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INTERVASCULAR PIT STRUCTURE IN SELECTED SPECIES OF THYMELAEACEAE.

Roland R. Dute [1]

Michael E. Miller [1,2]

Robert R. Carollo [1]

(1.) Department of Biological Sciences,

(2.) AU Research Instrumentation Facility

ABSTRACT

Intervascular pit pairs in woods of Gnidia caffra, Dirca palustris, and two species of Pimelea were observed with both light and scanning electron microscopy. The resulting images were compared with pits from Daphne spp. of a previous study. Unlike Daphne, the pit membranes of the other genera lack tori: Pit apertures of Gnidia and Pimelea were slit-like, whereas those of Daphne and Dirca tended toward circular. Vestures were present in intervascular pit pairs Gnidia, Pimelea, and, to a lesser extent, in Dirca, but absent from the Daphne species investigated in this study. Hypotheses regarding the function of tori and vestures are discussed.

INTRODUCTION

Pit pairs located between water-conducting cells (tracheary elements) in wood provide a low-resistance pathway for water movement but at the same time must inhibit gas embolisms from passing cell to cell. There are two basic mechanisms to accomplish these functions. In many conifers and Ginkgo, the pit membrane separating the pits consists of microfibrils associated with large openings. In the center of this screen-like barrier is an impermeable circle of wall material, the torus (Thomas, 1969). The openings through the pit membrane serve for water movement. In the presence of embolisms, however, the pit membrane is deflected or aspirated such that the torus blocks the aperture into the neighboring cell thus impeding movement of bubbles (Zimmermann, 1983). In contrast, pit membranes in most dicotyledonous woods consist of microfibrils associated with very small (or no) visible openings and no torus. Since the pressure differential needed to force an air bubble through a screen increases with decreasing size o f the openings, the intact pit membrane effectively blocks movement of most embolisms (Zimmermann, 1983). There are, however, a very few species of dicotyledons whose pit membranes have both the dicot arrangement of microfibrils as well as a torus. Among them are species of the genus Daphne (a shrub common to Eurasia), and it is this genus which has been the subject of intensive investigation in this laboratory.

The presence of tori in membranes of Daphne was first noted by ohtani and Ishida (1978). Dute et al. (1990) detailed torus development in this genus and hypothesized that such a structure prevented membrane rupture during aspiration. Both Ohtani (1983) and Dute et al. (1992) noted that not all species of Daphne possessed a torus, but in fact presence or absence of this feature was determined by systematics. Specifically, species of section Mezereum lacked a torus (Dute et al., 1996). This same study noted tori in wood of two of three subgenera of Wikstroemia, a sister genus to Daphne. At the same time, tori were absent from wood of Drapetes and Edgeworthia, genera within the same subfamily (Thymelaeoideae) as Daphne. Table 1 presents an abbreviated classification of the family Thymelaeaceae according to Engler (1964). Those genera within the subfamily Thymelaeoideae which have been investigated are indicated with asterisks.

Observations of these genera indicate that the torus-bearing pit membrane and the apertures work as a functional unit. When a torus is present, the aperture is small in diameter (smaller than the torus) and is circular to slightly elliptical in outline. In some species lacking a torus, pit apertures may also be circular, whereas in other species, the apertures are slit-like (Dute et al., 1996). The association of circular apertures with torus-bearing pit membranes has been noted by other authors (Beck et al., 1982; see also discussion in Morrow and Dute, 1998).

Vestures, wall protuberances associated with pits, are listed as a feature of the Thymelaeaceae (Bailey, 1933; Jansen et al., 1998; Metcalfe & Chalk, 1950). These structures have been hypothesized to reduce membrane rupture during aspiration (Zweypfenning, 1978) or to prevent formation of (gas) embolisms or aid in their resorption (Carlquist, 1988). Thus a knowledge of vesture structure and systematic occurrence as well as an understanding of the torus could be important to comprehending safety features in wood.

This manuscript represents a continuation of work on intervascular pits of the Thymelaeaceae. Specifically, it provides a characterization of pits in Gnidia caffra (Meisn.) Gilg, Dirca palustris L., and two species of Pimelea with emphases on the presence or absence of a torus, the outline of the pit apertures, and presence or absence of vestures. Images of pits from Daphne gnidioides, D. collina, and D. retusa are included for comparative purposes.

MATERIALS AND METHODS

The species used in this study are listed in Table 2. All specimens represent air-dried herbarium samples and with one exception were obtained from the Auburn University Herbarium (AUA). Daphne gnidioides samples included in this study were used in a previous publication (Dute et al., 1992). Only Daphne gnidioides was re-investigated in detail although individual micrographs of other Daphne species are presented. Branch segments of 3-6 mm diameter were split longitudinally to expose either radial or tangential surfaces. Samples were then affixed to aluminum stubs with double stick carbon tape and sputter-coated with gold-palladium. Observations were made with a Zeiss Digital Scanning Microscope (DSM 940) at voltages of 5, 10, and 15 kV. Measurements of SEM material were made using the system included with the microscope. All measurements were determined by counts of 25 unless otherwise noted.

SEM observations were supplemented with light microscopy. Herbarium material was treated and embedded in Spurr's resin (Spurr, 1969) according to the procedure of Dute et al. (1990). Thin sections of 1.5--3 [micro]m were cut on an ultramicrotome and heat-fixed to glass slides. The sections were stained in one of three ways: 1) 0.5% toluidine blue 0 (TBO), 2) 2% aqueous [KMnO.sub.4], or 3) [KMnO.sub.4] followed by TBO. The latter staining procedure provided higher contrast than either of the other two methods. Apparently, [KMnO.sub.4], in its role of oxidizing agent, exposed more potential binding sites for the subsequently applied TBO molecules.

Once stained, specimens destined for light microscopy were covered by mounting medium and a coverslip. Photographs were taken using T-Max 100 film.

RESULTS

General Information

Fig. 1 is an overall, radial longitudinal view of a water-conducting cell or vessel member in the wood of Dirca palustris. The large opening at the top, known as a perforation, is actually located on the inclined end wall of the cell. A similar hole is located at the bottom of the cell, but is slanted in the opposite direction and is therefore not exposed to the observer. Vessel members are stacked end to end with their end walls overlapping and their perforations juxtaposed. This series of cells is referred to as a vessel. The top and bottom elements of the vessel have only a single lower and upper perforation, respectively. Thus a vessel acts as a closed system. In addition, a second type of water-conducting cell, the tracheid, can also be present. This cell type differs from vessel members by the absence of perforations, but in other respects (i.e. pitting) is similar. Daphne, Dirca, and Pimelea have tracheids as well as vessel members; Gnidia has only the latter. For convenience, the general term "trache ary element" (Esau, 1965) will be used when referring to both kinds of conducting elements unless a distinction is warranted.

Lateral walls of the tracheary elements are pitted (Fig. 1), and it is the pits between tracheary elements (the so-called bordered pit pairs, Fig. 2) which provide a pathway for lateral movement of water. Fig. 1 shows these pits in face view for D. palustris. A detailed view of a similar aspect is provided in Fig. 3 for Gnidia caffra. Pit pairs can be viewed at different levels. For, example, letter A in Fig. 3 indicates the outer surface of a pit border. The hole or aperture through that border opens into the lumen or cavity of the tracheary element (which, for the cell in question, is below the surface of this figure and thus not visible). Letter B represents a pit membrane overlying the border. Letter C identifies the inner or lumen surface of the other pit border of the pair (with its own aperture). Thus the pit membrane is inserted between two pit borders. Fig. 4 provides a cross-sectional view of a pit pair of Daphne collina (at right angles to Fig. 3). The letters indicate the same surfaces as in the p revious figure. In this instance the pit membrane is displaced (aspirated) to one side and covers the outer opening of an aperture. Membrane displacement is a typical occurrence in air-dried wood.

Pit Membrane Structure

Figs. 5, 6, 7 & 8 present pit membrane structure in Daphne species for comparative purposes. In the center of the pit membrane is a thickening known as a torus. This thickening is found on both sides of the pit membrane and can be seen in cross section even with the light microscope (Fig. 7). In face view the torus is circular with a diameter greater than that of the associated pit apertures (Table 3). Detailed views of such pit membranes indicate the torus to be an impermeable structure, whereas the remainder of the pit membrane (the margo), which surrounds the torus, is fibrillar (Figs. 6 & 8). Although present, fibrils are not always observed in air-dried pit membranes as wound material released by surrounding cells as they die impregnates the pit membranes and obscures the fibrils (Dute et al., 1992; Morrow & Dute, 1999; Schmitt & Liese, 1990).

Detailed views of intervascular pit membranes in D. palustris (Figs. 9 & 10), both species of Pimelea (Figs. 11, 12), and G. caffra (Fig. 13) show no evidence of a torus.

Pit Aperture Structure

Species of Gnidia and Pimelea used in this study have irregularities known as vestures along the rims of their pit apertures (Figs. 11 & 13). Daphne gnidiodes does not (Fig. 5), and for the most part, Dirca palustris does not, although sometimes very small amounts of vesturing (best described as obscure) can be observed (Fig. 14). Vesture morphology of the Pimelea spp. differs from that of G. caffra. In the former, the vestures appear as irregularities at the very edge of the aperture (Fig. 11), whereas in Gnidia the apertures are peglike and cover part of the outer (non-lumen) surface of the pit cavity as well as the aperture rim (Fig. 13). Interestingly, fiber pits of Dirca, Gnidia, and Pimelea species observed in this study (as well those of Daphne gnidioides all have well-developed vestures.

The ratio of the short axis to the long axis of intervascular pit apertures was used as a measure of aperture circularity. Table 3 presents results for all genera investigated in this study. From the data, it is evident that apertures of D. palustris and D. gnidioides more closely approach a circular shape than those apertures of P. prostata, P. arenaria, and G. caffra.

DISCUSSION

Torus--distribution and function

Torus distribution in the Thymelaeaceae is of some value to systematics. In a study of 22 spp. of Daphne, Dute el al. (1992) observed 19 spp. with tori. This structure was absent from three spp. of the section Mezereum. A later study of the sister genus Wiskstroemia (Dute et al., 1996) showed tori to be present in the subgenera Diplomorpha and Daphnimorpha, but absent from the subgenus Wikstroemia. The presence of tori in the Thymelaeaceae must be tightly circumscribed. Although Daphne and Wikstroemia are within the same tribe (Daphneae, Table 1), so are Edgeworthia and Dirca but neither of the latter two genera possess tori (Dute et al, 1996; the present study). The more distantly related genera, Drapetes, Gnidia, and Pimelea (different tribe, same subfamily) also have no tori.

Torus function in Daphne pit membranes is indicated by its structure. Tori are typically circular with a diameter greater than that of the aperture (i.e. the greatest diameter of the aperture). In a developmental study of pit membranes of Daphne odora and D. cneorum, the tori were of greater diameter than the pit apertures and completely occluded them during aspiration (Dute et al., 1990). The torus and aperture diameters of D. gnidioides from this study (2.8 [micro]m torus; 1.6 [micro]m aperture) are not out of line with measurements of D. cneorum (3.6; 1.8) and D. odora (3.6; 1.4) from the previous investigation. It is hypothesized that the torus in dicots decreases possibility of rupture of the pit membrane during aspiration (Dute et al., 1990). D. odora pit membranes, dried after torus removal, were ruptured at the site where the torus once overlay the pit aperture. Similar ruptures were observed in air-dried material of D. mezereum that never had a torus. While pit membrane damage could well have occurre d during processing for SEM or due to heat of the electron beam, the fact remains that aspirated pit membranes tear where they overlay the pit aperture, whereas-membranes with tori do not. The weakness of non-torus bearing membranes can be observed in Pimelea membranes (Fig. 11) of the present study.

It appears as if pit membranes with circular tori are associated with more or less circular apertures, but the converse need not be true. Beck et al. (1982), writing with regard to gymnosperm wood, observed that circular apertures associated with circular tori would be "more highly adaptive" than slit-like apertures and provide an effective seal. By contrast, a less specialized homogeneous membrane would probably be adaptive in pits with slit-like apertures. However, they then cite Wright (1928), who states, "the presence of a round pore does not necessarily entail the development of a torus.' It appears as if the same can be said for angiosperms. Clearly, in this study the circularity ratio is much less for pit apertures of Pimelea and Gnidia than for Daphne and Dirca. The former genera have slit-like apertures and have no tori. Daphne with a more circular aperture has a torus, but Dirca whose aperture is of a similar circularity, does not. As mentioned earlier, Dirca is closely related to Daphne and perhaps is preadapted by virtue of its circular aperture to use a torus should one arise in the course of evolution. Further evidence for correlation of torus development and aperture outline comes from Daphne aurantiaca and D. genkwa (Dute et al., 1996). Both species have both narrow and wide tracheary elements. The narrow ones have circular apertures and pit membranes with well-developed tori, whereas the larger elements have elliptical to slit-like apertures associated with tori of variable development or with no torus at all.

Vestures--function and systematic distribution

Vestures, in the restricted sense, represent wall protuberances associated with pits (Jansen et al., 1998). Zweypfenning (1978) hypothesized that these structures reduced membrane deflection during aspiration and decreased the possibility of membrane tearing. But as Carlquist (1988) rightly indicates, vestures and warts (protuberances on the surfaces of lumen walls) are the same structures in different locations. Thus, any hypothesis put forward must explain both features. According to Carlquist (1982), warts and vestures, by increasing surface area, could increase bonding of water molecules at the cell surface (lumen surface). This in turn would prevent breaking of water columns and formation of vapor bubbles. At this point, we would disagree with both hypotheses. True, in our observations it appears as if vestures are associated with slit-like apertures and could in theory substitute for the torus as regards protection for the pit membrane. However, construction of the vestures in Pimelea (Fig. 11, this stu dy) is not such as to reduce membrane deflection and certainly does not prevent membrane rupture. Also, vestured pit membranes are present in fibers of all species examined in this study. These are cells which conduct little, if any, water. Ohtani (1987), noting the evidence for vestures (warts) in septate fibers and parenchyma cells, stated that vestures have no function associated specifically with pits of conductive elements, but are simply "formed by an oversupply of wall material from the protoplast at the final stage of secondary wall formation process."

Whatever their function, vestures are considered to be a feature of the wood of the Thymelaeaceae (Bailey 1933; Metcalfe & Chalk, 1950). As recent examples, vestures have been reported for vessel or fiber pits of some Daphne spp. (Dute el al., 1992; Ohtani & Ishida, 1976), vessel pits of Dirca and Ovidia (Record & Hess, 1943), and Aquilaria agallecha (Rao & Dayal, 1992). We have confirmed the presence of vestures in vessel pits of Dirca, although their presence is inconsistent, and when present, obscure. To the best of our knowledge, vestures in Gnidia are reported for the first time. There is conflicting evidence for the presence of vestures in various species of Pimelea. Ohtani et al. (1983) indicated that warts (and by extension vestures) are absent from both vessels and fibers of P. aridula, P. gnidia, P. oreophila, and P. traversii, yet a year later Ohtani et al. (1984) located vestures in P. gnidia, P. oreophila, P. pseudo-lyalli, and P. traversii. The presence of vestures in Pimelea has been extended t o the species P. prostata and P. arenaria by the present investigation.

ACKNOWLEDGEMENTS

We wish to thank Drs. Robert Boyd and Micheal Davis for procuring specimens of Guidia for the herbarium and Mr. Curtis Hansen, herbarium curator, for his assistance.

Beck C. B., K. Coy, and R. Schmid. 1982. Observations on the fine structure of Callixylon wood. Amer. J, Bot. 69: 54--76.

LITERATURE CITED

Bailey, I.W, 1933. The cambium and its derivative tissues: VIII. Structure, distribution, and diagnostic significance of vestured pits in dicotyledons. J. Arnold Arbor. 14: 259--273.

Carlquist, S. 1982. Wood anatomy of Onagraceae: further species; root anatomy; significance of vestured pits and allied structures in dicotyledons. Ann. Missouri Bot. Gard. 69: 755--769.

Carlquist, S. 1988. Comparative Wood Anatomy. Springer-Verlag, Berlin.

Dute, R.R., J.D. Freeman, F. Henning, and L.D. Barnard. 1996. Intervascular pit membrane structure in Daphne and Wikstroemia--Systematic implications. IAWA J. 17: 161--181.

Dute, R.R., A.E. Rushing, and J.D. Freeman. 1992. Survey of intervessel pit membrane structure in Daphne species. [AWA Bull. 13: 113--123.

Dute, R.R., A.E. Rushing, and J.W. Perry. 1990. Torus structure and development in species of Daphne. JAWA Bull. 11: 401--412.

Engler, A. 1964. Syllabus der Pflanzenfamilien. Gebruder Borntraeger, Berlin.

Esau, K. 1965. Plant Anatomy, 2nd edition. Wiley, New York.

Jansen, S., E. Smets, and P. Baas. 1998. Vestures in woody plants: a review. IAWA J. 19: 347-382.

Metcalfe, C.R. and L. Chalk. 1950. Anatomy of the Dicotyledons. Vol. 2. Oxford at the Clarendon Press.

Morrow, A.C. and R.R. Dute. 1998. Development and structure of pit membranes in the rhizome of the woody fern Botrychium dissectum. IAWA J. 19: 429--441.

Morrow, A. C. and R.R. Dute. 1999. Electron microscopic investigation of the coating found on torus-bearing pit membranes of Botrychium dissectum, the common grape fern. IAWA J. 20: 359--373.

Ohtani, J. 1983. SEM investigation on the micromorphology of vessel wall sculptures. Research Bulletins of the College Experiment Forests. College of Agriculture, Hokkaido University 40: 323--386.

Ohtani, J. 1987. Vestures in septate wood fibres. IAWA Bull. 8: 59--67.

Ohtani, J. and S. Ishida. 1976. Study on the pit of wood cells using scanning electron microscopy. Report 5. Vestured pits in Japanese dicotyledonous woods. Research Bulletins of tile College Experiment Forests, College of Agriculture, Hokkaido University. 33: 407--436.

Ohtani, J. and S. Ishida. 1978. Pit membrane with torus in dicotyledonous woods. J. Jap. Wood Res. Soc. 24: 673-675.

Ohtani, J., B.A. Meylan, and B.G. Butterfield. 1983. Occurrence of warts in the vessel elements and fibres of New Zealand woods. New Zealand J. Bot. 21: 359--372.

Ohtani, J., B.A. Meylan, and B. G. Butterfield. 1984. A note on vestures on helical thickenings. IAWA Bull. 5: 9--11.

Rao, K. R. and R. Dayal. 1992. The secondary xylem of Aquilaria agallocha (Thymelaeaceae) and the formation of'agar'. IAWA Bull. 13: 163--172.

Record, S.J. and R.W. Hess. 1943. Timbers of the New World. Yale University Press, New Haven.

Schmitt, U. and W. Liese 1990. Wound reaction of the parenchyma in Betula. IAWA Bull. 11: 413--420.

Spurr, A.R. 1969. A low viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26: 31--45.

Thomas, R.J. 1969. The ultrastructure of southern pine bordered pit membranes as revealed by specialized drying techniques. Wood and Fiber 1: 11O--123.

Wright, J.G. 1928. The pit-closing membrane in the wood of the lower gymnosperms. Proc. Trans. R. Soc. Canada, Ser 3, 22: 63--95.

Zimmermann, M.H. 1983. Xylem Structure and the Ascent of Sap. Spring-Verlag, Berlin.

Zweypfenning, R.C.V.J. 1978. A hypothesis on the function of vestured pits. JAWA Bull. 1978/1: 13--15.
Table 1.

An abbreviated classification of the Thymelaeaceae adapted from
Engler (1964). The genera marked with an asterisk have been previously
studied in this laboratory. The genera listed in boldface are examined
in the present study.


Family - Thymelaeaceae

Subfamily Tribe

Gonystyloideae

Aquilarioideae Microsemmataeae

 Solmsieae

 Octolepideae

 Aquilarieae

Gilgiodaphnoideae

Thymelaeoideae Dicranolepideae



 Phalerieae

 Daphneae



 Thymelaeeae





Family - Thymelaeaceae

Subfamily Genus

Gonystyloideae Gonystylus, Amyxa, Aetoxylon

Aquilarioideae Microsemma

 Solmsia, Deltaria

 Octolepis

 Aquilaria, Gryinops

Gilgiodaphnoideae Gilgiodaphne

Thymelaeoideae Linostoma, Lophostoma,
 Dicranolepsis, Craterosiphon,
 Synaptolepsis

 Phaleria, Peddiea

 [*] Wikstroemia, Dendrostellera,
 Daphnopsis, Dirca, [*] Daphne,
 [*] Edgeworthia

 Thymelaea, Gnidia, Struthiola,
 Passerina, Kelleria, [*] Drapetes,
 Pimelea
Table 2.

Sources of wood specimens examined in this study.


Taxon Herbarium or City Date of Collection

Pimelea arenaria (1) AUA 11 Oct 1979


---------------- (2) AUA 22 Dec 1979


Pimelea prostrata AUA 26 Jan 1980


Dirca palustris (1) AUA 27 Mar 1969

--------------- (2) AUA 27 Mar 1969

--------------- (3) AUA 19 Mar 1989


Gnidia caffra (1) AUA Jan 2000

--------------- (2) AUA Jan 2000

Daphne gnidiodes K 26 Jul 1960




Taxon Collector(s) No.

Pimelea arenaria (1) Cooper &
 Nickerson 6113

---------------- (2) Wilkinson &
 Nickerson 6386

Pimelea prostrata Nickerson &
 Nickerson 6458

Dirca palustris (1) Kral 34029

--------------- (2) Kral 34034

--------------- (3) Diamond &
 Freeman 5731

Gnidia caffra (1) Boyd & Davis s.n.

--------------- (2) Boyd & Davis s.n.

Daphne gnidiodes Khan, Prance &
 Ratcliffe 255
Table 3.

Dimensions of pit membranes, pit apertures, and tori.
All measurements are in micrometers and are taken from the non-lumen
side of the pit border. Means are based on 25 measurements.


species pit diameter long axis of short axis of
 aperture aperture

Pimelea 5.24 (4.37-- 1.89 (1.27-- 0.56 (0.42--
prostata 6.07) 2.61) 0.81)

P. arenaria (1) 5.46 (4.23-- 2.43 (1.76-- 0.71 (0.5--
 6.77) 3.60) 1.20)

P. arenaria (2) 5.14 (4.23-- 3.02 (2.04-- 1.10 (0.84--
 6.00) 4.23) 1.41)

Dirca palustris (1) 5.57 (4.58-- 1.60 (1.20-- 1.16 (0.63--
 7.05) 2.04) 1.69)

D. palustris (2) 6.68 (5.71-- 1.62 (1.05- 1.27 (0.88--
 7.58) 2.22) 1.58)

D. palustris (3) 6.31 (5.29-- 2.19 (1.12-- 1.39 (0.91--
 8.00) 3.64) 1.88)

Daphne 6.58 (5.41-- 1.62 (1.05-- 1.15 (0.88--
gnidiodes 8.82) 2.22) 1.58)

Gnidia caffra (1) 3.95 (2.96-- 2.22 (1.83-- 0.58 (0.40--
 5.29) 3.45) 0.84)

G. caffra (2) 4.88 (4.23-- 2.33 (1.54-- 0.65 (0.45-
 5.71) 2.96) 1.12)



species circularity torus
 ratio diameter

Pimelea 0.30 none
prostata

P. arenaria (1) 0.29 none


P. arenaria (2) 0.36 none


Dirca palustris (1) 0.73 none


D. palustris (2) 0.78 none


D. palustris (3) 0.63 none


Daphne 0.71 2.77 (2.28-3.29)
gnidiodes

Gnidia caffia (1) 0.26 none


G. caffra (2) 0.28 none
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Author:Dute, Roland R.; Miller, Michael E.; Carollo, Robert R.
Publication:Journal of the Alabama Academy of Science
Article Type:Statistical Data Included
Geographic Code:1U6AL
Date:Jan 1, 2001
Words:3934
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