Cellulose

, Volume 11, Issue 3–4, pp 419–435

Cellulose synthase (CesA) genes in algae and seedless plants

  • Alison W. Roberts
  • Eric Roberts
Article

Abstract

Microfibril structure is determined largely by the organization of arrays of integral plasma membrane protein particles known as “terminal complexes”, which include cellulose synthase catalytic subunits encoded by CesA genes. Although the CesA genes of plants and bacteria share conserved regions, variations in terminal complex and microfibril structure presumably result from sequence differences. Thus, the CesA domains that influence terminal complex assembly may be revealed by examining the differences between CesA genes from green algae in which terminal complex structure ranges from rosettes (plant-like) to linear (bacteria-like). This report describes a second CesA gene that has been cloned from Mesotaenium caldariorum, a unicellular green alga from the order Zygnematales, which have rosette terminal complexes. Both McCesA1 and McCesA2 are similar to seed plant CesAs in domain structure and intron position. Seed plants have multiple CesAs and CesA-like (Csl) genes, some of which appear to be expressed specifically during cell expansion, secondary cell wall deposition in vascular tissue, or tip growth. Diversification of the CesA and Csl gene families can be explored by comparing these genes in mosses, which lack vascular tissue with secondary cell walls, and early divergent vascular plants such as ferns. Degenerate primers were used to amplify and clone five unique CesA and Csl fragments from genomic DNA isolated from Physcomitrella patens. Probes derived from the cloned fragments were used to isolate several clones from a Physcomitrella genomic library. One Csl fragment was amplified from genomic DNA isolated from the fern Ceratopteris richardii. Phylogenetic analysis supports the presence of CslD genes in both mosses and ferns, but does not support the presence of secondary cell wall specific CesA orthologs in mosses.

Algae Bryophytes Cellulose Cellulose synthase gene superfamily Ceratopteris richardii CesA CslD Ferns Mesotaenium caldariorum Microfibril Physcomitrella patens Terminal complex Vascular evolution 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Altschul S.F., Gish W., Miller W., Myers E.W.and Lipman D.J.1990.Basic local alignment search tool.J.Mol.Biol. 215:403–410.Google Scholar
  2. Arioli T., Peng L., Betzner A.S., Burn J., Wittke W., Herth W., Camilleri C., Hofte H., Plazinski J., Birch R., Cork A., Glover J., Redmond J.and Williamson R.E.1998.Molecular analysis of cellulose biosynthesis in Arabidopsis. Science 279: 717–720.Google Scholar
  3. Bhattacharya D., Weber K., An S.S.and Berning-Koch W. 1998.Actin phylogeny identifies Mesostigma viride as a flagellate ancestor of the land plants.J.Mol.Evol.47:544–550.Google Scholar
  4. Blanton R.L., Fuller D., Iranfar N., Grimson M.J.and Loomis W.F.2000.The cellulose synthase gene of Dictyostelium. Proc.Natl.Acad.Sci.USA 97:2391–2396.Google Scholar
  5. Brown R.M.Jr.1990.Algae as tools in studying the biosynthesis of cellulose,nature 's most abundant macromolecule.In:Wiessner W., Robinson D.G.and Starr R.C.(eds), Experimental Phycology.Cell Walls and Surfaces,Reproduction,Photosynthesis.Springer-Verlag, Berlin,Germany, pp.20–39.Google Scholar
  6. Brown R.M.Jr., Haigler C.H., Suttie J., White A.R., Roberts E., Smith C., Itoh T.and Cooper K.1983.The biosynthesis and degradation of cellulose.J.Appl.Polymer Sci.37:33–78.Google Scholar
  7. Brown R.M.Jr., Willison J.H.M.and Richardson C.L.1976. Cellulose biosynthesis in Acetobacter xylinum:visualization of the site of synthesis and direct measurement of the in vivo process.Proc.Natl.Acad.Sci.USA 73:4565–4569.Google Scholar
  8. Burge C.and Karlin S.1997.Prediction of complete gene structures in human genomic DNA.J.Mol.Biol.268:78–94.Google Scholar
  9. 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.Google Scholar
  10. Burton R.A., Shirley N.J., King B.J., Harvey A.J.and Fincher G.B.2004.The CesA gene family of barley.Quantitative analysis of transcripts reveals two groups of co-expressed genes.Plant Physiol.134:224–236.Google Scholar
  11. Carlquist S.and Schneider E.L.2001.Vessels in ferns:struc-tural,ecological,and evolutionary signi cance.Am.J.Bot. 88:1–13.Google Scholar
  12. Cutler S.and Somerville C.1997.Cellulose synthesis:cloning in silico.Curr.Biol.7: R108–R111.Google Scholar
  13. Delmer D.P.1999.Cellulose biosynthesis:exciting times for a difficult field of study.Annu.Rev.Plant Physiol.Plant Mol. Biol.50:245–276.Google Scholar
  14. Desprez T., Vernhettes S., Fagard M., Refregier G., Desnos T., Aletti E., Py N., Pelletier S.and Hofte H.2002.Resistance against herbicide isoxaben and cellulose de ciency caused by distinct mutations in same cellulose synthase isoform CESA6. Plant Physiol.128:482–490.Google Scholar
  15. Dhugga K.S., Barreiro R., Whitten B., Stecca K., Hazebroek J., Randhawa G.S., Dolan M., Kinney A.J., Tomes D., Nichols S.and Anderson P.2004.Guar seed b mannan synthase is a member of the cellulose synthase super gene family.Science 303:363–366.Google Scholar
  16. Doblin M.S., De Melis L., Newbigin E., Bacic A.and Read S.M.2001.Pollen tubes of Nicotiana alata express two genes from different b glucan synthase families.Plant Physiol.125: 2040–2052.Google Scholar
  17. Doblin M.S., Kurek I., Jacob-Wilk D.and Delmer D.P.2002. Cellulose biosynthesis in plants:from genes to rosettes.Plant Cell Physiol.43:1407–1420.Google Scholar
  18. Emons A.M.C., Derksen J.and Sassen M.M.A.1992.Do microtubules orient plant cell wall micro brils?Physiol.Plant 84:486–493.Google Scholar
  19. Fagard M., Desnos T., Desprez T., Goubet F., Refregier G., Mouille G., McCann M., Rayon C., Vernhettes S.and Hofte H.2000.PROCUSTE1 encodes a cellulose synthase required for normal cell elongation specifically in roots and dark-grown hypocotyls of Arabidopsis. Plant Cell 12:2409–2423.Google Scholar
  20. Favery B., Ryan E., Foreman J., Linstead P., Boudonck K., Steer M., Shaw P.and Dolan L.2001.KOJAK encodes a cellulose synthase-like protein required for root hair cell morphogenesis in Arabidopsis.Genes Dev.15:79–89.Google Scholar
  21. Foster A.S.and Gifford E.M.Jr.1974.Comparative Morphology of Vascular Plants. W.H. Freeman,San Francisco, CA, 751 pp.Google Scholar
  22. Friedman W.E.and Cook M.E.2000.The origin and early evolution of tracheids in vascular plants:integration of pal-aeobotanical and neobotanical data.Phil.Trans.R.Soc. Lond.B 355:857–868.Google Scholar
  23. Gardiner J.C., Taylor N.G.and Turner S.R.2003.Control of cellulose synthase complex localization in developing xylem. Plant Cell 15:1740–1748.Google Scholar
  24. Giddings T.H.Jr., Brower D.L.and Staehelin L.A.1980. Visualization of particle complexes in the plasma membrane of Micrasterias denticulate associated with the formation of cellulose brils in primary and secondary cell walls.J.Cell Biol.84:327–339.Google Scholar
  25. Graham L.E., Cook M.E.and Busse J.S.2000.The origin of plants:Body plan changes contributing to a major evolutionary radiation.Proc.Natl.Acad.Sci.USA 97:4535–4540.Google Scholar
  26. Grimson M.J., Haigler C.H.and Blanton R.L.1996.Cellulose micro brils,cell motility,and plasma membrane protein organization change in parallel during culmination in Dictyostelium discoideum. J.Cell Sci.109:3079–3087.Google Scholar
  27. Ha M.-A., Apperley D.C., Evans B.W., Huxham I.M., Jardine W.G., Vietor R.J., Reis D., Vian B.and Jarvis M.C.1998. Fine structure in cellulose micro brils:NMR evidence from onion and quince.Plant J.16:183–190.Google Scholar
  28. Haigler C.H.1991.Relationship between polymerization and crystallization in micro bril biogenesis.In:Haigler C.H.and Weimer P.J.(eds),Biosynthesis and Biodegradation of Cellulose.Marcel Dekker Inc., New York,pp.99–124.Google Scholar
  29. Haigler C.H.and 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: 111–120.Google Scholar
  30. Haigler C.H., Brown R.M.Jr.and Benziman M.1980.Calcofluor white ST alters the in vivo assembly of cellulose mi-cro brils.Science 210:903–906.Google Scholar
  31. Hall B.G.2001.Phylogenetic Trees Made Easy.Sinauer Associates Inc., Sunderland,MA,179 pp.Google Scholar
  32. Harrison P.M.and Gerstein M.2002.Studying genomes through the aeons:protein families,pseudogenes and prote-ome evolution.J.Mol.Biol.318:1155–1174.Google Scholar
  33. Hebant C.1977.The Conducting Tissues of Bryophytes. J.Cramer,Vaduz,Liechtenstein,157 pp.Google Scholar
  34. Hebsgaard S.M., Korning P.G., Tolstrup N., Engelbrecht J., Rouze P.and Brunak S.1996.Splice site prediction in Arabidopsis thaliana pre-mRNA by combining local and global sequence information.Nucl.Acids Res.24:3439–3452.Google Scholar
  35. Henschel K., Kofuji R., Hasebe M., Saedler H., Munster T.and Theissen G.2002.Two ancient classes of MIKC-type MADS-box genes are present in the moss Physcomitrella patens. Mol.Biol.Evol.19: 801–814.Google Scholar
  36. Hepler P.K.1981.Morphogenesis of tracheary elements and guard cells.In:Kiermayer O.(ed.),Cytomorphogenesis in Plants.Springer-Verlag, Berlin,Germany,pp.327–347.Google Scholar
  37. Herth W.1983.Arrays of plasma-membrane 'rosettes 'involved in cellulose micro bril formation of Spirogyra. Planta 159: 347–356.Google Scholar
  38. Herth W.1985.Plasma-membrane rosettes involved in localized wall thickening during xylem vessel formation of Lepidium sativum L.Planta 164:12–21.Google Scholar
  39. Hickok L.G., Warne T.R.and Fribourg R.S.1995.The biology of the fern Ceratopteris and its use as a model system.Int.J. Plant Sci.156:332–345.Google Scholar
  40. Holland N., Holland D., Helentjaris T., Dhugga K.S., Xoco-nostle-Cazares B.and Delmer D.P.2000.A comparative analysis of the plant cellulose synthase (CesA)gene family. Plant Physiol.123:1313–1323.Google Scholar
  41. Hotchkiss A.T.1989a.Evolution of the cellulosic cell wall in the Charophyceae.In:Schuerch C.(ed.),Cellulose and Wood-Chemistry and Technology.Wiley, New York,pp.591–609.Google Scholar
  42. Hotchkiss A.T.Jr.1989b.Cellulose biosynthesis:the terminal complex hypothesis and its relationship to other contempo-rary research topics.In:Lewis N.G.and Paice M.G.(eds), Plant Cell Wall Polymers.Biogenesis and Biodegradation. American Chemical Society, Washington,DC,pp.232–247.Google Scholar
  43. Ingold E., Munetaka S.and Komamine A.1988.Secondary cell wall formation:changes in cell wall constituents during the differentiation of isolated mesophyll cells of Zinnia elegans to tracheary elements.Plant Cell Physiol.29:295–303.Google Scholar
  44. Itoh T.1990.Cellulose synthesizing complexes in some giant marine algae.J.Cell Sci.95:309–319.Google Scholar
  45. Itoh T.and Brown R.M.Jr.1984.The assembly of cellulose micro brils in Valonia macrophysa Ku ¨tz.Planta 160:372–381.Google Scholar
  46. Karol K.G., McCourt R.M., Cimino M.T.and Delwiche C.F. 2001.The closest living relatives of land plants.Science 294: 2351–2353.Google Scholar
  47. Kendrick P.and Crane P.R.1991.Water-conducting cells in early fossil land plants:implications for the early evolution of tracheophytes.Bot.Gaz.152:335–356.Google Scholar
  48. Kimura S.and Itoh T.1996.New cellulose synthesizing complexes (terminal complexes)involved in animal cellulose biosynthesis in the tunicate Metandrocarpa uedai. Proto-plasma 194:151–163.Google Scholar
  49. Kimura S., Laosinchai W., Itoh T., Cui X., Linder C.R.and Brown R.M.Jr.1999.Immunogold labeling of rosette terminal cellulose-synthesizing complexes in the vascular plant Vigna angularis. Plant Cell 11:2075–2085.Google Scholar
  50. Knight C.D., Cove D.J., Cuming A.C.and Quatrano R.S. 2002.Moss gene technology.In:Gilmartin P.M.and Bowler C.(eds),Molecular Plant Biology-A Practical Approach. Oxford Press, Oxford,New York,pp.285–301.Google Scholar
  51. Kurek I., Kawagoe Y., Jacob-Wilk D., Doblin M.and Delmer D.P.2002.Dimerization of cotton ber cellulose synthase catalytic subunits occurs via oxidation of the zinc-binding domains.Proc.Natl.Acad.Sci.USA 99: 11109–11114.Google Scholar
  52. Lagarias D.M., Wu S.-H.and Lagarias J.C.1995.Atypical phytochrome gene structure in the green alga Mesotaenium caldariorum. Plant Mol.Biol.29:1127–1142.Google Scholar
  53. Lemieux C., Otis C.and Turmel M.2000.Ancestral chloroplast genome in Mesostigma viride reveals an early branch of green plant evolution.Nature 403:649–652.Google Scholar
  54. Liang X.and Joshi C.P.2004.Molecular cloning of ten distinct hypervariable regions from the cellulose synthase gene superfamily in aspen trees.Tree Physiol.24:543–550.Google Scholar
  55. Ligrone R., Duckett J.G.and Renzaglia K.S.2000.Conducting tissues and phyletic relationships of bryophytes.Phil.Trans. R.Soc.Lond.B 355:795–813.Google Scholar
  56. Ligrone R., Vaughn K.C., Renzaglia K.S., Knox J.P.and Duckett J.G.2002.Diversity in the distribution of polysac-charide and glycoprotein epitopes in the cell walls of bryophytes:new evidence for the multiple evolution of water-conducting cells.New Phytol.156:491–508.Google Scholar
  57. Lukowitz W., Mayer U.and Jurgens G.1996.Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product.Cell 84:61–71.Google Scholar
  58. Martin W., Rujan T., Richly E., Hansen A., Cornelsen S., Lins T., Leister D., Stoebe B., Hasegawa M.and Penny D.2002. Evolutionary analysis of Arabidopsis,cyanobacterial,and chloroplast genomes reveals plastid phylogeny and thousands of of cyanobacterial genes in the nucleus.Proc.Natl.Acad.Sci.USA 99: 12246–12251.Google Scholar
  59. Matthysse A.G., Deschet K., Williams M., Marry M., White A.R.and Smith W.C.2004.A functional cellulose synthase from ascidian epidermis.Proc.Natl.Acad.Sci.USA 101: 986–991.Google Scholar
  60. McCourt R.M.1995.Green algal phylogeny.Tree 10:159–163.Google Scholar
  61. McFadden G.I.2001.Primary and secondary endosymbiosis and the origin of plastids.J.Phycol.37:951–959.Google Scholar
  62. Montezinos D.1982.The role of the plasma membrane in cellulose micro bril assembly.In:Lloyd C.W.(ed.),Plant Growth and Development.Academic Press, London, pp.147–162.Google Scholar
  63. Nakashima K., Yamada L., Satou Y., Azuma J.and Satoh N. 2004.The evolutionary origin of animal cellulose synthase. Dev.Genes Evol.214:81–88.Google Scholar
  64. 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.Google Scholar
  65. Okuda K.2002.Structure and phylogeny of cell coverings.J. Plant Res.115:283–288.Google Scholar
  66. Okuda K.and Brown R.M.Jr.1992.A new putative cellulose-synthesizing complex of Coleochaete scutata. Protoplasma 168:51–63.Google Scholar
  67. Okuda K.and Sekida S.2001.Organization of cellulose-synthesizing terminal complexes.In:Morohoshi N.and Komamine A.(eds),Molecular Breeding of Woody Plants. Elsevier, Amsterdam,The Netherlands,pp.93–100.Google Scholar
  68. Page R.D.M.1996.TREEVIEW:An application to display phylogenetic trees on personal computers.Comput.Appl. Biosci.12:357–358.Google Scholar
  69. Peng L., Kawagoe Y., Hogan P.and Delmer D.2002.Sitos-terol-b glucoside as primer for cellulose synthesis in plants. Science 295:147–150.Google Scholar
  70. Peng L., Xiang F., Roberts E., Kawagoe Y., Greve L.C., Kreuz K.and Delmer D.P.2001.The experimental herbicide CGA 325 '615 inhibits synthesis of crystalline cellulose and causes accumulation of non-crystalline b 1,4-glucan associated with CesA protein.Plant Physiol.126:981–992.Google Scholar
  71. Perrin R.M.2001.Cellulose:how many cellulose synthases to make a plant?Curr.Biol.11:R213–R216.Google Scholar
  72. Poli D., Jacobs M.and Cooke T.J.2003.Auxin regulation of axial growth in bryophytes sporophytes:its potential signi cance for the evolution of early land plants.Am.J.Bot. 90:1405–1415.Google Scholar
  73. Preston R.D.1974.The Physical Biology of Plant Cell Walls. Chapman &Hall, London,491 pp.Google Scholar
  74. Read S.M.and Bacic T.2002.Prime time for cellulose.Science 295:59–60.Google Scholar
  75. Reiss H.D., Schnepf E.and Herth W.1984.The plasma membrane of the Funaria caulonema tip cell:morphology and distribution of particle rosettes,and the kinetics of cel-lulose synthesis.Planta 160:428–435.Google Scholar
  76. Richmond T.2000.Higher plant cellulose synthases.Genome Biol.1:3001.1–3001.6.Google Scholar
  77. Richmond T.A.and Somerville C.R.2000.The cellulose syn-thase superfamily.Plant Physiol.124:495–498.Google Scholar
  78. Richmond T.A.and Somerville C.R.2001.Integrative ap-proaches to determining Csl function.Plant Mol.Biol.47: 131–143.Google Scholar
  79. Roberts A.W., Roberts E.M.and Delmer D.P.2002.Cellulose synthase (CesA)genes from the green alga Mesotaenium caldariorum. Eukaryotic Cell 1:847–855.Google Scholar
  80. Ross P., Mayer R.and Benziman M.1991.Cellulose biosyn-thesis and function in bacteria.Microbiol.Rev.55:35–58.Google Scholar
  81. Sambrook J., Fritsch E.F.and Maniatis R.1989.Molecular Cloning:A Laboratory Manual,2nd edn.Cold Spring Har-bor Laboratory Press, Cold Spring Harbor,NY.Google Scholar
  82. Saxena I.M.and Brown R.M.Jr.1995.Identi cation of a second cellulose synthase gene (acsAII )in Acetobacter xylinum J.Bacteriol.177:5276–5283.Google Scholar
  83. Saxena I.M., Lin F.C.and Brown R.M.Jr.1990.Cloning and sequencing of the cellulose synthase catalytic subunit gene of Acetobacter xylinum. Plant Mol.Biol.15:673–683.Google Scholar
  84. Scheible W.-R., Eshed R., Richmond T., Delmer D.and Somerville C.2001.Modi cations of cellulose synthase con-fer resistance to isoxaben and thiazolidinone herbicides in Arabidopsis Ixr1 mutants.Proc.Natl.Acad.Sci.USA 98: 10079–10084.Google Scholar
  85. Sugiyama J., Harada H., Fujiyoshi Y.and Uyeda N.1985.Lat-tice images from ultrathin sections of cellulose micro brils in the cell wall of Valonia macrophysa Kutz.Planta 166:161–168.Google Scholar
  86. 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.Google Scholar
  87. 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.USA 100:1450–1455.Google Scholar
  88. Taylor N.G., Laurie S.and Turner S.R.2000.Multiple cellulose synthase catalytic subunits are required for cellulose synthesis in Arabidopsis. Plant Cell 12:2529–2539.Google Scholar
  89. Taylor N.G., Scheible W.-R., Cutler S., Somerville C.R.and Turner S.R.1999.The irregular xylem3 locus of Arabidopsis encodes a cellulose synthase required for secondary cell wall synthesis.Plant Cell 11:769–779.Google Scholar
  90. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F. and Higgins D.G. 1997 The CLUSTAL_X windows interface:flexible strategies for multiple sequence alignment aided by quality analysis tools .Nucl.Acids Res. 5:4876–4882.Google Scholar
  91. Tsekos I.1999.The sites of cellulose synthesis in algae:Diver-sity and evolution of cellulose-synthesizing enzyme complexes. J.Phycol.35:635–655.Google Scholar
  92. Turmel M., Otis C.and Lemieux C.2002.The complete mitochondrial DNA sequence of Mesostigma viride identi es this green alga as the earliest green plant divergence and predicts a highly compact mitochondrial genome in the ancestor of all green plants.Mol.Biol.Evol.19: 24–38.Google Scholar
  93. Umeda Y., Hirano A., Ishibashi M., Akiyama H., Onizuka T., Ikeuchi M.and Inoue Y.1999.Cloning of cellulose synthase genes from Acetobacter xylinum JCM 7664:implication of a novel set of cellulose synthase genes.DNA Res.6: 109–115.Google Scholar
  94. Vergara C.E.and Carpita N.C.2001.b D-glycan synthases and the CesA gene family:lessons to be learned from the mixed-linkage (1 3),(1 4)b D-glucan synthase.Plant Mol. Biol.47:145–160.Google Scholar
  95. Wang X., Cnops G., Vanderhaeghen R., De Block S., Van Montagu M.and Van Lijsebettens M.2001.AtCSLD3,a cellulose synthase-like gene important for root hair growth in Arabidopsis.Plant Physiol.126:575–586.Google Scholar
  96. Wong H.C., Fear A.L., Calhoon R.D., Eichinger G.H., Mayer R., Amikam D., Benziman M., Gelfand D.H., Meade J.H., Emerick A.W., Bruner R., Ben-Bassat A.and Tal R.1990. Genetic organization of the cellulose synthase operon in Acetobacter xylinum. Proc.Natl.Acad.Sci.USA 87:8130–8134.Google Scholar
  97. Zogaj X., Nimtz M., Rohde M., Bokranz W.and Romling U. 2001.The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix.Mol.Microbiol. 39:1452–1463.Google Scholar

Copyright information

© Kluwer Academic Publishers 2004

Authors and Affiliations

  • Alison W. Roberts
    • 1
  • Eric Roberts
    • 2
  1. 1.Department of Biological SciencesUniversity of Rhode IslandKingstonUSA (e-mail
  2. 2.Department of Biology and Marine BiologyRoger Williams UniversityBristolUSA

Personalised recommendations