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Living Cells in Wood. 1. Absence, Scarcity and Histology of Axial

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Living Cells in Wood. 1. Absence, Scarcity and Histology of Axial bs_bs_banner Botanical Journal of the Linnean Society, 2015, 177, 291–321. With 13 figures Living cells in wood. 1. Absence, scarcity and histology of axial parenchyma as keys to function Downloaded from https://academic.oup.com/botlinnean/article-abstract/177/3/291/2416378 by guest on 15 November 2018 SHERWIN CARLQUIST FMLS* Santa Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, CA 93105, USA Received 22 September 2014; revised 15 December 2014; accepted for publication 16 December 2014 The diversity of expression in axial parenchyma (or lack of it) in woods is reviewed and synthesized with recent work in wood physiology, and questions and hypotheses relative to axial parenchyma anatomy are offered. Cell shape, location, abundance, size, wall characteristics and contents are all characteristics for the assessment of the physiological functions of axial parenchyma, a tissue that has been neglected in the consideration of how wood histology has evolved. Axial parenchyma occurrence should be considered with respect to mechanisms for the prevention and reversal of embolisms in tracheary elements. This mechanism complements cohesion–tension-based water movement and root pressure as a way of maintaining flow in xylem. Septate fibres can substitute for axial parenchyma (‘axial parenchyma absent’) and account for water movement in xylem and for the supply of carbohydrate abundance underlying massive and sudden events of foliation, flowering and fruiting, as can fibre dimorphism and the co-occurrence of septate fibres and axial parenchyma. Rayless woods may or may not contain axial parenchyma and are informative when analysing parenchyma function. Interconnections between ray and axial parenchyma are common, and so axial and radial parenchyma must be considered as complementary parts of a network, with distinctive but interactive functions. Upright ray cells and more numerous rays per millimetre enhance interconnection and are more often found in woods that contain tracheids. Vesselless woods in both gymnosperms and angiosperms have axial parenchyma, the distribution of which suggests a function in osmotic water shifting. Water and photosynthate storage in axial parenchyma may be associated with seasonal changes and with succulent or subsucculent modes of construction. Apotracheal axial parenchyma distribution often demon- strates storage functions that can be read independently of osmotic water shifting capabilities. Axial parenchyma may serve to both enhance mechanical strength or, when parenchyma is thin-walled, as a tissue that adapts to volume change with a change in water content. Other functions of axial parenchyma (contributing resistance to pathogens; a site for the recovery of physical damage) are considered. The diagnostic features of axial parenchyma and septate fibres are reviewed in order to clarify distinctions and to aid in cell type identification. Systematic listings are given for particular axial parenchyma conditions (e.g. axial parenchyma ‘absent’ with septate fibres substituting). A knowledge of the axial parenchyma information presented here is desirable for a full understand- ing of xylem function. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 177, 291–321. ADDITIONAL KEYWORDS: conductive safety – embolism reduction – osmotic water shifting – rays – septate fibres – water storage – wood evolution – wood physiology. INTRODUCTION the conducting cells of wood (vessel elements and tracheids, both with prominent bordered pits) and the Ray and axial parenchyma are often considered as the mechanically important fibrous cells (fibre-tracheids two living types of cell in woods and are figured in and libriform fibres), which are mostly dead at matu- textbooks, but their functions and diversity are rity, are linked in textbooks to conductive functions, mostly left unexplored in such sources. By contrast, and therefore have been the topic, if only indirectly, of much physiological experimentation. Septate fibres, which are mostly libriform fibres with prolonged lon- *E-mail: [email protected] gevity, are a type of living cell in wood that has been © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 177, 291–321 291 292 S. CARLQUIST little studied: one must reach back to the papers of impression, if only indirectly, that ‘primitive’ woods Wolkinger (1969, 1970a, b) to find even condensed are inefficient at conduction, whereas ‘advanced’ consideration. The phenomenon of fibre dimorphism woods excel at conduction, and that plants with (Carlquist, 1958, 1961, 2014), in which libriform ‘primitive’ woods are evolutionarily limited by their fibres of two sorts (narrower, thicker walled vs. wider, wood formulae and are marginalized by plants with thinner walled, often alive at maturity) are present in more efficient, upgraded, wood anatomy. However, a given wood, has been noticed by only a small plants with putatively plesiomorphic wood features number of workers, despite its conspicuous occur- coexist with those that have apomorphic wood fea- rence in such familiar woods as maple, Acer L. Even tures, so that both patterns must be entirely func- Downloaded from https://academic.oup.com/botlinnean/article-abstract/177/3/291/2416378 by guest on 15 November 2018 criteria for the recognition of the cell types mentioned tional, although in plants with different ecology and above are not easily located in wood anatomical lit- growth form. The present article takes the point of erature. The monographs of Wolkinger cover ‘leb- view that the various anatomical formulae of wood enden Fasern’, but we do not have a clear idea of how anatomy must be understood as varied but effective long ‘living fibres’ live. Septate fibres are assumed to ways of dealing with water economy. We cannot be ‘living fibres’, but some may not live much longer understand how xylem works by studying only Zea L. than non-septate libriform fibres. We have little infor- or Helianthus L., convenient though they may be. mation because wood anatomy is still largely based on Although wood physiology seems to be drifting away dried rather than liquid-preserved specimens. from the study of wood anatomical diversity, ulti- There is growing interest in axial parenchyma mately the two must coalesce. The present article among wood physiologists (Spicer, 2014), because of does not form such a bridge, but it does indicate the the conviction that such a commonly present cell complexity of axial parenchyma, a complexity which type, often distributed adjacent to vessels and trac- therefore must ultimately be explained in evolution- heids, must perform some function related to the ary and physiological terms. conductive process. The ‘osmotic water shifting’ ideas In order to satisfy the needs of descriptive wood of Braun (1970) proposed that the development of anatomy, Kribs (1935, 1937) and Metcalfe & Chalk higher osmotic pressures, chiefly through the conver- (1950) categorized types of ray and axial parenchyma sion of starch into sugar (both found in axial paren- on the basis of histological features. In the case of chyma as well as in rays), could draw water from one axial parenchyma, location with respect to vessels or cell into another and thus function in the conductive to growth rings, grouping and abundance were the process. This was formalized into a theory of com- main criteria used by Kribs (1937). Both Kribs (1937) pensating pressure by Canny (1995, 1998), although and Metcalfe & Chalk (1950) recognized an axial these ideas have been met with scepticism parenchyma type, ‘Absent’, which seems paradoxical (Comstock, 1999). However, there are other ways in at first glance. If axial parenchyma is absent, what which differential solute concentrations in axial substitutes for its functions? In turn, this raises the parenchyma may be achieved and function in con- question, what are the functions of axial parenchyma duction, as exemplified by Holbrook & Zwieniecki when it is present? These questions were asked vir- (1999) and Zwieniecki & Holbrook (2000, 2009). Wood tually not at all in the mid-20th century, in which physiologists currently express interest in, and offer accurate anatomical description of the woods of the varied hypotheses on, the function of axial paren- world was seen as the task at hand, and in which chyma. Several are of the opinion that no clear questions pertaining to wood evolution in a functional understanding of how parenchyma contributes to the context went unasked and therefore unanswered. conductive process exists. A consensus on exactly how Despite the obvious and pervasive modes of cell pres- axial parenchyma may function in the prevention or ence and diversity in woods, hypotheses about func- countering of embolisms has not yet been reached, tion were often considered as ‘speculative’ instead of but the current state of this field is discussed below. the legitimate hypotheses that they were, and thus The presence, absence, scarcity, distribution within a wood physiology was deprived of some pertinent ques- wood and histology of axial parenchyma are not inde- tions. For example, do all manifestations of axial pendent of wood physiology. Rather, they must even- parenchyma have the same function? The role of axial tually be integrated into any interpretations of parenchyma in the conductive process was probably parenchyma with relation to conduction in plants. also ignored because laboratory equipment, although The patterns described in this article are offered in easily connected
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