Download The History of Tissue Tension

Annals of Botany 77: 657-665, 1996
The History of Tissue Tension
W. S. PETERS* and A. D. TOMOS
School of Biological Sciences, University of Wales, Bangor, Gwynedd LL57 2UW, Wales, UK
Received: 4 August 1995 Accepted: 12 December 1995
In recent years the phenomenon of tissue tension and its functional connection to elongation growth has regained
much interest. In the present study we reconstruct older models of mechanical inhomogenities in growing plant
organs, in order to establish an accurate historical background for the current discussion. We focus on the
iatromechanic model developed in Stephen Hales' Vegetable Staticks, Wilhelm Hofmeister's mechanical model of
negative geotropism, Julius Sachs' explanation of the development of tissue tension, and the differential-auxinresponse-hypothesis by Kenneth Thimann and Charles Schneider. Each of these models is considered in the context
of its respective historic and theoretical environment. In particular, the dependency of the biomechanical hypotheses
on the cell theory and the hormone concept is discussed. We arrive at the conclusion that the historical development
until the middle of our century is adequately described as a development towards more detailed explanations of how
differential tensions are established during elongation growth in plant organs. Then we compare with the older models
the structure of more recent criticism of hormonal theories of tropic curvature, and particularly the epidermalgrowth-control hypothesis of Ulrich Kutschera. In contrast to the more elaborate of the older hypotheses, the recent
models do not attempt an explanation of differential tensions, but instead focus on mechanical processes in organs,
in which tissue tension already exists. Some conceptual implications of this discrepancy, which apparently were
overlooked in the recent discussion, are briefly evaluated.
© 1996 Annals of Botany Company
Key words: Auxin, biomechanical models (history of), cell theory, elongation growth, geotropism, hormone concept,
tissue tension.
The historian, and especially the historian-scientist, can, I
believe, become too easily beguiled by the power of present
scientific theory, and consequently imagine that its ancestor
theory carried the same logical implications, which are then
presumed to have stood clear to the earlier practitioners.
R. J. Richards (1992)
INTRODUCTION
Plant organs do not consist of mechanically homogenous
material, but usually are found to exist in states of mutual
tensions between their different parts. Such tissue tensions
become apparent upon organ dissection, when dramatic
bendings or coilings occur. Their nature was vividly debated
in the second half of the last century (e.g. Sachs, 1874).
Remarkably, original research on tissue tension seems to
have ceased at about 1940. Tissue tension has regained
interest in recent years (Firn and Digby, 1977; Heijnowicz
and Sievers, 1995), leading to the formulation of the
hypothesis that plant organ growth is controlled by the
epidermal tissue (Kutschera, 1987, 1992). Surprisingly, the
origin of this notion has been ascribed to scientists as distant
in time and theoretical background as Kraus (1867;
Kutschera, 1992) or Thimann and Schneider (1938;
Edelmann, Bergfeld and Schopfer, 1989). We feel that here,
and in some other cases, assessments of the historical
development of the topic are inaccurate. As a result
important aspects of the control of tissue tension have been
overlooked.
In the present paper we attempt to reconstruct some of
the more influential hypotheses on organ growth mechanics.
In particular we will concentrate on the theoretical
framework, in which the models were formulated, and on
the experimental strategies deduced from them. While
analysing the models, we purposefully will refrain from reevaluating the significance of experimental results per se. By
doing so we hope to avoid interpreting the historic theories
on the basis of present knowledge. Interpretations of the
latter type are likely to over-emphasize factors, which
presumptively correspond to modern views, and neglect
aspects, which have gone out of fashion, even if they were
highly important at their time. For due discussion of these
different historiographical approaches see Agassi (1963),
Kuhn (1969, 1977) and Bayertz (1980).
Our aim in this paper, however, is more than a mere
correction of inaccurate views of a historic process.
Experimental strategies do not simply emerge from bodies
of established knowledge; rather they are constructed on
the basis of hypotheses. One may doubt whether it is always
the most recent hypotheses which automatically provides
the soundest foundation for future research (Kuhn, 1969).
In returning some older concepts to the current discussion,
we hope to broaden the spectrum of justifiable research
strategies.
* For correspondence at: Institut fur Botanik 1, Senckenbergstr.
17-21, D-35390 Giessen, Germany.
0305-7364/96/060657 + 09 $18.00/0
1996 Annals of Botany Company
Peters and Tomos—The History of Tissue Tension
658
THE HISTORY OF TISSUE T E N S I O N
Vegetable Staticks
In the 17th century, the transfer to the medical sciences of
mathematical and mechanical principles, which had proven
so successful in physics, resulted in the ' iatromechanics' of
Sanctorius, Giovanni Borelli, William Harvey and others.
The iatromechanical concept, namely to search causal
N
N
explanations for life activities in their exact mechanical
descriptions, was applied to botany on a large scale by
Stephen Hales. In his Vegetable Staticks (1961; originally
published 1727) he described growth tests, which resemble
modern measurements of relative elemental growth rates,
and discussed the mechanical role of various parts of shoots
in elongation growth (see his Experiment CXXIII). He
based his considerations on Borelli's assumption (1927; first
published 1680), that elongation was driven by the attraction
of water by the 'spongy pith'. The 'dilating spongy
substance' exerted its force on 'plinths, or abutments',
which he identified with the partitions of the shoot at the
nodes (Fig. 1). Thereby the outer parts of the shoot
(' vessels') were' distended like soft wax'. This distention was
understood to be passive. Hales compared the lengthening
of the ' vessels' with the ' effect in melted glass tubes, which
retain a hollowness, tho' drawn out to the finest thread'.
Iatromechanic models typically interpreted organisms as
machines performing mechanical work. Iatromechanic
studies centred on the immediate causes (such as specific
structure), which determined the types of action a particular
machine could possibly perform. The question of how the
machines came into existence was beyond the scope of these
models (Reif, 1985), and therefore no developmental causes
were considered. Consequently, Hales did not comment on
the origin of the organismic machine he described. He
stressed that nature was ' always carefully providing for the
succeeding year's growth by preserving a tender ductile part
in the bud replete with succulent pith'. But this preservation
of en miniature machines as remnants of last year's ones
could not explain the origin of the mechanical apparatus
itself from the seed unless ideas of preformation were
employed.
The theoretical background in the 19th century
N
N
V
Pith
V
FIG. 1. Schematic cross-section of a growing stem as a model of the
mechanics of internode elongation growth as formulated by Stephen
Hales in the Vegetable Staticks of 1727. The pith expands due to water
uptake, and thus exerts pressure on the nodes (N), which act as
abutments. Thereby the nodes are pushed apart, leading to passive
lengthening of the 'vessels' (i.e. vascular bundles and other peripheral
tissues; V). Forming rigid cross-sectional bridges, the nodes prevent the
vessel cylinder from yielding in the radial direction.
One character of the development of biological sciences in
Europe during the first half of the 19th Century was the
controversy between the idealistic concepts of the Naturphilosophie on one side, and the reductionism of the
inductivistic programme on the other. A major breakthrough for the latter is marked by the formulation of the
cell theory (Schleiden, 1838; Schwann, 1839; for review see
Jahn, 1987). It stated that multicellular organisms are built
up from individual elementary organisms, namely the cells,
which as such were thought independent of each other, and
of the multicellular entity. The practical implication of this
concept was that ' the quest for the fundamental power of
organisms is thereby reduced to the quest for the fundamental power of single cells' [Schwann, 1839, p. 229 (All
translations of quotations from the German by WSP.)].
Relevant physiological research thus should be performed
on the cellular level, since the organism represents but an
arrangement of cells (Schleiden, 1842).
Wilhelm Hofmeister challenged the cell theoreticists'
doctrine (Hagemann, 1992; Kaplan, 1992), and maintained
that 'the growth of single cells within a meristem is
regulated and determined by...the mass increase of the
meristem as a whole. This mass increase cannot be construed
as the sum of the generating powers within the individual
Peters and Tomos—The History of Tissue Tension
cells' (Hofmeister, 1867, p. 129). Experimental strategies
derived from this organismal concept, within which 'the
degree to which so-called cell enlargement occurs is simply
a marker of organ expansion' (Kaplan, 1992, p. S31), will
obviously differ from the above. It appears that despite the
intervening 130 years the implications of this dichotomy
remain to be resolved (Kaplan and Hagemann, 1991; Sitte,
1992). We believe that the subsequent development of
theories on growth mechanics can only be properly
understood against this theoretical background.
659
1886; Kuster, 1899), before cellular mechanics in the modern
sense were unanimously accepted (see, e.g. Pfeffer, 1904).
Hofmeister did not go into detail regarding the developmental causes of tissue tension, which therefore remained
an unexplained presupposition in his model. There is but
one short remark on this issue in his description of
geotropism in rhizomes: 'During and after elongation,
differences of tension occur between the central tissues and
the epidermis of the elongated internode: the latter is
stretched due to the former's tendency to expand.'
(Hofmeister, 1863, p. 108). In his logic, elongation growth
somehow establishes the necessary condition (tissue tension)
Hofmeister's model of shoot tropisms
for the explanandum (geotropic curvature) to occur. We
Hofmeister (1859, 1863) gave precise descriptions of suggest that herein lies the reason for the lack of an explicit
tissue tension phenomena in growing shoots and discussed explanation of the developmental causes of differential
functional implications, thereby surpassing the contri- tensions. He considered tissue tension an effect of elongation
butions of his predecessors, which he briefly reviewed growth, the mechanism of which he had not set out to
(Hofmeister, 1863). Although he spoke of 'differences of explain. This lack of causal explanation of the ontogenetical
tension of tissues' {Dijferenzen der Spannung der Gewebe) development of shoot mechanical architecture is a character
instead of using the term 'tissue tension' (Gewebespannung), shared by Hofmeister's theory with the much older
he actually introduced the concept into modern botany.
iatromechanical models.
For our purpose, it is enlightening to understand how
Hofmeister established a role of differential tensions in his
The causes of tissue tension pursued
theories. He started with an investigation of the bending of
Julius Sachs' review-like essay of 1865 (chapter XIII)
shoots as induced by external mechanical stimuli
(Hofmeister, 1859). He found growing internodes bent in appears to mark the starting point of the developmental
response to vigorous shaking of the plant, or repeated gentle analysis of differential tensions. Kraus (1867, p. 106) judged
blows from one side (for a recent review of related effects see about this work:' What confers lucid clearness on the whole
Jaffe, 1985). He then looked into the mechanical architecture treatise, is that the fundamental cause of tissue tension is
of the stems to find that ' the pith possesses a tendency to recognized within the differential growth of the different
expand considerably, which is kept within bounds by the connected tissues. Thereby the whole of tissue tension
resistance offered by the cortex and wood' (p. 254). He phenomena became... a mere function of the best known
explained the mechanically-induced bending by assuming character of all tissues, namely growth'. In Sachs' hands
that the mechanical stimuli loosen the expansion-resisting Hofmeister's incidental remark mutated into a central
organ parts in an inhomogenous manner. Convex bending causal statement. To Sachs, tissue tension was a side-effect
occurred on the side in which greatest wall loosening had of elongation growth. This is clear not only from his texts
been induced. This hypothesis seemed corroborated by the (e.g. 1875, 1887), but also from the structure of his
fact that only growing internodes bend. Only those are in a arguments. For example, he inferred from the fact that
state of tissue tension, which was a precondition for the isolated root tissues elongate at different rates, that tissue
bending response.
tensions exist in the intact organs, although they are not
In 1860 Hofmeister (Hofmeister, 1863) used this very readily demonstrated directly (Sachs, 1875, p. 720). In this
argument to explain the mechanism of geotropic shoot context the term 'growth' on the cellular level meant the
curvature. Negative geotropic curvature occurred, because 'constant overstepping of the limit of elasticity of the
'in the lower half of an organ the extensibility of those walls, growing cell-wall constantly being neutralized by intuswhich restrict expansion..., increases' (p. 88) due to the susception' (Sachs, 1875, p. 712; compare Pfeffer, 1904,
gravitational force. Here gravitation is functionally an- §§9, 18).
alogous to the external mechanical stimuli discussed above.
The differential rates of cell growth established a
It can only cause an effect in shoot portions which are in a differentiated mechanical architecture, with consequences
state of tissue tension. Hofmeister consequently stressed for growth on the organ level:' We have seen how elongation
that negative geotropism occurs exclusively in those. To him growth in internodes is produced by two factors; how the
the change in differential tensions was the mechanical cause inner tissues, the pith in particular, form the actually
of the curvatures. In contrast, in his opinion positive expanding element or driving force of growth, and how an
geotropic curvatures in roots were brought about by entirely end is set to the steady elongation of those elements by the
different mechanisms, which did not depend on differential pressure which the very elastic peripheral tissues exert on
tensions in the organ.
them; how the peripheral tissues, so to speak, only determine
Hofmeister conceived the immediate cause for differential the extent of growth of the internode' (Kraus, 1867, p. 141.
tensions in different states of imbibition of different cell Note that' elastic' means' possessing a high elastic modulus'
walls, and denied a crucial role of' endosmosis' and turgor in Kraus' text). The importance of inner tissues for the
pressure. Similar ideas found supporters until the end of the growth of the whole organ was underlined by the tercentury (Sachs, 1865; Kraus, 1867; Muller, 1877; Boehm, minology used. Inner tissues were referred to as being in a
660
Peters and Tomos—The History of Tissue Tension
'state of active tension', in contrast to the 'passive tension'
of the outer tissues (Vines, 1886, pp. 343, our italics). [For
the proper understanding of the historic texts it is important
to note that 'tension' (Germ.: Spannung) was used as a
generic term, referring to both tensile and compressive
stresses (Germ.: Zugspannung and Druckspannung). 'Tissue
tension' (Germ.: Gewebespannung) as introduced by Sachs
therefore correctly describes the whole of mutual tissue
stresses in an organ.] In connection with the finding that
isolated pith keeps on growing for days, whereas isolated
outer tissues do not elongate at all (Sachs, 1875), this notion
led to the idea that some tissues (e.g. the epidermis) are only
capable of'passive growth', i.e. elongation driven by forces
from outside the growing cells (Sachs, 1875; for a
particularly straight-forward application of the concept see
Kiister, 1899). The causal analysis of differential tensions in
shoots thus seems to have supported a similar interpretation
of the role of the outer tissues in organ growth as that of
Hales' iatromechanical approach (see above).
The insight that 'tissue tension is indeed a result of
differential tissue growth' (Kraus, 1867, p. 108) had
consequences for Hofmeister's model of negative geotropism. Changes in the intensity of differential tensions now
were interpreted as results of growth processes, just like
differential tensions themselves resulted from growth. It
followed that' the change in tissue tension in the convex and
concave halves of bending plant organs is not the cause of
the movement, but results with mathematical necessity from
the curved form of the whole' (Frank, 1868, p. 74; cited
after the review by Schober, 1899).
Further research focused on the nature of cell growth in
general, and the regulation of differential growth in
particular. At the end of the century the cell theory was
practically unanimously accepted (Hansen, 1897). In this
theoretical environment, differential tensions had only
limited value, serving as indicators of prior differential cell
growth. Ludwig Jost (1908) put it unmistakably: 'In former
times tissue tension was studied with great care, since
insights into various physiological phenomena were expected from such investigations. However, these expectations
were not fulfilled. Therefore we will no longer discuss those
matters, but consider again the differentiation of cells in a
meristem' (p. 350). The mechanism of differential cell
growth was obscure still. Differential cell turgor was
suggested to play the key role (de Vries, 1919; Went, 1933).
But it was not before the application to the problem of the
hormone concept, that a generally accepted theory was
formulated.
The advent of hormones
One difficulty implicit to the cell theory lies in the
necessity to explain the neat coordination of the huge
number of individual 'elementary organisms', which form
the multicellular entity. The endocrinological hormone
concept provides a mechanism by which such correlations
could be explained. After a series of successes in zoological
fields in the 1920s (for review see Karlson, 1982), the
concept was readily acquired by plant physiologists (e.g.
Boysen-Jensen, 1936; Went and Thimann, 1937), although
100 -
&
50
10
8
6
4
Auxin concentration (-log M)
FIG. 2. Schematic representation of the differential-auxin-response
hypothesis (combined after Thimann and Schneider, 1938, 1939). Two
separate curves showing the dose-response to auxin of elongation
growth of the inner (
) and outer tissues (
) of a growing shoot.
Outer tissues are capable of faster growth at optimal auxin concentrations, but inner tissues react to smaller amounts of the hormone.
Physiological auxin concentrations are in the range of stronger responses in the inner tissues (a), which causes the observed tissue tensions.
By artificially elevating the auxin level into the range of optimal
response of the outer tissues, the direction of the tissue tension gradient
can be reversed (b). This is the mechanism of the Went-reaction in the
split-pea-test. Very low exogenous auxin concentrations induce
increased normal (concave) curvature in auxin-depleted segments (c).
numerous inconsistencies appeared (for discussion see
Zimmermann and Wilcoxon, 1935; Trewavas, 1981, 1986;
Firn and Myers, 1987; Hathway, 1990). Not surprisingly
'the leading idea that correlations in plants are due to the
influence of special substances' (Went and Thimann, 1937,
p. 2) was soon utilized to formulate a model for the
development of tissue tension in growing shoots.
Kenneth Thimann had proposed in 1937 that 'the curve
of response against auxin concentration is... of the same
general shape for each organ, though shifted horizontally or
vertically' (quoted from Thimann and Schneider, 1938, p.
635), namely bell-shaped. This differential-auxin-response
hypothesis is commonly found in modern textbooks still.
The explanation of how tissue tensions could arise was
constructed by transferring its logic from organs to cells:
'... the same relations hold for the individual layers of cells
within a given organ. In the pea stem, the innermost
layers—i.e. the pith—reach their maximum elongation at
relatively low auxin concentrations, the outermost, on the
other hand, at relatively high' (Thimann and Schneider,
1938, p. 635). Highest sensitivity in terms of lowest effective
auxin concentrations thus occurs in the pith. On the
contrary, highest sensitivity in terms of maximum inducible
effect is found in the epidermis (Fig. 2; compare Firn, 1986,
for a discussion of the ambiguity of the term 'sensitivity').
In the intact plant, however, auxin concentrations had to be
postulated to be in a range in which elongation was
promoted stronger in the inner tissues than in the epidermis,
in order to account for the observed direction of the tension
gradient (Fig. 2, arrow A). Following the logic of the
hypothesis, the Went-reaction (the auxin-dependent reversal
of tissue tension in the split-pea test; Went, 1934) had to be
Peters and Tomos—The History of Tissue Tension
interpreted as an effect induced by unphysiologically high
hormone concentrations (Fig. 2, arrow B).
Thimann and Schneider saw their theory supported by
several lines of evidence. First there was the finding that
' peeled sections of both Pisum and Avena respond very well
to auxin' (Thimann and Schneider, 1938, p. 629), or 'in
other words, the sensitivity of peeled material to auxin is
certainly no less than that of normal material in the same
experiment' (p. 630). Second, auxin dose-response curves of
isolated tissues appeared to be in accord with the theory
(Thimann and Schneider, 1938). Third, in auxin-depleted
material very low auxin concentrations seemed to increase
the naturally occurring concave bending, an effect readily
explained by the theory (Thimann and Schneider, 1938,
1939. Compare Fig. 2, arrow C). Thimann and Schneider
(1938, p. 641) believed they had solved a classical problem:
'The differences in the auxin response of different tissues are
the principal cause of the tissue tension studied by the older
botanists'.
The differential-auxin-response hypothesis was a typical
cell-theoretical model insofar as the cells in an organ were
envisaged as qualitatively identical entities, the behaviour of
which explained the behaviour of the organ as a whole. The
model bore two obvious implications. First, tissue tension
was a "solved problem within the cell-theoretical paradigm,
i.e. the elements of the compound phenomenon were
understood, and no more investigations into its nature were
necessary. In fact, Thimann and Schneider's (1938) graphs
were reproduced in numerous text-books and research
reports (e.g. Rietsema, 1950; Bunning, 1953). We suggest
that this situation explains the almost complete absence of
research on differential tensions and their relation to growth
in the following four decades. Second, for future research on
the cellular mechanism of auxin action the cell type studied
would be irrelevant. Against this theoretical background
any doubts about the qualitative identity of cells concerning
auxin action would, of course, necessitate reconsideration
of the developmental causes of tissue tension.
Criticism of the model, which was raised immediately
(Went, 1939), did not question the basic similarity of all cells
with respect to auxin action. Instead, cell-theoretical notions
were applied in an even stricter sense. Suggesting quantitatively identical auxin sensitivities in all cells, Went (1939,
p. 406) claimed that 'tissue tension is due to differential
auxin content of the inner and outer tissue'.
The epidermis in control
Studies on the nature of tissue tension, or the implications
of organ mechanical architecture for cell physiology, were
rare in the decades following Thimann and Schneider's
work, indicating a wide acceptance of their model. The few
exceptions (e.g. Masuda and Yamamoto, 1972; Yamamoto
et al., 1974), though undoubtedly valuable contributions,
did not trigger the elaboration of an alternative biomechanical hypothesis. Models of similar structure, i.e. explanations of complex developmental processes by gradients of
either growth hormone or hormone sensitivity, had been
established for many problems, particularly for tropic
curvatures (Cholodny, 1928; Went, 1928).
661
In a review on this topic Firn and Digby (1980) suggested
that 'it is now time to go back and look in detail what
happens during a tropic curvature and to build theories on
firmer foundations' (p. 145). Thus the hormone concept
within its cell-theoretical framework apparently was unsuccessful in supplying a unanimously accepted theory of
tropisms. Firn and Digby (1977) had indeed formulated a
model of shoot geotropism, which did not include hormones
at all. Their starting point was virtually identical to
Hofmeister's, inasmuch as a characterization of differential
tensions in an organ formed the basis of the modelling of the
mechanics of the organ's geotropic curvature. The outer
tissues, found to constrain organ elongation, were suggested
to be the sole geoperceptive and georesponsive elements
within the organ. Gravitation-induced elongation growth
would only occur in the peripheral layers of the lower side,
thus evoking the curvature. Again, a developmental explanation for differential tensions is beyond the scope of the
model. Tissue tension rather is included as a condition
under which the proposed mechanism can occur.
More recently, Kutschera (1987) proposed a similar
mechanism of auxin-mediated elongation growth. The
hypothesis is based on a mechanical model of growing plant
organs (Fig. 3), in which 'the peripheral wall(s) act
analogously to the wall of the Nitella cell, whereas the inner
tissue as a whole can be regarded as a giant, pressurized
protoplast' (Kutschera and Kohler, 1992, p. 1580). Since
such a system is characterized by the distribution of tensile
and compressive stresses, Kutschera (1989) suggested to
speak of'tissue stresses' rather than of'tissue tension' (but
see the above remark on the original meaning of the term
Gewebespannung).
The model departs from classical cell theory by interpreting the whole organ as one supercell, to which concepts
of cellular biomechanics can be applied. Just as the cell wall
restricts the expansion of the protoplast in a Nitella cell, the
outer tissues are thought to restrict growth in an organ. This
seems to imply that 'the control over the rate of organ
growth can only be brought about by changes in the
mechanical properties of the rigid, extension-limiting peripheral walls' (Kutschera, 1992, p. 251). The model of auxin
action in shoots is constructed accordingly. Auxin is
postulated to exert its growth promoting cellular effects
(leading to wall loosening) exclusively in the epidermis. On
the other hand, inner tissues elongate by means of an
unknown 'IAA-independent growth process' (Kutschera,
1987, p. 223). Consequently, cellular auxin effects should be
classifiable into growth-relevant and -irrelevant ones by the
criterion of their exclusive occurrence in the epidermal
tissue (Kutschera, 1987; Dietz, Kutschera and Ray, 1990).
Tissue tension forms a conditio sine qua non for the
suggested mechanism of auxin-mediated elongation. Wallloosening in the epidermis exclusively would remain without
effect if this issue would not have gained a special function
by the prior establishment of differential tensions. The
explanation for this developmental process, however, is
beyond the scope of the model. Kutschera (1992) lists a
number of structural features which appear to establish a
special mechanical role of the epidermal walls. However, no
developmental causation for differential tensions is offered.
662
Peters and Tomos—The History of Tissue Tension
functional implications of their concept:' Since the pith is in
a state of compression, any increased length of the cortical
tissue must result in an increase in the length of the whole
shoot' (Darwin and Acton, 1907). But since the cellanalogous organ was understood to be a result of the
growth process, the conclusions concerning the control of
organ growth, which appear plain and inevitable if the
existence of differential tensions is presupposed (Kutschera,
1987, 1992), had in fact never been drawn.
C O M M E N T S ON THE C U R R E N T
DISCUSSION
E
OT
E
IT
OT
tensile
compressive
Stress profile
FIG. 3. Model of a growing shoot, as formulated as the basis of the
epidermal-growth-control hypothesis (combined after Kutschera 1987,
1989, 1992). The thick and rigid walls of the outer tissues (OT),
especially the outer one of the epidermis (E), bear the turgor-induced
tensile stress of the whole organ. The walls of the inner tissues (IT) do
not contribute to this stress-bearing; they are kept in a state of
compression by the outer tissues, which resist their tendency to expand.
The mutually induced stresses in the different tissues are schematically
indicated in the stress profile at the bottom. Multicellular shoots are
thus mechanically analogous to the giant internode cells of Nitella: the
outer tissues resemble the cell wall, whereas the inner tissues are
equivalent to a single protoplast.
In the logic of the hypothesis, auxin occupies a position
identical to the one external mechanical stimuli did in
Hofmeister's model. Compared to the model of Thimann
and Schneider, the result is turned into a premise: auxin acts
on tissue tension—it does not cause it any more. It is a
telling detail that the mechanical analogy between single
cells (such as Nitella internodes) and multicellular organs
formerly had been employed to underline the significance of
differential tensions to the stiffness of non-lignified organs
(e.g. Sachs, 1875; Strasburger et al., 1898; Bennecke and
Jost, 1923; Bower, 1923). To judge from the contemporary
literature, these researchers were fully aware of the
In the present study we discuss the historical development in
the field of the biomechanics of elongating plant stems in the
context of major conceptual changes ('paradigm-changes'
in the sense of Kuhn, 1974), such as the establishment of the
cell theory, or the break-through of the hormone concept.
Our historical reconstruction suggests that a major line of
development led from predominantly descriptive models
(e.g. Hales' iatromechanic model) to functional hypotheses,
which considered differential tensions and their immediate
causes as a precondition for certain responses (e.g.
Hofmeister's theory of negative geotropism), and further to
causal hypotheses, which aimed to explain tissue tension
itself by providing developmental causes for its existence.
The most advanced theory of the latter type was the
differential-growth-response hypothesis by Thimann and
Schneider. We interpreted the almost complete absence of
original research on tissue tension in the four decades after
1940 as an indicator of the wide acceptance of this
hypothesis.
Functional and causal hypotheses as defined above differ
in scope. Therefore, a number of functional hypotheses
might be compatible with a single causal one. For example,
the ideas on shoot geotropism put forward by Firn and
Digby (1977) are as such compatible with the differentialgrowth-response hypothesis (Thimann and Schneider,
1938). The case is different with the currently muchdiscussed epidermal-growth-control hypothesis (Kutschera,
1987, 1992), which undoubtedly classifies as a functional
hypothesis. It is simply impossible that both this m'odel,
which explains auxin action on the background of preexisting differential tensions, and the differential-growthresponse hypothesis, which explains differential tensions as
an effect of auxin action, are equally valid. Similarly, the
claim that elongation growth is controlled by the epidermal
layers in general (Kutschera, 1992), calls into question all
interpretations of tissue tension since the 1860s, which
explained the elongation-restricting role of the epidermis as
a result of the growth process. Thus, if one accepts the
epidermal-growth-control hypothesis as it stands, one
abandons all causal hypotheses on differential tensions so
far formulated. As an alternative, it has been suggested that
structural characters of organs, such as different wall
diameters in different tissues, might be sufficient to explain
the occurrence of differential tensions (Kutschera, 1992).
However, such explanations are merely descriptive, and in
this respect do not differ from iatromechanic accounts.
Peters and Tomos—The History of Tissue Tension
Moreover, some older studies suggest that the evaluation
of the structural causes of tissue tensions might not be
simple at all. Tissue tensions are not only found in highly
developed plants, but also in organs lacking histological
differentiation such as mushroom stalks (Sachs, 1874;
Pfeffer, 1904). Pronounced tissue tensions occur in macroscopic marine algae as well. Here the outer tissues' small,
thick-walled cells are kept under compression by the bigger,
thin-walled ones of the central tissues (Kiister, 1899; we find
his results readily reproducible). The correlation between
wall-thickness distribution and differential tensions in
marine algae therefore is the reverse of that in stems of most
seed-plants. However, the situation in macroalgae may be
comparable to the formation of the central cavity in
angiosperm stems, where the thin-walled pith does not
follow the growth of the thick-walled outer tissues and
disintegrates (Kiister, 1899). Another argument questioning
the .validity of structural characters as causal explanations
for the occurrence of tissue tension can be drawn from the
function of pulvini, the motor organs for leaf movement. In
his historic sketch, Wetherell (1990, p. 73) concluded with
reference to Sachs (1887): 'Sachs understood pulvinar
movements, as we do today, in terms of reversible "... tissuetensions of extraordinary magnitude'...' (our italics).
Apparently, regular reversions of differential tension can
occur without modification of organ structure. Thus, tissue
tensions can certainly not be satisfactorily explained by
structural characters.
We have to infer that differential wall-thickness or
histological differentiation do not suffice to explain the
immediate, let alone developmental causes of differential
tensions. We conclude that to date we lack any sound
alternative to Sachs' assumption, that a mechanical architecture allowing for tissue tension to occur is established in
an organ by differential growth (i.e. differential rates of
wall-loosening; compare Tomos, Malone and Pritchard,
1989; Brown, Sommer and Pienaar, 1995). Recent data
from rice (Oryza sativa L.) internodes, in which gibberellin
is involved in the response to submergence by promoting
elongation growth (Raskin and Kende, 1984), should be
considered in this context. Whereas slowly growing internode sections in water do not possess significant tissue
tensions, sections growing rapidly in gibberellin solutions
do (Hoffmann-Benning and Kende, 1994). The induction of
tissue tension by gibberellin, concurrent with growth
promotion, suggests that this 'hormone' induces higher
rates of wall-loosening in the inner tissues than in the outer
ones, at least during the initial phase of the response.
Gibberellin action in rice internodes thus could provide a
model for the establishment of differential tensions during
organ elongation.
The above problems passed unnoticed in the current
debate. This may be because recent historical accounts did
not attempt to reconstruct historic hypotheses as they were
understood by contemporary practitioners. As a result,
gross misinterpretations occurred. For example, summarizing Sachs' contribution, Kutschera (1987, p. 216) claimed
that ' Sachs suggested that a plant organ can only grow as
long as tissue tension is established'. This interpretation is
not only untenable, since it reverses the cause-effect
663
relationship of tissue tension and growth as elaborated by
Sachs; it actually misconstrues Sachs' causal hypothesis as
a functional one, thereby obscuring the fundamental
difference between the epidermal-growth-control hypothesis
and its predecessor.
Finally, we feel that some remarks on the 'organismal
concept of multicellularity' (Kaplan, 1992) should be made.
In short, the organismal concept claims that the evolution
of multicellularity in plants took place by compartmentation
of unicellular organisms, and not by accumulation of the
latter (Kaplan and Hagemann, 1991). Noteworthily this is a
phylogenetic statement. As such the concept is compatible
with functional changes of different organ parts during
further evolutionary developments. The idea that plant
organs behave according to the concept, if their outermost
tissue functions analogously to the wall of a single cell
(Kutschera, 1995), interprets the phylogenetic concept as a
functional one. However, a functional interpretation of
plant organs as ' supercells' is not implied by the organismal
concept. In fact, on the background of the organismal
concept the suggestion has been put forward that the
adaptive significance of multicellularity lies within the inner
cell walls' contribution to the mechanical properties of the
whole organ (Niklas and Kaplan, 1991).
With respect to organ growth, the organismal concept
claims that an understanding of whole organ mechanics
forms the basis of the understanding of the mechanical role
single cells may play within the organ (Hofmeister, 1867;
Kaplan and Hagemann, 1991; Kaplan, 1992). Considering
differential tensions, one may doubt whether either type of
understanding has been achieved yet.
ACKNOWLEDGEMENTS
WSP thanks Prof. Dr Wolfgang Hagemann (Heidelberg)
and Dr Dieter Mollenhauer (Biebergemund) for helpful
discussion of the significance of the organismal concept and
the cell theory. Dr Richard Firn's (York) remarks on an
earlier version of the text made us aware of a number of
unclear formulations and ambiguous statements. This work
was supported by a NATO postdoc fellowship from the
Deutscher Akademischer Austauschdienst to WSP.
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