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Home , Tissue (biology)

Annals of 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 Downloaded from https://academic.oup.com/aob/article/77/6/657/2389842 by guest on 30 September 2021 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 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-- response-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 theory and the 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 of more recent criticism of hormonal theories of tropic curvature, and particularly the epidermal- growth-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), , elongation growth, geotropism, hormone concept, tissue tension.

The historian, and especially the historian-scientist, can, I important aspects of the control of tissue tension have been believe, become too easily beguiled by the power of present overlooked. scientific theory, and consequently imagine that its ancestor In the present paper we attempt to reconstruct some of theory carried the same logical implications, which are then the more influential hypotheses on growth mechanics. presumed to have stood clear to the earlier practitioners. In particular we will concentrate on the theoretical R. J. Richards (1992) framework, in which the models were formulated, and on the experimental strategies deduced from them. While analysing the models, we purposefully will refrain from re- INTRODUCTION evaluating the significance of experimental results per se. By Plant organs do not consist of mechanically homogenous doing so we hope to avoid interpreting the historic theories material, but usually are found to exist in states of mutual on the basis of present knowledge. Interpretations of the tensions between their different parts. Such tissue tensions latter type are likely to over-emphasize factors, which become apparent upon organ dissection, when dramatic presumptively correspond to modern views, and neglect bendings or coilings occur. Their was vividly debated aspects, which have gone out of fashion, even if they were in the second half of the last century (e.g. Sachs, 1874). highly important at their time. For due discussion of these Remarkably, original research on tissue tension seems to different historiographical approaches see Agassi (1963), have ceased at about 1940. Tissue tension has regained Kuhn (1969, 1977) and Bayertz (1980). interest in recent years (Firn and Digby, 1977; Heijnowicz Our aim in this paper, however, is more than a mere and Sievers, 1995), leading to the formulation of the correction of inaccurate views of a historic process. hypothesis that plant organ growth is controlled by the Experimental strategies do not simply emerge from bodies epidermal tissue (Kutschera, 1987, 1992). Surprisingly, the of established knowledge; rather they are constructed on origin of this notion has been ascribed to scientists as distant the basis of hypotheses. One may doubt whether it is always in time and theoretical background as Kraus (1867; the most recent hypotheses which automatically provides Kutschera, 1992) or Thimann and Schneider (1938; the soundest foundation for future research (Kuhn, 1969). Edelmann, Bergfeld and Schopfer, 1989). We feel that here, In returning some older concepts to the current discussion, and in some other cases, assessments of the historical we hope to broaden the spectrum of justifiable research development of the topic are inaccurate. As a result 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 658 Peters and Tomos—The History of Tissue Tension explanations for activities in their exact mechanical THE HISTORY OF TISSUE TENSION descriptions, was applied to botany on a large scale by Vegetable Staticks Stephen Hales. In his Vegetable Staticks (1961; originally published 1727) he described growth tests, which resemble In the 17th century, the transfer to the medical sciences of modern measurements of relative elemental growth rates, mathematical and mechanical principles, which had proven and discussed the mechanical role of various parts of so successful in physics, resulted in the ' iatromechanics' of in elongation growth (see his Experiment CXXIII). He Sanctorius, Giovanni Borelli, William Harvey and others. based his considerations on Borelli's assumption (1927; first The iatromechanical concept, namely to search causal 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 at the nodes (Fig. 1). Thereby the outer parts of the shoot Downloaded from https://academic.oup.com/aob/article/77/6/657/2389842 by guest on 30 September 2021 (' 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 as N N 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 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 unless ideas of preformation were employed.

The theoretical background in the 19th century 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 Natur- philosophie on one side, and the reductionism of the inductivistic programme on the other. A major break- through for the latter is marked by the formulation of the cell theory (Schleiden, 1838; Schwann, 1839; for review see N N 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 fun- damental power of single cells' [Schwann, 1839, p. 229 (All translations of quotations from the German by WSP.)]. Relevant physiological research thus should be performed V Pith V on the cellular level, since the represents but an FIG. 1. Schematic cross-section of a growing stem as a model of the arrangement of cells (Schleiden, 1842). mechanics of internode elongation growth as formulated by Stephen Wilhelm Hofmeister challenged the cell theoreticists' Hales in the Vegetable Staticks of 1727. The pith expands due to water doctrine (Hagemann, 1992; Kaplan, 1992), and maintained uptake, and thus exerts pressure on the nodes (N), which act as that 'the growth of single cells within a is abutments. Thereby the nodes are pushed apart, leading to passive regulated and determined by...the mass increase of the lengthening of the 'vessels' (i.e. vascular bundles and other peripheral tissues; V). Forming rigid cross-sectional bridges, the nodes prevent the meristem as a whole. This mass increase cannot be construed vessel cylinder from yielding in the radial direction. as the sum of the generating powers within the individual Peters and Tomos—The History of Tissue Tension 659 cells' (Hofmeister, 1867, p. 129). Experimental strategies 1886; Kuster, 1899), before cellular mechanics in the modern derived from this organismal concept, within which 'the sense were unanimously accepted (see, e.g. Pfeffer, 1904). degree to which so-called cell enlargement occurs is simply Hofmeister did not go into detail regarding the develop- a marker of organ expansion' (Kaplan, 1992, p. S31), will mental causes of tissue tension, which therefore remained obviously differ from the above. It appears that despite the an unexplained presupposition in his model. There is but intervening 130 years the implications of this dichotomy one short remark on this issue in his description of remain to be resolved (Kaplan and Hagemann, 1991; Sitte, geotropism in : 'During and after elongation, 1992). We believe that the subsequent development of differences of tension occur between the central tissues and theories on growth mechanics can only be properly the of the elongated internode: the latter is understood against this theoretical background. 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 Downloaded from https://academic.oup.com/aob/article/77/6/657/2389842 by guest on 30 September 2021 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 shoots as induced by external mechanical stimuli Julius Sachs' review-like essay of 1865 (chapter XIII) (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 and ' (p. 254). He phenomena became... a mere 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 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 intus- which 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 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 ter- century (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 (, 1886, pp. 343, our italics). [For the proper understanding of the historic texts it is important 100 - 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 & 50 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 Downloaded from https://academic.oup.com/aob/article/77/6/657/2389842 by guest on 30 September 2021 from outside the growing cells (Sachs, 1875; for a 10 8 6 4 particularly straight-forward application of the concept see Auxin concentration (-log M) Kiister, 1899). The causal analysis of differential tensions in shoots thus seems to have supported a similar interpretation FIG. 2. Schematic representation of the differential-auxin-response hypothesis (combined after Thimann and Schneider, 1938, 1939). Two of the role of the outer tissues in organ growth as that of separate curves showing the dose-response to auxin of elongation Hales' iatromechanical approach (see above). growth of the inner ( ) and outer tissues ( ) of a growing shoot. The insight that 'tissue tension is indeed a result of Outer tissues are capable of faster growth at optimal auxin concen- differential tissue growth' (Kraus, 1867, p. 108) had trations, but inner tissues react to smaller amounts of the hormone. consequences for Hofmeister's model of negative geotro- Physiological auxin concentrations are in the range of stronger re- sponses in the inner tissues (a), which causes the observed tissue tensions. pism. Changes in the intensity of differential tensions now By artificially elevating the auxin level into the range of optimal were interpreted as results of growth processes, just like response of the outer tissues, the direction of the tissue tension gradient differential tensions themselves resulted from growth. It can be reversed (b). This is the mechanism of the Went-reaction in the followed that' the change in tissue tension in the convex and split-pea-test. Very low exogenous auxin concentrations induce increased normal (concave) curvature in auxin-depleted segments (c). 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 numerous inconsistencies appeared (for discussion see after the review by Schober, 1899). Zimmermann and Wilcoxon, 1935; Trewavas, 1981, 1986; Further research focused on the nature of cell growth in Firn and Myers, 1987; Hathway, 1990). Not surprisingly general, and the regulation of differential growth in 'the leading idea that correlations in are due to the particular. At the end of the century the cell theory was influence of special substances' (Went and Thimann, 1937, practically unanimously accepted (Hansen, 1897). In this p. 2) was soon utilized to formulate a model for the theoretical environment, differential tensions had only development of tissue tension in growing shoots. limited value, serving as indicators of prior differential cell Kenneth Thimann had proposed in 1937 that 'the curve growth. Ludwig Jost (1908) put it unmistakably: 'In former of response against auxin concentration is... of the same times tissue tension was studied with great care, since general shape for each organ, though shifted horizontally or insights into various physiological phenomena were expec- vertically' (quoted from Thimann and Schneider, 1938, p. ted from such investigations. However, these expectations 635), namely bell-shaped. This differential-auxin-response were not fulfilled. Therefore we will no longer discuss those hypothesis is commonly found in modern textbooks still. matters, but consider again the differentiation of cells in a The explanation of how tissue tensions could arise was meristem' (p. 350). The mechanism of differential cell constructed by transferring its logic from organs to cells: growth was obscure still. Differential cell turgor was '... the same relations hold for the individual layers of cells suggested to play the key role (de Vries, 1919; Went, 1933). within a given organ. In the pea stem, the innermost But it was not before the application to the problem of the layers—i.e. the pith—reach their maximum elongation at hormone concept, that a generally accepted theory was relatively low auxin concentrations, the outermost, on the formulated. 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 The advent of contrary, highest sensitivity in terms of maximum inducible One difficulty implicit to the cell theory lies in the effect is found in the epidermis (Fig. 2; compare Firn, 1986, necessity to explain the neat coordination of the huge for a discussion of the ambiguity of the term 'sensitivity'). number of individual 'elementary organisms', which form In the intact plant, however, auxin concentrations had to be the multicellular entity. The endocrinological hormone postulated to be in a range in which elongation was concept provides a mechanism by which such correlations promoted stronger in the inner tissues than in the epidermis, could be explained. After a series of successes in zoological in order to account for the observed direction of the tension fields in the 1920s (for review see Karlson, 1982), the gradient (Fig. 2, arrow A). Following the logic of the concept was readily acquired by plant physiologists (e.g. hypothesis, the Went-reaction (the auxin-dependent reversal Boysen-Jensen, 1936; Went and Thimann, 1937), although of tissue tension in the split-pea test; Went, 1934) had to be Peters and Tomos—The History of Tissue Tension 661 interpreted as an effect induced by unphysiologically high In a review on this topic Firn and Digby (1980) suggested hormone concentrations (Fig. 2, arrow B). that 'it is now time to go back and look in detail what Thimann and Schneider saw their theory supported by happens during a tropic curvature and to build theories on several lines of evidence. First there was the finding that firmer foundations' (p. 145). Thus the hormone concept ' peeled sections of both Pisum and Avena respond very well within its cell-theoretical framework apparently was un- to auxin' (Thimann and Schneider, 1938, p. 629), or 'in successful in supplying a unanimously accepted theory of other words, the sensitivity of peeled material to auxin is tropisms. Firn and Digby (1977) had indeed formulated a certainly no less than that of normal material in the same model of shoot geotropism, which did not include hormones experiment' (p. 630). Second, auxin dose-response curves of at all. Their starting point was virtually identical to isolated tissues appeared to be in accord with the theory Hofmeister's, inasmuch as a characterization of differential (Thimann and Schneider, 1938). Third, in auxin-depleted tensions in an organ formed the basis of the modelling of the material very low auxin concentrations seemed to increase mechanics of the organ's geotropic curvature. The outer the naturally occurring concave bending, an effect readily tissues, found to constrain organ elongation, were suggested Downloaded from https://academic.oup.com/aob/article/77/6/657/2389842 by guest on 30 September 2021 explained by the theory (Thimann and Schneider, 1938, to be the sole geoperceptive and georesponsive elements 1939. Compare Fig. 2, arrow C). Thimann and Schneider within the organ. Gravitation-induced elongation growth (1938, p. 641) believed they had solved a classical problem: would only occur in the peripheral layers of the lower side, 'The differences in the auxin response of different tissues are thus evoking the curvature. Again, a developmental ex- the principal cause of the tissue tension studied by the older planation for differential tensions is beyond the scope of the botanists'. model. Tissue tension rather is included as a condition The differential-auxin-response hypothesis was a typical under which the proposed mechanism can occur. cell-theoretical model insofar as the cells in an organ were More recently, Kutschera (1987) proposed a similar envisaged as qualitatively identical entities, the behaviour of mechanism of auxin-mediated elongation growth. The which explained the behaviour of the organ as a whole. The hypothesis is based on a mechanical model of growing plant model bore two obvious implications. First, tissue tension organs (Fig. 3), in which 'the peripheral wall(s) act was a "solved problem within the cell-theoretical paradigm, analogously to the wall of the Nitella cell, whereas the inner i.e. the elements of the compound phenomenon were tissue as a whole can be regarded as a giant, pressurized understood, and no more investigations into its nature were protoplast' (Kutschera and Kohler, 1992, p. 1580). Since necessary. In fact, Thimann and Schneider's (1938) graphs such a system is characterized by the distribution of tensile were reproduced in numerous text-books and research and compressive stresses, Kutschera (1989) suggested to reports (e.g. Rietsema, 1950; Bunning, 1953). We suggest speak of'tissue stresses' rather than of'tissue tension' (but that this situation explains the almost complete absence of see the above remark on the original meaning of the term research on differential tensions and their relation to growth Gewebespannung). in the following four decades. Second, for future research on The model departs from classical cell theory by inter- the cellular mechanism of auxin action the cell type studied preting the whole organ as one supercell, to which concepts would be irrelevant. Against this theoretical background of cellular can be applied. Just as the any doubts about the qualitative identity of cells concerning restricts the expansion of the protoplast in a Nitella cell, the auxin action would, of course, necessitate reconsideration outer tissues are thought to restrict growth in an organ. This of the developmental causes of tissue tension. seems to imply that 'the control over the rate of organ Criticism of the model, which was raised immediately growth can only be brought about by changes in the (Went, 1939), did not question the basic similarity of all cells mechanical properties of the rigid, extension-limiting per- with respect to auxin action. Instead, cell-theoretical notions ipheral walls' (Kutschera, 1992, p. 251). The model of auxin were applied in an even stricter sense. Suggesting quan- action in shoots is constructed accordingly. Auxin is titatively identical auxin sensitivities in all cells, Went (1939, postulated to exert its growth promoting cellular effects p. 406) claimed that 'tissue tension is due to differential (leading to wall loosening) exclusively in the epidermis. On auxin content of the inner and outer tissue'. 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 The epidermis in control classifiable into growth-relevant and -irrelevant ones by the Studies on the nature of tissue tension, or the implications criterion of their exclusive occurrence in the epidermal of organ mechanical architecture for cell , were tissue (Kutschera, 1987; Dietz, Kutschera and Ray, 1990). rare in the decades following Thimann and Schneider's Tissue tension forms a conditio sine qua non for the work, indicating a wide acceptance of their model. The few suggested mechanism of auxin-mediated elongation. Wall- exceptions (e.g. Masuda and Yamamoto, 1972; Yamamoto loosening in the epidermis exclusively would remain without et al., 1974), though undoubtedly valuable contributions, effect if this issue would not have gained a special function did not trigger the elaboration of an alternative biomech- by the prior establishment of differential tensions. The anical hypothesis. Models of similar structure, i.e. explana- explanation for this developmental process, however, is tions of complex developmental processes by gradients of beyond the scope of the model. Kutschera (1992) lists a either growth hormone or hormone sensitivity, had been number of structural features which appear to establish a established for many problems, particularly for tropic special mechanical role of the epidermal walls. However, no curvatures (Cholodny, 1928; Went, 1928). 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 cell- analogous 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.

COMMENTS ON THE CURRENT Downloaded from https://academic.oup.com/aob/article/77/6/657/2389842 by guest on 30 September 2021 DISCUSSION In the present study we discuss the historical development in E E 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 OT IT OT 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 tensile hypothesis. Functional and causal hypotheses as defined above differ compressive in scope. Therefore, a number of functional hypotheses Stress profile might be compatible with a single causal one. For example, FIG. 3. Model of a growing shoot, as formulated as the basis of the the ideas on shoot geotropism put forward by Firn and epidermal-growth-control hypothesis (combined after Kutschera 1987, Digby (1977) are as such compatible with the differential- 1989, 1992). The thick and rigid walls of the outer tissues (OT), growth-response hypothesis (Thimann and Schneider, especially the outer one of the epidermis (E), bear the turgor-induced 1938). The case is different with the currently much- 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 discussed epidermal-growth-control hypothesis (Kutschera, compression by the outer tissues, which resist their tendency to expand. 1987, 1992), which undoubtedly classifies as a functional The mutually induced stresses in the different tissues are schematically hypothesis. It is simply impossible that both this m'odel, indicated in the stress profile at the bottom. Multicellular shoots are which explains auxin action on the background of pre- thus mechanically analogous to the giant internode cells of Nitella: the existing differential tensions, and the differential-growth- outer tissues resemble the cell wall, whereas the inner tissues are equivalent to a single protoplast. response 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 In the logic of the hypothesis, auxin occupies a position layers in general (Kutschera, 1992), calls into question all identical to the one external mechanical stimuli did in interpretations of tissue tension since the 1860s, which Hofmeister's model. Compared to the model of Thimann explained the elongation-restricting role of the epidermis as and Schneider, the result is turned into a premise: auxin acts a result of the growth process. Thus, if one accepts the on tissue tension—it does not cause it any more. It is a epidermal-growth-control hypothesis as it stands, one telling detail that the mechanical analogy between single abandons all causal hypotheses on differential tensions so cells (such as Nitella internodes) and multicellular organs far formulated. As an alternative, it has been suggested that formerly had been employed to underline the significance of structural characters of organs, such as different wall differential tensions to the stiffness of non-lignified organs diameters in different tissues, might be sufficient to explain (e.g. Sachs, 1875; Strasburger et al., 1898; Bennecke and the occurrence of differential tensions (Kutschera, 1992). Jost, 1923; Bower, 1923). To judge from the contemporary However, such explanations are merely descriptive, and in literature, these researchers were fully aware of the this respect do not differ from iatromechanic accounts. Peters and Tomos—The History of Tissue Tension 663 Moreover, some older studies suggest that the evaluation relationship of tissue tension and growth as elaborated by of the structural causes of tissue tensions might not be Sachs; it actually misconstrues Sachs' causal hypothesis as simple at all. Tissue tensions are not only found in highly a functional one, thereby obscuring the fundamental developed plants, but also in organs lacking histological difference between the epidermal-growth-control hypothesis differentiation such as mushroom stalks (Sachs, 1874; and its predecessor. Pfeffer, 1904). Pronounced tissue tensions occur in macro- Finally, we feel that some remarks on the 'organismal scopic marine as well. Here the outer tissues' small, concept of multicellularity' (Kaplan, 1992) should be made. thick-walled cells are kept under compression by the bigger, In short, the organismal concept claims that the thin-walled ones of the central tissues (Kiister, 1899; we find of multicellularity in plants took place by compartmentation his results readily reproducible). The correlation between of unicellular organisms, and not by accumulation of the wall-thickness distribution and differential tensions in latter (Kaplan and Hagemann, 1991). Noteworthily this is a marine algae therefore is the reverse of that in stems of most phylogenetic statement. As such the concept is compatible seed-plants. However, the situation in macroalgae may be with functional changes of different organ parts during Downloaded from https://academic.oup.com/aob/article/77/6/657/2389842 by guest on 30 September 2021 comparable to the formation of the central cavity in further evolutionary developments. The idea that plant angiosperm stems, where the thin-walled pith does not organs behave according to the concept, if their outermost follow the growth of the thick-walled outer tissues and tissue functions analogously to the wall of a single cell disintegrates (Kiister, 1899). Another argument questioning (Kutschera, 1995), interprets the phylogenetic concept as a the .validity of structural characters as causal explanations functional one. However, a functional interpretation of for the occurrence of tissue tension can be drawn from the plant organs as ' supercells' is not implied by the organismal function of pulvini, the motor organs for movement. In concept. In fact, on the background of the organismal his historic sketch, Wetherell (1990, p. 73) concluded with concept the suggestion has been put forward that the reference to Sachs (1887): 'Sachs understood pulvinar adaptive significance of multicellularity lies within the inner movements, as we do today, in terms of reversible "... tissue- cell walls' contribution to the mechanical properties of the tensions of extraordinary magnitude'...' (our italics). whole organ (Niklas and Kaplan, 1991). Apparently, regular reversions of differential tension can With respect to organ growth, the organismal concept occur without modification of organ structure. Thus, tissue claims that an understanding of whole organ mechanics tensions can certainly not be satisfactorily explained by forms the basis of the understanding of the mechanical role structural characters. single cells may play within the organ (Hofmeister, 1867; We have to infer that differential wall-thickness or Kaplan and Hagemann, 1991; Kaplan, 1992). Considering histological differentiation do not suffice to explain the differential tensions, one may doubt whether either type of immediate, let alone developmental causes of differential understanding has been achieved yet. tensions. We conclude that to date we lack any sound alternative to Sachs' assumption, that a mechanical archi- tecture allowing for tissue tension to occur is established in ACKNOWLEDGEMENTS an organ by differential growth (i.e. differential rates of wall-loosening; compare Tomos, Malone and Pritchard, WSP thanks Prof. Dr Wolfgang Hagemann (Heidelberg) 1989; Brown, Sommer and Pienaar, 1995). Recent data and Dr Dieter Mollenhauer (Biebergemund) for helpful from rice (Oryza sativa L.) internodes, in which gibberellin discussion of the significance of the organismal concept and is involved in the response to submergence by promoting the cell theory. Dr Richard Firn's (York) remarks on an elongation growth (Raskin and Kende, 1984), should be earlier version of the text made us aware of a number of considered in this context. Whereas slowly growing inter- unclear formulations and ambiguous statements. This work node sections in water do not possess significant tissue was supported by a NATO postdoc fellowship from the tensions, sections growing rapidly in gibberellin Deutscher Akademischer Austauschdienst to WSP. do (Hoffmann-Benning and Kende, 1994). The induction of tissue tension by gibberellin, concurrent with growth promotion, suggests that this 'hormone' induces higher LITERATURE CITED rates of wall-loosening in the inner tissues than in the outer Agassi J. 1963. 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