AOBPreview originally published online on March 6, 2006
Annals of Botany 2006 97(6):1045-1053; doi:10.1093/aob/mcl049
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Perforated Pit Membranes in Imperforate Tracheary Elements of Some Angiosperms
1 Laboratory of Wood Biology, Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan and 2 Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3DS, UK
* For correspondence. E-mail pirika{at}for.agr.hokudai.ac.jp
Received: 20 September 2005 Returned for revision: 15 December 2005 Accepted: 19 January 2006 Published electronically: 6 March 2006
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ABSTRACT |
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• Background and Aims The structure of pit membranes in angiosperms has not been fully examined and our understanding about the structure is incomplete. Therefore, this study aims to illustrate the micromorphology of pit membranes in fibres and tracheids of woody species from various families.
• Methods Specimens from ten species from ten genera and eight families were prepared using two techniques and examined by field-emission scanning electron microscopy.
• Key Results Interfibre pit membranes with an average diameter of <4 µm were frequently perforated or appeared to be very porous. In contrast, pit membranes in imperforate tracheary elements with distinctly bordered pits and an average diameter of 
4 µm were homogeneous and densely packed with microfibrils. These differences were observed consistently not only among species but also within a single species in which different types of imperforate tracheary elements were present.
• Conclusions This study demonstrates that the structure of interfibre pit membranes differs among cell types and the differences are closely associated with the specialization of the fibre cells. It is suggested that perforated pit membranes between specialized fibres contribute to the dehydration of the fibre cells at or soon after maturation.
Key words: Wood anatomy, angiosperms, field-emission scanning electron microscopy, pit, pit membrane, fibre, tracheid
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INTRODUCTION |
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A pit is a gap in the secondary wall of a plant cell. In general, a pit of one cell is located exactly opposite a pit of an adjacent cell wall. Such a complementary pair of pits is called a pit pair. The essential parts of a pit pair are the pit cavities, which are empty spaces connecting the lumen of each cell, and the pit membrane, which forms a partition between the adjacent pit cavities (Panshin and de Zeeuw, 1980
; Tsoumis, 1991; Dickison, 2000). The pit cavity is formed as a result of the localized absence of secondary wall deposition during the thickening of the cell wall. The pit membrane consists of material derived from the degraded primary cell walls and middle lamella of two opposing cells. Although several studies describe variation in the chemical composition of pit membranes (Bauch and Berndt, 1973; Coleman et al., 2004), much of the available evidence indicates that pit membranes are composed of tightly interwoven cellulose microfibrils in a matrix of hemicellulose and pectin polysaccharides (Brett and Waldron, 1996).
The pit membrane structure has been examined in previous studies largely using high-resolution transmission and scanning electron microscopy (Ohtani and Ishida, 1978; Dute and Rushing, 1990; Sano et al., 1999, 2005). These studies show that angiosperms possess a homogeneous pit membrane, while gymnosperms are characterized by a torus–margo pit membrane, i.e. a pit membrane with a central thickening (torus) that is surrounded by a more porous area (margo). This generalization holds true for the majority of angiosperms and gymnosperms, although exceptions have been reported both in angiosperms and in latewood of some gymnosperms (Bauch et al., 1972; Ohtani and Ishida, 1978; Wheeler, 1983; Dute and Rushing, 1990; Dute et al., 1992, 2004; Jansen et al., 2004a). In addition, there are several records of ‘pseudo-tori’, which are plasmodesmata-associated thickenings associated with pit membranes in narrow tracheary elements of some angiosperms (Parameswaran and Liese, 1981; Barnett, 1987; Lachaud and Maurousset, 1996). Other studies have shown that the surface structure of pit membranes may change with age, becoming progressively incrusted with non-microfibrillar materials (e.g. Wheeler, 1983; Sano and Nakada, 1998). All these observations illustrate that there is considerable variation in the structure of pit membranes and that the full anatomical variation of pit membranes remains poorly understood in various plant groups.
Pits play an important role in the movement of sap in living trees and in the penetration of liquids or gasses into timber (Panshin and de Zeeuw, 1980; Tsoumis, 1991); therefore, intensive efforts have been made to clarify their structures. Recent attention has been paid to the structure and function of intervessel pits, i.e. pits between adjacent vessel elements. Relevant topics studied include the systematic and ecological distribution of torus-bearing pit membranes and vestured pits, the basic structure of intervessel pit membranes, the relationship between the porosity of intervessel pit membranes and the susceptibility to the progression of water stress-induced cavitation, the possible function of vestured pits and the regulation of water flow by the matrix that is present in pit membranes (Zwieniecki et al., 2001; Choat et al., 2003, 2004; Jansen et al., 2004a, b; Sano 2004, 2005; Peracreta et al., 2005). However, information about the structure of other pit types is relatively limited, although some valuable information is available (Côté and Marton, 1962; Harada, 1963; Thomas, 1976; Parameswaran and Liese, 1981; Meylan and Butterfield, 1982; Wheeler, 1982; Barnett, 1987; Sano and Fukazawa, 1994; Lachaud and Maurousset, 1996; Feild et al., 2000; Sakamoto and Kato, 2002).
This report describes structural variations of pit membranes in imperforate tracheary elements of some woody angiosperm species. Ten species from various families were selected and the structure of the pit membranes was examined by field-emission scanning electron microscopy. The work is part of ongoing studies on the micromorphology of pit membranes (Sano and Nakada, 1998; Sano et al., 1999; Choat et al., 2004; Jansen et al., 2004a; Sano, 2004, 2005).
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MATERIALS AND METHODS |
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Materials
A total of ten species were examined (Table 1). For all species in this study, the outer sapwood that had been stored in 30 % ethanol or FAA (a mixture of formaldehyde, acetic acid and 50 % ethanol, 5 : 5 : 90, v/v/v; Ruzin, 1999
) was examined. For Acer mono, Fraxinus mandshurica ‘japonica’, Quercus crispula and Robinia pseudoacacia, specimens that had been stored in liquid nitrogen without rinsing in organic solvent after collection were also examined.
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Field-emission scanning electron microscopy
For examination of the superficial appearance of pit membranes, samples were prepared as described previously (Sano, 2004
). In brief, samples were cut into small cubes (approx. 5 mm3). The blocks that had been stored in 30 % ethanol and FAA were air-dried after dehydration in absolute ethanol. The blocks cut from frozen samples were freeze-dried without immersion in organic solvent. The dried blocks were split along a tangential or a radial plane and samples were affixed to aluminium stubs with electron-conductive carbon paste. They were coated with platinum by vacuum evaporation and examined with a field-emission scanning electron microscope (FE-SEM; JSM-6301F, Jeol, Tokyo, Japan) at an accelerating voltage of 2·5 kV.
Interfibre pits of sectioned material were also examined since it was often difficult to confirm the nature of the pit pairs on a split face. Surfaces of samples were exposed by the method devised by Yumoto et al. (1982). In brief, small cubes of wood (approx. 2 mm3) were cut and embedded in a methacrylate resin (a mixture of n-butyl methacrylate and methyl methacrylate, 1 : 2, v/v). Transverse surfaces were planed on an ultramicrotome with a glass knife. Then the methacrylate resin was removed by soaking in absolute acetone. The samples were subsequently air-dried and affixed with electron-conductive carbon paste to aluminium stubs. After coating with carbon and gold plus palladium by vacuum evaporation or with osmium by plasma polymerization (Sano et al., 1999), the samples were examined with the FE-SEM described above. More than 100 pit pairs were examined for each species.
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RESULTS |
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Perforated (incomplete) pit membranes
In nine of the ten species examined, there were interfibre pit membranes with a central region that was perforated and that appeared to be porous. This feature was found irrespective of the methods of storing and drying wood samples. The average diameter of pits with this type of pit membrane was <4 µm (Table 2). In six out of these nine species, only one type of fibre was present in the ground tissue of the xylem, and most of the interfibre pit membranes were perforated or very porous. In the other three species, in which two or more fibre types co-occurred in the xylem, there were perforated pit membranes between libriform fibres in R. pseudoacacia and A. mono, and between fibre-tracheids in Q. crispula.
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In Populus sieboldi, Salix sachalinensis, Betula platyphylla ‘japonica’, Tilia japonica, Osmanthus heterophyllus and F. mandshurica ‘japonica’, the central region of each interfibre pit membrane was frequently perforated (Figs 1A–G and 2A–C). The fine structure of such pit membranes varied among species. In P. sieboldi, S. sachalinensis and O. heterophyllus, the central region of most of the interfibre pit membranes was simply and extensively perforated (Fig. 1A–C). While the remnants of the pit membranes were thin and occasionally granular in P. sieboldi and S. sachalinensis (Fig. 1B), the remnants of pit membranes were dense in O. heterophyllus. In B. platyphylla ‘japonica’ and F. mandshurica ‘japonica’, the porosity of the pit membranes varied with each pit pair (Fig. 1E–G). In B. platyphylla ‘japonica’, the pit membranes were often incrusted with matrix material (Fig. 1F). The extent of this incrustation varied, and approx. 10 % of the interfibre pit membranes lacked visible openings because they were densely covered by matrix materials. In contrast, the remnants of interfibre pit membranes were thin in F. mandshurica ‘japonica’ (Fig. 1G). In T. japonica, the diameter of fibre pits varied considerably (Table 2). The central regions of the pit membranes between fibre-tracheids were frequently perforated in this species, irrespective of the diameter of the pits (Fig. 2A–C). These pit membranes also showed a microfibrillar texture (Fig. 2C).
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In R. pseudoacacia and A. mono, there were both libriform fibres and living fibres (Fig. 2D). In A. mono, most of the pit membranes between libriform fibres were perforated (Fig. 2D and E). In R. pseudoacacia, approx. 20 % of the pit membranes between libriform fibres were perforated (Fig. 2F), while other pit membranes were dense and lacked visible openings. The remnants of the pit membranes in A. mono had a microfibrillar texture (Fig. 2E). In contrast, the interfibre pit membranes were often covered with granular materials in R. pseudoacacia.
In Q. crispula, two types of imperforate tracheary elements were present. Although pit membranes between typical vasicentric tracheids were dense (see below), pit membranes between fibre-tracheids were often perforated (Figs. 3A and B). In the latter case, approx. 80 % of the pit membranes showed a simple or multiple perforation, while the remainder was covered with granular materials and lacked visible openings (Fig. 3C).
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Homogeneous pit membranes
In two of the ten species examined, homogeneous pit membranes were found in imperforate tracheary elements. The average diameter of pits with this type of pit membrane was >4 µm (Table 2).
In Eucalyptus camaldulensis, the imperforate tracheary elements were classified as fibre-tracheids, and all the pit membranes between these elements were of the homogeneous type (Fig. 4A–C). The pits were distinctly bordered, and vestures were always associated with the pit aperture (Fig. 4A–C). All pit membranes were densely and evenly packed with microfibrils (Fig. 4B, C). In regions from which the superficial layer had been partially removed, another layer of microfibrils appeared (Fig. 4B, C), which illustrates the two-layered structure of the pit membrane. The diameter of these fibre-tracheid pits was larger than the diameter of pit pairs with perforated pit membranes in the other species studied (Table 2).
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In Q. crispula, typical vasicentric tracheids and fibre-tracheids were present. The pit membranes between vasicentric tracheids were of the homogeneous type. Many of the pit membranes between vasicentric tracheids were densely and evenly packed with microfibrils (Fig. 4D). Nonetheless, in approx. 10 % of the pit membranes, microfibrils were sparsely packed in a small region of individual pit membranes, and there were openings of up to 0.4 µm in diameter in these regions (Fig. 4E, F). These localized porous zones tended to appear near the periphery of the pit membranes (Fig. 4E, F) and differed in this regard from the above-described perforated interfibre pit membranes. There was occasionally more than one porous zone per pit membrane (Fig. 4F). Each pit membrane consisted of at least two layers irrespective of the presence or absence of porous zones (Fig. 4D).
Pit membranes between living fibres and between a living fibre and a dead fibre
There were living fibres in both R. pseudoacacia and A. mono (Fig. 2D). In both species, there was always a dense septum, which seemed to be a complex of the pit membrane and the plasmalemma, between living fibres or between a living fibre and a dead (libriform) fibre (Fig. 2D).
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DISCUSSION |
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Since interfibre pit membranes with a perforated central area were found in nine out of the ten species examined, this feature seems to be more common in pits of libriform fibres and fibre-tracheids than previously thought. As far as we know, perforated pit membranes in imperforate tracheary elements in normal wood have only been recorded in Carya tomentosa, F. mandshurica ‘japonica’ and Amborella trichopoda (Thomas, 1976
; Sano and Fukazawa, 1994; Feild et al., 2000). Other studies on the structure of interfibre pit membranes do not report perforated pit membranes in normal wood (Côté and Marton, 1962; Harada, 1963; Parameswaran and Liese, 1981; Wheeler, 1982; Barnett, 1987; Lachaud and Maurousset, 1996; Sakamoto and Kato, 2002). It is unlikely that perforated interfibre pit membranes are so rare that they are present in only a limited number of species. Therefore, it is possible that similar degraded interfibre pit membranes might be present under normal conditions in many other angiosperm species.
The difference between perforated pit membranes and pit membranes with pores as observed in vasicentric tracheids of Q. crispula seems to be the central vs. peripheral position, respectively. The size of the opening in the pit membrane could also be used as a distinctive character, although this would be an artificial criterion. Moreover, perforated interfibre pit membranes show to some extent similarities with transitional forms between vessel perforation plates with pit membrane remnants and transitional pits (Carlquist and Schneider, 2002, 2004a, b). Perforation plates with pit membrane remnants are interpreted as a result of incomplete digestion of primary wall material (cellulose microfibrils) by cell enzymes at maturation in species that occupy highly mesic habitats. Pit membranes of fibres may have been subject to an enzymatic attack in much the same way as occurs for intervessel pit membranes and perforation plate partitions, although further developmental study of the mechanism and timing of enzymatic digestion of pit membranes in perforations and pits is needed to enhance our present understanding of this phenomenon.
In A. mono, F. mandshurica ‘japonica’, Q. crispula and R. pseudoacacia, the perforated pit membranes were present in samples that had been prepared without any immersion in organic solvents (Fig 1G, Fig 2E and Fig 3A). Therefore, we believe that the perforated interfibre pit membranes are not artificially produced as a result of the chemical treatment with ethanol, acetone or FAA during sample collection and preparation. It could also be suggested that surface tension forces generated during drying of the wood samples may cause tearing or may create artefacts of the pit membranes. Pit membranes that have been dehydrated before treatment or during preparation for microscopy are particularly suspect for artefacts (Shane et al., 2000). Obviously, however, there are still a large number of pit membranes intact irrespective of the method of drying. In our experience, critical point drying of wood samples does not make any difference compared with drying at room temperature (Jansen et al., 1998). Even if the perforation was induced or enlarged by other factors, it is possible to state that the structure of perforated pit membranes differs from that of homogeneous pit membranes and that the perforated pit membranes are easily degraded and cannot function as an effective partition between the adjacent cells. It would also be interesting to study perforated pit membranes using atomic force microscopy, as this technique allows for observation of pit membranes in their native state and does not require any special treatment that could actually affect the structure of pit membranes (Pesacreta et al., 2005).
The perforated pit membranes are probably too small to be detected with a light microscope. Even during examination of interfibre pits with an electron microscope, perforated interfibre pit membranes might easily be overlooked. Based on observations from the present study and previous studies, it is clear that interfibre pit membranes are not always perforated (Thomas, 1976; Sano and Fukazawa, 1994; Feild et al., 2000). In addition, even if ultra-thin sections for transmission electron microscopy are cut from a pit pair with perforated pit membranes, as has been widely used for studies of the fine structure of pits, the possibility exists that such sections do not include perforated portions of the pit membranes. In contrast, examination of complementary pairs of fractured planes by scanning electron microscopy can more easily confirm the presence of perforated pit membranes (Figs 1C and D, Fig 2A and B, and Fig 3A and B). Examination by scanning electron microscopy of sections that have been cleanly cut with a glass knife from embedded samples also seems to be useful since this method reveals not only the true section but also parts of the specimen that are deeper than the level of the cutting (Figs 1A and E, Fig 2D and E, and Fig 4A).
The frequency of perforated interfibre pit membranes was somewhat lower in R. pseudoacacia and in Q. crispula than in the other species examined. Although differentiating pit membranes are densely packed with matrix materials, some matrix materials are digested by enzymes and removed from developing pit membranes at the final stages of the formation of cell walls (e.g. Barnett, 1987; Dute and Rushing, 1990; Butterfield, 1995). The matrix material or additional deposits on the pit membranes of R. pseudoacacia and Q. crispula might make it more difficult to create a perforation or a pore in the pit membrane, because their chemical composition is slightly different, and pit membranes with these extra matrix components are more difficult to break down than perforated pit membranes.
The extent of degradation of interfibre pit membranes might be associated with the specialization of the fibre cells. Perforated pit membranes were found in interfibre pits with an average diameter of <4 µm, while pit membranes between imperforate tracheary elements with an average diameter of >4 µm were densely and evenly packed with microfibrils. These homogeneous pit membranes resembled the intervessel pit membranes of some species that were previously described (Sano, 2005) and the intertracheary pit membranes of vessel-less wood (Meylan and Butterfield, 1982). Differences in the presence or absence of a perforation in the pit membrane of libriform fibres and fibre-tracheids were observed consistently not only among species, but also within a single species in which two fibre types were present, as for example in Q. crispula. According to the morphological trends in tracheary element specialization as discovered by Bailey and Tupper (1918), there is a tendency for the size of pits and the extent of pit borders in fibres to decrease according to specialization. It is possible to link the morphological trends of interfibre pit membranes, as noted in the present study, to the specialization trend from tracheids to libriform fibres, which means that interfibre pit membranes are partially degraded or remain incomplete depending on the degree of fibre specialization. These trends can also be interpreted in terms of functional considerations as the function of libriform fibres is primarily one of support, while tracheids probably assist more with conduction than support. Fibre-tracheids are usually interpreted as representing an intermediate evolutionary form between the tracheid and libriform fibre. They function mainly in support and to a lesser extent in conduction (Carlquist, 2001; Sperry, 2003).
To date, there is no consensus on the classification of wood fibres (Baas, 1986; Carlquist, 1986, 2001 and references therein; IAWA Committee, 1989). In addition to differences in fibre length, wall thickness and the size of pit border, the presence of perforated pit membranes might help a distinction to be made between fibres that have been generated to provide mechanical support and true tracheids. It is necessary to compare the structures of pit membranes among different types of imperforate tracheary elements and to associate their structure with different fibre types in detail, as well as to evaluate whether and to what extent morphological tendencies of interfibre pit membranes might be common in a wide range of species.
The apparent occurrence of perforations or large pores in pit membranes between libriform fibres or fibre-tracheids with relatively small pits may contribute to the removal of water from the lumina of wood fibres at or soon after maturation. The moisture content of the sapwood of angiosperm trees is generally much lower than the water saturation level (e.g. Tsoumis, 1991), probably because most wood fibres are dehydrated at or soon after their maturation. Indeed, cryo-scanning electron microscopy has shown that wood fibres are dehydrated when or soon after cells have reached maturity in F. mandshurica ‘japonica’, S. sachalinensis and B. platyphylla ‘japonica’ (Utsumi et al., 1996, 1998). Moreover, the ‘air-seeding model’ (Zimmermann, 1983) suggests that the larger the pores of the pit membranes, the more easily cavitation can progress from a cavitated conduit to a water-filled conduit. Although details of the mechanisms remain unclear, it is likely that large pores or perforations in interfibre pit membranes are one of the factors that are involved in the dehydration of wood fibres.
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ACKNOWLEDGEMENTS |
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The authors thank Dr Yoko Watanabe for providing wood samples of Eucalyptus camaldulensis. This study was supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology, Japan (nos 16580127 and 15208016) and a small grant from the Daiwa Anglo-Japanese Foundation (no. 430/5326).
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