Summary
The concept of the cell wall organized in a helicoidal pattern was outlined. When studied in transmission electron microscopy, the observed textures appear as a deceptive figure,i.e., as a “trompe l'oeil”. Difficulties—both technological and visual in the reconstitution of the actual geometry (exposure of the microfibrillar framework, 3-dimensional and 4-dimensional restoration), and the interest of simple modelling to understand the changes in cellulose orientation according to space and time are emphasized.
The morphogenesis of helicoidal walls presents two main characteristics: it is both very defined and flexible, thus adaptable to varied programs of differentiation and to different environmental conditions. The observations of various cell examples and of responses to experimental treatments, lead to the following considerations: a) the shift of cellulose occurs continuously with time through a constant mutual angle. The wall seems to be built up as an indefinite continuum and forms a monotonous oscillatory system (unvarying motion); b) the shift of cellulose occurs through a mutual angle variable with time (varying motion, change from monotonous helicoid to bimodal helicoid, or sporadic bursts with arrested motion).
The helicoidal wall appears as a fibrous composite with multifunctional possibilities ranging from fluidity to stiffness. The helicoidal assembly is remarkably adaptable to different physiological conditions of growth and specialization.
Similar content being viewed by others
References
Abeyesekera RM, Willison JHM (1987) A spiral helicoid in a plant cell wall. Cell Biol Int Reports 11: 75–79
Albersheim P, Darvill AG, Davis KR, Lau JM, McNeil M, Sharp JK, York WS (1985) Why study the structure of biological molecules? In:Dugger WM, Bartnicki-Garcia S (eds) Structure, function and biosynthesis of plant cell walls. American Soc Plant Physiol, Riverside, pp 19–51
Bartnicki-Garcia S (1984) Kingdoms with walls. In:Dugger WM, Bartnicki-Garcia S (eds) Structure, function and biosynthesis of plant cell walls. American Soc Plant Physiol, Riverside, pp 1–18
Bonfante-Fasolo P, Vian B (1984) Wall texture in the spore of a vesicular-arbuscular mycorrhizal fungus. Protoplasma 120: 51–60
— —,Testa B (1986) Ultrastructural localization of chitin in the cell wall of a fungal spore. Biol Cell 57: 265–270
Bonnet N, Quintana C, Favard P, Favard N (1985) Threedimensional graphical reconstruction from HVEM stereoviews of biological specimens by mean of a microcomputer. Biol Cell 55: 125–138
Bouligand Y (1972) Twisted fibrous arrangement in biological materials and cholesteric mesophases. Tissue and Cell 4: 189–217
— (1986) Theory of microtomy artefacts in arthropod cuticle. Tissue and Cell 18: 621–643
Carpita NC (1985) Tensile strength of cell walls of living cells. Plant Physiol 79: 485–488
Catesson AM (1982) Cell wall architecture in the secondary sieve tubes ofAcer andPopulus. Ann Bot 49: 131–134
Chou TW, McCullough RL, Pipes RB (1986) Composites. Scientific American 255: 167–177
Cosgrove D (1986) Biophysical control of plant cell growth. Ann Rev Plant Physiol 37: 377–405
Cox G, Juniper BE (1983) High voltage electron microscopy of whole, critical-point dried plant cells. Fine cytoskeletal elements in the mossBryum tenuisetum. Protoplasma 115: 70–80
Crang RE, Pechak DG (1978) Serial section reconstruction of the black yeast,Aureobasidium pullulans by means of high voltage electron microscopy. Protoplasma 96: 225–234
Czaninski Y, Monties B (1982) Étude cytochimique ultrastructurale des parois du bois de Peuplier après extraction ménagée. CR Acad Sci Paris 295: 551–556
Davidson MT, Garland PB (1977) Structure of mitochondria and vacuoles ofCandida utilis andSchizosaccharomyces pombe studied by electron microscopy of serial thin sections and model building. J Gen Microbiol 98: 147–153
Emons AC (1986 a) Cell wall texture in root hairs of the genusEquisetum. Can J Bot 64, in press
- (1986 b) A helix model for helicoidal cell wall deposition. In:Vian B,Reis D,Goldberg R (eds) Cell Walls' 86, Paris, pp 30–33
—,Wolters-Art MC (1983) Cortical microtubules and microfibril deposition in the cell wall of root hairs ofEquisetum hyemale. Protoplasma 117: 68–81
Fry SC (1985) Primary cell wall metabolism. In:Miflin BJ (ed) Oxford Survey of plant molecular and cell biology. Clarendon, Oxford, pp 1–42
— (1986) Cross-linking of matrix polymers in the growing cell walls of Angiosperms. Ann Rev Plant Physiol 37: 165–186
Giraud-Guille MM (1986) Direct visualization of microtomy artefacts in sections of twisted fibrous extracellular matrices. Tissue and Cell 18: 603–620
Gourret JP (1981) Intérêt de la platine goniométrique pour l'étude d'analogues biologiques de cristaux-liquides à structures cholesteriques. Bull Soc Bot Fr 128: 55–59
Gunning BES, Hardham AR (1982) Microtubules. Ann Rev Plant Physiol 33: 351–398
Halversum LJ, Stacey G (1986) Signal exchange in plant-microbe interactions. Microbiol Rev 50: 193–225
Harada H,Cote WA (1985) Structure of wood. In:Higuchi T (ed) Biosynthesis and biodegradation of wood components
Harche M (1986) Un type original d'architecture pariétale: l'épiderme foliaire de l'Alfa (Stipa tenacissima). CR Acad Sci 303: 131–134
Harris N (1986) Organization of the endomembrane system. Ann Rev Plant Physiol 37: 73–92
Hepler PK (1976) Plant microtubules. In:Bonner J, Varner JE (eds) Plant biochemistry. Academic Press, New York, pp 147–187
—,Fosket DE (1971) The role of microtubules in vessel member differentiation. Protoplasma 72: 213–236
Herth W (1985) Plant cell wall formation. In:Robards AW (ed) Botanical microscopy 1985. Oxford University Press, Oxford, pp 285–310
Itoh T (1976) Microfibrillar orientation of radially enlarged cells of coumarin and colchicine-treated pine seedlings. Plant and Cell Physiol 17: 385–398
Jarvis MC (1984) Structure and properties of pectin gels in plant cell walls. Plant Cell Environm 7: 153–164
Juniper BE, Lawton JR, Harris PJ (1981) Cellular organelles and cell wall formation in fibres from the flowering stem ofLolium temulentum L. New Phytol 89: 609–619
Kishi K, Harada H, Saiki H (1979) An electron microscopy study of the layered structure of the secondary wall in vessels. Mokuzaî Gakkaishi 25: 521–527
— — — (1981) The structure of the primary wall of vessels in hardwood. J Soc Mat Sc 30: 673–678
Lamport DTA (1986) The primary cell wall: a new model. In:Young RA, Rowell R (eds) Cellulose: structure, modification and hydrolysis. Wiley Interscience, New York, in press
-Muldoon EP,Kieliszewski JW,Willard JJ,Terrune B,Everdeen D (1986) Molecular design of a molecular fabric. In:Vian B,Reis D,Goldberg R (eds) Cell Walls' 86. Paris, pp 8–11
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
Levy S (1986) The colchicine response ofNitella cell walls: a druginduced deposition of helicoidally oriented microfibrils. In:Vian B,Reis D,Goldberg R (eds) Cell Walls' 86. Paris, pp 66–67
-Neville AC (1986) Computer methods for 3-dimensional ultrastructural modelling and predictions of dynamic changes in the cell wall during growth. In:Vian B,Reis D,Goldberg R (eds) Cell Walls' 86, Paris, pp 18–19
Liberman M,Matar D,Catesson AM (1986) Architectural diversity of the sieve cell walls. In:Vian B,Reis D,Goldberg R (eds) Cell Walls' 86. Paris, pp 76–77
Livolant F, Giraud MM, Bouligand Y (1978) A goniometric effect observed in sections of twisted fibrous material. Biol Cell 31: 159–168
Lloyd CW (1984) Toward a dynamic helical model for the influence of microtubules on wall patterns in plants. Int Rev Cytol 86: 1–51
- (1987) The plant cytoskeleton: the impact of fluorescence microscopy. Ann Rev Plant Physiol, in press
—,Seagull RW (1985) A new spring for plant cell biology: microtubules as dynamic helices. Trends Biochem Sc 10: 476–478
MacLachlan G, Fevre M (1982) An overview of cell wall biosynthesis. In:Lloyd CW (ed) The cytoskeleton in plant growth and development. Academic Press, London, pp 127–146
McNeil M, Darvill AG, Fry SC, Albersheim P (1984) Structure and function of the primary cell wall of plants. Ann Rev Biochem 53: 625–663
Meekes HTHM (1986) Inhibition and recovery of cell wall formation in root hairs ofCeratopteris thalictroides. J Exp Bot 37: 1201–1210
Mizuta S, Wada S (1981) Microfibrillar structure of growing cell walls in a coenocytic alga,Boergesenia forbesii. Bot Mag 94: 343–353
Moore PJ, Darvill AG, Albersheim PA, Staehelin LA (1986) Immunogold localization of xyloglucan and rhamnogalacturonan I in the cell walls of suspension-cultured sycamore cells. Plant Physiol 82: 787–794
Mueller SC, Brown RM (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
Nanko S, Saiki H, Harada H (1978) Cell wall structure of the sclereids in the secondary phloem ofPopulus euamericana. Mozukaî Gakkaishi 24: 362–368
Neville AC (1985) Molecular and mechanical aspect of helicoid development in plant cell walls. Bio Essays 3: 4–8
—,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
Neville AC,Levy S (1985) The helicoidal concept in plant cell wall ultrastructure and morphogenesis. In:Brett CT,Hillman JR (eds) Biochemistry of plant cell walls. Cambridge University Press, pp 99–124
—,Gubb DC, Crawford RM (1976) A new model for cellulose architecture in some plant cell walls. Protoplasma 90: 307–317
Northcote DH (1985) Control of cell wall formation during growth. In:Brett CT, Hillman JR (eds) Biochemistry of plant cell walls. Cambridge University Press. Cambridge, pp 177–197
— (1986) Molecular and cell biology of plant cells. J Cell Sci 4: 115–135
Parameswaran N, Liese W (1981) Occurrence and structure of polylamellate walls in some lignified cells. In:Robinson DG, Quader H (eds) Cell Walls' 81. Wissenschaftliche Verlagsgesellschaft, Stuttgart, pp 171–188
— —, (1982) Ultrastructural localization of wall components in wood cells. Holz als Roh- und Werkstoff 40: 145–155
—,Sinner M (1979) Topochemical studies on the wall of beech bark sclereids by enzymatic and acidic degradation. Protoplasma 101: 197–215
Pellegrini M (1981) Application de la technique des coupes sériées ultrafines à l'étude des variations morphologiques qualitatives et quantitatives des organites cellulaires del'Euglena gracilis. Bull Soc Bot Fr 128: 43–45
—,Pellegrini L (1985) On the occurrence of twisted fibrillar structures in the cytoplasm of the red algaAlsidium helminthochorton (La Tourette) Kütz. Ultrastructural and cytochemical observations. Protoplasma 126: 54–61
Pluymakers HJ (1982) A helicoidal cell wall texture in root hairs ofLimnobium stoloniferum. Planta 133: 107–116
Prat R (1986) Effect of staining parameters in the aspect of helicoidal cell wall structure: microcomputer simulation. In:Vian B,Reis D,Goldberg R (eds) Cell Walls' 86. Paris, pp 374–375
Preston RD (1979) Polysaccharide conformation and cell wall function, Ann Rev Plant Physiol 30: 55–78
Quader H (1986) Cellulose microfibril orientation inOocystis solitaria: proof that microtubules control the alignment of the terminal complexes. J Cell Sci 83: 223–234
Reis D (1980–1981) Cytochimie ultrastructurale des parois en croissance par extractions ménagées. Effets comparés du dimethylsulfoxide et de la methylamine sur le démasquage de la texture. Ann Sci Nat 2–3: 121–136
—,Mosiniak M, Vian B, Roland JC (1982) Cell walls and cell shape. Changes in texture correlated with an ethylene-induced swelling. Ann Sci Nat 4: 115–133
-Vian B,Satiat-Jeunemaitre B,Roland JC (1986) 3-D-modelling of the basic ultratexture and alterations of the shift of cellulose in the helicoidal cell wall. In:Vian B,Reis D,Goldberg R (eds) Cell Walls' 86. Paris, pp 16–17
Richmond PA (1986) The relationship between microtubule organization and patterns of microfibril deposition inNitella. In:Vian B,Reis D,Goldberg R (eds) Cell Walls' 86. Paris, pp 28–29
Robinson DG, Kristen U (1982) Membrane flow via the Golgi apparatus of Higher Plant cells. Int Rev Cytol 77: 89–127
Roland JC (1981) Comparison of arced patterns in growing and non-growing polylamellate cell walls of higher plants. In:Robinson DG, Quader H (eds) Cell Walls' 81. Wissenschaftliche Verlagsgesellschaft, Stuttgart, pp 162–170
—,Mosiniak M (1983) On the twisting pattern, texture and layering on the secondary cell walls of lime wood. Proposals of an unifying model. IAWA Bull 4: 15–26
-Reis D (1986) Morphogenèse à un niveau supramoléculaire: l'assemblage rythmé des parois cellulaires. In press
—,Vian B (1979) The wall of the growing plant cell: its three-dimensional organization. Int Rev Cytol 61: 129–166
— — (1981) Use of purified endopolygalacturonase for a topochemical study of elongating cell walls at the ultrastructural level. J Cell Sci 48: 333–343
—,Reis D, Mosiniak M, Vian B (1982) Cell wall texture along the growth gradient of the mung bean hypocotyl: ordered assembly and dissipative processes. J Cell Sci 56: 303–318
— —,Vian B, Satiat-Jeunemaitre B (1983) Traduction du temps en espace dans les parois des cellules végétales. Ann Sci Nat 5: 173–192
Ruel K, Comtat J, Barnoud F (1977) Localisation histologique et ultrastructurale des xylanes dans les parois primaires des tissus d'Arundo donax, CR Acad Sci Paris 284: 1421–1424
—,Joseleau JP, Comtat J, Barnoud F (1976) Ultrastructural localization of xylans in the developing cell wall of Graminae fibers by the use of endoxylanase. Applied Polymer Symp 28: 971–981
Satiat-Jeunemaitre B (1980–1981) Texture et croissance des parois des deux épidermes du coléoptile de maïs. Ann Sci Nat 2–3: 163–176
— (1984a) Croissance et texture pariétales de maïs en obscurité et lumière continues. Physiol Veg 22: 745–753
— (1984 b) 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, in press
Selvendran RR (1986) Developments in the chemistry and biochemistry of pectic and hemicellulosic polymers. J Cell Sci [Suppl] 2: 51–88
—,Stevens BJH, O'Neil MA (1985) Developments in the isolation and analysis of cell walls from edible plants. In:Brett CT, Hillman JR (eds) Biochemistry of plant cell walls. Cambridge University Press, Cambridge, pp 39–78
Srivastava LM, Sawhney VK, Bonnetemaker M (1977) Cell growth, wall deposition, and correlated fine structure of colchicine-treated lettuce hypocotyl cells. Can J Bot 55: 902–917
Stevens BJ (1974) Variations du nombre de mitochondries et du volume du chondriome de la levure selon les conditions de croissance. J Microsc 20: 90 a
Taiz L (1984) Plant cell expansion: regulation of cell wall mechanical properties. Ann Rev Plant Physiol 35: 585–657
Takeda K, Shibaoka H (1978) Effects of gibberellin and colchicine on microfibril arrangement in epidermal cell walls ofVigna angularis Ohwi et Ohashi epicotyls. Planta 151: 393–398
— — (1981 a) Changes in microfibril arrangement on the inner surface of the epidermal cell walls in the epicotyl ofVigna angularis Ohwi et Ohashi during cell growth. Planta 151: 385–392
— — (1981 b) Effects of gibberellin and colchicine on microfibril arrangement in epidermal cell walls ofVigna angularis Ohwi et Ohashi epicotyls. Planta 151: 393–398
Vermeulen CA, Wessels JGH (1986) Chitin biosynthesis by a fungal membrane preparation. Evidence for a transient noncrystalline state of chitin. Eur J Biochem 158: 411–415
Vian B (1982) Organized microfibril assembly in higher plant cells. In:Brown RM (ed) Cellulose and other natural polymer systems. Plenum Publishing Corporation, New York, pp 23–43
—,Roland JC (1987) The helicoidal cell wall as a time register. New Phytol 105, 345–357
—,Mosiniak M, Reis D, Roland JC (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
Wilkie KCB (1985) New perspectives on non-cellulosic cell wall polysaccharides (hemicelluloses and pectic substances) of land plants. In:Brett CT, Hillman JR (eds) Biochemistry of plant cell walls, Cambridge University Press, Cambridge, pp 1–37
Wilson LG, Fry SC (1986) Extensin. A major cell wall glycoprotein. Plant Cell Environm 9: 239–260
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Roland, J.C., Reis, D., Vian, B. et al. Morphogenesis of plant cell walls at the supramolecular level: Internal geometry and versatility of helicoidal expression. Protoplasma 140, 75–91 (1987). https://doi.org/10.1007/BF01273716
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01273716