living cells in wood. 1. absence, scarcity and histology ...€¦ · work in wood physiology, and...

Living cells in wood. 1. Absence, scarcity and histologyof axial parenchyma as keys to function

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 recentwork in wood physiology, and questions and hypotheses relative to axial parenchyma anatomy are offered. Cellshape, location, abundance, size, wall characteristics and contents are all characteristics for the assessment of thephysiological functions of axial parenchyma, a tissue that has been neglected in the consideration of how woodhistology has evolved. Axial parenchyma occurrence should be considered with respect to mechanisms for theprevention and reversal of embolisms in tracheary elements. This mechanism complements cohesion–tension-basedwater movement and root pressure as a way of maintaining flow in xylem. Septate fibres can substitute for axialparenchyma (‘axial parenchyma absent’) and account for water movement in xylem and for the supply ofcarbohydrate abundance underlying massive and sudden events of foliation, flowering and fruiting, as can fibredimorphism and the co-occurrence of septate fibres and axial parenchyma. Rayless woods may or may not containaxial parenchyma and are informative when analysing parenchyma function. Interconnections between ray andaxial parenchyma are common, and so axial and radial parenchyma must be considered as complementary partsof a network, with distinctive but interactive functions. Upright ray cells and more numerous rays per millimetreenhance interconnection and are more often found in woods that contain tracheids. Vesselless woods in bothgymnosperms and angiosperms have axial parenchyma, the distribution of which suggests a function in osmoticwater shifting. Water and photosynthate storage in axial parenchyma may be associated with seasonal changes andwith 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 parenchymamay serve to both enhance mechanical strength or, when parenchyma is thin-walled, as a tissue that adapts tovolume change with a change in water content. Other functions of axial parenchyma (contributing resistance topathogens; a site for the recovery of physical damage) are considered. The diagnostic features of axial parenchymaand septate fibres are reviewed in order to clarify distinctions and to aid in cell type identification. Systematiclistings are given for particular axial parenchyma conditions (e.g. axial parenchyma ‘absent’ with septate fibressubstituting). A knowledge of the axial parenchyma information presented here is desirable for a full understand-ing of xylem function. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015,177, 291–321.

ADDITIONAL KEYWORDS: conductive safety – embolism reduction – osmotic water shifting – rays –septate fibres – water storage – wood evolution – wood physiology.

INTRODUCTION

Ray and axial parenchyma are often considered as thetwo living types of cell in woods and are figured intextbooks, but their functions and diversity aremostly left unexplored in such sources. By contrast,

the conducting cells of wood (vessel elements andtracheids, both with prominent bordered pits) and themechanically important fibrous cells (fibre-tracheidsand libriform fibres), which are mostly dead at matu-rity, are linked in textbooks to conductive functions,and therefore have been the topic, if only indirectly, ofmuch physiological experimentation. Septate fibres,which are mostly libriform fibres with prolonged lon-gevity, are a type of living cell in wood that has been*E-mail: [email protected]

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Botanical Journal of the Linnean Society, 2015, 177, 291–321. With 13 figures

© 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 177, 291–321 291

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little studied: one must reach back to the papers ofWolkinger (1969, 1970a, b) to find even condensedconsideration. The phenomenon of fibre dimorphism(Carlquist, 1958, 1961, 2014), in which libriformfibres of two sorts (narrower, thicker walled vs. wider,thinner walled, often alive at maturity) are present ina given wood, has been noticed by only a smallnumber of workers, despite its conspicuous occur-rence in such familiar woods as maple, Acer L. Evencriteria for the recognition of the cell types mentionedabove are not easily located in wood anatomical lit-erature. The monographs of Wolkinger cover ‘leb-enden Fasern’, but we do not have a clear idea of howlong ‘living fibres’ live. Septate fibres are assumed tobe ‘living fibres’, but some may not live much longerthan non-septate libriform fibres. We have little infor-mation because wood anatomy is still largely based ondried rather than liquid-preserved specimens.

There is growing interest in axial parenchymaamong wood physiologists (Spicer, 2014), because ofthe conviction that such a commonly present celltype, often distributed adjacent to vessels and trac-heids, must perform some function related to theconductive process. The ‘osmotic water shifting’ ideasof Braun (1970) proposed that the development ofhigher osmotic pressures, chiefly through the conver-sion of starch into sugar (both found in axial paren-chyma as well as in rays), could draw water from onecell into another and thus function in the conductiveprocess. This was formalized into a theory of com-pensating pressure by Canny (1995, 1998), althoughthese ideas have been met with scepticism(Comstock, 1999). However, there are other ways inwhich differential solute concentrations in axialparenchyma may be achieved and function in con-duction, as exemplified by Holbrook & Zwieniecki(1999) and Zwieniecki & Holbrook (2000, 2009). Woodphysiologists currently express interest in, and offervaried hypotheses on, the function of axial paren-chyma. Several are of the opinion that no clearunderstanding of how parenchyma contributes to theconductive process exists. A consensus on exactly howaxial parenchyma may function in the prevention orcountering of embolisms has not yet been reached,but the current state of this field is discussed below.The presence, absence, scarcity, distribution within awood and histology of axial parenchyma are not inde-pendent of wood physiology. Rather, they must even-tually be integrated into any interpretations ofparenchyma with relation to conduction in plants.The patterns described in this article are offered inthe hope that they will further the structure–function dialogue. The various anatomical plans ofwoods are considered here to represent parsimoniousformulations that suit the water economy of particu-lar species. In the earlier literature, one is given the

impression, if only indirectly, that ‘primitive’ woodsare inefficient at conduction, whereas ‘advanced’woods excel at conduction, and that plants with‘primitive’ woods are evolutionarily limited by theirwood formulae and are marginalized by plants withmore efficient, upgraded, wood anatomy. However,plants with putatively plesiomorphic wood featurescoexist with those that have apomorphic wood fea-tures, so that both patterns must be entirely func-tional, although in plants with different ecology andgrowth form. The present article takes the point ofview that the various anatomical formulae of woodanatomy must be understood as varied but effectiveways of dealing with water economy. We cannotunderstand how xylem works by studying only Zea L.or Helianthus L., convenient though they may be.Although wood physiology seems to be drifting awayfrom the study of wood anatomical diversity, ulti-mately the two must coalesce. The present articledoes not form such a bridge, but it does indicate thecomplexity of axial parenchyma, a complexity whichtherefore must ultimately be explained in evolution-ary and physiological terms.

In order to satisfy the needs of descriptive woodanatomy, Kribs (1935, 1937) and Metcalfe & Chalk(1950) categorized types of ray and axial parenchymaon the basis of histological features. In the case ofaxial parenchyma, location with respect to vessels orto growth rings, grouping and abundance were themain criteria used by Kribs (1937). Both Kribs (1937)and Metcalfe & Chalk (1950) recognized an axialparenchyma type, ‘Absent’, which seems paradoxicalat first glance. If axial parenchyma is absent, whatsubstitutes for its functions? In turn, this raises thequestion, what are the functions of axial parenchymawhen it is present? These questions were asked vir-tually not at all in the mid-20th century, in whichaccurate anatomical description of the woods of theworld was seen as the task at hand, and in whichquestions pertaining to wood evolution in a functionalcontext went unasked and therefore unanswered.Despite the obvious and pervasive modes of cell pres-ence and diversity in woods, hypotheses about func-tion were often considered as ‘speculative’ instead ofthe legitimate hypotheses that they were, and thuswood physiology was deprived of some pertinent ques-tions. For example, do all manifestations of axialparenchyma have the same function? The role of axialparenchyma in the conductive process was probablyalso ignored because laboratory equipment, althougheasily connected so as to measure processes quanti-tatively in tracheary elements (tubes, pressuretanks), could not be applied to actions in axial paren-chyma or rays. There are no indexed mentions ofaxial parenchyma (or rays) in Tyree & Zimmermann(2002). No listings were given by Kribs (1937) or

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© 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 177, 291–321

Metcalfe & Chalk (1950) of genera and families with‘Absent’ axial parenchyma. One type of axial paren-chyma, which I have called ‘Pervasive’, involves asecondary xylem ground plan in which axial paren-chyma predominates and contains no fibrous tissue,only vessels (Carlquist, 1988, 2001); this eludednotice in earlier literature, perhaps because of thepredominant focus on woodier plants.

‘Axial parenchyma absent’ and ‘Axial parenchymascarce’ are not uniform categories, and unravellingthe diversity within these artificial groupings is one ofthe goals of this article. All expressions relevant tothese categories are reviewed here, and an attempt ismade to analyse not the absence or scarcity of axialparenchyma, but what is the meaning of these struc-tural types. If they are alternative histological adap-tations to what axial parenchyma most commonlydoes, what do they show us? The differences betweenwhat axial parenchyma does and what other similarcell types (e.g. septate fibres) do have not yet beenappreciated. Septate fibres have secondary wallscapable of offering the support of non-septate fibresthat are dead at maturity, but their longevity andcontents (starch is common in them) suggest amechanical function and a function that involves pho-tosynthates. In some cases, reports of absent or scarceaxial parenchyma are not entirely correct, and suchcases are analysed here. Rayless woods are consid-ered here because, if rays are absent, do these woodslack axial parenchyma, which is commonly inter-linked with rays?

Axial parenchyma must have multiple functions, asdo other cell types (e.g. fibre dimorphism; Carlquist,2014). One of the prominent lessons of wood evolutionis that functional change is more easily accomplishedby small modifications of an existing cell type than bythe invention of new cell types. As one example, thewide axial parenchyma bands of Chorisia Kunth(Fig. 1F) are indicative of some kind of storage func-tion, whereas the occurrence of a few cells of axialparenchyma near vessels (Fig. 4E) or scattered resin-filled axial parenchyma (Fig. 12A) suggests functionsother than storage. In addition to ‘absent’ or ‘scanty’axial parenchyma, the polar opposite, which I havenamed ‘Pervasive’ parenchyma (Carlquist, 1988), inwhich the fascicular xylem consists wholly of paren-chyma plus vessels, as in Caricaceae (Carlquist, 1998)and some stem succulents, is considered here. Theterm ‘scanty’ here is not intended to include instancesin which an extremely small number of axial paren-chyma cells are present in a wood, because suchrarity of occurrence does not represent effective per-formance of a function for the wood as a whole.

Axial parenchyma is often associated with vesselsin woody angiosperms. This provides hints about pos-sible function, but we must also explain axial paren-

chyma function in vesselless woody plants, and sovesselless angiosperms, cycads and Ginkgo L. areincluded here, as are Gnetales.

Instances of ‘scarce’ (but characteristically present)axial parenchyma in angiosperm woods bring intoplay a hitherto unconsidered question: can rays com-posed of upright cells substitute in function, to somedegree, for axial parenchyma? The ray type ‘Paedo-morphic Type III’ (Carlquist, 1988) designates unise-riate rays composed of upright cells. Thus, they arelike radial sheets of axial parenchyma. One can alsoask whether or not conjunctive tissue formed ofparenchyma cells is a functional equivalent for bandsof apotracheal parenchyma. Conjunctive tissue occursonly in species with successive cambia, and is pro-duced by a master cambium, not a vascular cambium.

Septate fibres and axial parenchyma cells aresimilar in many respects: both are vertically orientedliving cells. Are they ‘interchangeable’ in phylogeneticterms? The intriguing case of Celastraceae, in whicheither one or the other, but not both, are present, isdescribed here. Going beyond Celastraceae, we tendto find differential distribution patterns for the twocell types which suggest modally different functions,although the functions may overlap. Instances inwhich both cell types are characteristically present inwood of a given species and those that lack one or theother give us a kind of circumstantial evidence on thispoint. There are very few mentions in the literature ofany cells intermediate between axial parenchyma andseptate fibres. The example of fibre dimorphism(Carlquist, 2014) is pertinent and is covered herebecause the divergence of fibriform cells into twomodes (with intermediacy between them) is not reallyan exception: in Acer, one has no difficulty in distin-guishing between the dimorphic fibres and axialparenchyma.

Axial parenchyma is scarce in some angiospermouswoods which have notably long vessel elements (andimperforate tracheary elements). These woods alsohave greater length of axial parenchyma strands(which are derived from the same fusiform cambialinitials as vessel elements and imperforate trachearyelements). Such woods also tend to have more numer-ous rays per millimetre (number of rays that intersectan imaginary transverse scale superimposed on atangential section). Thus, there are more points ofpotential contact between axial parenchyma and rays(especially uniseriate rays) in such woods. Does axialparenchyma scarcity correspond inversely to ray his-tology and ray abundance in such woods? In turn, thisquestion relates to the three-dimensional distributionand interconnections of the ray and axial parenchymasystems (see Kedrov, 2012).

The present article attempts to provide the under-pinnings for answers to questions such as those posed

AXIAL PARENCHYMA AND WOOD FUNCTION 293


Figure 1. Diagnostic features of axial parenchyma and septate fibres. A, B, Siphonodon australis Benth. (ForestryCommission of New South Wales). A, Axial parenchyma cells are much thinner walled than the imperforate trachearyelements. B, Radial section. Intercellular spaces in conjunction with cells of axial parenchyma strands. C, Bowkeriagerrardiana 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 imperforatetracheary 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 axialparenchyma and ray cells. ap, axial parenchyma; i, intercellular space; lf, libriform fibres; r, ray; s, septum.

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above. Wood physiologists may prefer not to begininvestigations with wood anatomical surveys, and yet,if they do not offer explanations for wood histology asseen under the light microscope, they are missingthe structure–function continuum that must exist.Current work in wood physiology is, however, encour-aging in this regard. In a recent synthesis (Carlquist,2012a), I attempted to include information from woodphysiology, ecology, habit, molecular systematics andultrastructure whilst surveying histological features.The present article also attempts to be inclusive, butthere is, as yet, little direct information on functionavailable. Consequently, the interpretations sug-gested by structure must be given a larger role, in theform of hypotheses and questions. The thesis under-lying this approach is that structure is a reliable keyto present-day function. I do not know of any workthat has proved that present-day wood structure isminimally functional, of vestigial or ‘historical’ impor-tance. Wood evolution seems too parsimonious toallow the persistence of features that are no longerfunctional: the investment of photosynthates in woodis considerable, and not likely to be wasted on char-acters that are no longer fully functional.

MATERIAL AND METHODS

The systematic listings given below for particularanatomical characteristics are not complete, althoughreporting of as many families and genera as possiblehas been attempted. The listings are culled largelyfrom the text of Metcalfe & Chalk (1950), supple-mented by information from other cited sources andfrom my own research. The identification and sourcesof the materials studied are given in the legends tothe figures. The present article consists of originalobservations, based on an extensive library of micro-scope slides of wood sections. Observations by othershave been incorporated, as the citations indicate. Thepresent article is neither a data paper nor a review,but has some aspects of both. Because this studyis based on a large number of microscope slidesaccumulated over decades, citation of the methodsemployed would not be appropriate.

AXIAL PARENCHYMA ASPECTSIS AXIAL PARENCHYMA ALWAYS DISTINGUISHABLE

FROM OTHER CELL TYPES?

The answer to this question is an almost unqualified‘yes’, but the criteria for the recognition of this celltype must be given and examined. These criteria needto be explicitly reviewed and described.

Wall thickness is often used as one criterion todistinguish between axial parenchyma and adjacent

imperforate tracheary elements (tracheids, fibre-tracheids and libriform fibres), which may appearsimilar in diameter as seen in transverse sections ofwood (Fig. 1A, B, E). Although axial parenchymacells often have thinner walls than those of imperfo-rate tracheary elements (fibrous tissue), wall thick-ness can be similar, so that one must always confirmthe identification of this cell type by examining radialsections (Figs 1B, F, 6B). In tangential section, axialparenchyma strands can look identical to uniseriaterays composed of upright cells, but axial parenchymacells do not form radial sheets as do ray cells. Typi-cally, ray cells are in horizontal rows as seen inradial sections. Axial parenchyma strands appear assingle strands or small groups of strands runningvertically in a radial section. If several axial paren-chyma strands are adjacent to each other, the crosswalls in them are staggered with respect to level(Fig. 6B), whereas ray cells form horizontally alignedrows. One can find only a few woods in which group-ings of axial parenchyma cells are subdivided atsimilar levels as seen in radial section (Fig. 1F). Inthe section shown in Figure 1F, the ray cells aresmaller than the axial parenchyma cells and thatfeature permits distinction.

Axial parenchyma cells may differ markedly in sizeamong angiosperms (compare Fig. 1A and 1D), andthis may prove to correspond to functional differences.In the case of Chorisia (Fig. 1D–F) and Erythrina L.(Fig. 2A, B), water storage and starch storage prob-ably correspond to larger parenchyma cell sizes.

The most important diagnostic difference betweenseptate fibres and axial parenchyma relates to thetiming of the transverse divisions (Fig. 1B, C). Inaxial parenchyma strands, transverse divisions takeplace early, soon after the derivation of a daughtercell from a fusiform cambial initial. Each cell in sucha strand is thus surrounded by its own (usuallysecondary) wall, so that the superposed cells in astrand are separated by a double transverse wall. Airspaces may often be seen adjacent to these transversewalls, because the earlier timing of the division ofcells in the parenchyma strand allows sufficient timefor this to happen (Fig. 1B, D, i).

In septate fibres, the protoplast has greater longev-ity than in typical non-septate libriform fibres, whichdie soon after maturation of their secondary walls.Transverse divisions occur late in septate fibres, andare membranous, with only a primary wall separatingthe two or more cells within a septate fibre. Theearlier formed secondary wall is not interrupted bythis late-developing primary wall (the septum). Theseptum usually stains differently from the axiallyoriented secondary wall because lignin is lacking inthe septum. This is especially prominent if counter-staining is employed (Fig. 1B, D).



Figure 2. Unusual features of axial parenchyma. A, B, Erythrina coralloides Moc. & Sessé, cult. Huntington BotanicalGardens, San Marino, CA, USA. A, Wood transverse section; axial parenchyma cells are much wider than the libriformfibres. B, Tangential section. In the axial parenchyma band, strands of one or two cells are present. C, D, Frankeniapalmeri 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 arenot subdivided into strands. E, Dirca occidentalis A.Gray, Abrams 106 (POM). Transverse section; axial parenchyma islimited to a single layer at the margin between earlywood and latewood. F, Gyrinopsis cumingiana Decne., PhilippineBureau 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 intostrands. ap, axial parenchyma; c, crystalliferous cell; f, fibre; ixp, interxylary phloem; lf, libriform fibre; mp, marginalparenchyma; nv+vt, narrower vessels + vasicentric tracheids; r, ray; s, storey levels; v, vessel).

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Living fibres tend to have easily visible contents.Starch is the most common component (Figs 1D, F,4A–C). Starch is also common in axial parenchyma.Chorisia has abundant starch in both types of cell andin ray parenchyma. Even if specific stains are notused for starch grains, they are easily recognized inpermanent slides by their dark hila and circular tooval outline (Fig. 1D).

Water storage is more difficult to prove by means ofhistological features than one might expect. Extremesucculence is easy to interpret, but can water storageoccur in woods that are not notably enlarged? Thereare reasons to believe that water storage in woods canbe measured (S. Carlquist, unpubl. data). In terms ofvisible features, one looks for cells of somewhat largerdiameter (Figs 1E, F, 2A, B). Various degrees of abun-dance (Figs 1E, 2A, 3A) may be keys to degree andkind of storage, when combined with other informa-tion from a given plant.

Axial parenchyma strands usually have terminalcells with mitred or bevelled tips (Fig. 2B), whereasseptate fibres have tapered tips. In transversesection, axial parenchyma cells, when larger andthinner walled, may be polygonal (Figs 1E, 2A),whereas, when smaller in diameter, and especiallywhen scattered in a diffuse fashion, they tend to beround in transverse section (Fig. 1A), thereby resem-bling imperforate tracheary elements.

The accumulation of secondary plant products(resins, etc.) is probably an indicator of prolongedlongevity for both axial parenchyma and septatefibres. Crystals can be present in axial parenchyma(Fig. 2C, D, F), septate fibres and libriform fibres.However, reports of crystals in woods mostly do notstate which of these cell types contains the crystals(e.g. Metcalfe & Chalk, 1950).

Axial parenchyma strands can be more than tencells long in some species with long fusiform cambialinitials. Mostly, they are shorter. One-celled axialparenchyma strands are shown in Fig. 2B for Eryth-rina, mixed with two-celled strands. The one-celledaxial parenchyma strands of Frankenia L. (Fig. 2C,D) are inconspicuous. One-celled axial parenchymastrands are usually found in species with short fusi-form cambial initials. Not surprisingly, fusiformcambial initials and their derivatives in these speciesare not infrequently storied (Fig. 2B–D). Most of thecells shown in the sections of Frankenia are notlibriform fibres, but vessel elements (often quitenarrow) and axial parenchyma cells (Fig. 2D).

AXIAL PARENCHYMA NOT ABSENT BUT NOT EASILY

DISTINGUISHABLE

The example of Frankenia highlights the difficulty ofdistinguishing between axial parenchyma strands one

cell tall and non-septate (but living) fibres. Metcalfe &Chalk (1950) reported the absence of axial paren-chyma in Dirca L. (Thymeleaceae), but my materialshows an inconspicuous layer of terminal (marginal)parenchyma (Fig. 2E, mp) at the end of a growth ring.This also proves to be true in Acer saccharum Mar-shall (Fig. 7B).

Axial parenchyma that accompanies strands ofphloem can easily be overlooked. Gyrinopsis Decne.(Thymeleaceae) illustrates this phenomenon (Fig. 2F,ap). Thinner walled axial parenchyma cells thatcontain crystals in this wood (Fig. 2F, ixp) are alsostrands that can easily be overlooked.

Axial parenchyma of indefinite extentThe intended meaning here is that cylinders of per-vasive axial parenchyma may vary in radial width,and may be supplanted by fibrous secondary xylem.This phenomenon differs from apotracheal bandedparenchyma, in which bands may be wide, but char-acteristically so. Crepidiastrum Nakai (Fig. 3A) isessentially a rosette herb, somewhat transitional to arosette shrub. The production of pervasive paren-chyma (pw) is characteristic of less woody stems, butsome stems are intermediate and can feature occa-sional cylinders of libriform fibres (fw). It should benoted that the vessel diameter is relatively constantacross these zones.

Members of Brassicaceae, such as Stanleya pinnata(Pursh) Britton (Fig. 3B), form bands of parenchyma-tous wood of varied width. These often occur as late-wood, but some are intercalated at other pointsduring a season. Such bands have been reported forother Brassicaceae by Metcalfe & Chalk (1950):Alyssum spinosum L., Brassica fruticulosa Cyrilloand Vella spinosa Boiss. Pervasive axial parenchymaoccurs in roots of Brassicaceae that are notably non-woody, such as Raphanus sativus L. and Armoracialapathifolia Gilib. These two species have morefibrous wood in non-domestic populations, but culti-vars (which are familiar as radishes and horseradish,respectively) represent selection for woods with per-vasive parenchyma.

A change from fibrous to non-fibrous secondaryxylem can be observed in some species, such as Cas-tilleja latifolia Hook. & Arn. (Fig. 3C, D). This is asubshrub in which new branches are innovated, butold branches may persist. The first-year wood tends tobe fibrous (Fig. 3C, D, fw). Parenchymatous wood(Fig. 3C, pw) is formed later. This pattern suggeststhe acquisition of mechanical strength and, whenlongitudinal growth of the shoot slows or ceases (andthus mechanical strength is of no value in subsequentwood), a change to non-fibrous wood occurs. Indeed,the C. latifolia pattern may be found in various herbsand subshrubs to various degrees depending on



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 offibres 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, Radialsection. 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.

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growth form and moisture availability. Some annualsthat typically dry as a dry season approaches (e.g.Raphanus sativus) can survive into a second year andform non-fibrous wood if moisture is available. Viningplants that encounter a surface on which to lean mayshift from fibrous xylem to xylem with fewer fibres(Mauseth, 1993). Experiments in which annuals per-ennate because of prolonged water availability (andunder frost-free conditions) should be studied toshow instances of this phenomenon and the factorsinvolved in a change in wood construction.

Sparse septate fibresThe growth habit of Isoplexis canariensis (L.) Loud.[ = Digitalis canariensis L.] is best described as arosette perennial, with several stems of varied dura-tion branching from the base. The wood as seen intransection (Fig. 3E) can be easily demarcated intolatewood and earlywood, because the diameter of thefibres is narrower in latewood. As observed in radialsection, the fibres of D. canariensis are not all septate;perhaps no more than a quarter or a third of thefibres contain one or more septa. Instances such asthis have not been reported previously, perhapsbecause they are subtle. If wood sections are thin, anobserver may assume, with justification, that a septamay be missing in any given septate fibre because ithas been excised. However, the number of septa infibres of D. canariensis is much lower than can beaccounted for by the thinness of sections (Fig. 3F).Septa in fibres of D. canariensis, as in most otherwoods with septate fibres, are located, if one per fibre,near the widest portion of the fibre.

AXIAL PARENCHYMA ABSENCE IS OFTEN SEPTATE

FIBRE PRESENCE

Two genera now placed in Stilbaceae on the basis ofmolecular evidence, Bowkeria Harv. and Halleria L.(Fig. 4A–C), have septate fibres of relatively uniformdiameter (Fig. 4A). These fibres contain numerousstarch grains, 2–3 μm in diameter. Moreover, the raycells of Halleria also contain abundant starch grains(Fig. 4C). Growth rings are absent or minimal. Hal-leria produces leaves, flowers and fruits wheneverwater is available, and the seasonally massivegrowth, flowering and fruiting events during wetterperiods of the year may be correlated with extensivestarch accumulations. Septate fibres offer a muchmore abundant storage area for starch than wouldaxial parenchyma strands, and yet the septate fibresalso offer appreciable mechanical strength, judgingfrom their wall thickness. Halleria lucida L. is asmall tree native to areas of eastern and southernAfrica that have dry and wet seasons of uncertaintiming and duration (Goldblatt & Manning, 2000).

Kogelbergia Rourke (Fig. 4D–G) is representative ofthe earlier concept of Stilbaceae, which included onlygenera of small subshrubs with narrow leaves. Thesegenera are found on areas of Cape Province Sand-stone in which rainfall occurs mostly in winter, as inother Mediterranean-type climates. The wood is xero-morphic, with numerous relatively narrow groupedvessels (Fig. 4D). Kogelbergia verticillata (Eckl. &Zeyh.) Rourke has abaxial parenchyma, which is ascattering of axial parenchyma on the abaxial side ofa vessel (Fig. 4E–G). The Kogelbergia pattern is con-sonant with the idea that axial parenchyma supportsthe functioning of the conductive system. This con-trasts markedly with the Halleria pattern, and dem-onstrates that a shift in growth form and ecologicaladaptation take place readily within a small family ofeudicots.

Septate fibres substitute for axial parenchyma:systematic listingThe listing below is based on information from origi-nal research and from the texts of Metcalfe & Chalk(1950), Butterfield & Meylan (1976) and Meylan &Butterfield (1978). Additions of more families are tobe expected. The listing of a particular family shouldnot be construed as the presence of septate fibres inthe entire family.

Acanthaceae (Beloperone Nees, Jacobinia Moric.)Argophyllaceae (Corokia A.Cunn., Lautea F.Br.)AtherospermataceaeBerberidaceaeBrunelliaceaeCelastraceaeCampanulaceaeClusiaceae (Hypericum L.)ConnaraceaeEricaceae (Agauria Benth. & Hook.f., Arbutus L.,

Arctostaphylos Adans., Oxydendron D.Dietr. and someVaccinioideae)

Euphorbiaceae (some Antidesmeae and Croto-noideae)

‘Flacourtiaceae’GesneriaceaeGrossulariaceaeHaloragaceaeHelwingiaceaeHippocrateaceae [ = Celastraceae]Hydrangeaceae (septate fibres present as a few

cells near vessels in Dichroa Lour., Hydrangea L. andSchizophragma Siebold & Zucc.)

LardizabalaceaeLoganiaceae s.l. [Antonia Pohl., Buddleja L. (Scro-

phulariaceae), Bonyunia M.R.Schomb. ex Progel,Chilianthus Burchell (= Buddleja), Fagraea Thunb.(Gentianaceae)]

Meliaceae



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, Starchgrains (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. Axialparenchyma cells indicated by arrows. F, Radial section. Abaxial parenchyma on right. G, Tangential section. Abaxialparenchyma in strands of two cells, centre. ap, axial parenchyma.

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Monimiaceae (Doryphora Endl., Laurelia Juss.)Olacaceae (Octoknema Pierre)PhyllanthaceaePittosporaceaeRubiaceae (26 genera listed by Metcalfe & Chalk,

1950)Scrophulariaceae (Oftia Adans.; plus see Logani-

aceae s.l.)Simaroubaceae (Guilfoylia F.Muell.)Theophrastaceae [ = Primulaceae p.p.]Violaceae

Both/and: co-occurrence of axial parenchyma andseptate fibresThe presence of both septate fibres and axial paren-chyma in a particular wood makes for some interestinginterpretative possibilities. Those who expect blanketexplanations that will cover all woods with a particularhistological pattern may be disappointed to learn thatthere are no firm and unexceptionable correlations.The nature of wood evolution is such that more than asingle plan can accomplish a particular adaptivescheme in a given ecological site. As evidence of this,one notes that, in woods that have both axial paren-chyma and septate fibres, the proportions of the twocell types can vary depending on the species (this offersfurther interpretative possibilities).

Members of Araliaceae have both axial parenchymaand septate fibres (Fig. 5A, B). In Araliaceae, leaves donot unfold sequentially one by one over a series ofmonths. Rather, there are flushes of growth, and morethan one such growth event can occur per year. Therapid development of leaves, flowers and fruits prob-ably requires more than the currently produced pho-tosynthates, so that stored photosynthates make therapidity of the events possible. Massive starch storageoccurs in septate fibres of Araliaceae. Septate fibres areapparently universal in the family (Metcalfe & Chalk,1950). Two other features may bolster this correlation.Septate fibres are reported to be more common close tovessels than distal to them in Araliaceae; septate fibresare relatively wide, and are only about 50% longerthan the vessel elements they accompany (Metcalfe &Chalk, 1950: 733). This suggests a shift away from asolely mechanical role for the fibres.

In Polemoniaceae, Cantua Juss. (Fig. 5C, D) andLoeselia L. have relatively abundant axial parenchymaand septate fibres (Carlquist, Eckhart & Michener,1984). These genera are the woodiest of Polemoniaceaeand have heteroblasty, so that the emergence of longshoots bearing indefinite numbers of flowers can becorrelated with a shift in function of wood towardsstorage rather than mechanical strength.

Xylococcus Nutt. (Fig. 5E, F) and Arctostaphyloscontain more septate fibres than do other genera ofEricaceae. Septate fibres in the two genera are less

abundant than septate fibres in Araliaceae, however.This accords with the fact that these Ericaceae do notexhibit the prominent flushes of growth one sees insuch families as Araliaceae or Fabaceae. Arctostaphy-los and Xylococcus produce prominent aggregations offlowers prior to leafing out, so that carbohydratestorage seems to be correlated with this growthsequence. These two genera of Ericaceae have largerquantities of septate fibres in lignotubers, which servefor survival through fires or extreme drought, and canyield shoots soon after these events have terminated.

At an opposite extreme from these Ericaceae interms of ecology are the woody lobelioids, which haveseptate fibres throughout the secondary xylem. Theseseptate fibres can be shown, in liquid-preserved mate-rial, to possess significant starch storage (Carlquist,1969).

Systematic listing of families with both axialparenchyma and septate fibres

Acanthaceae (Carlquist & Zona, 1988)Anacardiaceae (some)Araliaceae (most)Bignoniaceae (some)Elaeocarpaceae (Elaeocarpus L.)Ericaceae (Arbutus, Arctostaphylos, Xylococcus)Euphorbiaceae (Bridelia Willd.)Fabaceae (some)Gesneriaceae (some: Carlquist & Hoekman, 1986)Lauraceae [Umbellularia (Nees) Nutt.]Loganiaceae (Geniostoma J.R.Forst. & G.Forst.)Meliaceae (some)Myrsinaceae [ = Primulaceae p.p.]Myrtaceae (Eugenia Mich. ex L., Syzygium

P.Browne ex Gaertn.)NothofagaceaeOleaceae (Forsythia Vahl, Olea L.)OnagraceaePittosporaceaePolemoniaceae (Cantua, Loeselia)Rosaceae (some Prunoideae; Photinia Lindl.,

Spiraea L.)Violaceae (some)

Either/orMetcalfe & Chalk (1950: 394) called attention to apeculiar phenomenon in Celastraceae. Some specieshave tangential bands of septate fibres. These bands ofseptate fibres are exactly comparable in position andextent to bands of axial parenchyma in other speciesand, in a single genus, the bands may be composed ofseptate fibres in one species and parenchyma inanother. This phenomenon seems to indicate that, inpertinent Celastraceae, axial parenchyma and septatefibres are interchangeable in function.



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, andaxial parenchyma cells (diagonal walls), right. C, D, Cantua pyrifolia Juss., Carlquist 341 (RSA), radial section. C, Axialparenchyma 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, Radialsection. Details of septate fibres. ap, axial parenchyma; s, septum; sf, septate fibres; v, vessels.

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The materials illustrated here confirm the claimsof Metcalfe & Chalk (1950). In Siphonodon Griff.(Fig. 6A, B), axial parenchyma is present in tangentialbands. These bands vary in abundance and density,with wood mostly composed of libriform fibres at somepoints (Fig. 6A, centre), but with axial parenchymamuch more abundant elsewhere (Fig. 6A, top; Fig. 6B).The wall thickness of the two cell types permits easydiscrimination between axial parenchyma and libri-form (non-septate) fibres in Siphonodon (see alsoFig. 1A).

In Catha edulis (Vahl) Forssk. (Fig. 6C, D), bands ofseptate fibres are present. These bands are five or sixcells wide (Fig. 6C). They could be overlooked duringcasual observation, but are characteristically present.These septate fibres can be identified readily in radialsections (Fig. 6D).

In Elaeodendron capense Eckl. & Zeyh. (Fig. 6E, F),bands of septate fibres are more subtle. The bands aretypically three cells wide (Fig. 6E). In radial sections,the septa can be readily seen (Fig. 6F, sf). Libriform(non-septate) fibres (Fig. 6F, nf) are wider thanseptate fibres and have thinner walls (sf).

The seeming interchangeability of axial and septatefibres (in a broad phylogenetic sense, but not within aparticular wood sample) is a curious evolutionaryphenomenon that deserves further study. The presentarticle reveals considerable overlap in probable func-tions of the two cell types, and so Celastraceae mayrepresent a family in which the function of the twocell types is essentially identical.

Fibre dimorphism as a mode of axialparenchyma absenceFibre dimorphism was examined in detail in a recentstudy (Carlquist, 2014). One genus worth mentioningin this regard is Acer (Aceraceae, now referable toSapindaceae). Metcalfe & Chalk (1950) noted that, inAcer, ‘Holden (1912) has pointed out that the fibreshave noticeably thicker walls in the neighbourhood ofthe vessels . . .. . . Heimsch (1942) states that bandsor areas of starch-storing fibres are characteristic ofAcer, but points out that they may be renderedobscure by common section-cutting techniques.’ Thedistinction between narrower thick-walled fibres andwider thin-walled fibres can be seen readily in trans-verse sections of Acer wood (Fig. 7A). The relationshipclaimed by Holden (1912) between thick-walled fibresand vessel distribution does not seem rigid. Acersaccharum also has terminal bands, one cell thick, ofterminal (marginal) parenchyma (Fig. 7B). Thus, Acerhas the capability of producing axial parenchyma, butdoes so to a minimal extent. The wide thinner walledfibres, although non-septate, should be categorized asliving fibres (Vasquez-Cooz & Meyer, 2008).

A myrtalean genus, Sonneratia L.f. (Lythraceae s.l.or Sonneratiaceae), has septate fibres (Fig. 7D). Theseseptate fibres are wider and are located closer tovessels or bands of vessels, whereas fibres more distalto the vessels are narrower (Fig. 7C, D). The fibrescloser to vessels are reported to be thinner walled andto be less elongate with blunt ends, as compared withthe narrower fibres (Metcalfe & Chalk, 1950). Axialparenchyma is absent in Sonneratia (Metcalfe &Chalk, 1950). One can categorize the septate fibres ofSonneratia as representative of fibre dimorphism.However, the fibres that are wider and moreparenchyma-like are adjacent to vessels in Sonnera-tia, but distal to them in Acer (Fig. 7A). This under-lines the fact that fibre dimorphism is not a simplephenomenon, but a series of expressions (Carlquist,2014).

RAYLESSNESS: PARENCHYMA ABSENCE, PRESENCE

OR INCIPIENCE

Rayless woods are relatively few in number (Carlquist,1988), and few wood anatomists are familiar with anyexamples, although Meylan & Butterfield (1978)offered good illustrations of the wood of Hebe salicifolia(G.Forst.) Pennell (= Veronica salicifolia G.Forst.;molecular data support the merging of Hebe withVeronica in Plantaginaceae]. Rayless woods are rarelyfound in trees or large shrubs, and Hebe may containthe woodiest species in which rayless woods have beenreported.

Axial parenchyma cells as well as rays are absentin Hebe, so that the group offers a convenient startingpoint with relation to parenchyma absence. Theabsence of both rays and axial parenchyma is under-standable, because axial parenchyma and ray paren-chyma systems are physically and presumablyphysiologically interlinked (Kedrov, 2012).

How can a rayless wood form a cylinder of indefi-nite thickness and still be functional if axial paren-chyma and ray cells are essential to the functioning ofa wood? One possibility is that rayless woods do not,in fact, consist wholly of dead cells. Jacobinia carnea(Lindl.) G.Nicholson (Acanthaceae; Fig. 7E, F) is defi-nitely a rayless wood, as seen in a tangential section(Fig. 7E), but the fibres, when carefully examined,prove to be septate. Jacobinia has radial groupings ofvessels; in these groupings, one can see that axialparenchyma is present adjacent to vessels (Fig. 7F),as it is in woods of other Acanthaceae (Carlquist &Zona, 1988). Thus, the wood of Jacobinia can be saidto exist wholly of living cells, except for vessel ele-ments. Radial conduction at a slow rate may be pos-sible via the septate fibres.

Alseuosmia A.Cunn. (Alseuosmiaceae) is also aclearly rayless wood. Vessels are difficult to identify in



Figure 6. Axial parenchyma in woods of Celastraceae. A, B, Siphonodon australis Benth. (Forestry Commission of NewSouth Wales. A, Transverse section. Axial parenchyma diffuse but in zonal bands (white cells). B, Radial section showingstrands of cells comprising the axial parenchyma (ray near centre). C, D, Catha edulis (Forssk.) Vahl, cultivated in SantaBarbara, 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 septatefibres. 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 axialparenchyma 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 raylesscondition. F, Radial section; axial parenchyma among vessels in area denoted by bracket. lf, libriform fibre; mps, marginalparenchyma strand; nf, narrow fibres; np, patch of narrow fibres; nsf, narrow septate fibres; r, ray; v, vessel; wf, widerfibres; wsf, wider septate fibres.



transverse sections (Fig. 8A), and even in tangentialsections (Fig. 8B), because their diameter is so similarto the diameters of the fibrous cells (imperforatetracheary elements). Liquid-preserved material showsthat, in tangential section, the fibres have nucleate andprominent simple pits, like those of parenchyma cells(Fig. 8C). The fibres are all septate, as noted byButterfield & Meylan (1976) and Dickison (1986).Although septa are inconspicuous, starch grains canoften be seen adjacent to the septa (Fig. 8D). There areoccasional strands of axial parenchyma in the wood ofAlseuosmia (Fig. 8D, left). In the specimen studied, theaxial parenchyma strands are so sparse that they areprobably not of much functional value. However, therayless wood of Alseuosmia, like that of Jacobinia,consists entirely of living cells, except for the vesselelements.

Wood of Plantago maderensis Decne. (Fig. 8E, F) israyless, like that of other insular species of Plantago L.(Carlquist, 1970). Both P. maderensis and the Canar-ian P. arborescens Poir. are much-branched miniatureshrubs that accumulate a wood cylinder of < 1 cm indiameter. Larger stems in both species develop rays.Axial parenchyma is formed at the same time as raysare formed (Fig. 8E, F), although rays are more readilyidentified. Thus, the wood of P. maderensis resemblesthat of Artemisia L., Cyrtandra J.R.Forst. & G.Forst.,Geranium L. and Pelargonium L’Hér. ex Aiton: itbegins rayless, but rays are formed relatively soonthereafter. The amount of wood that lacks parenchymacells is therefore finite. One must concede that weknow relatively little about the longevity of nuclei inlibriform fibres, because liquid-preserved woods are sorarely studied. Families such as Solanaceae should bestudied in this regard. Most of the woods of Lobe-lioideae in an earlier study (Carlquist, 1969) weredried species and were not observed to have nuclei, butthe preparations made from liquid-preserved collec-tions were indeed septate and nucleate.

The emerging picture of rayless woods tends to showaxially elongate cells to a far greater extent thanradially elongate cells. Cells are, as a rule, elongate inthe direction of conduction, and more strongly elon-gate cells (vessel elements; procumbent cells ofmultiseriate rays) tend to be markedly elongate. Juve-nilistic woods show protracted production of verticallyelongate cells (Carlquist, 1962, 1988), and progressioninto adult patterns features horizontal subdivision ofboth fusiform initials and ray initials. Septate fibres inrayless woods probably accomplish relatively littleradial conduction, or accomplish it slowly. This is nota limitation if the woody cylinder is small in diameter.

Axial parenchyma in vesselless angiosperm woodsIn Winteraceae, axial parenchyma may be scanty anddiffuse, but is most commonly in tangential bands. In

Exospermum Tiegh., the tangential bands probablyinterconnect uniseriate rays, which are only one ortwo tracheids apart tangentially (Fig. 9A, B). Radialsubdivisions of axial parenchyma cells occur occasion-ally (Fig. 9C). This latter phenomenon is uncommonand may relate to the production of wider axial paren-chyma cells. Tangential bands of axial parenchymaare clearly evident in Belliolum haplopus (B.L.Burtt)A.C.Sm. (Fig. 9E), in which tangential bands extendacross several rays and are tangentially two cells inradial thickness.

Pseudowintera Dandy has massive multiseriaterays and numerous uniseriate rays (Fig. 9E). ‘Bridges’of axial parenchyma interconnect uniseriate rays atintervals (Fig. 9F). These tangential bands occurbetween latewood and earlywood; the wood of Pseu-dowintera has growth rings corresponding to the tem-perate Southern Hemisphere localities in which itoccurs.

Tetracentron Oliv. and Trochodendron Siebold &Zucc. (Trochodendraceae) are vesselless, but grow inmore markedly seasonal habitats than most Winter-aceae. Axial parenchyma is diffuse or grouped intoshort tangential bands, and is characteristically inlatewood (Metcalfe & Chalk, 1950). This suggests that,in Trochodendraceae, latewood may feature greatervulnerability to embolism formation, which is coun-tered by the action of axial parenchyma (see interpre-tations below), whereas strong negative pressureis less likely to develop in earlywood. This wouldaccord with the interpretations of Braun (1984) andZwieniecki & Holbrook (2009) in vessel-bearingangiosperms.

RAY–AXIAL PAPRENCHYMA CONTACTS

Contacts between rays and axial parenchyma char-acteristically occur in woody angiosperms and gym-nosperms (Kedrov, 2012). If osmotic water shifting isa significant factor in conduction, these numerouscontacts between rays and axial parenchyma arepotentially significant in vessel-bearing woods inwhich tracheids, a conductive cell type, are presentrather than fibre-tracheids or libriform fibres, whichare not conductive (Carlquist 1984; Carlquist, 2001;Sano et al., 2011). Conductive capability (freedomfrom embolisms) of tracheids can potentially bemaintained by axial parenchyma activity (Zwieniecki& Holbrook, 2009; see Fig. 13 below) in vessel-bearing woods, and union of rays into this network isvery probably a feature pertinent to this function.Thus, one should expect diffuse, diffuse-in aggregateand apotracheal banded patterns to be more commonin vessel-bearing woods with tracheids, and this istrue as a generalization (original observations basedon 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. Vesselelements 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 pairof axial parenchyma cells is to the left of the four septate fibres; granular contents are starch. E, F, Plantago maderensisDecne., 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.



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. Axialparenchyma cells identifiable by being narrower than tracheids. B, Tangential section. Uniseriate rays with upright cellsare 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 plusinconspicuous uniseriate rays. F, Portion of a tangential band of axial parenchyma. ap, axial parenchyma; apb, axialparenchyma band; mr, multiseriate ray; r, ray; ur, uniseriate ray; ur+t, uniseriate rays plus tracheids.

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angiosperms). In woods with fibre-tracheids or libri-form fibres, axial parenchyma is often limited to afew strands in contact with the vessels, as illustratedhere for Kogelbergia (Fig. 4E). In such a wood, thevessels are the only cells actively conducting water,and thus intimate contact between axial parenchymaand vessels is understandable if osmotic water shift-ing is a significant mechanism. Contacts betweenaxial parenchyma and rays are present in bothvessel-bearing woods with tracheids and vessel-bearing woods with fibre-tracheids and libriformfibres (Kedrov, 2012).

Ray density and interconnections withaxial parenchymaIn addition to a tendency towards apotracheal paren-chyma in vessel-bearing woods with tracheids, thereis a correlation with the number of rays per squaremillimetre (S. Carlquist, unpubl. data). The greaterthe number of strands of axial parenchyma of thetransverse section and the greater the density ofrays, the more likely that living cells contact trac-heids and thus potentially play a significant role intheir conduction, as well as that of vessels. Diffuseaxial parenchyma (or some minor variation) charac-terizes most vessel-bearing woods with tracheids(‘fibres with bordered pits’ of Metcalfe & Chalk,1950: xlv).

In Figure 10, all of the species have high raydensity. As a baseline, we can use the measurementsof Metcalfe & Chalk (1950) for the number of rays permillimetre. This represents the number of rays inter-secting an (imaginary) transverse line across a tan-gential section. This measurement has received littlecomment by wood anatomists, perhaps because itssignificance may be more physiological than taxo-nomic, and taxonomic differences have been the focusof most recent wood anatomical studies.

Metcalfe & Chalk (1950: xxvi) graphed the numberof rays per millimetre for angiosperm woods as awhole. Their graph shows a peak at about eight raysper millimetre. With respect to the families shown inFigure 10, Metcalfe & Chalk (1950) report 9–17 raysper millimetre in Theaceae (Fig. 10A–C), 13 raysper millimetre in Cercidiphyllum Siebold & Zucc.(Fig. 10D) and 10–27 (mostly 16–20) rays per milli-metre in Epacridaceae (= Ericaceae p.p.) (Fig. 10E, F).These all exceed the nine rays per millimetre cited asa median condition.

The contacts between axial parenchyma and rayscorrelate with a greater number of rays per millimetre,more frequent in the species selected for illustration(Fig. 10A, C, arrows). One can estimate the frequencyof contacts from the width of fascicular strips as seenin a transverse section (axial xylem portion separatedby rays on either side). Thus, Cercidiphyllum

(Fig. 10D) has fascicular strips one to four (mostly two)cells wide, as do the epacrids (Fig. 10F).

If vessel elements and tracheids in a particular woodare notably long (axially), it is more likely that theywill be in contact with the living cells of a wood. Thus,the tangential section of Figure 10B shows severalvessels longer than the portions included in the pho-tograph. The diffuse distribution of axial parenchymaalso correlates with scalariform perforation plates andgreater vessel element length (Metcalfe & Chalk, 1950:xlv).

A greater number of interconnections betweenrays and axial parenchyma is thus correlated withcharacter states commonly considered to be plesio-morphic in angiosperm woods. It should be notedthat the woods of Figure 10 all have scalariform per-foration plates, a feature often cited as plesiomor-phic in angiosperms.

The abundance of upright cells in rays, the pres-ence of uniseriate rays exclusively and the greateraxial height of uniseriate rays all characterize the raytype termed ‘Paedomorphic Type III’ (Fig. 10F), anextension of the ray types of Kribs (1935) necessary toreflect various degrees of juvenilism in various woods(Carlquist, 1988). Uniseriate rays are not exclusivelypresent in Cleyera Thunb., but are more commonthan multiseriate rays (Fig. 10B). The abundance ofupright cells in these rays increases the chance ofinterconnections between axial parenchyma and rays.

Kedrov (2012) illustrated contacts between raysand axial parenchyma in the outer one-third growthring of Alnus incana (L.) Moench. His illustrationshowed that each ray has three or more contacts withaxial parenchyma strands. No ray in this specieslacks ray–axial parenchyma contacts, and theminimum number of ray–axial parenchyma contactsper ray is two. Axial parenchyma in Alnus Mill. isdiffuse and terminal, and so the universality of thesecontacts is more noteworthy than it would be in aspecies with, for example, wide apotracheal bandedparenchyma. Rays are uniseriate or biseriate in Alnus(Metcalfe & Chalk, 1950), a fact that would make themultiplicity of ray–axial parenchyma contacts sur-prising. However, the number of rays per millimetreis 7–15 in Betulaceae, a ray density that would favournumerous ray–axial parenchyma contacts. A three-dimensional system of ray–axial parenchyma contactsis essential to the operation of an osmotic watershifting mechanism.

RADIAL CONTACTS

Braun (1970, 1984) called attention repeatedly to acidphosphatase as evidence of osmotic water shiftingin woods. This is conspicuous in paratracheal axialparenchyma sheaths, as his illustrations show. The



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 numberof 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, axialparenchyma; r, ray.

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presence of starch in axial parenchyma is also anindirect indication of osmotic water shifting. One cancite starch presence as ‘starch storage’, but evidenceof starch hydrolysis, such as prior to leafing out inAcer (Sauter, Iten & Zimmermann, 1973), is evidenceof osmotic water shifting. Rays and axial parenchymain angiosperms do not account for the radial conduc-tion of water (sap) in wood according to Kedrov(2012), but there is a radial flow of photosynthates inrays (Braun, 1970). Radial conduction of water bymeans of tracheids can occur because of pits on over-lapping radial walls of tracheids (Kedrov, 2012). Thatthere is a flow of photosynthate-laden fluid radiallythrough ray cells, especially procumbent ray cells, isevidenced by the occurrence of bordered pits on tan-gential walls of ray cells (Carlquist, 2007). Radial sapflow can occur in tracheids in the case of Pinaceae,which have ray tracheids (Greguss, 1955), and Tetra-centron sinense Oliv. (Thompson & Bailey, 1916).

AXIAL PARENCHYMA IN GYMNOSPERM WOODS

GnetalesGnetales have essentially all of the wood features ofangiosperms (Carlquist, 1996, 2012b), although theirwood is clearly derived from a conifer-like type. Thesimilarities to angiosperm woods are parallelisms(‘convergences’ of some authors).

The living cells of the genera of Gnetales can becharacterized as follows (data from Carlquist, 1996):

Ephedra L.: nucleated (but non-septate) fibre-tracheids with vestigially bordered pits (Fig. 11A, B).Axial parenchyma occurs in several species ofEphedra (Greguss, 1955; Carlquist, 1996), but isabsent from most species.

Gnetum L.: axial parenchyma with secondary wallsplus septate fibres (Fig. 11C, D).

Welwitschia Hook.f.: thin-walled axial parenchyma.The occurrence of multiseriate rays in secondary

xylem of Ephedra and Gnetum is familiar. Ray cells inthese genera have secondary walls, often with bor-dered pits (Carlquist, 2007, 2012b). The presence ofrays and axial parenchyma in Welwitschia will be lessfamiliar to most workers. Welwitschia has secondaryxylem with rays (Fig. 11E, r) and axial xylem com-posed of tracheids plus vessels (Fig. 11E, t+v). Axialparenchyma is intercalated into the axial xylem atvarious points (Fig. 11E, F, ap). Secondary phloem isalso present (Fig. 11E, spf). Secondary xylem andsecondary phloem are produced by vascular cambia(Fig. 11E, c). Welwitschia has successive cambia, andso increments of secondary xylem plus secondaryphloem are produced numerous times rather thanjust once. This does not in any way vitiate the ideathat Welwitschia has secondary xylem and that thissecondary xylem is comparable with that of Ephedraand Gnetum.

The non-septate fibre-tracheids of Ephedra arenucleate and can be compared, in abundance anddistribution, with diffuse axial parenchyma of angio-sperms, although the latter cells are in strandsrather than present as individual cells as inEphedra. As noted, several Ephedra spp. have axialparenchyma with secondary walls as well as non-septate fibre-tracheids.

The thin-walled nature of axial parenchyma cellsand rays in Welwitschia, in contrast with the second-ary walled nature of such cells in Ephedra andGnetum, probably relates to mechanical strength con-siderations. The massive strands of secondary phloemfibres provide potential mechanical strength, and mayserve as reservoirs for fluctuating water content. Thethin-walled cells in the secondary xylem and conjunc-tive tissue of Welwitschia may relate to expansion andcontraction of the Welwitschia axis with shifts inmoisture availability.

Thus, all three genera of Gnetales have axialparenchyma, except for some Ephedra spp. The dis-tribution of living non-septate fibre-tracheids inEphedra is analogous to that of axial parenchyma,and thus the non-septate fibre-tracheids of Ephedraare a distinctive feature, but probably comparablewith axial parenchyma in function.

ConifersConifers (excluding Gnetales) have axial parenchymastrands (Fig. 12A, B). Conifers rarely lack axialparenchyma; absence has been reported with cer-tainty only in Taxaceae (Greguss, 1955). In transec-tion, axial parenchyma may simulate tracheids inshape and wall thickness, but, in longitudinal sec-tions, the transverse walls of parenchyma (Fig. 12B)are readily evident. Resin deposits sometimes occur inaxial parenchyma of conifers (Fig. 12A), but tracheidscan sometimes contain resin deposits also. Kedrov(2012) demonstrated that axial parenchyma and raysare interconnected, forming a continuous network.This is reminiscent of the latewood axial parenchymain Tetracentron and Pseudowintera (Fig. 9). Latewoodaxial parenchyma may relate to deterrence (or evenremoval) of embolisms in the tracheids.

CycadsWoods of cycads as a whole have been described byGreguss (1968). Secondary xylem drawings of Cycasrevoluta Thunb. by Greguss (1955) show the expectedpresence of rays and axial parenchyma. The drawingsby Greguss (1955) show no cells intermediate betweenaxial and ray parenchyma. Axial xylem in cycads iscomposed mostly of tracheids, with thin-walled axialparenchyma interpolated in an irregular fashion(Fig. 12C).



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



GinkgoThe secondary xylem of Ginkgo short shoots(Fig. 12D) is remarkably similar to that of cycadswith respect to the irregular interpolation of axialparenchyma into groupings of tracheids. In wood ofthe long shoots, however, axial parenchyma strandsare comparatively infrequent and have secondarywalls (Fig. 12E, F). Axial parenchyma in the wood oflong shoots contains druses. These circumstancessuggest differential functions for axial parenchyma inshort shoots versus long shoots of Ginkgo. In the woodof long shoots, there may be differentiation intogroupings of tracheids with greater conductive capa-bilities and those with thicker walls and narrowerlumina. These differences, although minor, werefigured by Kedrov (2012) and hinted at in the illus-trations of Greguss (1955). Dimorphism in tracheidsmight be expected to be related to axial parenchymadistribution, but this has not been demonstrated inGinkgo wood, perhaps because axial parenchyma istoo sparse to reveal differential distributions.

AXIAL PARENCHYMA STRUCTURE RELATED TO

XYLEM PHYSIOLOGY

Axial parenchyma presenceThe present article is not and cannot serve as a reviewof physiological work on the function of axial paren-chyma in conduction. The resolution of some questionswill remain for the future. However, a brief discussionof wood physiological work can show that the commonassociations between axial parenchyma and vessels ortracheids have been repeatedly implicated in the con-ductive process. For a broader overview, the reviewby Clearwater & Goldstein (2005) can be consulted.Can axial parenchyma account for the reversal ofembolisms, or conceivably even the prevention ofembolisms, in associated tracheary elements? Thesefunctions have repeatedly been claimed to have experi-mental support (Braun, 1970, 1984; Salleo & Lo Gullo,1989, 1993; Edwards et al., 1994; Salleo et al., 1996;Trifilo et al., 2004; Salleo, Trifilo & Lo Gullo, 2006;Holbrook & Zwieniecki, 1999; Holbrook, Zwieniecki& Melcher, 2002; Zwieniecki & Holbrook, 2009;Brodersen & McElrone, 2013). Phloem may also beinvolved (Trifilo et al., 2004; Salleo et al., 2006), as maybordered pit structures of tracheary elements(Zwieniecki & Holbrook, 2000). According toZwieniecki & Holbrook (2009): ‘Sugar concentrationsin xylem have been little studied, but their involve-ment in [tracheary element] refilling is consistent withobserved dynamics of starch content in stems thatundergo embolism-refilling cycles (Bucci et al., 2003;Trifilo et al., 2004; Salleo et al., 2006).’

The process of ‘osmotic water shifting’ was envi-sioned by Braun (1984) as a process complementary

to the action of tension–cohesion governed conduc-tion. Braun (1984) stated: ‘The activity of the acces-sory tissues produces a high osmotic pressure in thetrees. This brings about an uptake of water, often apositive pressure (system pressure) and an osmoticwater shifting within the tree.’ This particular state-ment was intended to be primarily applicable towinter-deciduous trees, but Braun also extended hisinterpretation to other kinds of woody plants, e.g.tropical deciduous trees. Braun’s ideas did not includeother examples, and did not examine in detail howthis process might work. Ideas along these lines wereoffered by Canny (1995, 1998); they have been provento be problematic and have not been validated bycertain experimental tests (Comstock, 1999).

Zwieniecki & Holbrook (2009) presented a ratherdifferent detailed scheme in which axial parenchymaand (low-molecular-weight) sugars in axial paren-chyma are the driving force. These concepts have beenreproduced here as Figure 13. However, the pathwaysproposed may require modification as we learn moreabout how parenchyma cells function in the conductiveprocess. Secchi & Zwieniecki (2012) found that theconcentration of osmolytes might be too low to accountfor the reduction and elimination of embolisms. Theseauthors emphasized that the effect of sugars in influ-encing water movements within the xylem may not beextensive, affecting long portions of a vessel, but maybe confined to localized sites. Possibly, osmotic differ-entials may form locally or over short periods of timeand even occur at membrane sites: such events aredifficult to study. The studies of Borchert & Pockman(2005) and Plavcova & Hacke (2011) are relevant inthis regard. Although we often speak in terms of‘starch storage’ (Borchert & Pockman, 2005), we havefew data on events of starch mobilization in axialparenchyma and the pathways taken by sugars follow-ing mobilization. The work on Adansonia L. (Chapotin,Razanameharizaka & Holbrook, 2006a, b, c) illustratesthat the functions of starch storage should be studied,because they may be multiple in a given plant, andstarch storage may function differently in a range ofdifferent given species.

Axial parenchyma, so common in woods of angio-sperms, Gnetales, cycads and Ginkgo (but less commonin Coniferales), parallels vessels and tracheids spatiallyin wood and is implicated by its distribution as thesource of osmotic water shifting in these tracheary ele-ments (Braun, 1984; Holbrook & Zwieniecki, 1999;Zwieniecki & Holbrook, 2009). In the present article, thecharacteristics of axial parenchyma are used, in connec-tion with the absence or scarcity of axial parenchyma, inorder to explore the multiplicity of histological patternsand their probable functional significance.

Axial parenchyma is present in by far the majority ofangiosperm woods. The data of Kribs (1937) indicate

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that the percentage of angiosperms with axial paren-chyma absent is about 5%, and that axial parenchymais almost universal in woods that have vessel featuresconsidered as apomorphic. Exact percentages cannot beoffered because the sampling of Kribs (1937) may nothave been random (tropical species may be under-represented); the species he studied are not listed. Thecommonness of axial parenchyma in angiosperm woodssuggests an important role for this tissue, and theobserved presence of starch in axial parenchyma ofliquid-preserved material is a prime indicator that car-bohydrate activity must be involved. Osmotic watershifting is made possible by the hydrolysis of starch intosugars (Sauter et al., 1973; Braun, 1984). Mauseth &

Plemons-Rodriguez (1997) mention the idea of a ‘waterjacket’ of parenchyma cells completely ensheathing avessel, but concede that most angiosperms do not havethis. The reason seems clear: if parenchyma cells affectwater conduction, only a single parenchyma cell (cellstrand, as seen longitudinally) per vessel, or severalat most, could suffice. This condition is commonly real-ized in angiosperms, because most have axial paren-chyma in contact with vessels. At an ultrastructurallevel, the nature of vessel–parenchyma pits (Plavcova &Hacke, 2011) may represent a promising avenue forinvestigation.

Are some angiosperm woods limited in their abilityto react to function in conditions with a greater range

Figure 13. Embolism refilling scenario. (a) Living cells in contact with vessels release a small but steady amount of solublecarbohydrate into the xylem. (b) Starch stored in xylem parenchyma serves as a sugar capacitor. (c) These solutes arenormally swept away by the transpiration stream, keeping the concentration at very low levels, but (d) accumulate in avessel that has cavitated. (e) Sugar accumulation and the associated increase in apoplastic solute concentration triggerssignalling pathways (f) for refilling that regulate sugar and (g) water membrane transport, as well as (h) sugar metabolicactivity. (i) The accumulation of solutes results in water movement from xylem parenchyma cells by osmosis, formingdroplets with high osmotic activity on internal vessel walls. (j) The partially non-wettable walls of xylem conduits preventthese droplets from being removed by suction from still-functioning vessels. (k) Condensation of water vapour provides asecond pathway by which water refills cavitated conduits, allowing adjacent conduits to provide water for refilling. (l) As thehigh osmotic droplets grow to fill the vessel, the embolus is removed by forcing gas into solution and by pushing gas throughsmall pores through the vessel walls to intercellular spaces. (m) The flared opening of the bordered pit chamber acts as acheck 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; ahydrophobic layer within pit membranes might provide the needed simultaneity among multiple bordered pits. (FromZwieniecki & Holbrook, 2009; reproduced by permission of the authors and Elsevier Publishing).



of temperatures and moisture availabilities? Doesthis limit particular clades from advancing intoniches with more marked fluctuation in temperatureand moisture availability? One still sees this ideaexplicitly and implicitly expressed as a way ofexplaining the geographical distribution of wood fea-tures. This idea has also been basic to explaining thepersistence of plesiomorphic features (e.g. scalariformperforation plates) in some woods. Certainly, someclades have exploited a variety of niches to a greaterextent than others, and some have wide diversity inwood anatomy, whereas others are much more stereo-typed. However, what if we take the position that allwoods are functionally successful in the localities inwhich they exist? We must then consider plesiomor-phic structures as entirely functional, rather thanlimiting. By considering structures as functionalrather than to various extents vestigial and limiting,we can explain their existence at the present time.Bailey’s ideas on the evolution of xylem features didnot take into account function, and therefore arelacking in evolutionary respects (Olson, 2012).

Network considerationsBrodersen & McElrone (2013) stated that: ‘xylemnetworks should no longer be considered an assem-blage of dead cells, empty conduits, but instead ametabolically active tissue finely tuned to respond toever changing environmental cues.’ This statement isacceptable, but the nature of the functional networkis not specified in anatomical terms. Three-dimensional reconstructions of vessel anastomosesand interconnections between the ray and axialparenchyma systems (e.g. Kedrov, 2012) supply theneeded histological information. In both conifers andangiosperms, rays are interconnected with axialparenchyma, and no ray or axial parenchyma strandis isolated from this network (Kedrov, 2012). Animplicit feature of the living cell network in wood isits three-dimensionality, so that newer, active woodincrements participate in the network as older partsof the secondary xylem are de-activated. Thus, thereis a time dimension and the network of living cellsremains valid and functional, even though earlierportions are no longer functional and newer portionsof the network are brought into existence constantly,initiated by the cambium.

Cohesion–tension plus root pressureIn fact, a third mechanism, root pressure, as demon-strated in monocots (Nobel, 1988; Stiller, Sperry &Lafitte, 2005), is operative. This may be more wide-spread, and is to be expected in plants with adventi-tious roots (which occur in all monocots). However, inwhich plants are these three processes operative andto what degree? Experimental work must select indi-

vidual species, with the hope of finding universallyapplicable principles, but the path to universality isnot always obvious because of vascular plant diver-sity. Experimental work is also often confined to oneor several moments in time. Braun (1970, 1984) andSauter et al. (1973) reported periodicity in starchhydrolysis activity, with periodic changes in tempera-ture, as a triggering mechanism. Presumably, aftershoots leaf out, cohesion–tension replaces osmoticwater shifting as the predominant water ascentmechanism.

PlacementThe nature of the placement and abundance of axialparenchyma with respect to vessels is a subject thatrequires analysis from several disciplines. Vessellessangiosperms and gymnosperms have been includedin the present study as a way of asking questionsabout the location of axial parenchyma when vesselsare not present in a wood. Conifers, Tetracentron andsome Winteraceae tend to have more axial paren-chyma in latewood than in earlywood. One possiblehypothesis is the osmotic water shifting mechanism,which would be of more value in latewood, in whichtensions fluctuate more (with attendant embolismformation possibilities) than they do in earlywood.Latewood in conifers is more vulnerable to embolismformation than is earlywood (Domec & Gartner,2002) and, in this context, the figures of Kedrov(2012), showing that contacts between rays and axialparenchyma are frequent in Fitzroya Hook.f. exLindl., are noteworthy and similar in this respect tohis figure of Alnus wood.

By far the majority of angiosperm woods have axialparenchyma in contact with vessels (Kribs, 1937;Zhang, Fujiota & Takabe, 2003). Wider vessels aremore vulnerable to embolism formation than are late-wood tracheids (Lo Gullo & Salleo, 1993), but bothkinds of vessel are more vulnerable than tracheids;vasicentric tracheids also occur in the woods ofQuercus L. studied by Lo Gullo & Salleo, (1993).

If the axial parenchyma and ray systems form an‘accessory hydrosystem’ (Braun, 1984), the number ofcontacts may be important in its function. Thenumber of contacts with a vessel is increased whenthere are longer vessel elements and taller strands ofaxial parenchyma, both of which are the result ofhaving longer fusiform cambial initials, characteristicof angiosperm woods with more numerous plesiomor-phic features. Greater ray height, greater number ofrays per millimetre and a predominance of uprightray cells increase the potential number of contactsbetween the axial and radial parenchyma systems.We need to know whether woods with more numerouscontacts between the two systems also have greater‘conductive safety’ (resistance to embolism formation).

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MULTIPLE FUNCTIONS

Do septate fibres substitute for axial parenchyma?The seeming interchangeability of bands of septatefibres and similarly positioned apotracheal axialparenchyma bands in Celastraceae (Fig. 6) suggestsfunctional equivalence between the two cell types. Inthis case, not merely position, but also quantity, isinvolved. However, septate fibres usually do not showsuch through-going equivalence; they differ from axialparenchyma in either quantity or position. Septatefibres also differ from axial parenchyma in wall char-acteristics: they are usually thicker walled, suggest-ing that a mechanical function is being served.

Mechanical strength plus carbohydrate storageFunctional multiplicity is evident in the fibre dimor-phism of Acer wood, in which narrower, thicker walledfibres are formed proximal to the vessels, but wider,thinner walled fibres are formed distal to the vessels.The fibre dimorphism suggests that the wider fibresserve for both carbohydrate storage (as observed bySauter et al., 1973) and mechanical function. One cancontrast this with the marked difference in wall thick-ness between axial parenchyma cells and septatefibres in Siphonodon. In Halleria, the entire groundtissue of the secondary xylem consists of septatefibres that are rich in starch (as are ray cells), anotherinstance of carbohydrate storage. Both of these exam-ples suggest mechanical strength combined with car-bohydrate storage that can be used in osmotic watershifting. In addition to osmotic water shifting,massive carbohydrate storage of this sort may beinvolved in flushing of flowers and inflorescences (fol-lowed by a wave of fruit production), processes thatrequire larger carbohydrate input than can beachieved by the amount of photosynthesis duringthese events, and which therefore can draw on starchreserves in parenchyma. Does this actually happen?Studies at present are few.

Pervasive parenchymaThe massive stems of Adansonia have been consideredas prime examples of water storage, but is this theprimary purpose of this parenchyma ground tissue ofthe secondary xylem in this species? The stems of arelated genus, Chorisia, were examined earlier in thepresent article. Chapotin et al., (2006a, b, c) found thatwater storage in Adansonia corresponded not so muchto seasonal changes in soil moisture availability, butrather to a mechanical consideration, cell strengthachieved by turgor. This phenomenon is not unknownand occurs in such succulents as Crassula argenteaThunb., in which, during the dry season, stems shrinkand bend, no longer upright as turgor pressure in thepervasive parenchyma of secondary xylem decreases.

The maintenance of turgor pressure does not explain,however, the large quantities of starch in secondaryxylem ray and axial parenchyma of Chorisia. Morethan a single function is probably being served, and thedata of Chapotin et al. (2006a, b, c) do not completelyexclude functions other than mechanical for the paren-chyma in Adansonia.

Finding function by defaultThe analysis of earlywood versus latewood in theconifer Pseudotsuga Carrière (Domec & Gartner, 2002)showed that earlywood accounts for most of the con-duction. These authors also showed that earlywood is,not surprisingly, vulnerable to embolism formation.Their data showed that, under most conditions, late-wood is equally vulnerable to embolism formation. Iflatewood in Pseudotsuga does not conduct to a majorextent and yet is vulnerable to embolism formation,what is its value in the stem? The methods used byDomec & Gartner (2002) did not involve the analysis ofmechanical properties, but the implied result of theirstudy seems to be that the value of latewood may bemostly mechanical, in the formation of cells in whichthe wall to lumen area is much greater than inearlywood tracheids. This suggests that, sometimes,we may find the most important function of a tissue byidentifying what it does not do. Ultimately, the causa-tion of latewood must be involved in such explanations:in the case of latewood, decreased levels of auxinexplain the formation of cells with a narrower celldiameter (Aloni, 1987, 2001).

Functional overlapThe presence of septate fibres as a ground tissue insecondary xylem may be associated with smalleramounts of axial parenchyma in some genera, such asUmbellularia or Fuchsia L. (Carlquist, 1988). Thecoexistence of the two cell types in a given woodseems to provide evidence of functional overlap,because the extinction of a cell type in wood is evi-dently achieved readily in evolutionary terms, as thelist of plants with these two cell types concurrentlysuggests. Raylessness also illustrates this principle.In the case of woods with axial parenchyma plusseptate fibres, such as Araliaceae, we may want totest the hypothesis that mechanical strength, carbo-hydrate storage and osmotic water shifting arerelated to the presence of both cell types (in additionto ray parenchyma). Are all functions served equallyactively? The lesson from Adansonia secondary xylemis that some functions may be served to some extentor during short seasonal periods, whereas others,such as the mechanical strength offered by turgor inaxial parenchyma in Adansonia, are importantthroughout the life of the plant.



DIVERSITY RATHER THAN ADHERENCE TO A PLAN

Rayless woods have the interesting characteristic, insuch genera as Geranium, Pelargonium and Plantago,of having secondary xylem that begins rayless butforms rays at a certain point, sometimes after 1 year,sometimes later. We should note that not all raylesswoods conform to the same basic pattern, and thatwhat is true in one genus probably is not true inanother. Nevertheless, rayless woods show that, forexample, radial conduction of water and photosyn-thates may be negligible or may occur via septatefibres at first, but then may become appreciable whenrays begin to be formed. Ray formation is not simul-taneous with axial parenchyma formation in somerayless woods: Jacobinia has axial parenchyma, butstems remain rayless. In Jacobinia, septate fibresmay account for a slow but steady radial flow. As ageneralization, one may say that rayless woods firstexhibit the formation of a maximum amount of fibri-form cells to achieve greater mechanical strength,and then diversify to more numerous cell types withmore numerous functions as diameter increases. Thewood of Hebe (Veronica) salicifolia features neitherray nor axial parenchyma in the stems that have beensampled thus far (Meylan & Butterfield, 1978), whichsuggests a strong emphasis on mechanical strength.However, how can wood of such a species functionover a period of years without axial and ray paren-chyma? Our knowledge of the physiology of raylesswoods is minimal. Rayless woods are ideal experimen-tal material because one can compare wood of a singlespecies with rays and earlier-formed wood of the samespecies without rays. Although we need to know muchmore about rayless woods, our present knowledgesuggests that they represent a diverse assemblagerather than conformity to a single structural mode.

The woods of Castilleja, Crepidiastrum and Stan-leya (Fig. 3) show various timings in the production offibrous wood versus parenchymatous wood. Theyillustrate that mechanical strength can be enhancedat various times in secondary xylem production.Mechanical strength in these examples is enhancedby the substitution of fibrous wood for parenchyma-tous wood to varied radial extents.

PROTECTIVE FUNCTIONS

Axial parenchyma may have crystals as contents (asmay septate fibres). Secondary products, such asresins, terpenoids, etc., may be accumulated in axialparenchyma cells, which thus take on functions suchas herbivore deterrence or resistance to fungi andbacteria (Deflorio et al., 2008). In this context, paren-chyma can offer the segmentation of wood, walling offthe spread of pathogens by the production of suberinand other compounds. These functions are difficult to

prove, but the presence of these compounds seems torepresent compelling evidence. If pathogen deterrencewere the sole purpose of the presence of axial paren-chyma, however, it would not be distributed as it is,primarily in relation to conductive cells (vessel ele-ments and tracheids). Tyloses represent mainly theproducts of axial parenchyma: ballooning of axialparenchyma cells into vessels that have becomeembolized or otherwise deactivated. The functionalsignificance of tyloses may be the blockage of non-functional woods against pathogens. Crystals andstarch are occasionally reported in tyloses, suggestingthat tyloses may have more than one function.

AXIAL PARENCHYMA SCARCITY: VESTIGIAL DESIGN OR

PARSIMONIOUS STRUCTURE?

Metcalfe & Chalk (1950) characterized axial paren-chyma as sparse to absent in Aceraceae (= Sapin-daceae), Argophyllaceae, Berberidaceae, Brassicaceae,Calycanthaceae, Cercidiphyllaceae, Cistaceae, Con-naraceae, Crossosomataceae, Ericaceae (includingEpacridaceae and Vacciniaceae), ‘Flacourtiaceae’,Grubbiaceae, Hydrangeaceae, Illiciaceae, Lardizabal-aceae, Monimiaceae (Atherospermacaeae), Myrotham-naceae, Nyssaceae (= Cornaceae), Paeoniaceae andPapaveraceae. There is probably more than one expla-nation of why axial parenchyma should be sparse inthese families. ‘Sparse’ does not equate to ‘scarce’ inthis regard: axial parenchyma is characteristicallypresent, but not abundant in these families.

In addition, one can cite families in which axialparenchyma is diffuse and relatively inconspicuous.There seems to be some association between diffuse orscarce axial parenchyma and the presence of trac-heids (‘fibres with fully bordered pits’ of Metcalfe &Chalk, 1950). These families may have wood in whichair embolisms in vessels or tracheids are an infre-quent occurrence, and in which, therefore, the osmoticwater shifting role of axial parenchyma is minimal.

Paedomorphic Type III rays: a functionalassociation with axial parenchyma scarcity?The occurrence of Ericaceae s.l. in the list above leadsto an interesting association: woods with Paedomor-phic Type III rays. A preliminary list of families withPaedomorphic Type III rays overlaps with the listabove quite appreciably. The list of families in whichone can find uniseriate rays only, composed of uprightcells, includes: Caryophyllaceae (some subshrubbygenera), Celastraceae (Empleuridium Sond. & Harv.ex Harv., Euonymus L.), Cistaceae, Elaeocarpaceae(the subfamily formerly recognized as Treman-draceae), Ericaceae (including Empetraceae, Epacri-daceae and Vacciniaceae), Grubbiaceae, Haloragaceae(Gonocarpus Thunb.), Myrothamnaceae, Rubiaceae

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(Galium L.), Setchellanthaceae, Thymeleaceae (Dirca)and Valerianaceae (Patrinia Juss.) In GymnocarposForssk. and Polycarpaea Lam. of Caryophyllaceae,there appears to be little difference between axialparenchyma and rays. This invites us to speculatewhether the species in which Paedomorphic Type IIIrays occur have the upright ray cells serving thefunction of axial parenchyma. There is no a priorireason to believe that upright ray cells cannot takeover these functions. Experimental work on conductionprocesses is needed on the Paedomorphic III generaand families. Nearly all of the Paedomorphic III fami-lies are small- to medium-sized shrubs, and thisgrowth form has been rarely studied experimentallywith respect to conduction.

INTERPRETIVE OPPORTUNITIES AND DIFFICULTIES

The relative abundance of particular cell types in awood is not accidental, and does not appear to be anevolutionary phenomenon without a functional expla-nation. The instance of parenchyma scarcity in par-ticular woods, like other aspects of axial parenchyma,challenges us to link particular histological featuresof woods with one or more functions. Sometimesexperimental work will prove an association betweena particular cell type, or a particular distributionand/or location of a particular cell type, and a par-ticular function. Experimental work is of less value ifit applies only to one species. The goal of physiologicalexperiments in seed plants is usually to find resultsthat are widely applicable. If we can develop form–function associations of wood cell types and confor-mations in particular plants with physiologicalprocesses, we should be able to predict, with reason-able certainty, the function of histological conditionsreferable to these conditions in a range of plants notincluded in a particular study. Both experimentalwork and observational studies gain in significance ifwe can bridge the gap between them.

ACKNOWLEDGEMENTS

The help of several individuals in the field of woodphysiology, particularly N. Michele Holbrook, JohnSperry, Maciej Zwieniecki and anonymous reviewers,is acknowledged, as is the editorial work of Michael F.Fay. The wood samples I have used for informationabout axial parenchyma distribution in woods arederived from portions given by the wood collection ofthe Forest Products Laboratory, Madison, WI, USAand the wood collection of the US National Museumof Natural History (Smithsonian Institution). Thecurators of those collections, who have been willing toshare material with me, are gratefully acknowledged.

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living cells in wood. 1. absence, scarcity and histology ...€¦ · work in wood physiology, and...

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