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The mechanism and regulation of cellulose synthesis in primary walls: lessons from cellulose-deficient Arabidopsis mutants

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Abstract

Cellulose-deficient Arabidopsis mutants were identified using FT-IR microspectroscopy. The study of these mutants not only led to the identification of actors in cellulose synthesis, but also provided insights in the organization of the hexameric terminal complex from CESA mutants and identified unsuspected accessory proteins with so far unknown roles in the synthesis and/or assembly of cellulose microfibrils. Finally, mutant analysis established a role for protein glycosylation in cellulose synthesis and provided new perspectives on the developmental regulation of cell wall synthesis and the role that cellulose synthesis plays in the control of cell elongation.

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References

  • 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 

  • Beeckman T., Przemeck G.K., Stamatiou G., Lau R., Terryn N., De Rycke R., Inze D.and Berleth T.2002.Genetic complexity of cellulose synthase a gene function in Arabid-opsis embryogenesis. Plant Physiol.130:1883–1893.

    Google Scholar 

  • Boisson M., Gomord V., Audran C., Berger N., Dubreucq B., Granier F., Lerouge P., Faye L., Caboche M.and Lepiniec L. 2001.Arabidopsis glucosidase I mutants reveal a critical role of N-glycan trimming in seed development. Embo J.20:1010–1019.

    Google Scholar 

  • Burn J.E., Hocart C.H., Birch R.J., Cork A.C.and Williamson R.E.2002a.Functional analysis of the cellulose synthase genes CesA1,CesA2,and CesA3 in Arabidopsis. Plant Physiol.129:797–807.

    Google Scholar 

  • Burn J.E., Hurley U.A., Birch R.J., Arioli T., Cork A.and Williamson R.E.2002b.The cellulose-de cient Arabidopsis mutant rsw3 is defective in a gene encoding a putative glu-cosidase II,an enzyme processing N-glycans during ER quality control. Plant J.32:949–960.

    Google Scholar 

  • Cano-Delgado A., Penfield S., Smith C., Catley M.and Bevan M.2003.Reduced cellulose synthesis invokes ligni cation and defense responses in Arabidopsis thaliana. Plant J.34:351–362.

    Google Scholar 

  • Carpita N.and McCann M.2000.Cell walls.In:Buchanan B.B., Gruissem W.and Jones R.L.(eds),Biochemistry and Molecular Biology of Plants.American Society of Plant Physiologists,Rockville,MD,pp.52–108.

  • Chen L., Carpita N.C., Reiter W.D., Wilson R.H., Jeffries C. and McCann M.C.1998.A rapid method to screen for cell-wall mutants using discriminant analysis of Fourier trans-form infrared spectra. Plant J.16:385–392.

    Google Scholar 

  • Cheng J.C., Lertpiriyapong K., Wang S.and Sung Z.R.2000. The role of the Arabidopsis ELD1 gene in cell development and photomorphogenesis in darkness. Plant Physiol.123:509–520.

    Google Scholar 

  • Desnos T., Orbovic V., Bellini C., Kronenberger J., Caboche M., Traas J.and Hofte H.1996.Procuste1 mutants identify two distinct genetic pathways controlling hypocotyl cell elongation,respectively in dark-and light-grown Arabidopsis seedlings. Development 122:683–693.

    Google Scholar 

  • 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 

  • 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 

  • Ellis C., Karafyllidis I., Wasternack C.and Turner J.G.2002. The Arabidopsis mutant cev1 links cell wall signaling to jasmonate and ethylene responses. Plant Cell 14:1557–1566.

    Google Scholar 

  • Ellis C.and Turner J.G.2001.The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens. Plant Cell 13:1025–1033.

    Google Scholar 

  • 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 speci cally in roots and dark-grown hypocotyls of Arabidopsis. Plant Cell 12:2409–2424.

    Google Scholar 

  • Frank M., Guivarch A., Krupkova E., Lorenz-Meyer I., Chriqui D.and Schmulling T.2002.Tumorous shoot devel-opment (TSD)genes are required for co-ordinated plant shoot development. Plant J.29:73–85.

    Google Scholar 

  • 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 

  • Gendreau E., Traas J., Desnos T., Grandjean O., Caboche M. and Hofte H.1997.Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol.114:295–305.

    Google Scholar 

  • Gillmor C.S., Poindexter P., Lorieau J., Palcic M.M.and Somerville C.2002.a-Glucosidase I is required for cellulose biosynthesis and morphogenesis in Arabidopsis. J.Cell Biol.156:1003–1013.

    Google Scholar 

  • 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 

  • Hauser M.T., Morikami A.and Benfey P.N.1995.Conditional root expansion mutants of Arabidopsis. Development 121:1237–1252.

    Google Scholar 

  • Heim D.R., Roberts J.L., Pike P.D.and Larrinua I.M.1989. Mutation of a locus of Arabidopsis thaliana confers resistance to the herbicide isoxaben. Plant Physiol.90:146–150.

    Google Scholar 

  • Heim D.R., Skomp J.R., Waldron C.and Larrinua I.M.1991. Differential response to isoxaben of cellulose biosynthesis by wild-type and resistance strains of Arabidopsis thaliana. Pestic.Biochem.Physiol.39:93–99.

    Google Scholar 

  • His I., Driouich A., Nicol F., Jauneau A.and Hofte H.2001. Altered pectin composition in primary cell walls of korrigan, a dwarf mutant of Arabidopsis de cient in a membrane-bound endo-1,4-beta-glucanase. Planta 212:348–358.

    Google Scholar 

  • Kragh K.M., Hendriks T., de Jong A.J., Lo Schiavo F., Bucherna N., Hojrup P., Mikkelsen J.D.and de Vries S.C. 1996.Characterization of chitinases able to rescue somatic embryos of the temperature-sensitive carrot variant ts 11. Plant Mol.Biol. 31:631–645.

    Google Scholar 

  • Kurek I., Kawagoe Y., Jacob-Wilk D., Doblin M.and Delmer D.2002.Dimerization of cotton fiber cellulose synthase catalytic subunits occurs via oxidation of the zincbinding domains. Proc.Natl.Acad.Sci.USA 99:11109–11114.

    Google Scholar 

  • Lai Kee Him J., Chanzy H., Muller M., Putaux J.L., Imai T. and Bulone V.2002.In vitro versus in vivo cellulose micro brils from plant primary wall synthases:structural differffences.J.Biol.Chem. 277:36931–36939.

    Google Scholar 

  • Lane D.R., Wiedemeier A., Peng L., Hofte H., Vernhettes S., Desprez T., Hocart C.H., Birch R.J., Baskin T.I., Burn J.E., Arioli T., Betzner A.S.and Williamson R.E.2001.Temper-ature-sensitive alleles of rsw2 link the korrigan endo-1,4-beta-glucanase to cellulose synthesis and cytokinesis in arabidop-sis. Plant Physiol. 126:278–288.

    Google Scholar 

  • Lukowitz W., Nickle T.C., Meinke D.W., Last R.L., Conklin P.L. and Somerville C.R.2001.Arabidopsis cyt1 mutants are de cient in a mannose-1-phosphate guanylyltransferase and point to a requirement of N-linked glycosylation for cellulose biosynthesis. Proc.Natl.Acad.Sci.USA 98:2262–2267.

    Google Scholar 

  • Majira A., Domin M., Grandjean O., Gofron K.and Houba-Herin N.2002.Seedling lethality in Nicotiana plumbaginifolia conferred by Ds transposable element insertion into a plant-speci c gene. Plant Mol.Biol. 50:551–562.

    Google Scholar 

  • Matthysse A.G., Thomas D.L.and White A.R.1995a.Mech-anism of cellulose synthesis in Agrobacterium tumefaciens. J.Bacteriol. 177:1076–1081.

    Google Scholar 

  • Matthysse A.G., White S.and Lightfoot R.1995b.Genes required for cellulose synthesis in Agrobacterium tumefaciens. J.Bacteriol. 177:1069–1075.

    Google Scholar 

  • Molhoj M., Johansen B., Ulvskov P.and Borkhardt B.2001. Expression of a membrane-anchored endo-1,4-beta-glucanase from Brassica napus, orthologous to KOR from Ara-bidopsis thaliana,is inversely correlated to elongation in light-grown plants. Plant Mol.Biol. 45:93–105.

    Google Scholar 

  • Molhoj M., Pagant S.and Hofte H.2002.Towards understand-ing the role of membrane-bound endo-beta-1,4-glucanases in cellulose biosynthesis. Plant Cell Physiol. 43:1399–1406.

    Google Scholar 

  • Mouille G., Robin S., Lecomte M., Pagant S. and Ho¨fte H. 2003.Classi cation and identi cation of Arabidopsis cell wall mutants using Fourier Transform InfraRed (FTIR)micro-spectroscopy. Plant J. 35:393–404.

    Google Scholar 

  • Nickle T.C.and Meinke D.W.1998.A cytokinesis-defective mutant of Arabidopsis (cyt1)characterized by embryonic lethality,incomplete cell walls,and excessive callose accu-mulation. Plant J. 15:321–332.

    Google Scholar 

  • Nicol F., His I., Jauneau A., Vernhettes S., Canut H.and Hofte H.1998.A plasma membrane-bound putative endo-1,4-beta D-glucanase is required for normal wall assembly and cell elongation in Arabidopsis. Embo J. 17:5563–5576.

    Google Scholar 

  • Okamoto-Nakazato A.2002.A brief note on the study of yieldin,a wall-bound protein that regulates the yield thresh-old of the cell wall. J.Plant Res. 115:309–313.

    Google Scholar 

  • Pagant S., Bichet A., Sugimoto K., Lerouxel O., Desprez T., McCann M., Lerouge P., Vernhettes S.and Hofte H.2002. KOBITO1 encodes a novel plasma membrane protein nec-essary for normal synthesis of cellulose during cell expansion in Arabidopsis. Plant Cell 14:2001–2013.

    Google Scholar 

  • Peng L., Hocart C.H., Redmond J.W.and Williamson R.E. 2000.Fractionation of carbohydrates in Arabidopsis root cell walls shows that three radial swelling loci are speci cally involved in cellulose production. Planta 211:406–414.

    Google Scholar 

  • Peng L., Kawagoe Y., Hogan P.and Delmer D.2002.Sitos-terol-beta-glucoside as primer for cellulose synthesis in plants. Science 295:147–150.

    Google Scholar 

  • Refregier G., Pelletier S., Jaillard D.and Ho¨fte H.2004. Interaction between wall deposition and cell elongation in dark-grown hypocotyl cells in Arabidopis. Plant Physiol. 135:959–968.

    Google Scholar 

  • Richmond T.A.and Somerville C.R.2001.Integrative ap-proaches to determining Cs1 function. Plant Mol.Biol. 47:131–143.

    Google Scholar 

  • Robin S., Lecomte M., Höfte H.and Mouille G.2003.A procedure for the clustering of cell wall mutants in the model plant Arabidopsis based on Fourier-Transform InfraRed (FTIR)spectroscopy. J.Appl.Stat. 30(6):669–681.

    Google Scholar 

  • Roudier F., Schindelman G., DeSalle R.and Benfey P.N.2002. The COBRA family of putative GPI-anchored proteins in Arabidopsis.A new fellowship in expansion. Plant Physiol. 130:538–548.

    Google Scholar 

  • Sabba R.P.and Vaughn K.C.1999.Herbicides that inhibit cellulose biosynthesis. Weed Sci. 47:757–763.

    Google Scholar 

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

    Google Scholar 

  • Scheible W.R., Eshed R., Richmond T., Delmer D.and Somerville C.2001.Modi cations of cellulose synthase confer resistance to isoxaben and thiazolidinone herbicides in Ara-bidopsis Ixr1 mutants. Proc.Natl.Acad.Sci.USA 98:10079–10084.

    Google Scholar 

  • Scheible W.R., Fry B., Kochevenko A., Schindelasch D., Zimmerli L., Somerville S., Loria R.and Somerville C.2003. An Arabidopsis mutant resistant to thaxtomin A,a cellulose synthesis inhibitor from Streptomyces species. Plant Cell 15:1781–1794.

    Google Scholar 

  • Schindelman G., Morikami A., Jung J., Baskin T.I., Carpita N.C., Derbyshire P., McCann M.C.and 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. 15:1115–1127.

    Google Scholar 

  • Sene C., McCann M.C., Wilson R.H.and Grinter R.1994. Fourier-Transform Raman and Fourier-Transform Infrared Spectroscopy (An investigation of ve higher plant cell walls and their components). Plant Physiol. 106:1623–1631.

    Google Scholar 

  • Sugimoto K., Williamson R.E.and Wasteneys G.O.2001.Wall architecture in the cellulose-de cient rsw1 mutant of Ara-bidopsis thaliana:micro brils but not microtubules lose their transverse alignment before micro brils become unrecogniz-able in the mitotic and elongation zones of roots. Proto-plasma 215:172–183.

    Google Scholar 

  • 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 

  • van Hengel A.J., Tadesse Z., Immerzeel P., Schols H., van Kammen A.and de Vries S.C.2001.N-acetylglucosamine and glucosamine-containing arabinogalactan proteins con-trol somatic embryogenesis. Plant Physiol. 125:1880–1890.

    Google Scholar 

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

    Google Scholar 

  • Zhong R., Morrison W.H. 3rd., Freshour G.D., Hahn M.G. and Ye Z.H.2003.Expression of a mutant form of cellulose synthase AtCesA7 causes dominant negative e.ect on cellulose biosynthesis. Plant Physiol. 132:786–795.

    Google Scholar 

  • Zuo J., Niu Q.W., Nishizawa N., Wu Y., Kost B.and 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 12:1137–1152.

    Google Scholar 

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Correspondence to Herman Höfte.

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Robert, S., Mouille, G. & Höfte, H. The mechanism and regulation of cellulose synthesis in primary walls: lessons from cellulose-deficient Arabidopsis mutants. Cellulose 11, 351–364 (2004). https://doi.org/10.1023/B:CELL.0000046415.45774.80

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