Summary
The hypothesis that microtubules align microfibrils, termed the alignment hypothesis, states that there is a causal link between the orientation of cortical microtubules and the orientation of nascent microfibrils. I have assessed the generality of this hypothesis by reviewing what is known about the relation between microtubules and microfibrils in a wide group of examples: in algae of the family Characeae,Closterium acerosum, Oocystis solitaria, and certain genera of green coenocytes and in land plant tip-growing cells, xylem, diffusely growing cells, and protoplasts. The salient features about microfibril alignment to emerge are as follows. Cellulose microfibrils can be aligned by cortical microtubules, thus supporting the alignment hypothesis. Alignment of microfibrils can occur independently of microtubules, showing that an alternative to the alignment hypothesis must exist. Microfibril organization is often random, suggesting that self-assembly is insufficient. Microfibril organization differs on different faces of the same cell, suggesting that microfibrils are aligned locally, not with respect to the entire cell. Nascent microfibrils appear to associate tightly with the plasma membrane. To account for these observations, I present a model that posits alignment to be mediated through binding the nascent microfibril. The model, termed templated incorporation, postulates that the nascent microfibril is incorporated into the cell wall by binding to a scaffold that is oriented; further, the scaffold is built and oriented around either already incorporated microfibrils or plasma membrane proteins, or both. The role of cortical microtubules is to bind and orient components of the scaffold at the plasma membrane. In this way, spatial information to align the microfibrils may come from either the cell wall or the cell interior, and microfibril alignment with and without microtubules are subsets of a single mechanism.
Similar content being viewed by others
References
Abe H, Ohtani J, Fukazawa K (1991) FE-SEM observations on the microfibrillar orientation in the secondary wall of tracheids. IAWA Bull 12: 431–438
— — — (1992) Microfibrillar orientation of the innermost surface of conifer tracheid walls. IAWA Bull 13: 411–417
— — — (1994) A scanning electron microscopic study of changes in microtubule distributions during secondary wall formation in tracheids. IAWA J 15: 185–189
—, Funada R, Imaizumi H, Ohtani J, Fukazawa K (1995a) Dynamic changes in the arrangement of cortical microtubules in conifer tracheids during differentiation. Planta 197: 418–421
— —, Ohtani J, Fukazawa K (1995b) Changes in the arrangement of microtubules and microfibrils in differentiating conifer tracheids during the expansion of cells. Ann Bot 75: 305–310
Abe H, Funada R, Ohtani J, Fukazawa K (1997) Changes in the arrangement of cellulose microfibrils associated with the cessation of cell expansion in tracheids. Trees 11: 328–332
Akashi T, Shibaoka H (1991) Involvement of transmembrane proteins in the association of cortical microtubules with the plasma membrane in tobacco BY-2 cells. J Cell Sci 98: 169–174
—, Kawasaki S, Shibaoka H (1991) Stabilization of cortical microtubules by the cell wall in cultured tobacco cells. Planta 182: 363–369
Apostolakos P, Galatis B (1993) Interphase and preprophase microtubule organization in some polarized cell types of the liverwortMarchantia paleacea Bert. New Phytol 124: 409–421
— —, Panteris E (1991) Microtubules in cell morphogenesis and intercellular space formation inZea mays leaf mesophyll andPilea cadierei epithem. J Plant Physiol 137: 591–601
Barnett JR (1977) Tracheid differentiation inPinus radiata. Wood Sci Technol 11: 83–92
—, Chaffey NJ, Barlow PW (1998) Cortical microtubules and microfibril angle. In: Butterfleld BG (ed) Microfibril angle in wood. University of Canterbury, Christchurch, New Zealand, pp 253–271
Baskin TI, 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
Belford DS, Preston RD (1961) The structure and growth of root hairs. J Exp Bot 12: 157–168
Bergfeld R, Speth V, Schopfer P (1988) Reorientation of microfibrils and microtubules at the outer epidermal wall of maize coleoptiles during auxin-mediated growth. Bot Acta 101: 57–67
Boyd JD (1985) Biophysical control of microfibril orientation in plant cell walls. Nijhoff, Dordrecht
Brower DL, Hepler PK (1976) Microtubules and secondary wall deposition in xylem: the effects of isopropyl N-phenylcarbamate. Protoplasma 87: 91–111
Brown RM Jr (1999) Cellulose structure and biosynthesis. Pure Appl Chem 71: 767–775
—, Willison JHM (1977) Golgi apparatus and plasma membrane involvement in secretion and cell surface deposition, with special emphasis on cellulose biogenesis. In: Brinkley BR, Porter KR (eds) International cell biology 1976–1977. Rockefeller University Press, New York, pp 267–283
Burgess J, Linstead P (1984) Comparison of tracheary element differentiation in intact leaves and isolated mesophyll cells ofZinnia elegans. Micron Microsc Acta 15: 153–160
Chaffey N, Barlow P, Barnett J (1997a) Cortical microtubules rearrange during differentiation of vascular cambial derivatives, microfilaments do not. Trees 11: 333–341
—, Barnett JR, Barlow PW (1997b) Cortical microtubule involvement in bordered pit formation in secondary xylem vessel elements ofAesculus hippocastanum L. (Hippocastanaceae): a correlative study using electron microscopy and indirect immunofluorescence microscopy. Protoplasma 197: 64–75
— — — (1997c) Visualization of the cytoskeleton within the secondary vascular system of hardwood species. J Microsc 187: 77–84
—, Barlow PW, Barnett JR (1998) A seasonal cycle of cell wall structure is accompanied by a cyclical rearrangement of cortical microtubules in fusiform cambial cells within taproots ofAesculus hippocastanum (Hippocastanaceae). New Phytol 139: 623–635
— — — (1999) A cytoskeletal basis for wood formation in angiosperm trees: the involvement of cortical microtubules. Planta 208: 19–30
Colvin JR (1965) The morphology of synthetic polymer films as a guide for interpreting microfibrillar orientation in plant cell walls. Can J Bot 43: 1478–1479
Cyr RJ (1994) Microtubules in plant morphogenesis: role of the cortical array. Annu Rev Cell Biol 10: 153–180
Delmer DP (1999) Cellulose biosynthesis: exciting times for a difficult field of study. Annu Rev Plant Physiol Plant Mol Biol 50: 245–276
Doohan ME, Palevitz BA (1980) Microtubules and coated vesicles in guard-cell protoplasts ofAllium cepa L. Planta 149: 389–401
Eleftheriou EP (1990) Microtubules and sieve plate development in differentiationg protophloem sieve elements ofTriticum aestivum L. J Exp Bot 41: 1507–1515
Emons AMC (1985) Plasma-membrane rosettes in root hairs ofEquisetum hyemale. Planta 163: 350–359
— (1987) The cytoskeleton and secretory vesicles in root hairs ofEquisetum andLimnobium and cytoplasmic streaming in root hairs ofEquisetum. Ann Bot 60: 625–632
— (1989) Helicoidal microfibril deposition in a tip growing cell and microtubule alignment during tip morphogenesis: a dry cleaving and freeze substitution study. Can J Bot 67: 2401–2408
—, van Maaren N (1987) Helicoidal cell wall texture in root hairs. Planta 170: 145–151
—, Mulder BM (1998) The making of the architecture of the plant cell wall: how cells exploit geometry. Proc Natl Acad Sci USA 95: 7215–7219
—, Wolters-Arts AMC, Traas JA, Derksen J (1990) The effect of colchicine on microtubules and microfibrils on root hairs. Acta Bot Neerl 39: 19–27
—, Derksen J, Sassen MMA (1992) Do microtubules orient plant cell wall microfibrils? Physiol Plant 84: 486–493
Evert RF, Deshpande BP (1970) An ultrastructural study of cell division in the cambium. Am J Bot 57: 942–961
Falconer MM, Seagull RW (1985) Xylogenesis in tissue culture: taxol effects on microtubule reorientation and lateral association in differentiating cells. Protoplasma 128: 157–166
— (1986) Xylogenesis in tissue culture II: microtubules, cell shape and secondary wall patterns. Protoplasma 133: 140–148
Farrar JJ, Evert RF (1977) Ultrastructure of cell division in the fusiform cells of the vascular cambium ofRobinia pseudoacacia. Trees 11: 203–215
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
Fujino T, Itoh T (1998) Changes in the three dimensional architecture of the cell wall during lignification of xylem cells inEucalyptus tereticornis. Holzforschung 52: 111–116
Fujita M, Saiki H, Harada H (1974) Electron microscopy of microtubules and cellulose microfibrils in secondary wall formation of poplar tension wood fibers. Mokuzai Gakkaishi 20: 147–156
Fukuda H (1987) A change in tubulin synthesis in the process of tracheary element differentiation and cell division of isolatedZinnia mesophyll cells. Plant Cell Physiol 28: 517–528
—, Kobayashi H (1989) Dynamic organization of the cytoskeleton during tracheary-element differentiation. Dev Growth Differ 31: 9–16
—, Komamine A (1980) Direct evidence for cytodifferentiation of tracheary elements without intervening mitosis in a culture of single cells isolated from the mesophyll ofZinnia elegans. Plant Physiol 65: 61–64
Funada R, Abe H, Furusawa O, Imaizumi H, Fukazawa K, Ohtani J (1997) The orientation and localization of cortical microtubules in differentiating conifer tracheids during cell expansion. Plant Cell Physiol 38: 210–212
Galatis B (1988) Microtubules and epithem-cell morphogenesis in hydathodes ofPilea cadierei. Planta 176: 287–297
Galway ME, Hardham AR (1986) Microtubule reorganization, cell wall synthesis and establishment of the axis of elongation in regenerating protoplasts of the algaMougeotia. Protoplasma 135: 130–143
Giddings TH Jr, Staehelin LA (1988) Spatial relationship between microtubules and plasma-membrane rosettes during the deposition of primary wall microfibrils inClosterium sp. Planta 173: 22–30
— — (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, London, pp 85–99
—, Brower DL, Staehelin LA (1980) Visualization of particle complexes in the plasma membrane ofMicrasterias denticulata associated with the formation of cellulose fibrils in primary and secondary cell walls. J Cell Biol 84: 327–339
Green PB (1958) Structural characteristics of developingNitella internodal cell walls. J Biophys Biochem Cytol 4: 505–516
— (1960) Multinet growth in the cell wall ofNitella. J Biophys Biochem Cytol 7: 289–296
— (1962) Mechanism for plant cellular morphogenesis. Science 138: 1404–1405
— (1963) On mechanisms of elongation. In: Locke M (ed) Cytodifferentiation and macromolecular synthesis. Academic Press, New York, pp 203–234
— (1974) Morphogenesis of the cell and organ axis: biophysical models. Brookhaven Symp Biol 25: 166–190
Grimm I, Sachs H, Robinson DG (1976) Structure, synthesis and orientation of microfibrils II: the effect of colchicine on the wall ofOocystis solitaria. Cytobiologie 14: 61–74
Gunning BES, Hardham AR (1982) Microtubules. Annu Rev Plant Physiol 33: 651–698
Haigler CH, Brown RM Jr (1986) Transport of rosettes from the Golgi apparatus to the plasma membrane in isolated mesophyll cells ofZinnia elegans during differentiation to tracheary elements in suspension culture. Protoplasma 134: 111–120
Harada T, Côté WA Jr (1985) Structure of wood. In: Higuchi T (ed) Biosynthesis and biodegradation of wood components. Academic Press, Orlando, Fla, pp 1–42
Hardham AR, Gunning BES (1979) Interpolation of microtubules into cortical arrays during cell elongation and differentiation in roots ofAzolla pinnata. J Cell Sci 37: 411–442
— — (1980) Some effects of colchicine on microtubules and cell division in roots ofAzolla pinnata. Protoplasma 102: 31–51
—, McCully ME (1982) Reprogramming of cells following wounding in pea (Pisum sativum L.) roots II: the effects of caffeine and colchicine on the development of new vascular elements. Protoplasma 112: 152–166
Hasezawa S, Nozaki H (1999) Role of cortical microtubules in the orientation of cellulose microfibril deposition in higher-plant cells. Protoplasma 209: 98–104
—, Hogetsu T, Syono K (1988) Rearrangement of cortical microtubules in elongating cells derived from tobacco protoplasts: a time-course observation by immunofluorescence microscopy. J Plant Physiol 133: 46–51
— — — (1989) Changes in actin filaments and cellulose fibrils in elongating cells derived from tobacco protoplasts. J Plant Physiol 134: 115–119
Hayano S, Itoh T, Brown RM Jr (1988) Orientation of microtubules during regeneration of cell wall in selected giant marine algae. Plant Cell Physiol 29: 785–793
Heath IB (1974) A unified hypothesis for the role of membrane bound enzyme complexes and microtubules in plant cell wall synthesis. J Theor Biol 48: 445–449
—, Seagull RW (1982) Orientated cellulose fibrils and the cytoskeleton: a critical comparison of models. In: Lloyd CW (ed) The cytoskeleton in plant growth and development. Academic Press, London, pp 163–182
Hepler PK (1981) Morphogenesis of tracheary elements and guard cells. In: Kiermayer O (ed) Cytomorphogenesis in plants. Springer, Wien New York, pp 327–347 (Cell biology monographs, vol 8)
—, Fosket DE (1971) The role of microtubules in vessel member differentiation inColeus. Protoplasma 72: 213–236
—, Palevitz BA (1974) Microtubules and microfilaments. Annu Rev Plant Physiol 25: 309–362
—, Rice RM, Terranova WA (1972) Cytochemical localization of peroxidase activity in wound vessel members ofColeus. Can J Bot 50: 977–983
Herth W (1980) Calcofluor white and congo red inhibit chitin microfibril assembly ofPoterioochromonas: evidence for a gap between polymerization and microfibril formation. J Cell Biol 87: 442–450
— (1985) Plasma-membrane rosettes involved in localized wall thickening during xylem vessel formation inLepidium sativum L. Planta 164: 12–21
— (1989) Inhbitor effects on putative cellulose synthetase complexes of vascular plants. In: Schuerch C (ed) Cellulose and wood: chemistry and technology. Wiley, New York, pp 795–810
Heslop-Harrison J (1968) The emergence of pattern in the cell walls of higher plants. Dev Biol Suppl 2: 118–150
Hirai N, Sonobe S, Hayashi T (1998) In situ synthesis of β-glucan microfibrils on tobacco plasma membrane sheets. Proc Natl Acad Sci USA 95: 15102–15106
Hirakawa Y (1984) A SEM observation of microtubules in xylem cells forming secondary walls of trees. Res Bull Coll Exp For Hokkaido Univ 41: 535–550
—, Ishida S (1981) A SEM study on the layer structure of secondary wall of differentiating tracheids in conifers. Res Bull Coll Exp For Hokkaido Univ 38: 55–71
Hogetsu T (1983) Distribution and local activity of particle complexes synthesizing cellulose microfibrils in the plasma membrane ofClosterium acerosum (Schrank) Ehrenberg. Plant Cell Physiol 24: 777–781
— (1986) Orientation of wall microfibril deposition in root cells ofPisum sativum L. var. Alaska. Plant Cell Physiol 27: 947–951
— (1989) The arrangement of microtubules in leaves of monocotyledonous and dicotyledonous plants. Can J Bot 67: 3506–3512
— (1991) Mechanism for formation of the secondary wall thickening in tracheary elements: microtubules and microfibrils of tracheary elements ofPisum sativum L. andCommelina communis L. and the effects of amiprophosmethyl. Planta 185: 190–200
—, Oshima Y (1985) Immunofluorescence microscopy of microtubule arrangement inClosterium acerosum (Schrank) Ehrenberg. Planta 166: 169–175
— — (1986) Immunofluorescence microscopy of microtubule arrangement in root cells ofPisum sativum L. var Alaska. Plant Cell Physiol 27: 939–945
—, Shibaoka H (1978a) The change of pattern in microfibril arrangement on the inner surface of the cell wall ofClosterium acerosum during cell growth. Planta 140: 7–14
— — (1978b) Effects of colchicine on cell shape and on microfibril arrangement in the cell wall ofClosterium acerosum. Planta 140: 15–18
—, Yokoyama M (1979) Cell expansion and microfibril deposition inClosterium ehrenbergii. Bot Mag Tokyo 92: 299–303
Hoss S, Wernicke W (1995) Microtubules and the establishment of apparent cell wall invaginations in mesophyll cells ofPinus silvestris L. J Plant Physiol 147: 474–476
Hotchkiss AT, Brown RM Jr (1987) The association of rosette and globule terminal complexes with cellulose microfibril assembly inNitella translucens varaxillaris (Charophyceae). J Phycol 23: 229–237
Hush JM, Overall RL (1996) Cortical microtubule reorientation in higher plants: dynamics and regulation. J Microsc 181: 129–139
Inada S, Tominaga M, Shimmen T (2000) Regulation of root growth by gibberellin inLemna minor. Plant Cell Physiol 41: 657–665
Itoh T (1974a) Fine structure of secondary wall thickening and a role of microtubules in primary xylem cells of poplar. Wood Res 54: 48–69
— (1974b) Fine structure and formation of cell wall of developing cotton fiber. Wood Res 56: 49–61
— (1975) Fine structure of the plasmalemma surface of poplar parenchyma cells observed by the freeze etching technique. Bot Mag Tokyo 88: 131–143
— (1976a) Microfibrillar orientation of radially enlarged cells of coumarin- and colchicine-treated pine seedlings. Plant Cell Physiol 17: 385–398
— (1976b) Microscopic and submicroscopic observation of the effects of coumarin and colchicine during elongation of pine seedlings. Plant Cell Physiol 17: 367–384
— (1989) Biogenesis of cellulose microfibrils and the role of microtubules in green algae. In: Lewis NG, Paice MG (eds) Plant cell wall polymers: biosynthesis and degradation. American Chemical Society, Washington, DC, pp 257–277
— (1990) Cellulose synthesizing complexes in some giant marine algae. J Cell Sci 95: 309–319
—, Brown RM Jr (1984) The assembly of cellulose microfibrils inValonia macrophysa Kütz. Planta 160: 372–381
—, Shimaji K (1976) Orientation of microfibrils and microtubules in cortical parenchyma cells of poplar during elongation growth. Bot Mag Tokyo 89: 291–308
Iwata K, Hogetsu T (1988) Arrangement of cortical microtubules inAvena coleoptiles and mesocotyls andPisum epicotyls. Plant Cell Physiol 29: 807–815
— — (1989) Orientation of wall microfibrils inAvena coleoptiles and mesocotyls and inPisum epicotyls. Plant Cell Physiol 30: 749–757
Jung G, Wernicke W (1990) Cell shaping and microtubules in developing mesophyll of wheat (Triticum aestivum L.). Protoplasma 153: 141–148
Kadota A, Wada M (1989) Circular arrangement of cortical F-actin around the subapical region of a tip-growing fern protonemal cell. Plant Cell Physiol 30: 1183–1186
— — (1992a) Reorganization of the cortical cytoskeleton in tip-growing fern protonemal cells during phytochrome-mediated phototropism and blue light-induced apical swelling. Protoplasma 166: 35–41
— — (1992b) The circular arrangement of cortical microtubules around the subapex of tip-growing fern protonemata is sensitive to cytochalasin b. Plant Cell Physiol 33: 99–102
Kagawa T, Kadota A, Wada M (1992) The junction between the plasma membrane and the cell wall in fern protonemal cells, as visualized after plasmolysis, and its dependence on arrays of cortical microtubules. Protoplasma 170: 186–190
Kakimoto T, Shibaoka H (1986) Calcium-sensitivity of cortical microtubules in the green algaMougeotia. Plant Cell Physiol 27: 91–101
Karyophyllis D, Katsaros C, Galatis B (2000) F-actin involvement in apical cell morphogenesis ofSphacelaria rigidula (Phaeophyceae): mutual alignment between cortical actin filaments and cellulose microfibrils. Eur J Phycol 35: 195–203
Kataofca Y, Saiki H, Fujita M (1992) Arrangement and superimposition of cellulose microfibrils in the secondary walls of coniferous tracheids. Mokuzai Gakkaishi 38: 327–335
Kengen HMP, de Graaf BHJ (1991) Microtubules and actin filaments co-localize extensively in non-fixed cells of tobacco. Protoplasma 163: 62–65
—, Derksen J (1991) Organization of microtubules and microfilaments in protoplasts from suspension cells ofNicotiana plumbaginifolia: a quantitative analysis. Acta Bot Neerl 40: 29–40
Kiermayer O (1968) The distribution of microtubules in differentiating cells ofMicrasterias denticulata Bréb. Planta 83: 223–236
— (1981) Cytoplasmic basis of morphogenesis in Micrasterias. In: Kiermayer O (ed) Cytomorphogenesis in plants. Springer, Wien New York, pp 147–189 (Cell biology monographs, vol 8)
—, Fedtke C (1977) Strong anti-microtubule action of amiprophosmethyl (APM) inMicrasterias. Protoplasma 92: 163–166
—, Sleyter UB (1979) Hexagonally ordered “rosettes” of particles in the plasma membrane ofMicrasterias denticulata Bréb and their significance for microfibril formation and orientation. Protoplasma 101: 133–138
Kimura S, Mizuta S (1994) Role of the microtubular cytoskeleton in alternating changes in cellulose-microfibril orientation in the coenocytic green alga,Chaetomorpha moniligera. Planta 193: 21–31
Kishi K, Harada H, Saiki H (1981) The structure of the primary wall of vessels in hardwoods. Nihon Zairyo Gakkai 30: 673–678 (in Japanese with English abstract and figure captions)
Klein AS, Montezinos D, Delmer DP (1981) Cellulose and 1,3-glucan synthesis during the early stages of wall regeneration in soybean protoplasts. Planta 152: 105–114
Kobayashi H, Fukuda H, Shibaoka H (1987) Reorganization of actin filaments associated with the differentiation of tracheary elements inZinnia mesophyll cells. Protoplasma 138: 69–71
— — — (1988) Interrelation between the spatial disposition of actin filaments and microtubules during the differentiation of tracheary elements in culturedZinnia cells. Protoplasma 143: 29–37
Lang JM, Eisinger WR, Green PB (1982) Effects of ethylene on the orientation of microtubules and cellulose microfibrils of pea epicotyl cells with polylamellate cell walls. Protoplasma 110: 5–14
Ledbetter MC, Porter KR (1963) A “microtubule” in plant cell fine structure. J Cell Biol 19: 239–250
Lloyd CW, Wells B (1985) Microtubules are at the tips of root hairs and form helical patterns corresponding to inner wall fibrils. J Cell Sci 75: 225–238
—, Slabas AR, Powell AJ, Lowe SB (1980) Microtubules, protoplasts and plant cell shape: an immunofluorescent study. Planta 147: 500–506
Marchant HJ (1978) Microtubules associated with the plasma membrane isolated from the protoplasts of the green algaMougeotia. Exp Cell Res 115: 25–30
—, Hines ER (1979) The role of microtubules and cell-wall deposition in elongation of regeneration protoplasts ofMougeotia. Planta 146: 41–48
Melan MA (1990) Taxol maintains organized microtubule patterns in protoplasts which lead to the resynthesis of organized cell wall microfibrils. Protoplasma 153: 169–177
Mineyuki Y, Palevitz BA (1990) Relationship between preprophase band organization, f-actin and the division site inAllium: fluorescence and morphometric studies on cytochalasin-treated cells. J Cell Sci 97: 283–295
Mizuta S, Okuda K (1987a) A comparative study of cellulose synthesizing complexes in certain cladophoralean and siphonocladalean algae. Bot Mar 30: 205–215
— — (1987b)Boodlea cell wall microfibril orientation unrelated to cortical microtubule arrangement. Bot Gaz 148: 297–307
—, Wada S (1981) Microfibrillar structure of growing cell wall in coenocytic green alga,Boergesenia forbesii. Bot Mag Tokyo 94: 343–353
— — (1982) Effects of light and inhibitors on polylamellation and shift of microfibril orientation inBoergesenia cell wall. Plant Cell Physiol 23: 257–264
—, Sawada K, Okuda K (1985) Cell wall regeneration of new spherical cells developed from the protoplasm of a coenocytic green alga,Boergesenia forbesii. Jpn J Phycol 33: 32–44
—, Kurogi U, Okuda K, Brown RM Jr (1989) Microfibrillar structure, cortical microtubule arrangement and the effect of amiprophosmethyl on microfibril orientation in the thallus cells of the filamentous green alga,Chamaedoris orientalis. Ann Bot 64: 383–394
—, Katoh S, Harada T, Yamada H, Okuda K, Morinaga T (1991) Involvement of cytoskeletal microtubules in microfibrillar patterns in the cell walls of the developing coenocytic green alga,Boodlea coacta. Bot Mar 34: 417–424
—, Kaneko M, Kimura S, Okuda K (1994a) Experimental studies on the stability of the cortical microtubule cytoskeleton in relation to polarity and cell elongation in the coenocytic green alga,Chaetomorpha moniligera. Ann Bot 73: 273–280
—, Watanabe A, Kimura S, Yoshida K (1994b) Possible involvement of membrane fluidity in helicoidal microfibrillar orientation in the coenocytic green alga,Boergesenia forbesii. Protoplasma 180: 82–91
—, Tsuji T, Morinaga T, Tsurumi S (1995) Structure and assembly of the cortical microtubule cytoskeleton in the green alga,Boodlea coacta. Protoplasma 189: 113–122
Montezinos D (1982) A cytological model of cellulose biogenesis in the algaOocystis apiculata. In: Brown RM Jr (ed) Cellulose and other natural polymer systems: biogenesis, structure, and degradation. Plenum, New York, pp 3–21
—, Brown RM Jr (1976) Surface architecture of the plant cell: biogenesis of the cell wall, with special emphasis on the role of the plasma membrane in cellulose biosynthesis. J Supramol Struct 5: 277–290
— — (1979) Cell wall biogenesis inOocystis: experimental alteration of microfibril assembly and orientation. Cytobios 23: 119–139
Mueller SC, Brown RM Jr (1982a) The control of cellulose microfibril deposition in the cell wall of higher plants I: can directed membrane flow orient cellulose microfibrils? Indirect evidence from freeze-fractured plasma membranes of maize and pine seedlings. Planta 154: 489–500
— — (1982b) 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
Murata T, Wada M (1989a) Effects of colchicine and amiprophosmethyl on microfibril arrangement and cell shape inAdiantum protonemal cells. Protoplasma 151: 81–87
— — (1989b) Organization of cortical microtubules and microfibril deposition in response to blue-light-induced apical swelling in a tip-growingAdiantum protonema cell. Planta 178: 334–341
—, Kadota A, Hogetsu T, Wada M (1987) Circular arrangement of cortical microtubules around the subapical part of a tip-growing fern protonema. Protoplasma 141: 135–138
Nakashima J, Mizuno T, Takabe K, Fugita M, Saiki H (1997) Direct visualization of lignifying secondary wall thickenings inZinnia elegans cell in culture. Plant Cell Physiol 38: 818–827
Nelmes BJ, Preston RD, Ashworth D (1973) A possible function of microtubules suggested by their abnormal distribution in rubbery wood. J Cell Sci 13: 741–751
Neville AC (1993) Biology of fibrous composites. Cambridge University Press, Cambridge
—, Levy S (1984) Helicoidal orientation of cellulose microfibrils inNitella opaca internode cells: ultrastructure and computed theoretical effects of strain reorientation during wall growth. Planta 162: 370–384
Newcomb EH (1969) Plant microtubules. Annu Rev Plant Physiol 20: 253–288
—, Bonnett HT Jr (1965) Cytoplasmic microtubule and wall microfibril orientation in root hairs of radish. J Cell Biol. 27: 575–589
Northcote DH, Davey R, Lay J (1989) Use of antisera to localize callose, xylan and arabinogalactan in the cell plate, primary and secondary cell walls of plant cells. Planta 178: 353–366
Okuda K, Mizuta S (1985) Analysis of cellulose microfibril arrangement patterns in the cell wall of new spherical cells regenerated fromBoodlea coacta (Chlorophyceae). Jpn J Phycol 33: 301–311
— — (1987) Modification in cell shape unrelated to cellulose microfibril orientation in growing thallus cells ofChaetomorpha moniligera. Plant Cell Physiol 28: 461–473
—, Matsuo K, Mizuta S (1990) Characteristics of the deposition of microfibrils during formation of the polylamellate walls in the coenocytic green alga,Chamaedoris orientalis. Plant Cell Physiol 31: 357–364
— — — (1993) The meridional arrangement of cortical microtubules defines the site of tip growth in the coenocytic green alga,Chamaedoris orientalis. Bot Mar 36: 53–62
Oparka KJ (1994) Plasmolysis: new insights into an old process. New Phytol 126: 571–591
Panteris E, Apostolakos P, Galatis B (1993a) Microtubule organization, mesophyll cell morphogenesis, and intercellular space formation inAdiantum capillus-veneris leaflets. Protoplasma 172: 97–110
— — — (1993b) Microtubules and morphogenesis in ordinary epidermal cells ofVigna sinensis leaves. Propoplasma 174: 91–100
— — — (1994) Sinuous ordinary epidermal cells: behind several patterns of waviness, a common morphogenetic mechanism. New Phytol 127: 771–780
Pickett-Heaps JD (1967) The effects of colchicine on the ultrastructure of dividing plant cells, xylem wall differentation and distribution of cytoplasmic microtubules. Dev Biol 15: 206–236
Preston RD (1988) Cellulose-microfibril-orienting mechanisms in plant cells walls. Planta 174: 67–74
Probine MC (1963) Cell growth and the structure and mechanical properties of the wall in internodal cells ofNitella opaca III: spiral growth and cell wall structure. J Exp Bot 14: 101–113
—, Barber NF (1966) The structure and plastic properties of the cell wall ofNitella in relation to extension growth. Aust J Biol Sci 19: 439–457
—, Preston RD (1961) Cell growth and the structure and mechanical properties of the wall in internodal cells ofNitella opaca I: wall structure and growth. J Exp Bot 12: 261–282
Prodhan AKMA, Funada R, Ohtani J, Abe H, Fukazawa K (1995a) Orientation of microfibrils and microtubules in developing tension-wood fibers of Japanese ash (Fraxinus mandshurica var. japonica). Planta 196: 577–585
—, Ohtani J, Funada R, Abe H, Fukazawa K (1995b) Ultrastructural investigation of tension wood fiber inFraxinus mandshurica Rupr. var. japonica maxim. Ann Bot 75: 311–317
Quader H (1986) Cellulose microfibril orientation inOocystis solitaria: proof that microtubules control the alignment of terminal complexes. J Cell Sci 83: 223–234
—, Robinson DG (1979) Structure, synthesis, and orientation of microfibrils VI: the role of ions in microfibril deposition inOocystis solitaria. Eur J Cell Biol 20: 51–56
—, Deichgräber G, Schnepf E (1986) The cytoskeleton ofCobaea seed hairs: patterning during cell-wall differentiation. Planta 168: 1–10
Richmond PA (1983) Patterns of cellulose microfibril deposition and rearrangement inNitella: in vivo analysis by a birefringence index. J Appl Polymer Sci Appl Polymer Symp 37: 107–122
Robards AW, Humpherson PG (1967) Microtubules and angiosperm bordered pit formation. Planta 77: 233–238
—, Kidwai P (1972) Microtubules and microfibrils in xylem fibers during secondary wall formation. Cytobiologie 6: 1–21
Roberts K, Burgess J, Roberts I, Linstead P (1985) Microtubule rearrangement during plant cell growth and development: an immunofluorescent study. In: Robards AW (ed) Botanical microscopy 1985. Oxford University Press, Oxford, pp 263–283
Roberts LW, Baba S (1968) IAA-induced xylem differentiation in the presence of colchicine. Plant Cell Physiol 9: 315–321
Robinson DG (1977a) Plant cell wall synthesis. Adv Bot Res 5: 89–151
—, (1977b) Structure, synthesis, and orientation of microfibrils IV: microtubules and microfibrils inGlaucocystis. Cytobiologie 15: 475–484
—, Quader H (1981) Structure, synthesis, and orientation of microfibrils IX: a freeze-fracture investigation of theOocystis plasma membrane after inhibitor treatment. Eur J Cell Biol 25: 278–228
— — (1982) The microtubule-microfibril syndrome. In: Lloyd CW (ed) The cytoskeleton in plant growth and development. Academic Press, London, pp 109–126
—, White RK, Preston RD (1972) Fine structure of swarmers ofCladophora andChaetomorpha III: wall synthesis and development. Planta 107: 131–144
Roland JC, Mosiniak M (1983) On the twisting pattern, texture and layering of the secondary cell walls of lime wood: proposal of an unifying model. IAWA Bull 4: 15–26
—, Vian B (1979) The wall of the growing plant cell: its three dimensional organization. Int Rev Cytol 61: 129–166
Savidge RA, Barnett JR (1993) Protoplasmic changes in cambial cells induced by a tracheid-differentiation factor from pine needles. J Exp Bot 44: 395–405
Sachs H, Grimm I, Robinson DG (1976) Structure, synthesis and orientation of microfibrils I: architecture and development of the wall ofOocystis solitaria. Cytobiologie 14: 49–60
Sakaguchi S, Hogetsu T, Kara N (1988) Arrangement of cortical microtubules in the shoot apex ofVinca major L. Planta 175: 403–411
Sako Y, Nagafuchi A, Tsukita S, Takeichi M, Kusumi A (1998) Cytoplasmic regulation of the movement of e-cadherin on the free cell surface as studied by optical tweezers and single particle tracking: corralling and tethering by the membrane skeleton. J Cell Biol 140: 1227–1240
Sassen MMA, Wolters-Arts AMC (1986) Cell wall texture and cortical microtubules in growing staminal hairs ofTradescantia virginiana. Acta Bot Neerl 35: 351–360
— — (1992) Cell-wall texture in shoot apex cells. Acta Bot Neerl 41: 25–29
—, Pluymaekers HJ, Meekes HTHM, de Jong-Emons AMC (1981) Cell wall texture in root hairs. In: Robinson DG, Quader H (eds) Cell walls 81. Wissenschaftliche Verlagsgesellschaft, Stuttgart, pp 189–197
—, Traas JA, Wolters-Arts AMC (1985) Deposition of cellulose microfibrils in cell walls of root hairs. Eur J Cell Biol 37: 21–26
Satiat-Jeunemaitre B (1984) Experimental modifications of the twisting and rhythmic pattern in the cell walls of maize coleoptile. Biol Cell 51: 373–380
— (1987) Inhibition of the helicoidal assembly of the cellulose-hemicellulose complex by 2,6-dichlorobenzonitrile (DCB). Biol Cell 59: 89–96
Sauter M, Seagull RW, Kende H (1993) Internodal elongation and orientation of cellulose microfibrils and microtubules in deepwater rice. Planta 190: 354–362
Sawhney VK, Srivastava LM (1975) Wall fibrils and microtubules in normal and gibberellic-acid-induced growth of lettuce hypocotyl cells. Can J Bot 53: 824–835
Schmid VHR, Meindl U (1992) Microtubules do not control orientation of secondary cell wall microfibril deposition inMicrasterias. Protoplasma 169: 148–154
Schneider B, Herth W (1986) Distribution of plasma membrane rosettes and kinetics of cellulose formation in xylem development of higher plants. Protoplasma 131: 142–152
Schnepf E (1974) Microtubules and cell wall formation. Portugal Acta Biol Ser A 14: 451–461
—, Deichgräber G (1983a) Structure and formation of fibrillar mucilages in seed epidermis cells I:Collomia grandiflora (Polimoniaceae). Protoplasma 114: 210–221
—, Deichgraber G (1983b) Structure and formation of fibrillar mucilages in seed epidermis cells II:Ruellia (Acanthaceae). Protoplasma 114: 222–234
Seagull RW (1983) The role of the cytoskeleton during oriented microfibril deposition I: elucidation of the possible interaction between microtubules and cellulose synthetic complexes. J Ultrastruct Res 83: 168–175
— (1986) Changes in microtubule organization and wall microfibril orientation during in vitro cotton fiber development: an immunofluorescent study. Can J Bot 64: 1373–1381
— (1989) The role of the cytoskeleton during oriented microfibril deposition II: microfibril deposition in cells with disrupted cytoskeletons. In: Schuerch C (ed) Cellulose and wood: chemistry and technology. Wiley, New York, pp 811–825
— (1990) The effects of microtubule and microfilament disrupting agents on cytoskeletal arrays and wall deposition in developing cotton fibers. Protoplasma 159: 44–59
— (1992) A quantitative electron microscopic study of changes in microtubule arrays and wall microfibril orientation during in vitro cotton fiber development. J Cell Sci 101: 561–577
—, Falconer MM (1991) In vitro xylogenesis. In: Lloyd CW (ed) The cytoskeletal basis of plant growth and form. Academic, London, pp 183–194
—, Heath IB (1980) The organization of cortical microtubule arrays in the radish root hair. Protoplasma 103: 205–229
Sellen DB (1980) The mechanical properties of plant cell walls. In: Vincent JFV, Currey JD (eds) The mechanical properties of biological materials. Cambridge University Press, Cambridge, pp 315–329
Shibaoka H (1994) Plant hormone-induced changes in the orientation of cortical microtubules: alterations in the cross-linking between microtubules and the plasma membrane. Annu Rev Plant Physiol Plant Mol Biol 45: 527–544
Simmonds DH, Setterfield (1986) Aberrant microtubule organization can result in genetic abnormalities in protoplast cultures ofVicia hajastana Grossh. Planta 167: 460–468
Smith-Huerta NL, Jernstedt JA (1989) Root contraction in hyacinth III: orientation of cortical microtubules visualized by immunofluorescence microscopy. Protoplasma 151: 1–10
— — (1990) Root contraction in hyacinth IV: orientation of cellulose microfibrils in radial longitudinal and transverse cell walls. Protoplasma 154: 161–171
Srivastava LM, Sawhney VK, Bonettmaker M (1977) Cell growth, wall deposition, and correlated fine structure of colchicine-treated lettuce hypocotyl cells. Can J Bot 55: 902–917
Suzuki K, Ingold E, Sugiyama M, Fukuda H, Komamine A (1992) Effects of 2,6-dichlorobenzonitrile on differentiation to tracheary elements of isolated mesophyll cells ofZinnia elegans and formation of secondary cell walls. Physiol Plant 86: 43–48
—, Itoh T, Sasamoto H (1998) Cell wall architecture prerequisite for the cell division in the protoplasts of white poplar,Populus alba L. Plant Cell Physiol 39: 632–638
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 JG, Owen POJ, Koonce LT, Haigler CH (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
Traas JA, Derksen J (1988) Microtubules and cellulose microfibrils in plant cells: simultaneous demonstration in dry cleave preparations. Eur J Cell Biol 48: 159–164
—, Braat P, Emons AMC, Meekes H, Derksen J (1985) Microtubules in root hairs. J Cell Sci 76: 303–320
Uehara K, Hogetsu T (1993) Arrangement of cortical microtubules during formation of bordered pit in the tracheids ofTaxus. Protoplasma 172: 145–153
van Amstel ANM, Derksen J (1993) The complex helical texture of the secondary cell wall ofUtrica dioica is not controlled by microtubules: a quantitative analysis. Acta Bot Neerl 42: 141–151
—, Kengen HMP (1996) Callose deposition in the primary wall of suspension cells and regenerating protoplasts, and its relationship to patterned cellulose synthesis. Can J Bot 74: 1040–1049
van der Valk P, Rennie PJ, Connolly JA, Fowke LC (1980) Distribution of cortical microtubules on tobacco protoplasts: an immunofluorescence microscopic and ultrastructural study. Protoplasma 105: 27–43
Vian B, Mosiniak M, Reis D, Roland J-C (1982) Dissipative process and experimental retardation of the twisting in the growing plant cell wall. Effect of ethylene-generating agent and colchicine: a morphogenetic revaluation. Biol Cell 46: 301–310
Wada M, Murata T, Shibata M (1990a) Changes in microtubule and microfibril arrangement during polarotropism inAdiantum protonemata. Bot Mag Tokyo 103: 391–401
— —, Shimuzu H, Kondo N (1990b) A model system to study the effect of SO2 on plant cells III: effects of sulfite on the ultrastructure of fern protonemal cells. Bot Mag Tokyo 103: 403–417
Wang H, Cutler AJ, Saleem M, Fowke LC (1989) Microtubules in maize protoplasts derived from cell suspension cultures: effect of calcium and magnesium ions. Eur J Cell Biol 49: 80–86
Wardrop AB (1958) The organization of the primary wall in differentiating conifer tracheids. Aust J Bot 6: 299–305
— (1964) The structure and formation of the cell wall in xylem. In: Zimmermann MH (ed) The formation of wood in forest trees. Academic Press, New York, pp 87–134
Wasteneys GO, Williamson RE (1987) Microtubule orientation in developing internodal cells ofNitella: a quantitative analysis. Eur J Cell Biol 43: 14–22
— — (1993) Cortical microtubule organization and internodal cell maturation inChara corallina. Bot Acta 106: 136–142
Weerdenburg C, Seagull RW (1988) The effects of taxol and colchicine on microtubule and microfibril arrays in elongating plant cells in culture. Can J Bot 66: 1707–1716
Wernicke W, Jung G (1992) Role of cytoskeleton in cell shaping of developing mesophyll of wheat (Triticum aestivum L.). Eur J Cell Biol 57: 88–94
—, Günther P, Jung G (1993) Microtubules and cell shaping in the mesophyll ofNigella damascena L. Protoplasma 173: 8–12
Williamson FA, Fowke LC, Weber G, Constabel F, Gamborg O (1977) Microfibril deposition on cultured protoplasts ofVicia hajastana. Protoplasma 91: 213–219
Williamson RE (1991) Orientation of cortical microtubules in interphase plant cells. Int Rev Cytol 129: 135–206
Willison JHM, Brown RM Jr (1977) An examination of the developing cotton fiber: wall and plasmalemma. Protoplasma 92: 21–41
— — (1978) Cell wall s structure and deposition inGlaucocystis. J Cell Biol 77: 103–119
—, Cocking EC (1975) Microfibril synthesis at the surfaces of isolated tobacco mesophyll protoplasts: a freeze-etch study. Protoplasma 84: 147–159
—, Grout BWW (1978) Further observations on cell-wall formation around isolated protoplasts of tobacco and tomato. Planta 140: 53–58
Wilms FHA, Derksen J (1988) Reorganization of cortical microtubules during cell differentiation in tobacco explants. Protoplasma 146: 127–132
—, Wolters-Arts AMC, Derksen J (1990) Orientation of cellulose microfibrils in cortical cells of tobacco explants: effects of microtubule-depolymerizing drugs. Planta 182: 1–8
Wymer C, Lloyd C (1996) Dynamic microtubules: implications for cell wall patterns. Trends Plant Sci 1: 222–228
Yatsu LY (1983) Morphological and physical effects of colchicine treatment on cotton (Gossypium hirsutum L.) fibers. Textile Res J 53: 515–519
—, Jacks TJ (1981) An ultrastructural study of the relationship between microtubules and microfibrils in cotton (Gossypium hirsutum L.) cell wall reversals. Am J Bot 68: 771–777
Author information
Authors and Affiliations
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
Baskin, T.I. On the alignment of cellulose microfibrils by cortical microtubules: A review and a model. Protoplasma 215, 150–171 (2001). https://doi.org/10.1007/BF01280311
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01280311