Summary
Thersw1 mutant ofArabidopsis thaliana has a single amino acid substitution in a putative glycosyl transferase that causes a temperature-dependent reduction in cellulose production. We used recently described methods to examine root growth by surface marker particles, cell wall structure by field emission scanning electron microscopy and microtubule alignment by immunofluorescence after the mutant is transferred to its restrictive temperature. We find that raising the temperature quickly accelerates root elongation in both wild type and mutant, presumably as a result of general metabolic stimulation, but that in the mutant, the rate declines within 7–8 h and elongation almost ceases after 24 h. Radial swelling begins at about 6 h in the mutant and root diameter continues to increase until about 24 h. The normal transverse alignment of microfibrils is severely impaired in the mutant after 8 h, and chemical inhibition of cellulose synthesis by 2,6-dichlorobenzonitrile causes a similar loss of orientation. After 24 h, microfibrils are not clearly visible in the walls of cells that would have been in the mitotic and early-elongation zone of wild-type roots. Changes in older cells are less marked; loss of transverse microfibril orientation occurs without disruption to the transverse orientation of cortical microtubules. The wild type shows none of the changes except for acceleration of elongation, which in its case is sustained. We conclude that microfibril alignment requires the normal functioning of RSW1 and that, in view of the effects of dichlorobenzonitrile, there may be a more general linkage between the rate of cellulose production and its proper alignment.
Similar content being viewed by others
Abbreviations
- DCB:
-
2,6-dichlorobenzonitrile
- REGR:
-
relative elemental growth rate
References
Arioli T, Peng L, Betzner AS, Burn J, Wittke W, Herth W, Camilleri C, Höfte H, Plazinski J, Birch R, Cork A, Glover J, Redmond J, Williamson RE (1998) Molecular analysis of cellulose biosynthesis inArabidopsis. Science 279: 717–720
Baskin TI, Betzner AS, Hoggart R, Cork A, Williamson RE (1992) Root morphology mutants inArabidopsis thaliana. Aust J Plant Physiol 19: 427–437
—, Cork A, Williamson RE, Gorst JR (1995)STUNTED PLANT 1, a gene required for expansion in rapidly elongating but not in dividing cells, and mediating root growth responses to applied cytokinin. Plant Physiol 107: 233–243
—, Meekes HTHM, Liang BM, Sharp RE (1999) Regulation of growth anisotropy in well-watered and water-stressed maize roots II: role of cortical microtubules and cellulose microfibrils. Plant Physiol 119: 681–692
Beemster GTS, Baskin TI (1998) Analysis of cell division and elongation underlying the developmental acceleration of root growth inArabidopsis thaliana. Plant Physiol 116: 1515–1526
Emons AMC, Kieft H (1994) Winding threads around plant cells: applications of the geometrical model for microfibril deposition. Protoplasma 180: 59–69
—, Mulder BM (2000) How the deposition of cellulose microfibrils builds cell wall architecture. Trends Plant Sci 5: 35–40
Fisher DD, Cyr RJ (1998) Extending the microtubule/microfibril paradigm: cellulose synthesis is required for normal cortical microtubule alignment in elongating cells. Plant Physiol 116: 1043–1051
Gendreau E, Traas J, Desnos T, Grandjean O, Caboche M, Höfte H (1997) Cellular basis of hypocotyl growth inArabidopsis thaliana. Plant Physiol 114: 295–305
Gertel ET, Green PB (1977) Cell growth pattern and wall microfibrillar arrangement: experiments withNitella. Plant Physiol 60: 247–254
Giddings TH, Staehelin LA (1991) Microtubule-mediated control of microfibril deposition; a re-examination of the hypothesis. In: Lloyd CW (ed) The cytoskeletal basis of plant growth and form. Academic Press, San Diego, pp 85–100
Green PB (1962) Mechanism of plant cell morphogenesis. Science 138: 1404–1405
Heim DR, Skomp JR, Waldron C, Larrinua IM (1991) Differential response to isoxaben of cellulose biosynthesis by wild-type and resistant strains ofArabidopsis thaliana. Pestic Biochem Physiol 39: 93–99
Herth W (1987) Effects of 2,6-DCB on plasma membrane rosettes of wheat root cells. Naturwissenschaften 74: 556–557
Hogetsu T, Shibaoka H (1978) Effects of colchicine on cell shape and on microfibril arrangement in the cell wall ofClosterium acerosum. Planta 140: 15–18
— —, Shimokoriyama M (1974) Involvement of cellulose synthesis in actions of gibberellin and kinetin on cell expansion: 2,6-dichlorobenzonitrile as a new cellulose-synthesis inhibitor. Plant Cell Physiol 15: 389–393
Marchant HJ, Hines ER (1979) The role of microtubules and cell-wall deposition in elongation of regenerating protoplasts ofMougeotia. Planta 146: 41–48
McCann MC, Wells B, Roberts K (1990) Direct visualization of cross-links in the primary plant cell wall. J Cell Sci 96: 323–334
Mueller SC, Brown RM Jr (1982) The control of cellulose microfibril deposition in the cell wall of higher plants II: freeze fracture microfibril patterns in maize seedling tissues following experimental alteration with colchicine and ethylene. Planta 154: 501–515
Mullen JL, Ishikawa H, Evans ML (1998) Analysis of changes in relative elemental growth rate patterns in the elongation zone ofArabidopsis roots upon gravistimulation. Planta 206: 598–603
Peng L, Hocart CH, Redmond JW, Williamson RE (2000) Fractionation of carbohydrates inArabidopsis root cell walls shows that three radial swelling loci are involved specifically in cellulose production. Planta 211: 406–414
Roberts RM, Butt VS (1967) Patterns of cellulose synthesis in maize root-tips: a chemical and autoradiographic study. Exp Cell Res 46: 495–510
Robinson DG, Quader H (1982) The microtubule-microfibril syndrome. In: Lloyd CW (ed) The cytoskeleton in plant growth and development. Academic Press, New York, pp 109–126
Rudolph U, Gross H, Schnepf E (1989) Investigation of the turnover of the putative cellulose-synthesising particle “rosettes” within the plasma membrane ofFunaria hygrometrica. Protoplasma 148: 57–69
Satiat-Jeunemaitre B (1987) Inhibition of the helicoidal assembly of the cellulose-hemicellulose complex by 2,6-dichlorobenzonitrile (DCB). Biol Cell 59: 89–96
Sugimoto K, Williamson RE, Wasteneys GO (2000) New techniques enable comparative analysis of microtubule orientation, wall texture and growth rate in intact roots ofArabidopsis thaliana. Plant Physiol 124: 1493–1506
Takeda K, Shibaoka H (1981) Effects of gibberellin and colchicine on microfibril arrangement in epidermal cell walls ofVigna angularis Ohwi et Ohashi epicotyls. Planta 151: 393–398
Taylor NG, Scheible W-R, Cutler S, Somerville CR, Turner SR (1999) Theirregular xylem3 locus ofArabidopsis encodes a cellulose synthase required for secondary cell wall synthesis. Plant Cell 11: 769–780
Williamson RE (1991) Orientation of cortical microtubules in interphase plant cells. Int Rev Cytol 129: 135–206
—, Birch R, Baskin TI, Arioli T, Betzner AS, Cork A (2001) Morphology of the cellulose-deficientrsw1 mutant ofArabidopsis thaliana. Protoplasma 215: 116–127
Author information
Authors and Affiliations
Corresponding author
Additional information
Dedicated to Professor Brian E. S. Gunning on the occasion of his 65th birthday
Rights and permissions
About this article
Cite this article
Sugimoto, K., Williamson, R.E. & Wasteneys, G.O. Wall architecture in the cellulose-deficientrsw1 mutant ofArabidopsis thaliana: Microfibrils but not microtubules lose their transverse alignment before microfibrils become unrecognizable in the mitotic and elongation zones of roots. Protoplasma 215, 172–183 (2001). https://doi.org/10.1007/BF01280312
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01280312