Perturbation of wood cellulose synthesis causes pleiotropic effects in transgenic aspen

Molecular Plant

Volumn 4, Issue 2, 2011, Pages 331-345

  Joshi, Chandrashekhar P ^a,b   Thammannagowda, Shivegowda ^a   Fujino, Takeshi ^a   Gou, Ji Qing ^a   Avci, Utku ^c   Haigler, Candace H ^c   McDonnell, Lisa M ^d   Mansfield, Shawn D ^d   Mengesha, Bemnet ^e   Carpita, Nicholas C ^e   Harris, Darby ^f   Debolt, Seth ^f   Peter, Gary F ^g  

^a MICHIGAN TECHNOLOGICAL UNIVERSITY   (United States)

^b Chonnam National University   (South Korea)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^e PURDUE UNIVERSITY   (United States)

^f UNIVERSITY OF KENTUCKY   (United States)

^g UNIVERSITY OF FLORIDA   (United States)

Author keywords

Aspen; cell wall; cellulose synthesis; crystallinity; growth; irregular xylem; lignin; transgenic trees; xylem development

Indexed keywords

POPULUS TREMULOIDES;

EID: 79953186957     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/ssq081     Document Type: Article

References (56)

1. Arioli, T., et al. (1998). Molecular analysis of cellulose biosynthesis in Arabidopsis. Science. 279, 717-720. (Pubitemid 28144553)
2. Betancur, L., Singh, B., Rapp, R.A., Wendel, J.F., Marks, M.D., Roberts, A.R., and Haigler, C.H. (2010). Phylogenetically distinct cellulose synthase genes support secondary wall thickening in Arabidopsis shoot trichomes and cotton fiber. J. Integrative Plant Biol. 52, 205-220.
3. Bevan, M. (1984). Binary Agrobacterium vectors for plant transformation. Nucleic Acids Res. 12, 8711-8721.
4. Bhandari, S., Fujino, T., Thammanagowda, S., Zhang, D., Xu, F., and Joshi, C.P. (2006). Coordinate expression of tension stress-responsive and secondary cell wall-associated KORRIGAN endo-glucanase and three cellulose synthase genes in aspen trees. Planta. 224, 828-837. (Pubitemid 44286374)
5. Burn, J.E., Hocart, C.H., Birch, R.J., Cork, A.C., and Williamson, R.E. (2002). Functional analysis of the cellulose synthase genes CesA1, CesA2 and CesA3 in Arabidopsis. Plant Physiol. 129, 797-807. (Pubitemid 34689163)
6. Carpita, N., and Vergara, C. (1998). A recipe for cellulose. Science. 279, 672-673. (Pubitemid 28144537)
7. Carpita, N.C., and McCann, M.C. (1996). Some new methods to study plant polyuronic acids and their esters. In Progress in Glycobiology, Townsend R., and Hotchkiss A., eds (New York: Marcell Dekker), pp. 595-611.
8. Carpita, N.C., and Shea, E.M. (1989). Linkage structure of carbohydrates by gas chromatography-mass spectrometry (GC-MS) of partially methylated alditol acetates. In Analysis of Carbohydrates by GLC and MS, Biermann C.J. and MacGinnis G.D., eds (Boca Raton, FL: CRS Press), pp. 157-216.
9. Coleman, H.D., Samuels, A.L., Guy, R.D., and Mansfield, S.D. (2008). Perturbed lignification impacts tree growth in hybrid poplar - a function of sink strength, vascular integrity and photosynthetic assimilation. Plant Physiol. 148, 1229-1237. (Pubitemid 352847487)
10. Delmer, D.P. (1999). Cellulose biosynthesis: exciting times for a difficult field of study. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 245-276. (Pubitemid 129491963)
11. Deshpande, B.P. (1976). Observations on the fine structure of plant cell walls. 1. Use of permanganate staining. Ann. Bot. 40, 433-437.
12. Doblin, M., Kurek, I., Jacob-Wilk, D., and Delmer, D.P. (2002). Cellulose biosynthesis in plants: from genes to rosettes. Plant Cell Physiol. 43, 1407-1420. (Pubitemid 36100978)
13. Dubois, M., Gilles, D.A., Hamilton, J.K., Rebers, P.R., and Smith, F. (1956). Colorimetric method for determination of sugars and related substances. Anal. Chem. 28, 350-356.
14. Filisetti-Cozzi, T.M.C.C., and Carpita, N.C. (1991). Measurement of uronic acids without interference from neutral sugars. Anal. Biochem. 197, 157-162.
15. Gibeaut, D.M., and Carpita, N.C. (1991). Tracing the biosynthesis of the cell wall in intact cells and plants: selective turnover and alteration of cytoplasmic and cell wall polysaccharides of proso millet cells in liquid culture and Zea mays seedlings. Plant Physiol. 97, 551-561. (Pubitemid 21914255)
16. Gonzales-Benecke, C.A., Martin, T.A., and Peter, G.F. (2010). Hydraulic architecture and tracheid allometry in mature Pinus palustris and Pinus elliottii trees. Tree Physiology. 30, 361-375.
17. Harris, D., Stork, J., and DeBolt, S. (2009). Genetic modification in cellulose-synthase reduces crystallinity and improves biochemical conversion to fermentable sugar. Global Change Biology Bioenergy. 1, 51-61.
18. Hildebrand, T., and Ruegsegger, P. (1997). A new method for the model independent assessment of thickness in three dimensional images. J. Microsc. 185, 67-75. (Pubitemid 27060526)
19. Holland, N., Holland, D., Helentjaris, T., Dhugga, K.S., Xoconostle-Cazares, B., and Delmer, D.P. (2000). A comparative analysis of the plant cellulose synthase (CesA) gene family. Plant Physiol. 123, 1313-1323. (Pubitemid 30656690)
20. Holsters, M., de Waele, D., Depicker, A., Messens, E., van Montagu, M., and Schell, J. (1978). Transfection and transformation of Agrobacterium tumefaciens. Mol. Gen. Genet. 163, 181-187. (Pubitemid 8374271)
21. Huntley, S.K., Ellis, D., Gilbert, M., Chapple, C., and Mansfield, S.D. (2003). Improved pulping efficiency in C4H-F5H transformed poplar. J. Agri. Food Chem. 51, 6178-6183.
22. Joshi, C.P., and Mansfield, S.D. (2007). The cellulose paradox: simple molecule, complex biosynthesis. Curr. Opi. Plant Sci. 10, 220-226. (Pubitemid 46722692)
23. Joshi, C.P., Bhandari, S., Ranjan, P., Kalluri, U.C., Liang, X., Fujino, T., and Samuga, A. (2004). Genomics of cellulose biosynthesis in poplars. New Phytol. 164, 53-61. (Pubitemid 39260329)
24. Kalluri, U., and Joshi, C.P. (2004). Differential expression of two cellulose synthase genes associated with primary wall and secondary wall development in aspen trees. Planta. 220, 47-55. (Pubitemid 40032998)
25. Kenrick, P., and Crane, P.R. (1997). The origin and early evolution of plants on land. Nature. 389, 33-39. (Pubitemid 27387682)
26. Kim, J.-B., and Carpita, N.C. (1992). Changes in esterification of the uronic acid groups of cell wall polysaccharides during elongation of maize coleoptiles. Plant Physiol. 98, 646-653.
27. Kimura, S., Laosinchai, W., Itoh, T., Cui, X., Linder, C.R., and Brown, R.M. (1999). Immunogold labeling of rosette terminal cellulose-synthesizing complexes in the vascular plant Vigna angularis. Plant Cell. 11, 2075-2085.
28. Kumar, M., et al. (2009). An update on the nomenclature for the cellulose synthases genes from Populus. Trends Plant Sci. 14, 248-254.
29. Liu, Y.G., Mitsukawa, N., Oosumi, T., and Whittier, R.F. (1995). Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J. 8, 457-463.
30. Megraw, R.A., Leaf, G., and Bremmer, D. (1998). Longitudinal shrinkage and microfibril angle in loblolly pine. In Microfibril Angle in Wood, Butterfield, B.A., ed. (Christchurch, New Zealand: University of Canterbury Press), pp. 27-61.
31. Mellerowicz, E.J., and Sundberg, B. (2008). Wood cell walls: biosynthesis, developmental dynamics and their implications for wood properties. Curr. Opin. Plant Biol. 11, 293-300.
32. Mellerowicz, E.J., Baucher, M., Sundberg, B., and Boerjan, W. (2001). Unravelling cell wall formation in the woody dicot stem. Plant Mol. Biol. 47, 239-274. (Pubitemid 32804507)
33. Niklas, K.J. (1992). Plant Biomechanics (Chicago, IL, USA: University of Chicago Press), p. 111.
34. Nobles, D.R., Romanovicz, D.K., and Brown, R.M., Jr. (2001). Cellulose in cyanobacteria: origin of vascular plant cellulose synthase? Plant Physiol. 127, 529-542. (Pubitemid 32996755)
35. Pear, J.R., Kawagoe, Y., Schreckengost, W.E., Delmer, D.P., and Stalker, D.M. (1996). Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit of cellulose synthase. Proc. Natl Acad. Sci. U S A. 93, 12637-12642. (Pubitemid 26367197)
36. Reynolds, E.S. (1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208-212.
37. Roberts, A.W., and Bushoven, J.T. (2007). The cellulose synthase (CESA) gene superfamily of the moss Physcomitrella patens. Plant Mol. Biol. 63, 207-219. (Pubitemid 46058725)
38. Samuga, A., and Joshi, C.P. (2002). A new cellulose synthase gene (PtrCesA2) from aspen xylem is orthologous to Arabidopsis AtCesA7 (irx3) gene associated with secondary cell wall synthesis. Gene. 296, 37-44. (Pubitemid 35287322)
39. Sandhu, A.P.S., Randhawa, G.S., and Dhugga, K.S. (2009). Plant cell wall matrix polysaccharide biosynthesis. Mol. Plant. 2, 840-850.
40. Schweingruber, F.H., Borner, A., and Schulze, E.-D. (2006). Atlas of Woody Plant Stems: Evolution, Structure, and Environmental Modifications. (Berlin: Springer-Verlag), p. 229.
41. Segal, L., Creely, J.J., Martin, A.E., and Conrad, C.M. (1959). An empirical method for estimating the degree of crystallinity of native cellulose using the X-ray diffractometer. Textile Res. J. 29, 786-794.
42. Somerville, C.R. (2006). Cellulose synthesis in higher plants. Annu. Rev. Cell Dev. Biol. 22, 53-78.
43. Tanaka, K., Murata, K., Yamazaki, M., Onosato, K., Miyao, A., and Hirochika, H. (2003). Three distinct rice cellulose synthase catalytic subunit genes required for cellulose synthesis in the secondary wall. Plant Physiol. 133, 73-83. (Pubitemid 37144083)
44. Taylor, J.G., Owen, T.P., Koonce, L.T., and Haigler, C.H. (1992). Dispersed lignin in tracheary elements treated with cellulose synthesis inhibitors provides evidence that molecules of the secondary cell wall mediate wall patterning. Plant J. 2, 959-970.
45. Taylor, N.G. (2008). Cellulose biosynthesis and deposition in higher plants. New Phytol. 178, 239-252. (Pubitemid 351441663)
46. Taylor, N.G., Gardiner, J.C., Whiteman, R., and Turner, S.R. (2004). Cellulose synthesis in the Arabidopsis secondary cell wall. Cellulose. 11, 329-338.
47. Taylor, N.G., Howells, R.M., Huttly, A.K., Vickers, K., and Turner, S.R. (2003). Interactions among three distinct CesA proteins essential for cellulose synthesis. Proc. Natl Acad. Sci. U S A. 100, 1450-1455. (Pubitemid 36184022)
48. Timmers, J., Vernhettes, S., Desprez, T., Vincken, J.-P., Visser, R.G.F., and Trindade, L.M. (2009). Interactions between membrane-bound cellulose synthases involved in the synthesis of the secondary cell wall. FEBS Lett. 583, 978-982.
49. Tsai, C.-J., Podila, G.K., and Chiang, V.L. (1994). Agrobacterium- mediated transformation of quaking aspen(Populus tremuloides) and regeneration of transgenic plants. Plant Cell Rep. 14, 94-97.
50. Turner, S.R., and Somerville, C.R. (1997). Collapsed xylem pheno-type of Arabidopsis identifies mutants deficient in cellulose deposition in the secondary cell wall. Plant Cell. 9, 689-701. (Pubitemid 28104500)
51. Tuskan, G.A., et al. (2006). The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science. 313, 1596-1604. (Pubitemid 44414027)
52. Updegraf, D.M. (1969). Semimicro determination of cellulose in biological materials. Anal. Biochem. 32, 420-424.
53. Vergara, C.E., and Carpita, N.C. (2001). β-D-glycan synthases and the CesA gene family: lessons to be learned from the mixed-linkage (1→3),(1→4)-β-D-glucan synthase. Plant Mol. Biol. 47, 145-160. (Pubitemid 32804502)
54. Wu, L., Joshi, C.P., and Chiang, V.L. (2000). A xylem-specific cellulose synthase gene from aspen (Populus tremuloides) is responsive to mechanical stress. Plant J. 22, 495-502. (Pubitemid 30427758)
55. Zhong, R., Morrison, W.H., Freshour, G.D., Hahn, M.G., and Ye, Z.H. (2003). Expression of a mutant form of cellulose synthase AtCesA7 causes dominant negative effect on cellulose biosynthesis. Plant Physiol. 132, 786-795. (Pubitemid 36715077)
56. Zhu, X., Pattahil, S., Mazumdar, K., Brehmm, A., Hahn, M.G., Dinesh-Kumar, S.P., and Joshi, C.P. (2010). Virus-induced gene silencing offers a functional genomics platform for studying plant cell wall formation. Mol. Plant. 3, 818-833.