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

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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 understanding 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 so as to measure processes quanti- the hope that they will further the structure– tatively in tracheary elements (tubes, pressure function dialogue. The various anatomical plans of tanks), could not be applied to actions in axial paren- woods are considered here to represent parsimonious chyma or rays. There are no indexed mentions of formulations that suit the water economy of particu- axial parenchyma (or rays) in Tyree & Zimmermann lar species. In the earlier literature, one is given the (2002). No listings were given by Kribs (1937) or

Metcalfe & Chalk (1950) of genera and families with chyma function in vesselless woody plants, and so ‘Absent’ axial parenchyma. One type of axial paren- vesselless angiosperms, cycads and Ginkgo L. are chyma, which I have called ‘Pervasive’, involves a included here, as are Gnetales. secondary xylem ground plan in which axial paren- Instances of ‘scarce’ (but characteristically present) chyma predominates and contains no ﬁbrous tissue, axial parenchyma in angiosperm woods bring into only vessels (Carlquist, 1988, 2001); this eluded play a hitherto unconsidered question: can rays com- notice in earlier literature, perhaps because of the posed of upright cells substitute in function, to some predominant focus on woodier plants. degree, for axial parenchyma? The ray type ‘Paedo-

‘Axial parenchyma absent’ and ‘Axial parenchyma morphic Type III’ (Carlquist, 1988) designates unise- Downloaded from https://academic.oup.com/botlinnean/article-abstract/177/3/291/2416378 by guest on 15 November 2018 scarce’ are not uniform categories, and unravelling riate rays composed of upright cells. Thus, they are the diversity within these artificial groupings is one of like radial sheets of axial parenchyma. One can also the goals of this article. All expressions relevant to ask whether or not conjunctive tissue formed of these categories are reviewed here, and an attempt is parenchyma cells is a functional equivalent for bands made to analyse not the absence or scarcity of axial of apotracheal parenchyma. Conjunctive tissue occurs parenchyma, but what is the meaning of these struc- only in species with successive cambia, and is pro- tural types. If they are alternative histological adap- duced by a master cambium, not a vascular cambium. tations to what axial parenchyma most commonly Septate fibres and axial parenchyma cells are does, what do they show us? The differences between similar in many respects: both are vertically oriented what axial parenchyma does and what other similar living cells. Are they ‘interchangeable’ in phylogenetic cell types (e.g. septate fibres) do have not yet been terms? The intriguing case of Celastraceae, in which appreciated. Septate fibres have secondary walls either one or the other, but not both, are present, is capable of offering the support of non-septate fibres described here. Going beyond Celastraceae, we tend that are dead at maturity, but their longevity and to find differential distribution patterns for the two contents (starch is common in them) suggest a cell types which suggest modally different functions, mechanical function and a function that involves pho- although the functions may overlap. Instances in tosynthates. In some cases, reports of absent or scarce which both cell types are characteristically present in axial parenchyma are not entirely correct, and such wood of a given species and those that lack one or the cases are analysed here. Rayless woods are consid- other give us a kind of circumstantial evidence on this ered here because, if rays are absent, do these woods point. There are very few mentions in the literature of lack axial parenchyma, which is commonly inter- any cells intermediate between axial parenchyma and linked with rays? septate fibres. The example of fibre dimorphism Axial parenchyma must have multiple functions, as (Carlquist, 2014) is pertinent and is covered here do other cell types (e.g. fibre dimorphism; Carlquist, because the divergence of fibriform cells into two 2014). One of the prominent lessons of wood evolution modes (with intermediacy between them) is not really is that functional change is more easily accomplished an exception: in Acer, one has no difficulty in distin- by small modifications of an existing cell type than by guishing between the dimorphic fibres and axial the invention of new cell types. As one example, the parenchyma. wide axial parenchyma bands of Chorisia Kunth Axial parenchyma is scarce in some angiospermous (Fig. 1F) are indicative of some kind of storage func- woods which have notably long vessel elements (and tion, whereas the occurrence of a few cells of axial imperforate tracheary elements). These woods also parenchyma near vessels (Fig. 4E) or scattered resin- have greater length of axial parenchyma strands filled axial parenchyma (Fig. 12A) suggests functions (which are derived from the same fusiform cambial other than storage. In addition to ‘absent’ or ‘scanty’ initials as vessel elements and imperforate tracheary axial parenchyma, the polar opposite, which I have elements). Such woods also tend to have more numer- named ‘Pervasive’ parenchyma (Carlquist, 1988), in ous rays per millimetre (number of rays that intersect which the fascicular xylem consists wholly of paren- an imaginary transverse scale superimposed on a chyma plus vessels, as in Caricaceae (Carlquist, 1998) tangential section). Thus, there are more points of and some stem succulents, is considered here. The potential contact between axial parenchyma and rays term ‘scanty’ here is not intended to include instances (especially uniseriate rays) in such woods. Does axial in which an extremely small number of axial paren- parenchyma scarcity correspond inversely to ray his- chyma cells are present in a wood, because such tology and ray abundance in such woods? In turn, this rarity of occurrence does not represent effective per- question relates to the three-dimensional distribution formance of a function for the wood as a whole. and interconnections of the ray and axial parenchyma Axial parenchyma is often associated with vessels systems (see Kedrov, 2012). in woody angiosperms. This provides hints about pos- The present article attempts to provide the under- sible function, but we must also explain axial paren- pinnings for answers to questions such as those posed

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Figure 1. Diagnostic features of axial parenchyma and septate fibres. A, B, Siphonodon australis Benth. (Forestry Commission of New South Wales). A, Axial parenchyma cells are much thinner walled than the imperforate tracheary elements. B, Radial section. Intercellular spaces in conjunction with cells of axial parenchyma strands. C, Bowkeria gerrardiana Harv. ex Hiern., cult. Orpet Park, Santa Barbara, CA, USA. Septate fibres showing septa at varied levels. D–F, Chorisia (Ceiba) speciosa A.St.Hil., cultivated in Claremont, CA, USA. D, Radial section to show imperforate tracheary elements interspersed with axial parenchyma; starch prominent in axial parenchyma. E, Transverse section. Libriform fibres (narrow cells) are scattered in the pervasive parenchyma. F, Radial section. Starch is present in axial parenchyma and ray cells. ap, axial parenchyma; i, intercellular space; lf, libriform fibres; r, ray; s, septum.

© 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 177, 291–321 AXIAL PARENCHYMA AND WOOD FUNCTION 295 above. Wood physiologists may prefer not to begin imperforate tracheary elements (tracheids, fibre- investigations with wood anatomical surveys, and yet, tracheids and libriform fibres), which may appear if they do not offer explanations for wood histology as similar in diameter as seen in transverse sections of seen under the light microscope, they are missing wood (Fig. 1A, B, E). Although axial parenchyma the structure–function continuum that must exist. cells often have thinner walls than those of imperfo- Current work in wood physiology is, however, encour- rate tracheary elements (fibrous tissue), wall thick- aging in this regard. In a recent synthesis (Carlquist, ness can be similar, so that one must always confirm 2012a), I attempted to include information from wood the identification of this cell type by examining radial physiology, ecology, habit, molecular systematics and sections (Figs 1B, F, 6B). In tangential section, axial Downloaded from https://academic.oup.com/botlinnean/article-abstract/177/3/291/2416378 by guest on 15 November 2018 ultrastructure whilst surveying histological features. parenchyma strands can look identical to uniseriate The present article also attempts to be inclusive, but rays composed of upright cells, but axial parenchyma there is, as yet, little direct information on function cells do not form radial sheets as do ray cells. Typi- available. Consequently, the interpretations sug- cally, ray cells are in horizontal rows as seen in gested by structure must be given a larger role, in the radial sections. Axial parenchyma strands appear as form of hypotheses and questions. The thesis under- single strands or small groups of strands running lying this approach is that structure is a reliable key vertically in a radial section. If several axial paren- to present-day function. I do not know of any work chyma strands are adjacent to each other, the cross that has proved that present-day wood structure is walls in them are staggered with respect to level minimally functional, of vestigial or ‘historical’ impor- (Fig. 6B), whereas ray cells form horizontally aligned tance. Wood evolution seems too parsimonious to rows. One can find only a few woods in which group- allow the persistence of features that are no longer ings of axial parenchyma cells are subdivided at functional: the investment of photosynthates in wood similar levels as seen in radial section (Fig. 1F). In is considerable, and not likely to be wasted on char- the section shown in Figure 1F, the ray cells are acters that are no longer fully functional. smaller than the axial parenchyma cells and that feature permits distinction. Axial parenchyma cells may differ markedly in size MATERIAL AND METHODS among angiosperms (compare Fig. 1A and 1D), and this may prove to correspond to functional differences. The systematic listings given below for particular In the case of Chorisia (Fig. 1D–F) and Erythrina L. anatomical characteristics are not complete, although (Fig. 2A, B), water storage and starch storage prob- reporting of as many families and genera as possible ably correspond to larger parenchyma cell sizes. has been attempted. The listings are culled largely The most important diagnostic difference between from the text of Metcalfe & Chalk (1950), supple- septate fibres and axial parenchyma relates to the mented by information from other cited sources and timing of the transverse divisions (Fig. 1B, C). In from my own research. The identification and sources axial parenchyma strands, transverse divisions take of the materials studied are given in the legends to place early, soon after the derivation of a daughter the figures. The present article consists of original cell from a fusiform cambial initial. Each cell in such observations, based on an extensive library of micro- a strand is thus surrounded by its own (usually scope slides of wood sections. Observations by others secondary) wall, so that the superposed cells in a have been incorporated, as the citations indicate. The strand are separated by a double transverse wall. Air present article is neither a data paper nor a review, spaces may often be seen adjacent to these transverse but has some aspects of both. Because this study walls, because the earlier timing of the division of is based on a large number of microscope slides cells in the parenchyma strand allows sufficient time accumulated over decades, citation of the methods for this to happen (Fig. 1B, D, i). employed would not be appropriate. In septate fibres, the protoplast has greater longevity than in typical non-septate libriform fibres, which AXIAL PARENCHYMA ASPECTS die soon after maturation of their secondary walls. Transverse divisions occur late in septate fibres, and IS AXIAL PARENCHYMA ALWAYS DISTINGUISHABLE are membranous, with only a primary wall separating FROM OTHER CELL TYPES? the two or more cells within a septate fibre. The The answer to this question is an almost unqualified earlier formed secondary wall is not interrupted by ‘yes’, but the criteria for the recognition of this cell this late-developing primary wall (the septum). The type must be given and examined. These criteria need septum usually stains differently from the axially to be explicitly reviewed and described. oriented secondary wall because lignin is lacking in Wall thickness is often used as one criterion to the septum. This is especially prominent if counter- distinguish between axial parenchyma and adjacent staining is employed (Fig. 1B, D).

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Figure 2. Unusual features of axial parenchyma. A, B, Erythrina coralloides Moc. & Sessé, cult. Huntington Botanical Gardens, San Marino, CA, USA. A, Wood transverse section; axial parenchyma cells are much wider than the libriform fibres. B, Tangential section. In the axial parenchyma band, strands of one or two cells are present. C, D, Frankenia palmeri S.Watson, C. Davidson s.n., San Ignacio, B.C., Mexico (RSA), tangential wood sections. C, Storied structure; arrows indicate the approximate cell terminus levels of the stories. D, Details of cell types; axial parenchyma cells are not subdivided into strands. E, Dirca occidentalis A.Gray, Abrams 106 (POM). Transverse section; axial parenchyma is limited to a single layer at the margin between earlywood and latewood. F, Gyrinopsis cumingiana Decne., Philippine Bureau of Science 49177 (UC). Radial section. Median section of interxylary phloem strand on the right shows crystals (cell walls did not stain); in the non-median section on the left (lighter grey strip), axial parenchyma is subdivided into strands. ap, axial parenchyma; c, crystalliferous cell; f, fibre; ixp, interxylary phloem; lf, libriform fibre; mp, marginal parenchyma; nv+vt, narrower vessels + vasicentric tracheids; r, ray; s, storey levels; v, vessel).

Living fibres tend to have easily visible contents. cell tall and non-septate (but living) fibres. Metcalfe & Starch is the most common component (Figs 1D, F, Chalk (1950) reported the absence of axial paren- 4A–C). Starch is also common in axial parenchyma. chyma in Dirca L. (Thymeleaceae), but my material Chorisia has abundant starch in both types of cell and shows an inconspicuous layer of terminal (marginal) in ray parenchyma. Even if specific stains are not parenchyma (Fig. 2E, mp) at the end of a growth ring. used for starch grains, they are easily recognized in This also proves to be true in Acer saccharum Mar- permanent slides by their dark hila and circular to shall (Fig. 7B). oval outline (Fig. 1D). Axial parenchyma that accompanies strands of

Water storage is more difficult to prove by means of phloem can easily be overlooked. Gyrinopsis Decne. Downloaded from https://academic.oup.com/botlinnean/article-abstract/177/3/291/2416378 by guest on 15 November 2018 histological features than one might expect. Extreme (Thymeleaceae) illustrates this phenomenon (Fig. 2F, succulence is easy to interpret, but can water storage ap). Thinner walled axial parenchyma cells that occur in woods that are not notably enlarged? There contain crystals in this wood (Fig. 2F, ixp) are also are reasons to believe that water storage in woods can strands that can easily be overlooked. be measured (S. Carlquist, unpubl. data). In terms of visible features, one looks for cells of somewhat larger Axial parenchyma of indefinite extent diameter (Figs 1E, F, 2A, B). Various degrees of abun- The intended meaning here is that cylinders of per- dance (Figs 1E, 2A, 3A) may be keys to degree and vasive axial parenchyma may vary in radial width, kind of storage, when combined with other informa- and may be supplanted by fibrous secondary xylem. tion from a given plant. This phenomenon differs from apotracheal banded Axial parenchyma strands usually have terminal parenchyma, in which bands may be wide, but char- cells with mitred or bevelled tips (Fig. 2B), whereas acteristically so. Crepidiastrum Nakai (Fig. 3A) is septate fibres have tapered tips. In transverse essentially a rosette herb, somewhat transitional to a section, axial parenchyma cells, when larger and rosette shrub. The production of pervasive paren- thinner walled, may be polygonal (Figs 1E, 2A), chyma (pw) is characteristic of less woody stems, but whereas, when smaller in diameter, and especially some stems are intermediate and can feature occa- when scattered in a diffuse fashion, they tend to be sional cylinders of libriform fibres (fw). It should be round in transverse section (Fig. 1A), thereby resem- noted that the vessel diameter is relatively constant bling imperforate tracheary elements. across these zones. The accumulation of secondary plant products Members of Brassicaceae, such as Stanleya pinnata (resins, etc.) is probably an indicator of prolonged (Pursh) Britton (Fig. 3B), form bands of parenchyma- longevity for both axial parenchyma and septate tous wood of varied width. These often occur as late- fibres. Crystals can be present in axial parenchyma wood, but some are intercalated at other points (Fig. 2C, D, F), septate fibres and libriform fibres. during a season. Such bands have been reported for However, reports of crystals in woods mostly do not other Brassicaceae by Metcalfe & Chalk (1950): state which of these cell types contains the crystals Alyssum spinosum L., Brassica fruticulosa Cyrillo (e.g. Metcalfe & Chalk, 1950). and Vella spinosa Boiss. Pervasive axial parenchyma Axial parenchyma strands can be more than ten occurs in roots of Brassicaceae that are notably non- cells long in some species with long fusiform cambial woody, such as Raphanus sativus L. and Armoracia initials. Mostly, they are shorter. One-celled axial lapathifolia Gilib. These two species have more parenchyma strands are shown in Fig. 2B for Eryth- fibrous wood in non-domestic populations, but culti- rina, mixed with two-celled strands. The one-celled vars (which are familiar as radishes and horseradish, axial parenchyma strands of Frankenia L. (Fig. 2C, respectively) represent selection for woods with per- D) are inconspicuous. One-celled axial parenchyma vasive parenchyma. strands are usually found in species with short fusi- A change from fibrous to non-fibrous secondary form cambial initials. Not surprisingly, fusiform xylem can be observed in some species, such as Cas- cambial initials and their derivatives in these species tilleja latifolia Hook. & Arn. (Fig. 3C, D). This is a are not infrequently storied (Fig. 2B–D). Most of the subshrub in which new branches are innovated, but cells shown in the sections of Frankenia are not old branches may persist. The first-year wood tends to libriform fibres, but vessel elements (often quite be fibrous (Fig. 3C, D, fw). Parenchymatous wood narrow) and axial parenchyma cells (Fig. 2D). (Fig. 3C, pw) is formed later. This pattern suggests the acquisition of mechanical strength and, when longitudinal growth of the shoot slows or ceases (and AXIAL PARENCHYMA NOT ABSENT BUT NOT EASILY thus mechanical strength is of no value in subsequent DISTINGUISHABLE wood), a change to non-fibrous wood occurs. Indeed, The example of Frankenia highlights the difficulty of the C. latifolia pattern may be found in various herbs distinguishing between axial parenchyma strands one and subshrubs to various degrees depending on

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Figure 3. Unusual axial parenchyma and septate fibre conformations. A, Crepidiastrum linguifolium A.Gray, S. Car- lquist 15768 (RSA), Hahajima Island, Japan. Transverse section of stem; axial parenchyma is pervasive, but a band of fibres is interpolated. B, Stanleya pinnata (Pursh) B.L.Burtt, cultivated in Rancho Santa Ana Botanic Garden, Claremont. CA, USA. The band of parenchyma corresponds to a dry season. C, D, Castilleja latifolia Hook. & Arn., Michener 4196 (RSA). C, Transverse section; upper one-third is parenchymatous wood, lower two-thirds is fibrous wood. D, Radial section. Left half, fibrous wood; right half, parenchymatous wood. E, F, Isoplexis canariensis (L.) Steud., Carlquist 2453 (RSA). E, Transverse section, margin of growth ring. F, Radial section. Septate fibres are occasional. ew, earlywood; fw, fibrous wood; lw, latewood; pw, parenchymatous wood; r, ray; s, septum.

© 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 177, 291–321 AXIAL PARENCHYMA AND WOOD FUNCTION 299 growth form and moisture availability. Some annuals Kogelbergia Rourke (Fig. 4D–G) is representative of that typically dry as a dry season approaches (e.g. the earlier concept of Stilbaceae, which included only Raphanus sativus) can survive into a second year and genera of small subshrubs with narrow leaves. These form non-fibrous wood if moisture is available. Vining genera are found on areas of Cape Province Sand- plants that encounter a surface on which to lean may stone in which rainfall occurs mostly in winter, as in shift from fibrous xylem to xylem with fewer fibres other Mediterranean-type climates. The wood is xero- (Mauseth, 1993). Experiments in which annuals per- morphic, with numerous relatively narrow grouped ennate because of prolonged water availability (and vessels (Fig. 4D). Kogelbergia verticillata (Eckl. & under frost-free conditions) should be studied to Zeyh.) Rourke has abaxial parenchyma, which is a Downloaded from https://academic.oup.com/botlinnean/article-abstract/177/3/291/2416378 by guest on 15 November 2018 show instances of this phenomenon and the factors scattering of axial parenchyma on the abaxial side of involved in a change in wood construction. a vessel (Fig. 4E–G). The Kogelbergia pattern is con- sonant with the idea that axial parenchyma supports Sparse septate fibres the functioning of the conductive system. This con- The growth habit of Isoplexis canariensis (L.) Loud. trasts markedly with the Halleria pattern, and dem- [=Digitalis canariensis L.] is best described as a onstrates that a shift in growth form and ecological rosette perennial, with several stems of varied dura- adaptation take place readily within a small family of tion branching from the base. The wood as seen in eudicots. transection (Fig. 3E) can be easily demarcated into latewood and earlywood, because the diameter of the Septate fibres substitute for axial parenchyma: fibres is narrower in latewood. As observed in radial systematic listing section, the fibres of D. canariensis are not all septate; The listing below is based on information from origi- perhaps no more than a quarter or a third of the nal research and from the texts of Metcalfe & Chalk fibres contain one or more septa. Instances such as (1950), Butterfield & Meylan (1976) and Meylan & this have not been reported previously, perhaps Butterfield (1978). Additions of more families are to because they are subtle. If wood sections are thin, an be expected. The listing of a particular family should observer may assume, with justification, that a septa not be construed as the presence of septate fibres in may be missing in any given septate fibre because it the entire family. has been excised. However, the number of septa in Acanthaceae (Beloperone Nees, Jacobinia Moric.) fibres of D. canariensis is much lower than can be Argophyllaceae (Corokia A.Cunn., Lautea F.Br.) accounted for by the thinness of sections (Fig. 3F). Atherospermataceae Septa in fibres of D. canariensis, as in most other Berberidaceae woods with septate fibres, are located, if one per fibre, Brunelliaceae near the widest portion of the fibre. Celastraceae Campanulaceae Clusiaceae (Hypericum L.) AXIAL PARENCHYMA ABSENCE IS OFTEN SEPTATE Connaraceae FIBRE PRESENCE Ericaceae (Agauria Benth. & Hook.f., Arbutus L., Two genera now placed in Stilbaceae on the basis of Arctostaphylos Adans., Oxydendron D.Dietr. and some molecular evidence, Bowkeria Harv. and Halleria L. Vaccinioideae) (Fig. 4A–C), have septate fibres of relatively uniform Euphorbiaceae (some Antidesmeae and Croto- diameter (Fig. 4A). These fibres contain numerous noideae) starch grains, 2–3 μm in diameter. Moreover, the ray ‘Flacourtiaceae’ cells of Halleria also contain abundant starch grains Gesneriaceae (Fig. 4C). Growth rings are absent or minimal. Hal- Grossulariaceae leria produces leaves, flowers and fruits whenever Haloragaceae water is available, and the seasonally massive Helwingiaceae growth, flowering and fruiting events during wetter Hippocrateaceae [ = Celastraceae] periods of the year may be correlated with extensive Hydrangeaceae (septate fibres present as a few starch accumulations. Septate fibres offer a much cells near vessels in Dichroa Lour., Hydrangea L. and more abundant storage area for starch than would Schizophragma Siebold & Zucc.) axial parenchyma strands, and yet the septate fibres Lardizabalaceae also offer appreciable mechanical strength, judging Loganiaceae s.l.[Antonia Pohl., Buddleja L. (Scro- from their wall thickness. Halleria lucida L. is a phulariaceae), Bonyunia M.R.Schomb. ex Progel, small tree native to areas of eastern and southern Chilianthus Burchell (= Buddleja), Fagraea Thunb. Africa that have dry and wet seasons of uncertain (Gentianaceae)] timing and duration (Goldblatt & Manning, 2000). Meliaceae

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Figure 4. Woods of Stilbaceae. A–C, Halleria lucida L., cultivated in Santa Barbara, CA, USA. A, Transverse section. Three vessels in a background of starch-rich septate ﬁbres. B, Radial section. Starch grains in septate ﬁbres. C, Starch grains (pale dots) in ray cells. D–G, Kogelbergia verticillata (Edel. & Seyh.) Rourke (Stilbe mucronata N.E.Br.), P. J, Brown 493 (RSAw). D, Transverse section; axial parenchyma is abaxial, inconspicuous. E, Transverse section. Axial parenchyma cells indicated by arrows. F, Radial section. Abaxial parenchyma on right. G, Tangential section. Abaxial parenchyma in strands of two cells, centre. ap, axial parenchyma.

Monimiaceae (Doryphora Endl., Laurelia Juss.) abundant than septate fibres in Araliaceae, however. Olacaceae (Octoknema Pierre) This accords with the fact that these Ericaceae do not Phyllanthaceae exhibit the prominent flushes of growth one sees in Pittosporaceae such families as Araliaceae or Fabaceae. Arctostaphy- Rubiaceae (26 genera listed by Metcalfe & Chalk, los and Xylococcus produce prominent aggregations of 1950) flowers prior to leafing out, so that carbohydrate Scrophulariaceae (Oftia Adans.; plus see Logani- storage seems to be correlated with this growth aceae s.l.) sequence. These two genera of Ericaceae have larger

Simaroubaceae (Guilfoylia F.Muell.) quantities of septate fibres in lignotubers, which serve Downloaded from https://academic.oup.com/botlinnean/article-abstract/177/3/291/2416378 by guest on 15 November 2018 Theophrastaceae [ = Primulaceae p.p.] for survival through fires or extreme drought, and can Violaceae yield shoots soon after these events have terminated. At an opposite extreme from these Ericaceae in Both/and: co-occurrence of axial parenchyma and terms of ecology are the woody lobelioids, which have septate fibres septate fibres throughout the secondary xylem. These The presence of both septate fibres and axial paren- septate fibres can be shown, in liquid-preserved mate- chyma in a particular wood makes for some interesting rial, to possess significant starch storage (Carlquist, interpretative possibilities. Those who expect blanket 1969). explanations that will cover all woods with a particular histological pattern may be disappointed to learn that Systematic listing of families with both axial there are no firm and unexceptionable correlations. parenchyma and septate fibres The nature of wood evolution is such that more than a Acanthaceae (Carlquist & Zona, 1988) single plan can accomplish a particular adaptive Anacardiaceae (some) scheme in a given ecological site. As evidence of this, Araliaceae (most) one notes that, in woods that have both axial paren- Bignoniaceae (some) chyma and septate fibres, the proportions of the two Elaeocarpaceae (Elaeocarpus L.) cell types can vary depending on the species (this offers Ericaceae (Arbutus, Arctostaphylos, Xylococcus) further interpretative possibilities). Euphorbiaceae (Bridelia Willd.) Members of Araliaceae have both axial parenchyma Fabaceae (some) and septate fibres (Fig. 5A, B). In Araliaceae, leaves do Gesneriaceae (some: Carlquist & Hoekman, 1986) not unfold sequentially one by one over a series of Lauraceae [Umbellularia (Nees) Nutt.] months. Rather, there are flushes of growth, and more Loganiaceae (Geniostoma J.R.Forst. & G.Forst.) than one such growth event can occur per year. The Meliaceae (some) rapid development of leaves, flowers and fruits prob- Myrsinaceae [ = Primulaceae p.p.] ably requires more than the currently produced pho- Myrtaceae (Eugenia Mich. ex L., Syzygium tosynthates, so that stored photosynthates make the P.Browne ex Gaertn.) rapidity of the events possible. Massive starch storage Nothofagaceae occurs in septate fibres of Araliaceae. Septate fibres are Oleaceae (Forsythia Vahl, Olea L.) apparently universal in the family (Metcalfe & Chalk, Onagraceae 1950). Two other features may bolster this correlation. Pittosporaceae Septate fibres are reported to be more common close to Polemoniaceae (Cantua, Loeselia) vessels than distal to them in Araliaceae; septate fibres Rosaceae (some Prunoideae; Photinia Lindl., are relatively wide, and are only about 50% longer Spiraea L.) than the vessel elements they accompany (Metcalfe & Violaceae (some) Chalk, 1950: 733). This suggests a shift away from a solely mechanical role for the fibres. In Polemoniaceae, Cantua Juss. (Fig. 5C, D) and Either/or Loeselia L. have relatively abundant axial parenchyma Metcalfe & Chalk (1950: 394) called attention to a and septate fibres (Carlquist, Eckhart & Michener, peculiar phenomenon in Celastraceae. Some species 1984). These genera are the woodiest of Polemoniaceae have tangential bands of septate fibres. These bands of and have heteroblasty, so that the emergence of long septate fibres are exactly comparable in position and shoots bearing indefinite numbers of flowers can be extent to bands of axial parenchyma in other species correlated with a shift in function of wood towards and, in a single genus, the bands may be composed of storage rather than mechanical strength. septate fibres in one species and parenchyma in Xylococcus Nutt. (Fig. 5E, F) and Arctostaphylos another. This phenomenon seems to indicate that, in contain more septate fibres than do other genera of pertinent Celastraceae, axial parenchyma and septate Ericaceae. Septate fibres in the two genera are less fibres are interchangeable in function.

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Figure 5. Woods with both axial parenchyma and septate fibres. A, B, Cheirodendron helleri Sherff (USw-15309). A, B. Radial section. Axial parenchyma near vessel, background cells are all septate fibres. B, Details of septate fibres, left, and axial parenchyma cells (diagonal walls), right. C, D, Cantua pyrifolia Juss., Carlquist 341 (RSA), radial section. C, Axial parenchyma and septate fibres, indicated by arrow and brackets. D, Details of axial parenchyma and septate fibres. E, F, Xylococcus bicolor Nutt., Wallace 1380 (RSA). E, Transverse section. Septate fibres indicated by bracket. F, Radial section. Details of septate fibres. ap, axial parenchyma; s, septum; sf, septate fibres; v, vessels.

The materials illustrated here confirm the claims A myrtalean genus, Sonneratia L.f. (Lythraceae s.l. of Metcalfe & Chalk (1950). In Siphonodon Griff. or Sonneratiaceae), has septate fibres (Fig. 7D). These (Fig. 6A, B), axial parenchyma is present in tangential septate fibres are wider and are located closer to bands. These bands vary in abundance and density, vessels or bands of vessels, whereas fibres more distal with wood mostly composed of libriform fibres at some to the vessels are narrower (Fig. 7C, D). The fibres points (Fig. 6A, centre), but with axial parenchyma closer to vessels are reported to be thinner walled and much more abundant elsewhere (Fig. 6A, top; Fig. 6B). to be less elongate with blunt ends, as compared with The wall thickness of the two cell types permits easy the narrower fibres (Metcalfe & Chalk, 1950). Axial discrimination between axial parenchyma and libri- parenchyma is absent in Sonneratia (Metcalfe & Downloaded from https://academic.oup.com/botlinnean/article-abstract/177/3/291/2416378 by guest on 15 November 2018 form (non-septate) fibres in Siphonodon (see also Chalk, 1950). One can categorize the septate fibres of Fig. 1A). Sonneratia as representative of fibre dimorphism. In Catha edulis (Vahl) Forssk. (Fig. 6C, D), bands of However, the fibres that are wider and more septate fibres are present. These bands are five or six parenchyma-like are adjacent to vessels in Sonnera- cells wide (Fig. 6C). They could be overlooked during tia, but distal to them in Acer (Fig. 7A). This under- casual observation, but are characteristically present. lines the fact that fibre dimorphism is not a simple These septate fibres can be identified readily in radial phenomenon, but a series of expressions (Carlquist, sections (Fig. 6D). 2014). In Elaeodendron capense Eckl. & Zeyh. (Fig. 6E, F), bands of septate fibres are more subtle. The bands are typically three cells wide (Fig. 6E). In radial sections, RAYLESSNESS: PARENCHYMA ABSENCE, PRESENCE the septa can be readily seen (Fig. 6F, sf). Libriform OR INCIPIENCE (non-septate) fibres (Fig. 6F, nf) are wider than Rayless woods are relatively few in number (Carlquist, septate fibres and have thinner walls (sf). 1988), and few wood anatomists are familiar with any The seeming interchangeability of axial and septate examples, although Meylan & Butterfield (1978) fibres (in a broad phylogenetic sense, but not within a offered good illustrations of the wood of Hebe salicifolia particular wood sample) is a curious evolutionary (G.Forst.) Pennell (= Veronica salicifolia G.Forst.; phenomenon that deserves further study. The present molecular data support the merging of Hebe with article reveals considerable overlap in probable func- Veronica in Plantaginaceae]. Rayless woods are rarely tions of the two cell types, and so Celastraceae may found in trees or large shrubs, and Hebe may contain represent a family in which the function of the two the woodiest species in which rayless woods have been cell types is essentially identical. reported. Axial parenchyma cells as well as rays are absent in Hebe, so that the group offers a convenient starting Fibre dimorphism as a mode of axial point with relation to parenchyma absence. The parenchyma absence absence of both rays and axial parenchyma is under- Fibre dimorphism was examined in detail in a recent standable, because axial parenchyma and ray paren- study (Carlquist, 2014). One genus worth mentioning chyma systems are physically and presumably in this regard is Acer (Aceraceae, now referable to physiologically interlinked (Kedrov, 2012). Sapindaceae). Metcalfe & Chalk (1950) noted that, in How can a rayless wood form a cylinder of indefi- Acer, ‘Holden (1912) has pointed out that the fibres nite thickness and still be functional if axial paren- have noticeably thicker walls in the neighbourhood of chyma and ray cells are essential to the functioning of the vessels ...... Heimsch (1942) states that bands a wood? One possibility is that rayless woods do not, or areas of starch-storing fibres are characteristic of in fact, consist wholly of dead cells. Jacobinia carnea Acer, but points out that they may be rendered (Lindl.) G.Nicholson (Acanthaceae; Fig. 7E, F) is defi- obscure by common section-cutting techniques.’ The nitely a rayless wood, as seen in a tangential section distinction between narrower thick-walled fibres and (Fig. 7E), but the fibres, when carefully examined, wider thin-walled fibres can be seen readily in trans- prove to be septate. Jacobinia has radial groupings of verse sections of Acer wood (Fig. 7A). The relationship vessels; in these groupings, one can see that axial claimed by Holden (1912) between thick-walled fibres parenchyma is present adjacent to vessels (Fig. 7F), and vessel distribution does not seem rigid. Acer as it is in woods of other Acanthaceae (Carlquist & saccharum also has terminal bands, one cell thick, of Zona, 1988). Thus, the wood of Jacobinia can be said terminal (marginal) parenchyma (Fig. 7B). Thus, Acer to exist wholly of living cells, except for vessel ele- has the capability of producing axial parenchyma, but ments. Radial conduction at a slow rate may be pos- does so to a minimal extent. The wide thinner walled sible via the septate fibres. fibres, although non-septate, should be categorized as Alseuosmia A.Cunn. (Alseuosmiaceae) is also a living fibres (Vasquez-Cooz & Meyer, 2008). clearly rayless wood. Vessels are difficult to identify in

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Figure 6. Axial parenchyma in woods of Celastraceae. A, B, Siphonodon australis Benth. (Forestry Commission of New South Wales. A, Transverse section. Axial parenchyma diffuse but in zonal bands (white cells). B, Radial section showing strands of cells comprising the axial parenchyma (ray near centre). C, D, Catha edulis (Forssk.) Vahl, cultivated in Santa Barbara, CA, USA. C, Transverse section; band of septate fibres. D, Radial section; details of ray cells and septate fibres. E, F, Elaeodendron australe Vent. (Forestry Commission of New South Wales). E, Transverse section; two bands of septate fibres. F, Radial section; vessel with scalariform perforation plate (left) and several septate fibres. nf, non-septate fibres; r, ray; sf, septate fibres; sfb, band of septate fibres.

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Figure 7. Instances of fibre dimorphism (A–D) and raylessness (E, F). A, B, Acer saccharum Marshal (Ripon Microslides). A, Transverse section. Vaguely delimited zones of narrow fibres and wide fibres. B, Radial section. Marginal axial parenchyma strand defines latewood terminus. C, D, Sonneratia alba Sm., Carlquist 15465 (RSA). C, Transverse section. Zones of narrow and wide fibres. D, Radial section. Details of ray cells and of wide and narrow septate fibres. E, F, Jacobinia carnea (Lindl.) C.Nicholson, cultivated in Santa Barbara, CA, USA E, Tangential section showing rayless condition. F, Radial section; axial parenchyma among vessels in area denoted by bracket. lf, libriform fibre; mps, marginal parenchyma strand; nf, narrow fibres; np, patch of narrow fibres; nsf, narrow septate fibres; r, ray; v, vessel; wf, wider fibres; wsf, wider septate fibres.

© 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 177, 291–321 306 S. CARLQUIST transverse sections (Fig. 8A), and even in tangential Exospermum Tiegh., the tangential bands probably sections (Fig. 8B), because their diameter is so similar interconnect uniseriate rays, which are only one or to the diameters of the fibrous cells (imperforate two tracheids apart tangentially (Fig. 9A, B). Radial tracheary elements). Liquid-preserved material shows subdivisions of axial parenchyma cells occur occasion- that, in tangential section, the fibres have nucleate and ally (Fig. 9C). This latter phenomenon is uncommon prominent simple pits, like those of parenchyma cells and may relate to the production of wider axial paren- (Fig. 8C). The fibres are all septate, as noted by chyma cells. Tangential bands of axial parenchyma Butterfield & Meylan (1976) and Dickison (1986). are clearly evident in Belliolum haplopus (B.L.Burtt)

Although septa are inconspicuous, starch grains can A.C.Sm. (Fig. 9E), in which tangential bands extend Downloaded from https://academic.oup.com/botlinnean/article-abstract/177/3/291/2416378 by guest on 15 November 2018 often be seen adjacent to the septa (Fig. 8D). There are across several rays and are tangentially two cells in occasional strands of axial parenchyma in the wood of radial thickness. Alseuosmia (Fig. 8D, left). In the specimen studied, the Pseudowintera Dandy has massive multiseriate axial parenchyma strands are so sparse that they are rays and numerous uniseriate rays (Fig. 9E). ‘Bridges’ probably not of much functional value. However, the of axial parenchyma interconnect uniseriate rays at rayless wood of Alseuosmia, like that of Jacobinia, intervals (Fig. 9F). These tangential bands occur consists entirely of living cells, except for the vessel between latewood and earlywood; the wood of Pseu- elements. dowintera has growth rings corresponding to the tem- Wood of Plantago maderensis Decne. (Fig. 8E, F) is perate Southern Hemisphere localities in which it rayless, like that of other insular species of Plantago L. occurs. (Carlquist, 1970). Both P. maderensis and the Canar- Tetracentron Oliv. and Trochodendron Siebold & ian P. arborescens Poir. are much-branched miniature Zucc. (Trochodendraceae) are vesselless, but grow in shrubs that accumulate a wood cylinder of < 1cmin more markedly seasonal habitats than most Winter- diameter. Larger stems in both species develop rays. aceae. Axial parenchyma is diffuse or grouped into Axial parenchyma is formed at the same time as rays short tangential bands, and is characteristically in are formed (Fig. 8E, F), although rays are more readily latewood (Metcalfe & Chalk, 1950). This suggests that, identified. Thus, the wood of P. maderensis resembles in Trochodendraceae, latewood may feature greater that of Artemisia L., Cyrtandra J.R.Forst. & G.Forst., vulnerability to embolism formation, which is coun- Geranium L. and Pelargonium L’Hér. ex Aiton: it tered by the action of axial parenchyma (see interpre- begins rayless, but rays are formed relatively soon tations below), whereas strong negative pressure thereafter. The amount of wood that lacks parenchyma is less likely to develop in earlywood. This would cells is therefore finite. One must concede that we accord with the interpretations of Braun (1984) and know relatively little about the longevity of nuclei in Zwieniecki & Holbrook (2009) in vessel-bearing libriform fibres, because liquid-preserved woods are so angiosperms. rarely studied. Families such as Solanaceae should be studied in this regard. Most of the woods of Lobe- lioideae in an earlier study (Carlquist, 1969) were RAY–AXIAL PAPRENCHYMA CONTACTS dried species and were not observed to have nuclei, but Contacts between rays and axial parenchyma char- the preparations made from liquid-preserved collec- acteristically occur in woody angiosperms and gym- tions were indeed septate and nucleate. nosperms (Kedrov, 2012). If osmotic water shifting is The emerging picture of rayless woods tends to show a significant factor in conduction, these numerous axially elongate cells to a far greater extent than contacts between rays and axial parenchyma are radially elongate cells. Cells are, as a rule, elongate in potentially significant in vessel-bearing woods in the direction of conduction, and more strongly elon- which tracheids, a conductive cell type, are present gate cells (vessel elements; procumbent cells of rather than fibre-tracheids or libriform fibres, which multiseriate rays) tend to be markedly elongate. Juve- are not conductive (Carlquist 1984; Carlquist, 2001; nilistic woods show protracted production of vertically Sano et al., 2011). Conductive capability (freedom elongate cells (Carlquist, 1962, 1988), and progression from embolisms) of tracheids can potentially be into adult patterns features horizontal subdivision of maintained by axial parenchyma activity (Zwieniecki both fusiform initials and ray initials. Septate fibres in & Holbrook, 2009; see Fig. 13 below) in vessel- rayless woods probably accomplish relatively little bearing woods, and union of rays into this network is radial conduction, or accomplish it slowly. This is not very probably a feature pertinent to this function. a limitation if the woody cylinder is small in diameter. Thus, one should expect diffuse, diffuse-in aggregate and apotracheal banded patterns to be more common Axial parenchyma in vesselless angiosperm woods in vessel-bearing woods with tracheids, and this is In Winteraceae, axial parenchyma may be scanty and true as a generalization (original observations based diffuse, but is most commonly in tangential bands. In on a random sampling of woods of 100 species of

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Figure 8. Rayless woods. A–D, Alseuosmia macrophylla A.Cunn., Gardner 1021 (AKU). A, Transverse section. Vessel elements are only slightly wider than the septate fibres. B, Tangential section. No axial parenchyma or rays are visible. C, Tangential section. Nuclei visible in septate fibres; pits on tangential fibre walls conspicuous. D, Radial section; a pair of axial parenchyma cells is to the left of the four septate fibres; granular contents are starch. E, F, Plantago maderensis Decne., Carlquist 262 (RSA). Two portions of a tangential section. E, A vertical pair of axial parenchyma cells indicated. F, Incipient ray indicated by arrow. ap, axial parenchyma; pf, pitted fibre wall; r, ray; ssf, starchy septate fibres.

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Figure 9. Woods of Winteraceae to show range of axial parenchyma and ray expressions in vesselless woods. A–C, Exospermum stipitatum (Baill.) Tiegh. (Zygogynum stipitatum Baill), Carlquist 1590 (RSA). A, Transverse section. Axial parenchyma cells identiﬁable by being narrower than tracheids. B, Tangential section. Uniseriate rays with upright cells are abundant. C, Radial section. At centre, a tangentially subdivided axial parenchyma cell. D, Belliolum (Zygogynum) haplopus (B.L.Burtt) A.C.Sm., MADw-22694. Transverse section. Two tangential bands of axial parenchyma. E, F, Pseudowintera colorata (Raoul) Dandy, Carlquist 4173 (RSA), tangential sections. E, Massive multiseriate rays plus inconspicuous uniseriate rays. F, Portion of a tangential band of axial parenchyma. ap, axial parenchyma; apb, axial parenchyma band; mr, multiseriate ray; r, ray; ur, uniseriate ray; ur+t, uniseriate rays plus tracheids.

© 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 177, 291–321 AXIAL PARENCHYMA AND WOOD FUNCTION 309 angiosperms). In woods with fibre-tracheids or libri- (Fig. 10D) has fascicular strips one to four (mostly two) form fibres, axial parenchyma is often limited to a cells wide, as do the epacrids (Fig. 10F). few strands in contact with the vessels, as illustrated If vessel elements and tracheids in a particular wood here for Kogelbergia (Fig. 4E). In such a wood, the are notably long (axially), it is more likely that they vessels are the only cells actively conducting water, will be in contact with the living cells of a wood. Thus, and thus intimate contact between axial parenchyma the tangential section of Figure 10B shows several and vessels is understandable if osmotic water shift- vessels longer than the portions included in the pho- ing is a significant mechanism. Contacts between tograph. The diffuse distribution of axial parenchyma axial parenchyma and rays are present in both also correlates with scalariform perforation plates and Downloaded from https://academic.oup.com/botlinnean/article-abstract/177/3/291/2416378 by guest on 15 November 2018 vessel-bearing woods with tracheids and vessel- greater vessel element length (Metcalfe & Chalk, 1950: bearing woods with fibre-tracheids and libriform xlv). fibres (Kedrov, 2012). A greater number of interconnections between rays and axial parenchyma is thus correlated with Ray density and interconnections with character states commonly considered to be plesio- axial parenchyma morphic in angiosperm woods. It should be noted In addition to a tendency towards apotracheal paren- that the woods of Figure 10 all have scalariform per- chyma in vessel-bearing woods with tracheids, there foration plates, a feature often cited as plesiomor- is a correlation with the number of rays per square phic in angiosperms. millimetre (S. Carlquist, unpubl. data). The greater The abundance of upright cells in rays, the pres- the number of strands of axial parenchyma of the ence of uniseriate rays exclusively and the greater transverse section and the greater the density of axial height of uniseriate rays all characterize the ray rays, the more likely that living cells contact trac- type termed ‘Paedomorphic Type III’ (Fig. 10F), an heids and thus potentially play a significant role in extension of the ray types of Kribs (1935) necessary to their conduction, as well as that of vessels. Diffuse reflect various degrees of juvenilism in various woods axial parenchyma (or some minor variation) charac- (Carlquist, 1988). Uniseriate rays are not exclusively terizes most vessel-bearing woods with tracheids present in Cleyera Thunb., but are more common (‘fibres with bordered pits’ of Metcalfe & Chalk, than multiseriate rays (Fig. 10B). The abundance of 1950: xlv). upright cells in these rays increases the chance of In Figure 10, all of the species have high ray interconnections between axial parenchyma and rays. density. As a baseline, we can use the measurements Kedrov (2012) illustrated contacts between rays of Metcalfe & Chalk (1950) for the number of rays per and axial parenchyma in the outer one-third growth millimetre. This represents the number of rays inter- ring of Alnus incana (L.) Moench. His illustration secting an (imaginary) transverse line across a tan- showed that each ray has three or more contacts with gential section. This measurement has received little axial parenchyma strands. No ray in this species comment by wood anatomists, perhaps because its lacks ray–axial parenchyma contacts, and the significance may be more physiological than taxo- minimum number of ray–axial parenchyma contacts nomic, and taxonomic differences have been the focus per ray is two. Axial parenchyma in Alnus Mill. is of most recent wood anatomical studies. diffuse and terminal, and so the universality of these Metcalfe & Chalk (1950: xxvi) graphed the number contacts is more noteworthy than it would be in a of rays per millimetre for angiosperm woods as a species with, for example, wide apotracheal banded whole. Their graph shows a peak at about eight rays parenchyma. Rays are uniseriate or biseriate in Alnus per millimetre. With respect to the families shown in (Metcalfe & Chalk, 1950), a fact that would make the Figure 10, Metcalfe & Chalk (1950) report 9–17 rays multiplicity of ray–axial parenchyma contacts sur- per millimetre in Theaceae (Fig. 10A–C), 13 rays prising. However, the number of rays per millimetre per millimetre in Cercidiphyllum Siebold & Zucc. is 7–15 in Betulaceae, a ray density that would favour (Fig. 10D) and 10–27 (mostly 16–20) rays per milli- numerous ray–axial parenchyma contacts. A three- metre in Epacridaceae (= Ericaceae p.p.) (Fig. 10E, F). dimensional system of ray–axial parenchyma contacts These all exceed the nine rays per millimetre cited as is essential to the operation of an osmotic water a median condition. shifting mechanism. The contacts between axial parenchyma and rays correlate with a greater number of rays per millimetre, more frequent in the species selected for illustration RADIAL CONTACTS (Fig. 10A, C, arrows). One can estimate the frequency Braun (1970, 1984) called attention repeatedly to acid of contacts from the width of fascicular strips as seen phosphatase as evidence of osmotic water shifting in a transverse section (axial xylem portion separated in woods. This is conspicuous in paratracheal axial by rays on either side). Thus, Cercidiphyllum parenchyma sheaths, as his illustrations show. The

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Figure 10. Sections of eudicot woods to illustrate contacts between parenchyma types. A–C, Cleyera japonica Thunb., USw-14116. A, Tangential section, illustrating contacts between axial parenchyma and uniseriate rays. B, Large number of rays per millimetre. C, Contacts between axial parenchyma and rays (arrows). D, Cercidiphyllum japonicum Sieb. & Zucc., Aw-5393. Transverse section. Fascicular zones are one to four cells wide. E, F, Dracophyllum acerosum Berggr., Carlquist 1186 (RSA). E, Fascicular zones are one to three cells wide. F, Rays are Paedomorphic Type III. ap, axial parenchyma; r, ray.

© 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 177, 291–321 AXIAL PARENCHYMA AND WOOD FUNCTION 311 presence of starch in axial parenchyma is also an The non-septate fibre-tracheids of Ephedra are indirect indication of osmotic water shifting. One can nucleate and can be compared, in abundance and cite starch presence as ‘starch storage’, but evidence distribution, with diffuse axial parenchyma of angio- of starch hydrolysis, such as prior to leafing out in sperms, although the latter cells are in strands Acer (Sauter, Iten & Zimmermann, 1973), is evidence rather than present as individual cells as in of osmotic water shifting. Rays and axial parenchyma Ephedra. As noted, several Ephedra spp. have axial in angiosperms do not account for the radial conduc- parenchyma with secondary walls as well as non- tion of water (sap) in wood according to Kedrov septate fibre-tracheids.

(2012), but there is a radial flow of photosynthates in The thin-walled nature of axial parenchyma cells Downloaded from https://academic.oup.com/botlinnean/article-abstract/177/3/291/2416378 by guest on 15 November 2018 rays (Braun, 1970). Radial conduction of water by and rays in Welwitschia, in contrast with the second- means of tracheids can occur because of pits on over- ary walled nature of such cells in Ephedra and lapping radial walls of tracheids (Kedrov, 2012). That Gnetum, probably relates to mechanical strength con- there is a flow of photosynthate-laden fluid radially siderations. The massive strands of secondary phloem through ray cells, especially procumbent ray cells, is fibres provide potential mechanical strength, and may evidenced by the occurrence of bordered pits on tan- serve as reservoirs for fluctuating water content. The gential walls of ray cells (Carlquist, 2007). Radial sap thin-walled cells in the secondary xylem and conjunc- flow can occur in tracheids in the case of Pinaceae, tive tissue of Welwitschia may relate to expansion and which have ray tracheids (Greguss, 1955), and Tetra- contraction of the Welwitschia axis with shifts in centron sinense Oliv. (Thompson & Bailey, 1916). moisture availability. Thus, all three genera of Gnetales have axial AXIAL PARENCHYMA IN GYMNOSPERM WOODS parenchyma, except for some Ephedra spp. The dis- Gnetales tribution of living non-septate fibre-tracheids in Gnetales have essentially all of the wood features of Ephedra is analogous to that of axial parenchyma, angiosperms (Carlquist, 1996, 2012b), although their and thus the non-septate fibre-tracheids of Ephedra wood is clearly derived from a conifer-like type. The are a distinctive feature, but probably comparable similarities to angiosperm woods are parallelisms with axial parenchyma in function. (‘convergences’ of some authors). The living cells of the genera of Gnetales can be Conifers characterized as follows (data from Carlquist, 1996): Conifers (excluding Gnetales) have axial parenchyma Ephedra L.: nucleated (but non-septate) fibre- strands (Fig. 12A, B). Conifers rarely lack axial tracheids with vestigially bordered pits (Fig. 11A, B). parenchyma; absence has been reported with cer- Axial parenchyma occurs in several species of tainty only in Taxaceae (Greguss, 1955). In transec- Ephedra (Greguss, 1955; Carlquist, 1996), but is tion, axial parenchyma may simulate tracheids in absent from most species. shape and wall thickness, but, in longitudinal sec- Gnetum L.: axial parenchyma with secondary walls tions, the transverse walls of parenchyma (Fig. 12B) plus septate fibres (Fig. 11C, D). are readily evident. Resin deposits sometimes occur in Welwitschia Hook.f.: thin-walled axial parenchyma. axial parenchyma of conifers (Fig. 12A), but tracheids The occurrence of multiseriate rays in secondary can sometimes contain resin deposits also. Kedrov xylem of Ephedra and Gnetum is familiar. Ray cells in (2012) demonstrated that axial parenchyma and rays these genera have secondary walls, often with bor- are interconnected, forming a continuous network. dered pits (Carlquist, 2007, 2012b). The presence of This is reminiscent of the latewood axial parenchyma rays and axial parenchyma in Welwitschia will be less in Tetracentron and Pseudowintera (Fig. 9). Latewood familiar to most workers. Welwitschia has secondary axial parenchyma may relate to deterrence (or even xylem with rays (Fig. 11E, r) and axial xylem com- removal) of embolisms in the tracheids. posed of tracheids plus vessels (Fig. 11E, t+v). Axial parenchyma is intercalated into the axial xylem at various points (Fig. 11E, F, ap). Secondary phloem is Cycads also present (Fig. 11E, spf). Secondary xylem and Woods of cycads as a whole have been described by secondary phloem are produced by vascular cambia Greguss (1968). Secondary xylem drawings of Cycas (Fig. 11E, c). Welwitschia has successive cambia, and revoluta Thunb. by Greguss (1955) show the expected so increments of secondary xylem plus secondary presence of rays and axial parenchyma. The drawings phloem are produced numerous times rather than by Greguss (1955) show no cells intermediate between just once. This does not in any way vitiate the idea axial and ray parenchyma. Axial xylem in cycads is that Welwitschia has secondary xylem and that this composed mostly of tracheids, with thin-walled axial secondary xylem is comparable with that of Ephedra parenchyma interpolated in an irregular fashion and Gnetum. (Fig. 12C).

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Figure 11. Living cells in wood of Gnetales. A, B, Ephedra pedunculata Engelm. ex S.Watson, Carlquist 15815 (RSA). A, Living fibre-tracheids indicated by arrows. B, Radial section. Living fibre-tracheid (dark cell) among tracheids. C, D, Gnetum gnemon L., Aw-32395, radial sections. C, Co-occurrence of axial parenchyma and septate fibres. D, Details of axial parenchyma cells; bordered pits are present on some cells. E, F, Welwitschia mirabilis Hook.f., Carlquist 8071 (RSA). E, Transverse section of axis. Thin-walled axial parenchyma cells are scattered in the fascicular xylem. F, Tangential section of secondary xylem, showing axial parenchyma and ray. ap, axial parenchyma; c, vascular cambium; r, multiseriate ray; s, septum; spf, secondary phloem fibres; t+v, tracheids plus vessels.

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Figure 12. Axial parenchyma in gymnosperms, seen in transections (A, C, D) and radial sections (B, E, F). A, Callitris canescens (Parl.) S.T.Blake. B, Juniperus communis L. (Ripon Microslides). One axial parenchyma strand (centre) within a tracheid background. C, Zamia ﬂoridana A.DC., A. W. Haupt 1933. Occasional axial parenchyma cells scattered in fascicular areas. D–F, Ginkgo biloba L., cultivated in Claremont, CA, USA D, Short shoot with secondary growth; axial parenchyma cells within fascicular zones indicated by arrows. E, Axial parenchyma in relation to ray. F, Details of two adjacent axial parenchyma strands to show druses. ap, axial parenchyma; c, vascular cambium; cw, cross wall of axial parenchyma strands; d, druse; ew, earlywood; lw, latewood; p, pith; r, ray; sp, secondary phloem; t, tracheid.

Ginkgo to the action of tension–cohesion governed conduc- The secondary xylem of Ginkgo short shoots tion. Braun (1984) stated: ‘The activity of the acces- (Fig. 12D) is remarkably similar to that of cycads sory tissues produces a high osmotic pressure in the with respect to the irregular interpolation of axial trees. This brings about an uptake of water, often a parenchyma into groupings of tracheids. In wood of positive pressure (system pressure) and an osmotic the long shoots, however, axial parenchyma strands water shifting within the tree.’ This particular state- are comparatively infrequent and have secondary ment was intended to be primarily applicable to walls (Fig. 12E, F). Axial parenchyma in the wood of winter-deciduous trees, but Braun also extended his long shoots contains druses. These circumstances interpretation to other kinds of woody plants, e.g. Downloaded from https://academic.oup.com/botlinnean/article-abstract/177/3/291/2416378 by guest on 15 November 2018 suggest differential functions for axial parenchyma in tropical deciduous trees. Braun’s ideas did not include short shoots versus long shoots of Ginkgo. In the wood other examples, and did not examine in detail how of long shoots, there may be differentiation into this process might work. Ideas along these lines were groupings of tracheids with greater conductive capa- offered by Canny (1995, 1998); they have been proven bilities and those with thicker walls and narrower to be problematic and have not been validated by lumina. These differences, although minor, were certain experimental tests (Comstock, 1999). figured by Kedrov (2012) and hinted at in the illus- Zwieniecki & Holbrook (2009) presented a rather trations of Greguss (1955). Dimorphism in tracheids different detailed scheme in which axial parenchyma might be expected to be related to axial parenchyma and (low-molecular-weight) sugars in axial paren- distribution, but this has not been demonstrated in chyma are the driving force. These concepts have been Ginkgo wood, perhaps because axial parenchyma is reproduced here as Figure 13. However, the pathways too sparse to reveal differential distributions. proposed may require modification as we learn more about how parenchyma cells function in the conductive process. Secchi & Zwieniecki (2012) found that the AXIAL PARENCHYMA STRUCTURE RELATED TO concentration of osmolytes might be too low to account XYLEM PHYSIOLOGY for the reduction and elimination of embolisms. These Axial parenchyma presence authors emphasized that the effect of sugars in influ- The present article is not and cannot serve as a review encing water movements within the xylem may not be of physiological work on the function of axial paren- extensive, affecting long portions of a vessel, but may chyma in conduction. The resolution of some questions be confined to localized sites. Possibly, osmotic differ- will remain for the future. However, a brief discussion entials may form locally or over short periods of time of wood physiological work can show that the common and even occur at membrane sites: such events are associations between axial parenchyma and vessels or difficult to study. The studies of Borchert & Pockman tracheids have been repeatedly implicated in the con- (2005) and Plavcova & Hacke (2011) are relevant in ductive process. For a broader overview, the review this regard. Although we often speak in terms of by Clearwater & Goldstein (2005) can be consulted. ‘starch storage’ (Borchert & Pockman, 2005), we have Can axial parenchyma account for the reversal of few data on events of starch mobilization in axial embolisms, or conceivably even the prevention of parenchyma and the pathways taken by sugars follow- embolisms, in associated tracheary elements? These ing mobilization. The work on Adansonia L. (Chapotin, functions have repeatedly been claimed to have experi- Razanameharizaka & Holbrook, 2006a, b, c) illustrates mental support (Braun, 1970, 1984; Salleo & Lo Gullo, that the functions of starch storage should be studied, 1989, 1993; Edwards et al., 1994; Salleo et al., 1996; because they may be multiple in a given plant, and Trifilo et al., 2004; Salleo, Trifilo & Lo Gullo, 2006; starch storage may function differently in a range of Holbrook & Zwieniecki, 1999; Holbrook, Zwieniecki different given species. & Melcher, 2002; Zwieniecki & Holbrook, 2009; Axial parenchyma, so common in woods of angio- Brodersen & McElrone, 2013). Phloem may also be sperms, Gnetales, cycads and Ginkgo (but less common involved (Trifilo et al., 2004; Salleo et al., 2006), as may in Coniferales), parallels vessels and tracheids spatially bordered pit structures of tracheary elements in wood and is implicated by its distribution as the (Zwieniecki & Holbrook, 2000). According to source of osmotic water shifting in these tracheary ele- Zwieniecki & Holbrook (2009): ‘Sugar concentrations ments (Braun, 1984; Holbrook & Zwieniecki, 1999; in xylem have been little studied, but their involve- Zwieniecki & Holbrook, 2009). In the present article, the ment in [tracheary element] refilling is consistent with characteristics of axial parenchyma are used, in connec- observed dynamics of starch content in stems that tion with the absence or scarcity of axial parenchyma, in undergo embolism-refilling cycles (Bucci et al., 2003; order to explore the multiplicity of histological patterns Trifilo et al., 2004; Salleo et al., 2006).’ and their probable functional significance. The process of ‘osmotic water shifting’ was envi- Axial parenchyma is present in by far the majority of sioned by Braun (1984) as a process complementary angiosperm woods. The data of Kribs (1937) indicate

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Figure 13. Embolism refilling scenario. (a) Living cells in contact with vessels release a small but steady amount of soluble carbohydrate into the xylem. (b) Starch stored in xylem parenchyma serves as a sugar capacitor. (c) These solutes are normally swept away by the transpiration stream, keeping the concentration at very low levels, but (d) accumulate in a vessel that has cavitated. (e) Sugar accumulation and the associated increase in apoplastic solute concentration triggers signalling pathways (f) for refilling that regulate sugar and (g) water membrane transport, as well as (h) sugar metabolic activity. (i) The accumulation of solutes results in water movement from xylem parenchyma cells by osmosis, forming droplets with high osmotic activity on internal vessel walls. (j) The partially non-wettable walls of xylem conduits prevent these droplets from being removed by suction from still-functioning vessels. (k) Condensation of water vapour provides a second pathway by which water refills cavitated conduits, allowing adjacent conduits to provide water for refilling. (l) As the high osmotic droplets grow to fill the vessel, the embolus is removed by forcing gas into solution and by pushing gas through small pores through the vessel walls to intercellular spaces. (m) The flared opening of the bordered pit chamber acts as a check valve until the lumen is filled, thus preventing contact with the highly wettable bordered pit membranes. Reconnection occurs once the pressure in the lumen exceeds that of the entry threshold into the bordered pit chambers; a hydrophobic layer within pit membranes might provide the needed simultaneity among multiple bordered pits. (From Zwieniecki & Holbrook, 2009; reproduced by permission of the authors and Elsevier Publishing). that the percentage of angiosperms with axial paren- Plemons-Rodriguez (1997) mention the idea of a ‘water chyma absent is about 5%, and that axial parenchyma jacket’ of parenchyma cells completely ensheathing a is almost universal in woods that have vessel features vessel, but concede that most angiosperms do not have considered as apomorphic. Exact percentages cannot be this. The reason seems clear: if parenchyma cells affect offered because the sampling of Kribs (1937) may not water conduction, only a single parenchyma cell (cell have been random (tropical species may be under- strand, as seen longitudinally) per vessel, or several represented); the species he studied are not listed. The at most, could suffice. This condition is commonly real- commonness of axial parenchyma in angiosperm woods ized in angiosperms, because most have axial paren- suggests an important role for this tissue, and the chyma in contact with vessels. At an ultrastructural observed presence of starch in axial parenchyma of level, the nature of vessel–parenchyma pits (Plavcova & liquid-preserved material is a prime indicator that car- Hacke, 2011) may represent a promising avenue for bohydrate activity must be involved. Osmotic water investigation. shifting is made possible by the hydrolysis of starch into Are some angiosperm woods limited in their ability sugars (Sauter et al., 1973; Braun, 1984). Mauseth & to react to function in conditions with a greater range

© 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 177, 291–321 316 S. CARLQUIST of temperatures and moisture availabilities? Does vidual species, with the hope of finding universally this limit particular clades from advancing into applicable principles, but the path to universality is niches with more marked fluctuation in temperature not always obvious because of vascular plant diver- and moisture availability? One still sees this idea sity. Experimental work is also often confined to one explicitly and implicitly expressed as a way of or several moments in time. Braun (1970, 1984) and explaining the geographical distribution of wood fea- Sauter et al. (1973) reported periodicity in starch tures. This idea has also been basic to explaining the hydrolysis activity, with periodic changes in tempera- persistence of plesiomorphic features (e.g. scalariform ture, as a triggering mechanism. Presumably, after perforation plates) in some woods. Certainly, some shoots leaf out, cohesion–tension replaces osmotic Downloaded from https://academic.oup.com/botlinnean/article-abstract/177/3/291/2416378 by guest on 15 November 2018 clades have exploited a variety of niches to a greater water shifting as the predominant water ascent extent than others, and some have wide diversity in mechanism. wood anatomy, whereas others are much more stereo- typed. However, what if we take the position that all Placement woods are functionally successful in the localities in The nature of the placement and abundance of axial which they exist? We must then consider plesiomor- parenchyma with respect to vessels is a subject that phic structures as entirely functional, rather than requires analysis from several disciplines. Vesselless limiting. By considering structures as functional angiosperms and gymnosperms have been included rather than to various extents vestigial and limiting, in the present study as a way of asking questions we can explain their existence at the present time. about the location of axial parenchyma when vessels Bailey’s ideas on the evolution of xylem features did are not present in a wood. Conifers, Tetracentron and not take into account function, and therefore are some Winteraceae tend to have more axial paren- lacking in evolutionary respects (Olson, 2012). chyma in latewood than in earlywood. One possible hypothesis is the osmotic water shifting mechanism, Network considerations which would be of more value in latewood, in which Brodersen & McElrone (2013) stated that: ‘xylem tensions fluctuate more (with attendant embolism networks should no longer be considered an assem- formation possibilities) than they do in earlywood. blage of dead cells, empty conduits, but instead a Latewood in conifers is more vulnerable to embolism metabolically active tissue finely tuned to respond to formation than is earlywood (Domec & Gartner, ever changing environmental cues.’ This statement is 2002) and, in this context, the figures of Kedrov acceptable, but the nature of the functional network (2012), showing that contacts between rays and axial is not specified in anatomical terms. Three- parenchyma are frequent in Fitzroya Hook.f. ex dimensional reconstructions of vessel anastomoses Lindl., are noteworthy and similar in this respect to and interconnections between the ray and axial his figure of Alnus wood. parenchyma systems (e.g. Kedrov, 2012) supply the By far the majority of angiosperm woods have axial needed histological information. In both conifers and parenchyma in contact with vessels (Kribs, 1937; angiosperms, rays are interconnected with axial Zhang, Fujiota & Takabe, 2003). Wider vessels are parenchyma, and no ray or axial parenchyma strand more vulnerable to embolism formation than are late- is isolated from this network (Kedrov, 2012). An wood tracheids (Lo Gullo & Salleo, 1993), but both implicit feature of the living cell network in wood is kinds of vessel are more vulnerable than tracheids; its three-dimensionality, so that newer, active wood vasicentric tracheids also occur in the woods of increments participate in the network as older parts Quercus L. studied by Lo Gullo & Salleo, (1993). of the secondary xylem are de-activated. Thus, there If the axial parenchyma and ray systems form an is a time dimension and the network of living cells ‘accessory hydrosystem’ (Braun, 1984), the number of remains valid and functional, even though earlier contacts may be important in its function. The portions are no longer functional and newer portions number of contacts with a vessel is increased when of the network are brought into existence constantly, there are longer vessel elements and taller strands of initiated by the cambium. axial parenchyma, both of which are the result of having longer fusiform cambial initials, characteristic Cohesion–tension plus root pressure of angiosperm woods with more numerous plesiomor- In fact, a third mechanism, root pressure, as demon- phic features. Greater ray height, greater number of strated in monocots (Nobel, 1988; Stiller, Sperry & rays per millimetre and a predominance of upright Lafitte, 2005), is operative. This may be more wide- ray cells increase the potential number of contacts spread, and is to be expected in plants with adventi- between the axial and radial parenchyma systems. tious roots (which occur in all monocots). However, in We need to know whether woods with more numerous which plants are these three processes operative and contacts between the two systems also have greater to what degree? Experimental work must select indi- ‘conductive safety’ (resistance to embolism formation).

MULTIPLE FUNCTIONS The maintenance of turgor pressure does not explain, Do septate fibres substitute for axial parenchyma? however, the large quantities of starch in secondary The seeming interchangeability of bands of septate xylem ray and axial parenchyma of Chorisia. More fibres and similarly positioned apotracheal axial than a single function is probably being served, and the parenchyma bands in Celastraceae (Fig. 6) suggests data of Chapotin et al. (2006a, b, c) do not completely functional equivalence between the two cell types. In exclude functions other than mechanical for the paren- this case, not merely position, but also quantity, is chyma in Adansonia. involved. However, septate fibres usually do not show Downloaded from https://academic.oup.com/botlinnean/article-abstract/177/3/291/2416378 by guest on 15 November 2018 such through-going equivalence; they differ from axial Finding function by default parenchyma in either quantity or position. Septate The analysis of earlywood versus latewood in the fibres also differ from axial parenchyma in wall char- conifer Pseudotsuga Carrière (Domec & Gartner, 2002) acteristics: they are usually thicker walled, suggest- showed that earlywood accounts for most of the con- ing that a mechanical function is being served. duction. These authors also showed that earlywood is, not surprisingly, vulnerable to embolism formation. Mechanical strength plus carbohydrate storage Their data showed that, under most conditions, late- Functional multiplicity is evident in the fibre dimor- wood is equally vulnerable to embolism formation. If phism of Acer wood, in which narrower, thicker walled latewood in Pseudotsuga does not conduct to a major fibres are formed proximal to the vessels, but wider, extent and yet is vulnerable to embolism formation, thinner walled fibres are formed distal to the vessels. what is its value in the stem? The methods used by The fibre dimorphism suggests that the wider fibres Domec & Gartner (2002) did not involve the analysis of serve for both carbohydrate storage (as observed by mechanical properties, but the implied result of their Sauter et al., 1973) and mechanical function. One can study seems to be that the value of latewood may be contrast this with the marked difference in wall thick- mostly mechanical, in the formation of cells in which ness between axial parenchyma cells and septate the wall to lumen area is much greater than in fibres in Siphonodon.InHalleria, the entire ground earlywood tracheids. This suggests that, sometimes, tissue of the secondary xylem consists of septate we may find the most important function of a tissue by fibres that are rich in starch (as are ray cells), another identifying what it does not do. Ultimately, the causa- instance of carbohydrate storage. Both of these exam- tion of latewood must be involved in such explanations: ples suggest mechanical strength combined with car- in the case of latewood, decreased levels of auxin bohydrate storage that can be used in osmotic water explain the formation of cells with a narrower cell shifting. In addition to osmotic water shifting, diameter (Aloni, 1987, 2001). massive carbohydrate storage of this sort may be involved in flushing of flowers and inflorescences (fol- Functional overlap lowed by a wave of fruit production), processes that The presence of septate fibres as a ground tissue in require larger carbohydrate input than can be secondary xylem may be associated with smaller achieved by the amount of photosynthesis during amounts of axial parenchyma in some genera, such as these events, and which therefore can draw on starch Umbellularia or Fuchsia L. (Carlquist, 1988). The reserves in parenchyma. Does this actually happen? coexistence of the two cell types in a given wood Studies at present are few. seems to provide evidence of functional overlap, because the extinction of a cell type in wood is evi- Pervasive parenchyma dently achieved readily in evolutionary terms, as the The massive stems of Adansonia have been considered list of plants with these two cell types concurrently as prime examples of water storage, but is this the suggests. Raylessness also illustrates this principle. primary purpose of this parenchyma ground tissue of In the case of woods with axial parenchyma plus the secondary xylem in this species? The stems of a septate fibres, such as Araliaceae, we may want to related genus, Chorisia, were examined earlier in the test the hypothesis that mechanical strength, carbo- present article. Chapotin et al., (2006a, b, c) found that hydrate storage and osmotic water shifting are water storage in Adansonia corresponded not so much related to the presence of both cell types (in addition to seasonal changes in soil moisture availability, but to ray parenchyma). Are all functions served equally rather to a mechanical consideration, cell strength actively? The lesson from Adansonia secondary xylem achieved by turgor. This phenomenon is not unknown is that some functions may be served to some extent and occurs in such succulents as Crassula argentea or during short seasonal periods, whereas others, Thunb., in which, during the dry season, stems shrink such as the mechanical strength offered by turgor in and bend, no longer upright as turgor pressure in the axial parenchyma in Adansonia, are important pervasive parenchyma of secondary xylem decreases. throughout the life of the plant.

DIVERSITY RATHER THAN ADHERENCE TO A PLAN prove, but the presence of these compounds seems to Rayless woods have the interesting characteristic, in represent compelling evidence. If pathogen deterrence such genera as Geranium, Pelargonium and Plantago, were the sole purpose of the presence of axial paren- of having secondary xylem that begins rayless but chyma, however, it would not be distributed as it is, forms rays at a certain point, sometimes after 1 year, primarily in relation to conductive cells (vessel ele- sometimes later. We should note that not all rayless ments and tracheids). Tyloses represent mainly the woods conform to the same basic pattern, and that products of axial parenchyma: ballooning of axial what is true in one genus probably is not true in parenchyma cells into vessels that have become another. Nevertheless, rayless woods show that, for embolized or otherwise deactivated. The functional Downloaded from https://academic.oup.com/botlinnean/article-abstract/177/3/291/2416378 by guest on 15 November 2018 example, radial conduction of water and photosyn- significance of tyloses may be the blockage of non- thates may be negligible or may occur via septate functional woods against pathogens. Crystals and fibres at first, but then may become appreciable when starch are occasionally reported in tyloses, suggesting rays begin to be formed. Ray formation is not simul- that tyloses may have more than one function. taneous with axial parenchyma formation in some rayless woods: Jacobinia has axial parenchyma, but AXIAL PARENCHYMA SCARCITY: VESTIGIAL DESIGN OR stems remain rayless. In Jacobinia, septate fibres PARSIMONIOUS STRUCTURE? may account for a slow but steady radial flow. As a generalization, one may say that rayless woods first Metcalfe & Chalk (1950) characterized axial paren- exhibit the formation of a maximum amount of fibri- chyma as sparse to absent in Aceraceae (= Sapin- form cells to achieve greater mechanical strength, daceae), Argophyllaceae, Berberidaceae, Brassicaceae, and then diversify to more numerous cell types with Calycanthaceae, Cercidiphyllaceae, Cistaceae, Con- more numerous functions as diameter increases. The naraceae, Crossosomataceae, Ericaceae (including wood of Hebe (Veronica) salicifolia features neither Epacridaceae and Vacciniaceae), ‘Flacourtiaceae’, ray nor axial parenchyma in the stems that have been Grubbiaceae, Hydrangeaceae, Illiciaceae, Lardizabal- sampled thus far (Meylan & Butterfield, 1978), which aceae, Monimiaceae (Atherospermacaeae), Myrotham- suggests a strong emphasis on mechanical strength. naceae, Nyssaceae (= Cornaceae), Paeoniaceae and However, how can wood of such a species function Papaveraceae. There is probably more than one expla- over a period of years without axial and ray paren- nation of why axial parenchyma should be sparse in chyma? Our knowledge of the physiology of rayless these families. ‘Sparse’ does not equate to ‘scarce’ in woods is minimal. Rayless woods are ideal experimen- this regard: axial parenchyma is characteristically tal material because one can compare wood of a single present, but not abundant in these families. species with rays and earlier-formed wood of the same In addition, one can cite families in which axial species without rays. Although we need to know much parenchyma is diffuse and relatively inconspicuous. more about rayless woods, our present knowledge There seems to be some association between diffuse or suggests that they represent a diverse assemblage scarce axial parenchyma and the presence of trac- rather than conformity to a single structural mode. heids (‘fibres with fully bordered pits’ of Metcalfe & The woods of Castilleja, Crepidiastrum and Stan- Chalk, 1950). These families may have wood in which leya (Fig. 3) show various timings in the production of air embolisms in vessels or tracheids are an infre- fibrous wood versus parenchymatous wood. They quent occurrence, and in which, therefore, the osmotic illustrate that mechanical strength can be enhanced water shifting role of axial parenchyma is minimal. at various times in secondary xylem production. Mechanical strength in these examples is enhanced Paedomorphic Type III rays: a functional by the substitution of fibrous wood for parenchyma- association with axial parenchyma scarcity? tous wood to varied radial extents. The occurrence of Ericaceae s.l. in the list above leads to an interesting association: woods with Paedomor- phic Type III rays. A preliminary list of families with PROTECTIVE FUNCTIONS Paedomorphic Type III rays overlaps with the list Axial parenchyma may have crystals as contents (as above quite appreciably. The list of families in which may septate fibres). Secondary products, such as one can find uniseriate rays only, composed of upright resins, terpenoids, etc., may be accumulated in axial cells, includes: Caryophyllaceae (some subshrubby parenchyma cells, which thus take on functions such genera), Celastraceae (Empleuridium Sond. & Harv. as herbivore deterrence or resistance to fungi and ex Harv., Euonymus L.), Cistaceae, Elaeocarpaceae bacteria (Deflorio et al., 2008). In this context, paren- (the subfamily formerly recognized as Treman- chyma can offer the segmentation of wood, walling off draceae), Ericaceae (including Empetraceae, Epacri- the spread of pathogens by the production of suberin daceae and Vacciniaceae), Grubbiaceae, Haloragaceae and other compounds. These functions are difficult to (Gonocarpus Thunb.), Myrothamnaceae, Rubiaceae

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