Abstract:
The mechanisms underlying the biosynthesis of cellulose in plants are complex and still poorly understood. A central question concerns the mechanism of microfibril structure and how this is linked to the catalytic polymerization action of cellulose synthase (CESA). Furthermore, it remains unclear whether modification of cellulose microfibril structure can be achieved genetically, which could be transformative in a bio-based economy. To explore these processes in planta, we developed a chemical genetic toolbox of pharmacological inhibitors and corresponding resistance-conferring point mutations in the C-terminal transmembrane domain region of CESA1 A903V and CESA3 T942I in Arabidopsis thaliana. Using 13C solidstate nuclear magnetic resonance spectroscopy and X-ray diffraction, we show that the cellulose microfibrils displayed reduced width and an additional cellulose C4 peak indicative of a degree of crystallinity that is intermediate between the surface and interior glucans of wild type, suggesting a difference in glucan chain association during microfibril formation. Consistent with measurements of lower microfibril crystallinity, cellulose extracts from mutated CESA1 A903V and CESA3 T942I displayed greater saccharification efficiency than wild type. Using live-cell imaging to track fluorescently labeled CESA, we found that these mutants show increased CESA velocities in the plasma membrane, an indication of increased polymerization rate. Collectively, these data suggest that CESA1 A903Vand CESA3 T942I have modified microfibril structure in terms of crystallinity and suggest that in plants, as in bacteria, crystallization biophysically limits polymerization.
Registro:
| Documento: |
Artículo
|
| Título: | Cellulose microfibril crystallinity is reduced by mutating C-terminal transmembrane region residues CESA1 A903V and CESA3 T942I of cellulose synthase |
| Autor: | Harris, D.M.; Corbin, K.; Wang, T.; Gutierrez, R.; Bertolo, A.L.; Petti, C.; Smilgies, D.-M.; Estevez, J.M.; Bonetta, D.; Urbanowicz, B.R.; Ehrhardt, D.W.; Somerville, C.R.; Rose, J.K.C.; Hong, M.; DeBolt, S. |
| Filiación: | Department of Horticulture, University of Kentucky, Lexington, KY 40546, United States Department of Chemistry and Ames Laboratory, Iowa State University, Ames, IA 50011, United States Department of Plant Biology, Carnegie Institution for Science, Stanford, CA 94305, United States Department of Plant Biology, Cornell University, Ithaca, NY 14853, United States Cornell High Energy Synchrotron Source (CHESS) Wilson Laboratory, Cornell University, Ithaca, NY 14853, United States Instituto de Fisiología, Biología Molecular y Neurociencias, Universidad de Buenos Aires, Buenos Aires C1428EGA, Argentina Faculty of Science, University of Ontario Institute of Technology, ON L1H 7K4, Canada Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720, United States Complex Carbohydrate Research Center, University of Georgia, Athens, GA 30602, United States
|
| Palabras clave: | Cell wall; Polysaccharide; Quinoxyphen; cellulose; hemicellulose; allelism; Arabidopsis; article; carbon nuclear magnetic resonance; cell membrane; cell wall; crystallization; cytoskeleton; fiber; fibrin polymerization; germination; IC 50; nonhuman; plant growth; plant stem; point mutation; priority journal; saccharification; X ray diffraction; Alleles; Amino Acid Sequence; Amino Acid Substitution; Arabidopsis; Arabidopsis Proteins; Cell Membrane; Cellulose; Crystallization; Drug Resistance; Genes, Dominant; Glucosyltransferases; Magnetic Resonance Spectroscopy; Microfibrils; Molecular Sequence Data; Mutant Proteins; Mutation; Protein Transport; Quinolines; Structure-Activity Relationship; Arabidopsis thaliana |
| Año: | 2012
|
| Volumen: | 109
|
| Número: | 11
|
| Página de inicio: | 4098
|
| Página de fin: | 4103
|
| DOI: |
http://dx.doi.org/10.1073/pnas.1200352109 |
| Título revista: | Proceedings of the National Academy of Sciences of the United States of America
|
| Título revista abreviado: | Proc. Natl. Acad. Sci. U. S. A.
|
| ISSN: | 00278424
|
| CODEN: | PNASA
|
| CAS: | cellulose, 61991-22-8, 68073-05-2, 9004-34-6; hemicellulose, 63100-39-0, 63100-40-3, 9034-32-6; Arabidopsis Proteins; CESA1 protein, Arabidopsis, 2.4.1.-; Cellulose, 9004-34-6; CesA3 protein, Arabidopsis, 2.4.1.-; Glucosyltransferases, 2.4.1.-; Mutant Proteins; Quinolines; quinoxyfen
|
| Registro: | https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00278424_v109_n11_p4098_Harris |
Referencias:
- Brown Jr., R., Montezinos, D., Cellulose microfibrils: Visualization of biosynthetic and orienting complexes in association with the plasma membrane (1976) Proc Natl Acad Sci USA, 73, pp. 143-147
- Tsekos, I., The sites of cellulose synthesis in algae: Diversity and evolution of cellulose-synthesizing enzyme complexes (1999) J Phycol, 35, pp. 635-655
- Atalla, R.H., VanderHart, D.L., Native cellulose: A composite of two distinct crystalline forms (1984) Science, 223, pp. 283-285
- Nishiyama, Y., Langan, P., Chanzy, H., Crystal structure and hydrogen-bonding system in cellulose Ib from synchrotron X-ray and neutron fiber diffraction (2002) Journal of the American Chemical Society, 124 (31), pp. 9074-9082. , DOI 10.1021/ja0257319
- Nishiyama, Y., Sugiyama, J., Chanzy, H., Langan, P., Crystal Structure and Hydrogen Bonding System in Cellulose Is from Synchrotron X-ray and Neutron Fiber Diffraction (2003) Journal of the American Chemical Society, 125 (47), pp. 14300-14306. , DOI 10.1021/ja037055w
- Viëtor, R.J., Newman, R.H., Ha, M.-A., Apperley, D.C., Jarvis, M.C., Conformational features of crystal-surface cellulose from higher plants (2002) Plant J, 30, pp. 721-731
- Sturcova, A., His, I., Apperley, D.C., Sugiyama, J., Jarvis, M.C., Structural details of crystalline cellulose from higher plants (2004) Biomacromolecules, 5 (4), pp. 1333-1339. , DOI 10.1021/bm034517p
- Jarvis, M., Chemistry: Cellulose stacks up (2003) Nature, 426, pp. 611-612
- Haigler, C.H., Brown Jr., R.M., Benziman, M., Calcofluor white ST alters the in vivo assembly of cellulose microfibrils (1980) Science, 210 (4472), pp. 903-906
- Benziman, M., Haigler, C.H., Brown Jr., R.M., Cellulose biogenesis: Polymerization and crystallization are coupled processes in Acetobacter xylinum (1980) Proceedings of the National Academy of Sciences of the United States of America, 77 (11 I), pp. 6678-6682. , DOI 10.1073/pnas.77.11.6678
- Anderson, C.T., Carroll, A., Akhmetova, L., Somerville, C., Real-time imaging of cellulose reorientation during cell wall expansion in Arabidopsis roots (2010) Plant Physiol, 152, pp. 787-796
- Richmond, T., Higher plant cellulose synthases (2000) Genome Biol, 1, pp. 30011-30016
- Desprez, T., Juraniec, M., Crowell, E.F., Jouy, H., Pochylova, Z., Parcy, F., Hofte, H., Vernhettes, S., Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana (2007) Proceedings of the National Academy of Sciences of the United States of America, 104 (39), pp. 15572-15577. , DOI 10.1073/pnas.0706569104
- Persson, S., Paredez, A., Carroll, A., Palsdottir, H., Doblin, M., Poindexter, P., Khitrov, N., Somerville, C.R., Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis (2007) Proceedings of the National Academy of Sciences of the United States of America, 104 (39), pp. 15566-15571. , DOI 10.1073/pnas.0706592104
- Taylor, N.G., Howells, R.M., Huttly, A.K., Vickers, K., Turner, S.R., Interactions among three distinct CesA proteins essential for cellulose synthesis (2003) Proceedings of the National Academy of Sciences of the United States of America, 100 (3), pp. 1450-1455. , DOI 10.1073/pnas.0337628100
- Arioli, T., Peng, L., Betzner, A.S., Burn, J., Wittke, W., Herth, W., Camilleri, C., Williamson, R.E., Molecular analysis of cellulose biosynthesis in Arabidopsis (1998) Science, 279 (5351), pp. 717-720. , DOI 10.1126/science.279.5351.717
- Stewart, G.C., Poindexter, P., Lorieau, J., Palcic, M.M., Somerville, C., α-glucosidase I is required for cellulose biosynthesis and morphogenesis in Arabidopsis (2002) Journal of Cell Biology, 156 (6), pp. 1003-1013. , DOI 10.1083/jcb.200111093
- Somerville, C., Cellulose synthesis in higher plants (2006) Annu Rev Cell Dev Biol, 22, pp. 53-78
- Paredez, A.R., Somerville, C.R., Ehrhardt, D.W., Visualization of cellulose synthase demonstrates functional association with microtubules (2006) Science, 312 (5779), pp. 1491-1495. , DOI 10.1126/science.1126551
- DeBolt, S., Gutierrez, R., Ehrhardt, D.W., Melo, C.V., Ross, L., Cutler, S.R., Somerville, C., Bonetta, D., Morlin, an inhibitor of cortical microtubule dynamics and cellulose synthase movement (2007) Proceedings of the National Academy of Sciences of the United States of America, 104 (14), pp. 5854-5859. , DOI 10.1073/pnas.0700789104
- Gu, Y., Identification of a cellulose synthase-associated protein required for cellulose biosynthesis (2010) Proc Natl Acad Sci USA, 107, pp. 12866-12871
- Fujita, M., Cortical microtubules optimize cell-wall crystallinity to drive unidirectional growth in Arabidopsis (2011) Plant J, 66, pp. 915-928
- Bischoff, V., Phytochrome regulation of cellulose synthesis in Arabidopsis (2011) Curr Biol, 21, pp. 1822-1827
- Chen, S., Ehrhardt, D.W., Somerville, C., Mutations of cellulose synthase (CESA1) phosphorylation sites modulate anisotropic cell expansion and bidirectional mobility of cellulose synthase (2010) Proc Natl Acad Sci USA, 107, pp. 17188-17193
- Scheible, W.-R., Eshed, R., Richmond, T., Delmer, D., Somerville, C., Modifications of cellulose synthase confer resistance to isoxaben and thiazolidinone herbicides in Arabidopsis Ixr1 mutants (2001) Proceedings of the National Academy of Sciences of the United States of America, 98 (18), pp. 10079-10084. , DOI 10.1073/pnas.191361598
- Desprez, T., Vernhettes, S., Fagard, M., Refregier, G., Desnos, T., Aletti, E., Py, N., Hofte, H., Resistance against herbicide isoxaben and cellulose deficiency caused by distinct mutations in same cellulose synthase isoform CESA6 (2002) Plant Physiology, 128 (2), pp. 482-490. , DOI 10.1104/pp.128.2.482
- Gutierrez, R., Lindeboom, J.J., Paredez, A.R., Emons, A.M.C., Ehrhardt, D.W., Arabidopsis corticalmicrotubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments (2009) Nat Cell Biol, 11, pp. 797-806
- Segal, L., Creely, J.J., Martin, A.E., Conrad, C.M., An empirical method for estimating the degree of crystallinity of native cellulose using the X-ray diffractometer (1959) Text Res J, 29, pp. 786-794
- Andersson, S., Serimaa, R., Paakkari, T., Saranpaa, P., Pesonen, E., Crystallinity of wood and the size of cellulose crystallites in Norway spruce (Picea abies) (2003) Journal of Wood Science, 49 (6), pp. 531-537
- Thygesen, A., Oddershede, J., Lilholt, H., Thomsen, A.B., Stahl, K., On the determination of crystallinity and cellulose content in plant fibres (2005) Cellulose, 12 (6), pp. 563-576. , DOI 10.1007/s10570-005-9001-8
- Patterson, A.L., The Scherrer formula for X-ray particle size determination (1939) Phys Rev, 56, pp. 978-982
- Fernandes, A.N., Nanstructure of cellulose microfibrils in spruce wood (2011) Proc Natl Acad Sci USA, 108, pp. 1195-1203
- Newman, R.H., Estimation of the lateral dimensions of cellulose crystallites using 13C NMR signal strengths (1999) Solid State Nucl Magn Reson, 15, pp. 21-29
- Hall, M., Bansal, P., Lee, J.H., Realff, M.J., Bommarius, A.S., Cellulose crystallinity - A key predictor of the enzymatic hydrolysis rate (2010) FEBS J, 277, pp. 1571-1582
- Harris, D., Stork, J., DeBolt, S., Genetic modification in cellulose-synthase reduces crystallinity and improves biochemical conversion to fermentable sugar (2009) Glob Change Biol Bioenergy, 1, pp. 51-61
- Carpita, N.C., Update on mechanisms of plant cell wall biosynthesis: How plants make cellulose and other (1 → 4)-β-D-glycans (2011) Plant Physiol, 155, pp. 171-184
- Hu, S.-Q., Structure of bacterial cellulose synthase subunit D octamer with four inner passageways (2010) Proc Natl Acad Sci USA, 107, pp. 17957-17961
- Wang, J., Howles, P.A., Cork, A.H., Birch, R.J., Williamson, R.E., Chimeric proteins suggest that the catalytic and/or C-terminal domains give CesA1 and CesA3 access to their specific sites in the cellulose synthase of primary walls (2006) Plant Physiology, 142 (2), pp. 685-695. , DOI 10.1104/pp.106.084004
- Foulkes-Murzycki, J.E., Scott, W.R.P., Schiffer, C.A., Hydrophobic Sliding: A Possible Mechanism for Drug Resistance in Human Immunodeficiency Virus Type 1 Protease (2007) Structure, 15 (2), pp. 225-233. , DOI 10.1016/j.str.2007.01.006, PII S0969212607000354
- Dick-Pérez, M., Structure and interactions of plant cell-wall polysaccharides by two-and three-dimensional magic-angle-spinning solid-state NMR (2011) Biochemistry, 50, pp. 989-1000
Citas:
---------- APA ----------
Harris, D.M., Corbin, K., Wang, T., Gutierrez, R., Bertolo, A.L., Petti, C., Smilgies, D.-M.,..., DeBolt, S.
(2012)
. Cellulose microfibril crystallinity is reduced by mutating C-terminal transmembrane region residues CESA1 A903V and CESA3 T942I of cellulose synthase. Proceedings of the National Academy of Sciences of the United States of America, 109(11), 4098-4103.
http://dx.doi.org/10.1073/pnas.1200352109---------- CHICAGO ----------
Harris, D.M., Corbin, K., Wang, T., Gutierrez, R., Bertolo, A.L., Petti, C., et al.
"Cellulose microfibril crystallinity is reduced by mutating C-terminal transmembrane region residues CESA1 A903V and CESA3 T942I of cellulose synthase"
. Proceedings of the National Academy of Sciences of the United States of America 109, no. 11
(2012) : 4098-4103.
http://dx.doi.org/10.1073/pnas.1200352109---------- MLA ----------
Harris, D.M., Corbin, K., Wang, T., Gutierrez, R., Bertolo, A.L., Petti, C., et al.
"Cellulose microfibril crystallinity is reduced by mutating C-terminal transmembrane region residues CESA1 A903V and CESA3 T942I of cellulose synthase"
. Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 11, 2012, pp. 4098-4103.
http://dx.doi.org/10.1073/pnas.1200352109---------- VANCOUVER ----------
Harris, D.M., Corbin, K., Wang, T., Gutierrez, R., Bertolo, A.L., Petti, C., et al. Cellulose microfibril crystallinity is reduced by mutating C-terminal transmembrane region residues CESA1 A903V and CESA3 T942I of cellulose synthase. Proc. Natl. Acad. Sci. U. S. A. 2012;109(11):4098-4103.
http://dx.doi.org/10.1073/pnas.1200352109