Biophysical control of microfibril orientation in plant cell walls: Aquatic and terrestrial plants including trees

209 Pages·1985·5.07 MB·English

by  J. D. Boyd (auth.)

BIOPHYSICAL CONTROL OF MICROFIBRIL ORIENTATION IN PLANT
CELL WALLS
FORESTRY SCIENCES
Baas P, ed: New Perspectives in Wood Anatomy. 1982. ISBN 90-247-2526-7
Prins CFL, ed: Production, Marketing and Use of Finger-Jointed Sawnwood. 1982.
ISBN 90-247-2569-0
Oldeman RAA, et aI., eds: Tropical Hardwood Utilization: Practice and Prospects. 1982.
ISBN 90-247-2581-X
Den Ouden P and Boom BK: Manual of Cultivated Conifers: Hardy in Cold and Warm
Temperate Zone. 1982. ISBN 90-247-2148-2 paperback; ISBN 90-247-2644-1 hard
bound.
Bonga JM and Durzan DJ, eds: Tissue Culture in Forestry. 1982. ISBN 90-247-2660-3
Satoo T and Magwick HAl: Forest Biomass. 1982. ISBN 90-247-2710-3
Van Nao T, ed: Forest Fire Prevention and Control. 1982. ISBN 90-247-3050-3
Douglas J: A Re-appraisal of Forestry Development in Developing Countries. 1983.
ISBN 90-247-2830-4
Gordon JC and Wheeler CT, eds: Biological Nitrogen Fixation in Forest Ecosystems:
Foundations and Applications. 1983. ISBN 90-247-2849-5
Hummel FC, ed: Forest Policy: A Contribution to Resource Development. 1984.
ISBN 90-247-2883-5
Duryea ML and Landis TD, eds: Forest Nursery Manual: Production of Bareroot Seed-
lings. 1984. ISBN 90-247-2913-0
Manion PD, ed: Scleroderris Canker of Conifers. 1984. ISBN 90-247-2912-2
Staaf KAG and Wiksten NA: Tree Harvesting Techniques. 1984. ISBN 90-247-2994-7
Duryea ML and Brown GN, eds: Seedling Physiology and Reforestation Success. 1984.
ISBN 90-247-2949-1
Boyd JD: Biophysical Control of Microfibril Orientation in Plant Cell Walls. 1985.
ISBN 90-247-3101-1
Biophysical control of microfibril
orientation in plant cell walls
Aquatic and terrestrial plants induding trees
by
J.D. BOYD
CSIRO
Highet!, Victoria
Australia
1985 MARTINUS NIJHOFF/DR W. JUNK PUBLISHERS
a member of the KLUWER ACADEMIC PUBLISHERS GROUP
DORDRECHT / BOSTON / LANCASTER
Distributors
for the United States and Canada: Kluwer Academic Publishers, 190 Old Derby
Street, Hingham, MA 02043, USA
for the UK and Ireland: Kluwer Academic Publishers, MTP Press Limited,
Falcon House, Queen Square, Lancaster LA1 1RN, UK
foral! otherc()unrries: Kluwer Academic Publishers Group, Distribution Ccntcr,
P.O. Box 322, 3300 AH Dordrecht, The Netherlands
Library of Congress Cataloging in Publication Data
Boyd, J. D.
Biophysical control of microfibril orientation in
plant cell walls.
(Forestry sciences)
Bibliography: p.
1. Microfibril.. 2. Plont cell walls. 3. Bio
physics. I. Title. [I. Title: Microfibril orientation
in plant cell walls. 1)[. Series.
QK725.B67 1985 581.87'5 84-22709
IS8:-1·13:978·94-010-8742-1 t·1 S 11 ,·1.1 :'178-94·009·5065·8
001: IO.I007/978-94-00(1-5()65-H
Copyright
©
1985 by Martinus Nijhoff/Dr W. Junk Publishers, Dordrecht.
Softcover reprint of the hardcover 1985
All rights reserved. No part of this publication may be reproduced, stored in a
retrieval system, or transmitted in any form or by any means, mechanical,
photocopying, recording, or otherwise, without the prior written permission of
the publishers,
Martinus NijhofflDr W. Junk Publishers, P.O. Box 163,3300 AD Dordrecht,
The Netherlands.
Contents
Preface IX
I. Introduction 1
II. Reassessment of data relating to the multinet theory of microfibril
reorientation 6
1. Data obtained by Probine and Preston (1961) and Green and Chapman
(1955) 6
2. Data obtained by Frei and Preston (1961a, b) 11
3. Data obtained by Green (1960a) 15
4. Data obtained by Gertel and Green (1977) 18
5. Recent observations claimed to support MGH 25
III. Significance of biophysics and genetics in primary growth 27
1. Biophysical interaction with microfibril arrangement in the meristema-
tic area 27
2. Genetic influence on orientations of microfibril additions during exten-
sion growth 31
IV. Reassessment of data on tip growth and conclusions on MGH 35
1. Reorientation of microfibrils during tip growth 35
2. Conclusions on the multinet hypothesis and reorientation possibilities 40
V. Wide variety of microfibril arrangements in plant cell walls 45
VI. Critical preliminary considerations for a new theory on microfibril
orientation 47
1. Fundamental requirements 48
2. Indicators of the importance of physical factors 50
3. Physical interactions between microfibrils and matrix materials 51
4. Effect of bonding of microfibrils and stress direction on cell wall
stiffness and orientation of microfibrils 52
VI
5. Stress distribution effects through the cell wall thickness 55
6. Relationship between helical orientation and the direction of cell
extension 58
VII. Biophysics of orientation of microfibrils in surface growth 60
1. Identification of the fundamental control factors 60
2. Induction of helical orientation in extension growth 62
3. Reduction of initial helical angle with reducing extension rate 63
4. Operation of critical structural controls in tubular cells with one domi-
nant helical orientation of microfibrils 64
5. Biophysical considerations in the optimum use of plant energy 68
6. Orientation interaction with experimental limitation on strain 70
7. Spiral growth induced by the helical orientation of microfibrils 74
8. Effects of extension growth on the variability of orientation within
microfibrils 79
9. The nature and significance of axial striations in Nitella internodal cells 80
10. Formation of branches and development of characteristic orientation
of microfibrils 87
11. General nature of lamellae development and induced reactions 93
12. Controls for microfibril orientation changes between lamellae 96
13. Biophysical influence in thickening walls of epidermal and col-
lenchyma cells 101
14. Biophysics of corner thickenings in collenchyma cells 106
15 ..A ssociation of axial rib thickenings and prominent regular pit fields in
parenchyma 109
VIII. Helicoidal structure and comparable texture variations 112
1. Helicoidal structure 113
2. Herringbone texture 116
3. Problems in classifying texture as helicoidal, or herringbone, or other
type 120
4. Classification of textures of particular plant tissues 123
5. Provisional general conclusions on cell wall texture 138
IX. Biophysics of cell wall architecture in secondary wall formation 142
1. Preliminary considerations 142
2. Microfibril organization in the S2 wall layer 145
3. Microfibril organization in the S] wall layer 148
4. Microfibril organization in the S3 wall layer 152
5. Alternating helical directions between Sl' S2 and S3 155
6. Absence of an S3 layer in reaction wood and phloem fibres 155
X. Biophysical basis for wall layer nomenclature 161
VII
XI. General discussion of the significance of biophysics in plant morphology 166
XII. Literature cited 171
List of appendices
Appendix I
Reorientation possible prior to microfibrils being fractured by overstrain 179
Appendix II
Possible reorientation of microfibril fragments 182
1. Effect of extension growth on orientation of microfibril fragments 182
2. The effect of spiral growth on reorientation of microfibril fragments 184
Appendix III
Hypothetical mean orientation of microfibrils resulting from extension
growth in accordance with the multinet growth hypothesis 185
1. General assumptions 185
2. Results 186
Appendix IV
Interpretation of Green's (1960a) data on passive reorientation of micro-
fibrils 187
1. Assumption of constant proportional crystallinity through the wall
thickness 187
2. Green's extrapolation of curves 190
3. Curve slopes near outside face of wall 190
4. Microfibril orientation indicated by micrograph of polarized light
effects. 192
Appendix V
Alternative models for extension of cell walls 193
1. The isotropic cylinder model 193
2. The helical spring model 194
3. Comparison of isotropic cylinder and helical spring models 195
Appendix VI
Strain stimulation for microfibril orientation in epidermal cells 196
Preface
Within the extreme diversity of aquatic and terrestrial plant genera, each has
characteristic cell wall forms. A number of hypotheses have been advanced to
explain differences in microfibril arrangements across anyone such wall. Of
those, only the 'multinet' theory, which involves the postulation of reorientation
of microfibrils caused by cell extension, now has a substantial number of ad
herents. However, many scientists are sceptical of its validity; obviously it is
incompatible with various observed microfibril arrangements.
The tenet of this study is that any such hypothesis can be valid only if it is
applicable to all plant forms and wall types. Initially, reanalyses are made of data
claimed to confirm justification for multi net postulations. The results show that
previous deductions from those data, in support of multinet, are subject to serious
challenge. Similarly, a re-examination of the observations, which inspired the
multinet theory, shows they have a more logical explanation. Herein, it is
concluded that cell wall development involves biophysical factors, which neces
sarily prevent multinet's postulated large reorientations of microfibrils, after
their formation. Unfortunately the previously most recent published theory,
which is based on the absence of reorientation during extension, fails to answer
the fundamental question of how alternating orientations between lamellae are
controlled, or explain variations in thickness of wall layers.
Extensive published data are used to identify forces involved in cell wall
development. Analysis of the effects of those biophysical forces led to formula
tion of a new theory; this is based on strains generated in the cell wall and the
plasmalemma, as a consequence of extension growth, and associated and sub
sequent wall thickening. The cogency of the theory, to provide rational explana
tions for an unlimited variety of cell wall forms and microfibril arrangements, is
tested extensively.
Features of different primary wall forms so enveloped include: one dominant
general or average microfibril orientation throughout; spiral growth; effects of
experimental imposition of physical constraints; changes between lamellae in the
degree of parallelism of microfibrils; axial striations in Nitella internodal cells;
x
establishment of characteristic microfibril orientation during initiation of
branches; large changes in orientation between lamellae; axial orientation in
corner thickenings of collenchyma cells, in association with lamellae showing
transverse orientations; and development of axial ribs amid general transverse
orientation in parenchyma cells.
Some general discussion is presented on the different types of transition in
microfibril orientations, between lamellae within wall layers, and between layers.
That discussion includes particular reference to 'herring bone' and 'helicoidal'
textures. In respect of secondary wall formation, special attention is given to
wood fibres, partly because of their great economic importance, but particularly
because the wealth of technical studies of their characteristics enables the making
of critical tests of any theory on microfibril arrangements.
For wood, the strain theory is shown to support explanations for differences in
microfibril orientation between wall layers of fibres. That includes changes from
'random' orientation in the primary wall, to a transverse helical arrangement in
the thin outer layer of the secondary wall; then to near axial orientation in the
thick middle layer; and to a transverse direction in the usual final, thin layer of
microfibrils. Additionally, the theory facilitates explanations for the absence of a
final transverse layer in both tension wood and compression wood fibres, and also
in normal phloem fibres.
It is concluded that the multi net theory is unsatisfactory even for a limited
range of primary growth. On the other hand, a more recent theory, which
involves 'ordered sub-units' (or sequences of units), with microfibril orientation
alternating from transverse to axial between units, fails to provide any substanti
ated identification and explanation for control of those orientations. In contrast
to that situation, it appears that the strain theory, as presented herein, is compati
ble with a very wide range of variations of cell forms and microfibril arrange
ments, in both primary and secondary wall development in general.
1. Introduction
The general physical and chemical nature of the walls of plant cells has become
known through the researches of many scientists over long periods. Important
physical features, which are similar for a wide variety of types of plant cell walls
include: (i) basic structural elements of crystalline polysaccharides, which are
aggregated in the form of microfibrils, and thus provide high strength and
stiffness in their longitudinal direction; (ii) the microfibrils apparently develop in
random directions in the thin walls formed prior to the separation of the cell from
the meristematic zone, but generally the microfibrils formed subsequently are
oriented in increasingly more orderly, systematically varying, or nearly parallel
directions within layers of the cell wall; (iii) during the primary and extension
growth stages, the microfibrillar framework is formed within an amorphous
hydrophylic gel or matrix of hemicelluloses and pectin; (iv) usually the micro
fibrils form in lamellae, each of thickness comparable to that of the microfibrils.
The successive lamellae develop immediately outside the living cell and its
enclosing plasma membrane. Thus each new lamella is added at the inner face of
previously-formed, comparable layers of crystalline microfibrils. Collectively
they constitute a porous, increasingly-strong structural wall, which encloses and
supports the relatively weak outer membrane of the living cell. Furthermore,
generally a large number of such 'semi-rigid' cell walls constitute a major struc
tural system, which supports upper parts of the plant.
Gradually, typical arrangements of microfibrils in plant cell walls of various
types have been illustrated and described in the literature. The initial work was
dependent on simple light microscopy, but definition and clarity were improved
progressively, first with polarized light, then with X-ray analyses, and finally with
electron microscopy. These developments have stimulated plant physiologists
and anatomists to seek links between cell growth forms, and the variations in cell
wall architecture that characterize different cell types and species. Early, it
became a central aim to determine whether the observed microfibril arrange
ments resulted from the form and extent of primary growth of the cells, or
whether the direction at which microfibrils formed was the basic factor, which