Functional genomic analysis supports conservation of function among cellulose synthase-like a gene family members and suggests diverse roles of mannans in plants

Plant Physiology

Volumn 143, Issue 4, 2007, Pages 1881-1893

  Liepman, Aaron H ^a   Nairn, C Joseph ^c   Willats, William G T ^d   Sørensen, Iben ^d   Roberts, Alison W ^e   Keegstra, Kenneth ^b  

^a EASTERN MICHIGAN UNIVERSITY   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

^e UNIVERSITY OF RHODE ISLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATES; CELLULOSE; ENZYMES; PLANTS (BOTANY);

CAULONEMAL FILAMENTS; CELLULOSE SYNTHASE; TRANSCRIPTION-POLYMERASE CHAINS;

GENETIC ENGINEERING;

CARBOHYDRATES; CELLULOSE; ENZYMES; GENETIC ENGINEERING; MANNANS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; CYAMOPSIS; CYAMOPSIS TETRAGONOLOBA; EMBRYOPHYTA; GYMNOSPERMAE; HEXAPODA; LOTUS; MAGNOLIOPHYTA; PHYSCOMITRELLA; PHYSCOMITRELLA PATENS; PINUS TAEDA; POPULUS TRICHOCARPA;

EID: 34249811782     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.106.093989     Document Type: Article

References (65)

1. Aspeborg H, Schrader J, Coutinho PM, Stam M, Kallas A, Djerbí S, Nilsson P, Denman S, Amini B, Sterky F, et al (2005) Carbohydrate-active enzymes involved in the secondary cell wall biogenesis in hybrid aspen. Plant Physiol 137: 983-997
2. Auxtova O, Liskova D, Kakoniova D, Kubackova M, Karacsonyi S, Bílisics L (1995) Effect of galactoglucomannan-derived oligosaccharides on elongation growth of pea and spruce stem segments stimulated by auxin. Planta 196: 420-424
3. Baldauf SL (2003) Phylogeny for the faint of heart: a tutorial. Trends Genet 19: 345-351
4. Benova-Kakosova A, Digonnet C, Goubet F, Ranocha P, Jauneau A, Pesquet E, Barbier O, Zhang Z, Capek P, Dupree P, et al (2006) Galactoglucomannans increase cell population density and alter the protoxylem/metaxylem tracheary element ratio in xylogenic cultures of zinnia. Plant Physiol 142: 696-709
5. Bilisics L, Vojtassak J, Capek P, Kollarova K, Liskova D (2004) Changes in glycosidase activities during galactoglucomannan oligosaccharide inhibition of auxin induced growth. Phytochemistry 65: 1903-1909
6. Brennan CS, Blake DE, Ellís PR, Schofield JD (1996) Effects of guar galactomannan on wheat bread microstructure and on the in vitro and in vivo digestibility of starch in bread. J Cereal Sci 24: 151-160
7. Brown DM, Zeef LAH, Ellis J, Turner SR (2005) Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17: 2281-2295
8. Burton RA, Wilson SM, Hrmova M, Harvey AJ, Shirley NJ, Medhurst A, Stone BA, Newbigin EJ, Bacic A, Fincher GB (2006) Cellulose synthase-like CslF genes mediate the synthesis of cell wall (1,3;1,4)-beta-D-glucans. Science 311: 1940-1942
9. Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11: 113-116
10. Clausen MH, Willats WG, Knox JP (2003) Synthetic methyl hexagalacturonate hapten inhibitors of anti-homogalacturonan monoclonal antibodies LM7, J1M5 and JIM7. Carbohydr Res 338: 1797-1800
11. Dhugga KS, Barreiro R, Whitten B, Stecca K, Hazebroek J, Randhawa GS, Dolan M, Kinney AJ, Tomes D, Nichols S, et al (2004) Guar seed β-mannan synthase is a member of the cellulose synthase super gene family. Science 303: 363-366
12. Djerbi S, Lindskog M, Arvestad L, Sterky F, Teeri TT (2005) The genome sequence of black cottonwood (Populus trichocarpa) reveals 18 conserved cellulose synthase (CesA) genes. Planta 221: 739-746
13. Edwards ME, Dickson CA, Chengappa S, Sidebottom C, Gidley MJ, Reid JSG (1999) Molecular characterization of a membrane-bound galactosyltransferase of plant cell wall matrix polysaccharide biosynthesis. Plant J 19: 691-697
14. Filichkin SA, Leonard JM, Monteros A, Liu PP, Nonogaki H (2004) A novel endo-β-mannanase gene in tomato LeMAN5 is associated with anther and pollen development. Plant Physiol 134: 1080-1087
15. Frei E, Preston RD (1968) Non-cellulosic structural polysaccharides in algal cell walls. III. Mannan in siphoneous green algae. Proc R Soc Lond B Biol Sci 169: 127-145
16. Freshour G, Bonin CP, Reiter WD, Albersheim P, Darvill AG, Hahn MG (2003) Distribution of fucose-containing xyloglucans in cell walls of the mur1 mutant of Arabidopsis. Plant Physiol 131: 1602-1612
17. Fry SC (2000) The Growing Plant Cell Wall: Chemical and Metabolic Analysis. Blackburn Press, Caldwell, NJ
18. Geisler-Lee J, Geisler M, Coutinho PM, Segerman B, Nishikubo N, Takahashi J, Aspeborg H, Djerbi S, Master E, Andersson-Gunneras S, et al (2006) Poplar carbohydrate-active enzymes: gene identification and expression analyses. Plant Physiol 140: 946-962
19. Goubet F, Misrahi A, Park SK, Zhang Z, Twell D, Dupree P (2003) AtCslA7, a cellulose synthase-like putative glycosyltransferase, is important for pollen tube growth and embryogenesis in Arabidopsis. Plant Physiol 131: 547-557
20. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95-98
21. Hamann T, Osborne E, Youngs H, Misson J, Nussaume L, Somerville C (2004) Global expression analysis of CESA and CSL genes in Arabidopsis. Cellulose 11: 279-286
22. Handford MG, Baldwin TC, Goubet F, Prime TA, Miles J, Yu X, Dupree P (2003) Localisation and characterisation of cell wall mannan polysaccharides in Arabidopsis thaliana. Planta 218: 27-36
23. Harholt J, Jensen JK, Sorensen SO, Orfila C, Pauly M, Scheller HV (2006) ARABINAN DEFICIENT 1 is a putative arabinosyltransferase involved in biosynthesis of pectic arabinan in Arabidopsis. Plant Physiol 140: 49-58
24. Harlow E, Lane D (1988) Antibodies: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
25. Hazen SP, Scott-Craig JS, Walton JD (2002) Cellulose synthase-like (CSL) genes of rice. Plant Physiol 128: 336-340
26. Honys D, Twell D (2003) Comparative analysis of the Arabidopsis pollen transcriptome. Plant Physiol 132: 640-652
27. Keegstra K, Raikhel NV (2001) Plant glycosy ltransferases. Curr Opin Plant Biol 4: 219-224
28. Keegstra K, Walton J (2006) Plant science: beta-glucans - brewer's bane, dietician's delight. Science 311: 1872-1873
29. Kikuchi S, Satoh K, Nagata T, Kawagashira N, Doi K, Kishimoto N, Yazaki J, Ishikawa M, Yamada H, Ooka H, et al (2003) Collection, mapping, and annotation of over 28,000 cDNA clones from japonica rice. Science 301: 376-379
30. Knight CD, Cove DJ, Cumíng AC, Quatrano RS (2002) Moss gene technology. In PM Gilmartin, C Bowler, eds. Molecular Plant Biology: A Practical Approach. Oxford Press, Oxford, pp 285-301
31. Lerouxel O, Cavalier DM, Liepman AH, Keegstra K (2006) Biosynthesis of plant cell wall polysaccharides: a complex process. Curr Opin Plant Biol 9: 621-630
32. Liepman AH, Cavalier DM, Lerouxel O, Keegstra K (2007) Cell wall structure, biosynthesis, and assembly. In J Roberts, Z Gonzalez-Carranza, eds. Plant Cell Separation and Adhesion. Blackwell Publishing, Oxford
33. Liepman AH, Wilkerson CG, Keegstra K (2005) Expression of cellulose synthase-like (Csl) genes in insect cells reveals that CslA family members encode mannan synthases. Proc Natl Acad Sci USA 102: 2221-2226
34. Liskova D, Auxtova O, Kakoniova D, Kubackova M, Karacsonyi S, Bilisics L (1995) Biological activity of galactoglucomannan-derived oligosaccharides. Planta 196: 425-429
35. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)). Methods 25: 402-408
36. Lorenz WW, Dean JFD (2002) SAGE profiling and demonstration of differential gene expression along the axial developmental gradient of lignifying xylem in loblolly pine (Pinus taeda). Tree Physiol 22: 301-310
37. Maeda Y, Awano T, Takabe K, Fujita M (2000) Immunolocalization of glucomannans in the cell wall of differentiating tracheids in Chamaecyparis obtusa. Protoplasma 213: 148-156
38. McCartney L, Steele-King CG, Jordan E, Knox JP (2003) Cell wall pectic (1-→4)-beta-d-galactan marks the acceleration of cell elongation in the Arabidopsis seedling root meristem. Plant J 33: 447-454
39. Meier H, Reid JSG (1982) Reserve polysaccharides other than starch in higher plants. In FA Loewus, W Tanner, eds. Encyclopedia of Plant Physiology, Vol 13A. Springer, Berlin, pp 418-471
40. Nairn CJ, Haselkorn T (2005) Three loblolly pine CesA genes expressed in developing xylem are orthologous to secondary wall CesA genes of angiosperms. New Phytol 166: 907-915
41. Nobles DR, Brown RM (2004) The pivotal role of cyanobacteria in the evolution of cellulose synthases and cellulose synthase-like proteins. Cellulose 11: 437-448
42. Pear JR, Kawagoe Y, Schrechengost WE, Delmer DP, Stalker DM (1996) Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit of cellulose synthase. Proc Natl Acad Sci USA 93: 12637-12642
43. Perrin RM, DeRocher AE, Bar-Peled M, Zeng W, Norambuena L, Orellana A, Raikhel NV, Keegstra K (1999) Xyloglucan fucosyltransferase, an enzyme involved in plant cell wall biosynthesis. Science 284: 1976-1979
44. Pettolino FA, Hoogenraad NJ, Ferguson C, Bacic A, Johnson E, Stone BA (2001) A (1→4)-β-mannan-specific monoclonal antibody and its use in the immunocytochemical location of galactomannans. Planta 214: 235-242
45. Popper ZA, Fry SC (2003) Primary cell wall composition of bryophytes and charophytes. Ann Bot (Lond) 91: 1-12
46. Preston RD (1968) Plants without cellulose. Sci Am 216: 102-108
47. Richmond T, Somerville CR (2001) Integrative approaches to determining Csl function. Plant Mol Biol 47: 131-143
48. Richmond TA, Somerville CR (2000) The cellulose synthase superfamily. Plant Physiol 124: 495-498
49. Roberts AW, Bushoven JT (2007) The cellulose synthase (CESA) gene superfamily of the moss Physcomitrella patens. Plant Mol Biol 63: 207-219
50. Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In S Krawetz, S Misener, eds, Bioinformatics Methods and Protocols. Humana Press, Totowa, NJ, pp 365-386
51. Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463-5467
52. Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vlngron M, Scholkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development, Nat Genet 37: 501-506
53. Schroder R, Wegrzyn TF, Bolitho KM, Redgwell RJ (2004) Mannan transglycosylase: a novel enzyme activity in cell walls of higher plants. Planta 219: 590-600
54. Schroder R, Wegrzyn TF, Sharma NN, Atkinson RG (2006) LeMAN4 endoβ-mannanase from ripe tomato fruit can act as a mannan transglycosylase or hydrolase. Planta 224: 1091-1102
55. Seki M, Narusaka M, Kamiya A, Ishida J, Satou M, Sakurai T, Nakajima M, Enju A, Akiyama K, Oono Y, et al (2002) Functional annotation of a full-length Arabidopsis cDNA collection. Science 296: 141-145
56. Somerville C, Bauer S, Brininstool G, Facette M, Hamann T, Milne J, Osborne E, Paredez A, Perrson S, Raab T, et al (2004) Toward a systems approach to understanding plant cell walls. Science 306: 2206-2211
57. Sterling JD, Atmodjo MA, Inwood SE, Kumar Kolli VS, Quigley HF, Hahn MG, Mohnen D (2006) Functional identification of an Arabidopsis pectin biosvnthetic homogalacturonan galacturonosyltransferase. Proc Natl Acad Sci USA 103: 5236-5241
58. Suzuki S, Li L, Sun YH, Chiang VL (2006) The cellulose synthase gene superfamily and biochemical functions of xylem-specific cellulose synthase-like genes in Populus trichocarpa. Plant Physiol 142: 1233-1245
59. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680
60. Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313: 1596-1604
61. Yokoyama R, Nishitani K (2004) Genomic basis for cell-wall diversity in plants: a comparative approach to gene families in rice and Arabidopsis. Plant Cell Physiol 45: 1111-1121
62. Zablackis E, Huang J, Darvill AG, Albersheim P (1995) Characterization of the cell wall polysaccharides of Arabidopsis thaliana leaves. Plant Physiol 107: 1129-1138
63. Zhong R, Burk DH, Ye ZH (2001) Fibers: a model for studying cell differentiation, cell elongation, and cell wall biosynthesis. Plant Physiol 126: 477-479
64. Zhong R, Pena MJ, Zhou GK, Nairn CJ, Wood-Jones A, Richardson EA, Morrison WH III, Darvill AG, York WS, Ye ZH (2005) Arabidopsis fragile fiber8, which encodes a putative glucuronyltransferase, is essential for normal secondary wall synthesis. Plant Cell 17: 3390-3408
65. Zhu Y, Nam J, Carpita N, Matthysse AG, Gelvin SB (2003) Agrobacterium-mediated root transformation is inhibited by mutation of an Arabidopsis cellulose synthase-like gene. Plant Physiol 133: 1000-1010