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 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 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-auxin- 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 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 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), cell theory, 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 organ 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 nature 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 life 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 shoots 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 shoot 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 organisms 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 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 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 organism 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 meristem 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