-276

[11] Desprez T, Juraniec M, Crowell E F, 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(39): 15572-15577

[12] Dettmer J, Hong-Hermesdorf A, Stierhof Y D, Schumacher K (2006). Vacuolar H⁺-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell, 18(3): 715-730

[13] Doblin M S, Kurek I, Jacob-Wilk D, Delmer D P (2002). Cellulose biosynthesis in plants: from genes to rosettes. Plant Cell Physiol, 43(12): 1407-1420

[14] Gardiner J C, Taylor N G, Turner S R (2003). Control of cellulose synthase complex localization in developing xylem. Plant Cell, 15(8): 1740-1748

[15] Gu Y, Kaplinsky N, Bringmann M, Cobb A, Carroll A, Sampathkumar A, Baskin T I, Persson S, Somerville C R (2010). Identification of a cellulose synthase-associated protein required for cellulose biosynthesis. Proc Natl Acad Sci USA, 107(29): 12866-12871

[16] Gu Y, Somerville C (2010). Cellulose synthase interacting protein: a new factor in cellulose synthesis. Plant Signal Behav, 5(12): 1571-1574

[17] Gutierrez R, Lindeboom J J, Paredez A R, Emons A M C, Ehrhardt D W (2009). Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nat Cell Biol, 11(7): 797-806

[18] Haigler C H, Brown R M Jr (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(2-3): 111-120

[19] Kimura S, Laosinchai W, Itoh T, Cui X, Linder C R, Brown R M Jr (1999). Immunogold labeling of rosette terminal cellulose-synthesizing complexes in the vascular plant Vigna angularis. Plant Cell, 11(11): 2075-2086

[20] Konopka C A, Bednarek S Y (2008). Comparison of the dynamics and functional redundancy of the Arabidopsis dynamin-related isoforms DRP1A and DRP1C during plant development. Plant Physiol, 147(4): 1590-1602

[21] Lane D R, Wiedemeier A, Peng L, Höfte H, Vernhettes S, Desprez T, Hocart C H, Birch R J, Baskin T I, Burn J E, Arioli T, Betzner A S, Williamson R E (2001). Temperature-sensitive alleles of RSW2 link the KORRIGAN endo-1,4-β-glucanase to cellulose synthesis and cytokinesis in Arabidopsis. Plant Physiol, 126(1): 278-288

[22] Mølhøj M, Pagant S, Höfte H (2002). Towards understanding the role of membrane-bound endo-β-1,4-glucanases in cellulose biosynthesis. Plant Cell Physiol, 43(12): 1399-1406

[23] Mueller S C, Brown R M Jr (1980). Evidence for an intramembrane component associated with a cellulose microfibril-synthesizing complex in higher plants. J Cell Biol, 84(2): 315-326

[24] Nicol F, His I, Jauneau A, Vernhettes S, Canut H, Höfte H (1998). A plasma membrane-bound putative endo-1,4-β-D-glucanase is required for normal wall assembly and cell elongation in Arabidopsis. EMBO J, 17(19): 5563-5576

[25] Pagant S, Bichet A, Sugimoto K, Lerouxel O, Desprez T, McCann M, Lerouge P, Vernhettes S, Höfte H (2002). KOBITO1 encodes a novel plasma membrane protein necessary for normal synthesis of cellulose during cell expansion in Arabidopsis. Plant Cell, 14(9): 2001-2013

[26] Paredez A R, Somerville C R, Ehrhardt D W (2006). Visualization of cellulose synthase demonstrates functional association with microtubules. Science, 312(5779): 1491-1495

[27] Persson S, Paredez A, Carroll A, Palsdottir H, Doblin M, Poindexter P, Khitrov N, Auer M, Somerville C R (2007). Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis. Proc Natl Acad Sci USA, 104(39): 15566-15571

[28] Rajangam A S, Kumar M, Aspeborg H, Guerriero G, Arvestad L, Pansri P, Brown C J L, Hober S, Blomqvist K, Divne C, Ezcurra I, Mellerowicz E, Sundberg B, Bulone V, Teeri T T (2008). MAP20, a microtubule-associated protein in the secondary cell walls of hybrid aspen, is a target of the cellulose synthesis inhibitor 2,6-dichlorobenzonitrile. Plant Physiol, 148(3): 1283-1294

[29] Sato S, Kato T, Kakegawa K, Ishii T, Liu Y G, Awano T, Takabe K, Nishiyama Y, Kuga S, Sato S, Nakamura Y, Tabata S, Shibata D (2001). Role of the putative membrane-bound endo-1,4-β-glucanase KORRIGAN in cell elongation and cellulose synthesis in Arabidopsis thaliana. Plant Cell Physiol, 42(3): 251-263

[30] Scheible W R, Eshed R, Richmond T, Delmer D, Somerville C (2001). Modifications of cellulose synthase confer resistance to isoxaben and thiazolidinone herbicides in ArabidopsisIxr1 mutants. Proc Natl Acad Sci USA, 98(18): 10079-10084

[31] Schindelman G, Morikami A, Jung J, Baskin T I, Carpita N C, Derbyshire P, McCann M C, Benfey P N (2001). COBRA encodes a putative GPI-anchored protein, which is polarly localized and necessary for oriented cell expansion in Arabidopsis. Genes Dev, 15(9): 1115-1127

[32] Somerville C (2006). Cellulose synthesis in higher plants. Annu Rev Cell Dev Biol, 22(1): 53-78

[33] Szyjanowicz P M, McKinnon I, Taylor N G, Gardiner J, Jarvis M C, Turner S R (2004). The irregular xylem 2 mutant is an allele of korrigan that affects the secondary cell wall of Arabidopsis thaliana. Plant J, 37(5): 730-740

[34] Taylor N G, Howells R M, Huttly A K, Vickers K, Turner S R (2003). Interactions among three distinct CesA proteins essential for cellulose synthesis. Proc Natl Acad Sci USA, 100(3): 1450-1455

[35] Taylor N G, Laurie S, Turner S R (2000). Multiple cellulose synthase catalytic subunits are required for cellulose synthesis in Arabidopsis. Plant Cell, 12(12): 2529-2540

[36] Taylor N G, Scheible W R, Cutler S, Somerville C R, Turner S R (1999). The irregular xylem3 locus of Arabidopsis encodes a cellulose synthase required for secondary cell wall synthesis. Plant Cell, 11(5): 769-780

[37] Tewari R, Bailes E, Bunting K A, Coates J C (2010). Armadillo-repeat protein functions: questions for little creatures. Trends Cell Biol, 20(8): 470-481

[38] Timmers J, Vernhettes S, Desprez T, Vincken J P, Visser R G F, Trindade L M (2009). Interactions between membrane-bound cellulose synthases involved in the synthesis of the secondary cell wall. FEBS Lett, 583(6): 978-982

[39] Wang J, Elliott J E, Williamson R E (2008). Features of the primary wall CESA complex in wild type and cellulose-deficient mutants of Arabidopsis thaliana. J Exp Bot, 59(10): 2627-2637

[40] Wightman R, Marshall R, Turner S R (2009). A cellulose synthase-containing compartment moves rapidly beneath sites of secondary wall synthesis. Plant Cell Physiol, 50(3): 584-594

[41] Wightman R, Turner S (2010). Trafficking of the cellulose synthase complex in developing xylem vessels. Biochem Soc Trans, 38(3): 755-760

[42] Wightman R, Turner S R (2008). The roles of the cytoskeleton during cellulose deposition at the secondary cell wall. Plant J, 54(5): 794-805

[43] Xiong G, Li R, Qian Q, Song X, Liu X, Yu Y, Zeng D, Wan J, Li J, Zhou Y (2010). The rice dynamin-related protein DRP2B mediates membrane trafficking, and thereby plays a critical role in secondary cell wall cellulose biosynthesis. Plant J, 64(1): 56-70

[44] Zhong R, Burk D H, Morrison W H 3rd, Ye Z H (2004). FRAGILE FIBER3, an Arabidopsis gene encoding a type II inositol polyphosphate 5-phosphatase, is required for secondary wall synthesis and actin organization in fiber cells. Plant Cell, 16(12): 3242-3259

[45] Zhong R, Kays S J, Schroeder B P, Ye Z H (2002). Mutation of a chitinase-like gene causes ectopic deposition of lignin, aberrant cell shapes, and overproduction of ethylene. Plant Cell, 14(1): 165-179

[46] Zuo J R, Niu Q W, Nishizawa N, Wu Y, Kost B, Chua N H (2000). KORRIGAN, an Arabidopsis endo-1,4-beta-glucanase, localizes to the cell plate by polarized targeting and is essential for cytokinesis. Plant Cell, 12(7): 1137-1152

Acknowledgements

This work was supported, in part, by grants from National Science Foundation (1121375), and The Center for LignoCellulose Structure and Formation, an Energy Frontier Research Center funded by the US Department of Energy, Office of Science.

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