Bordered pits in ray cells and axial parenchyma: the histology of conduction, storage, and strength in living wood cells

Bordered pits occur in walls of living ray cells of numerous species of woody dicotyledons. The occurrence of this feature has been minimally reported because the pits are relatively small and not easily observed in face view. Bordered pits are illustrated in sectional view with light microscopy and with scanning electron microscopy in face view for dicotyledonous and gnetalean woods. Bordered pits are more numerous and often have prominent borders on tangential walls of procumbent ray cells, but also occur on radial walls; they are approximately equally abundant on tangential and horizontal walls of upright cells, suggesting parallels to cell shape in flow pathway design. Axial parenchyma typically has secondary walls thinner than those of ray cells, but bordered pits or large simple pit areas occur on some cross walls of parenchyma strands. There is no apparent correlation between the phylogenetic position of species and the presence of borders in ray cells or axial parenchyma. Bordered pits represent a compromise between maximal mechanical strength and maximal conductive capability. High rates of flow of sugar solutions may occur if starch in ray cells or axial parenchyma is mobilized for sudden osmotic enhancement of the conductive stream or for rapid development of foliage, flowers, or fruits. Measurement of the secondary wall thickness of ray cells may offer simple inferential information about the role that rays play in the mechanical strength of woods. © 2007 The Linnean Society of London, Botanical Journal of the Linnean Society , 2007, 153 , 157–168.     

Wood structure of Aegiceras corniculatum and its ecological adaptations to salinities

We describe the wood structure of Aegiceras corniculatum and its differences under various soil salinities. This species had diffuse-porous wood with poorly defined growth rings. Vessels which had single perforations occurred abundantly and in multiples and were storeyed. Intervascular pits between contiguous vessels were alternate bordered ones while half-bordered pit-pairs existed between both vessel-ray and vessel-parenchyma. Homogenous xylem rays were multiseriate and uniseriate. Fiber-tracheids with bordered pits often had thinner walls. Xylem parenchyma cells were scant and distributed diffusely and paratracheally. Differences in the structural and quantitative characters of vessels, xylem rays and fiber-tracheids under diverse soil salinities are described. This revised version was published online in August 2006 with corrections to the Cover Date.     

Myosin,microtubules, and microfilaments: co-operation between cytoskeletal components during cambial cell division and secondary vascular differentiation in trees

The immunolocalisation of unconventional myosin VIII ('myosin') in the cells of the secondary vascular tissues of angiosperm (Populus tremula L. x P. tremuloides Michx. and Aesculus hippocastanum L.) and gymnosperm (Pinus pinea L.) trees is described for the first time and related to other cytoskeletal elements, as well as to callose. Both myosin and callose are located at the cell plate in dividing cambial cells, whereas actin microfilaments are found alongside the cell plate; actin and tubulin are both associated with the phragmoplast. Myosin and callose also localise to the plasmodesmata-rich pit fields in the walls of living cells, which are particularly abundant within the common walls between ray cells and between ray cells and axial parenchyma cells in the phloem and xylem. In those xylem ray cells that contact developing vessel elements and tracheids, myosin, tubulin, actin and callose are localised at the periphery of developing contact and cross-field pits; the respective antibodies also highlight the bordered pits between vessels and between tracheids. The aperture of the bordered pits, whose diameter diminishes as the over-arching border of these pits develops, also houses myosin, actin and tubulin. Myosin, actin and callose are also found together around the sieve pores of sieve elements and sieve cells. We suggest that an acto-myosin contractile system (a 'plant muscle') is present at the cell plate, the sieve pores, the plasmodesmata within the walls of long-lived parenchyma cells, and at the apertures of bordered pits during their development.     

Living Cells in Wood 3. Overview; Functional Anatomy of the Parenchyma Network

The very different evolutionary pathways of conifers and angiosperms are very informative precisely because their wood anatomy is so different. New information from anatomy, comparative wood physiology, and comparative ultrastructure can be combined to provide evidence for the role of axial and ray parenchyma in the two groups. Gnetales, which are essentially conifers with vessels, have evolved parallel to angiosperms and show us the value of multiseriate rays and axial parenchyma in a vessel-bearing wood. Gnetales also force us to re-examine optimum anatomical solutions to conduction in vesselless gymnosperms. Axial parenchyma in vessel-bearing woods has diversified to take prominent roles in storage of water and carbohydrates as well as maintenance of conduction in vessels. Axial parenchyma, along with other modifications, has superseded scalariform perforation plates as a safety mechanism and permitted angiosperms to succeed in more seasonal habitats. This diversification has required connection to rays, which have concomitantly become larger and more diverse, acting as pathways for photosynthate passage and storage. Modes of growth such as rapid flushing, vernal leafing-out, drought deciduousness and support of large leaf surfaces become possible, advantaging angiosperms over conifers in various ways. Prominent tracheid-ray pitting (conifers) and axial parenchyma/ray pitting to vessels (angiosperms) are evidence of release of photosynthates into conductive cells; in angiosperms, this system has permitted vessels to survive hydrologic stresses and function in more seasonal habitats. Flow in ray and axial parenchyma cells, suggested by greater length/width ratios of component cells, is confirmed by pitting on end walls of elongate cells: pits are greater in area, more densely placed, and are often bordered. Bordered pit areas and densities on living cells, like those on tracheids and vessels, represent maximal contact areas between cells while minimizing loss of wall strength. Storage cells in rays can be distinguished from flow cells by size and shape, by fewer and smaller pits and by contents. By lacking secondary walls, the entire surfaces of phloem ray and axial phloem parenchyma become conducting areas across which sugars can be translocated. The intercontinuous network of axial parenchyma and ray parenchyma in woods is confirmed; there are no “isolated” living cells in wood when three-dimensional studies are made. Water storage in living cells is reported anatomically and also in the form of percentile quantitative data which reveal degrees and kinds of succulence in angiosperm woods, and norms for “typically woody” species. The diversity in angiosperm axial and ray parenchyma is presented as a series of probable optimal solutions to diverse types of ecology, growth form, and physiology. The numerous homoplasies in these anatomical modes are seen as the informative results of natural experiments and should be considered as evidence along with experimental evidence. Elliptical shape of rays seems governed by mechanical considerations; unusually long (vertically) rays represent a tradeoff in favor of flexibility versus strength. Protracted juvenilism (paedomorphosis) features redirection of flow from horizontal to vertical by means of rays composed predominantly or wholly of upright cells, and the reasons for this anatomical strategy are sought. Protracted juvenilism, still little appreciated, occurs in a sizeable proportion of the world’s plants and is a major source of angiosperm diversification.     

Tetracentron Wood from the Miocene of Noto Peninsula,Central Japan,with a short revision of homoxylic fossil woods

A vesselless fossil wood was discovered in the Miocene Yanagida Formation in the Noto Peninsula, central Japan. This fossil has distinct growth rings with gradual transition from the early- to the latewood ; tracheids, which are called 'usual traeheids' here, constitute the ground mass of the wood and have typical scalariform bordered pits on radial walls in the earlywood and circular sparse pits on those in the latewood ; rays are 1\2-4 cells wide and heterogeneous with low to high uniseriate wings; axial parenchyma strands are scattered in the latewood. This wood has a peculiar feature; sporadic radial files of broad tracheids whose tangential walls have crowded alternate bordered pits. The radial walls have crowded half-bordered pits to ray cells, but no pits to the usual tracheids. Among all of the extant and extinct angiosperms and gymnosperms, these unusual tracheids occur only in Tetracentron. From these features, we refer the fossil to the extant genus Tetracentron, and name it T. japonoxylum. A revision of homoxylic woods is made for comparision with the present fossil. Tetracentron japonoxylum is the only fossil wood of Tetracentron.     

Wood, bark and stem anatomy of New World species of Gnetum

Quantitative and qualitative data are presented for 11 collections of six species. The wide range of character states for the species is presented in the form of a key to emphasize their potential systematic correlations. Distinctive among these are phcllem characteristics. Fibre-tracheids are newly reported for lianoid Gnetum species. Cells previously thought to be like companion cells in secondary phloem are shown to be uniseriate rays, counterparts to uniseriate xylem rays. Laticifers are abundant in most of the species, and are newly described for secondary tissues of Gnetum. Presence of tyloses in laticifers of two species is apparently a new report for vascular plants. Tori are present in two New World Gnetum species, adding to the report in African species. Perforation plates are simple except near or in primary xylem, where they are simple or foraminate. Torus presence and foraminate perforation plate presence are features more reminiscent of Ephedra and other gymnosperms than of angiosperms. The bark of Gnetum is also very similar to that of Ephedra.     

A cytoskeletal basis for wood formation in angiosperm trees: the involvement of cortical microtubules

Rearrangements of cortical microtubules (CMTs) during the differentiation of axial secondary xylem elements within taproots and shoots of Aesculus hippocastanum L. (horse-chestnut) are described. A correlative approach was employed using indirect immunofluorescence microscopy of α-tubulin in 6- to 10-μm sections and transmission electron microscopy of ultrathin sections. All cell types – fibres, vessel elements and axial parenchyma – derive from fusiform cambial cells which contain randomly oriented CMTs. At the early stages of development, fibres and axial parenchyma cells possess helically arranged CMTs, which increase in number as secondary wall thickening proceeds and simple pits develop. In contrast, incipient vessel elements are distinguished by the marking out of sites of bordered pits; these sites first appear as microtubule-free regions within the reticulum of randomly oriented CMTs that characterises their precursor fusiform cambial cells. Subsequently, the ring of CMTs which develops at the periphery of the microtubule-free region decreases in diameter as the over-arching pit border is formed. Like bordered pits, large-diameter, non-bordered pits (contact pits) which develop between vessel elements and adjacent contact ray cells originate as microtubule-free regions and are also associated with development of a ring of CMTs at the periphery. In the case of contact pits, however, there is no reduction in the diameter of the CMT ring during pit development. Tertiary cell wall thickenings are also a feature of vessel elements and appear to form at sites where bands of laterally associated, transversely oriented CMTs, separated from each other by microtubule-free zones, are found. Later, these bands of CMTs become narrower, and separate into pairs of microtubule bundles located on each side of the developing wall thickening. Development of perforations between vessel elements is also associated with the presence of a ring of CMTs at their periphery. Received: 13 July 1998 / Accepted: 30 November 1998     

Modelling the hydrodynamic resistance of bordered pits

Previous studies of the hydrodynamics of plant stems have shown that resistance to flow through bordered pits on the side walls of tracheids makes up a significant proportion of their total resistance, and that this proportion increases with tracheid diameter. This suggests a possible reason why tracheids with a diameter above around 100 microm have failed to evolve. This possibility has been investigated by obtaining an estimate for the resistance of a single pit, and incorporating it into analytical models of tracheid resistance and wood resistivity. The hydrodynamic resistance of the bordered pits of Tsuga canadensis was investigated using large-scale physical models. The importance of individual components of the pit were investigated by comparing the resistance of models with different pore sizes in their pit membrane, and with or without the torus and border. The estimate for the resistance of a real bordered pit was 1.70x10(15) Pa s m(-3). Resistance of pits varied with morphology as might be predicted; the resistance was inversely proportional to the pore size to the power of 0.715; removing the torus reduced resistance by 28%, while removal of the torus and border together reduced it by 72%. It was estimated that in a 'typical tracheid' pit resistance should account for 29% of the total. Incorporating the results into the model for the resistivity of wood showed that resistivity should fall as tracheid diameter increases. However, to minimize resistance wider tracheids would also need to be proportionally much longer. It is suggested that the diameter of tracheids in conifers is limited by upper limits to cell length or cell volume. This limitation is avoided by angiosperms because they can digest away the ends of their cells to produce long, wide vessels composed of many short cells.     

ULTRASTRUCTURE OF THE SUBGLANDULAR CELLS FROM THE FOLIAR NECTARIES OF COTTON IN RELATION TO THE DISTRIBUTION OF PLASMODESMATA AND THE SYMPLASTIC TRANSPORT OF NECTAR

Foliar nectaries on the midveins of 7-cm leaves from cotton (Gossypium hirsutum L., cv. Stoneville 213) were examined by light and electron microscopy. The nectaries consist of external multicellular papillae and internal subglandular tissue that extends from the bases of the papillae to the vascular tissue of the midveins. The subglandular tissue is composed of small parenchyma cells; it does not contain sieve elements or xylem vessels. The parenchyma cells are rich in mitochondria, and their walls contain numerous pit fields having a high concentration of plasmodesmata. The absence of vascular tissue and the significance of the pit fields in the subglandular tissue are discussed in relation to symplastic transport of nectar secretions.     

Wood and bark anatomy of the African species of Gnetum

Quantitative and qualitative data are given for the two African species of Gnetum ( Gnetum section Gnetum subsection Micrognemones ). These species are lianoid and lack the fibre-tracheids of G. gnemon but have about the same vessel element and tracheid length as in that species. Vessel diameter is related to stem age and organography. Tori are clearly present in tracheary elements of the African Gnetum species, a first report for the genus. In these two species, origin of the lateral meristem, which produces vascular tissue and cambia, can be traced directly and indirecdy to cortical parenchyma. A second kind of meristematic action, newly reported for Gnetum, is produced by proliferation of axial parenchyma, fragmenting secondary xylem. Both presence of tori and site of origin of lateral meristematic activity in Gnetum contrast with corresponding conditions in Welwitschia.     

The vestured pits of Eucalyptus regnans F. Muell.: a study using scanning electron microscopy

Scanning electron microscopy has been used to examine the surface architecture, before and after various chemical treatments, of the pits in the walls of vessels, vasicentric and fibre tracheids, and parenchyma cells, which together make up the wood of Eucalyptus regnans. The treatments included water at 150°C under pressure, hydrofluoric acid, delignifying agents and potassium permanganate. All bordered pits were vestured; half-bordered pits were vestured, partially vestured or non-vestured. No distinction could be made between warts and vestures on morphological or chemical grounds. An hypothesis is advanced which relates vesture formation to prolongation of the activity of the protoplast in pits as the cells die. Vestures, on the basis of this hypothesis, could be regarded as enlarged or conglomerate warts.     

广义锦葵科火绳树属4个种的枝条木材解剖及其分类学意义

研究了广义锦葵科火绳树属4个种枝条的木材解剖。火绳树属枝条为散孔至半环孔材,管孔主要为单管孔和2～3个管孔组成的径列复管孔;导管间纹孔式和射线导管间纹孔式互列、小;侵填体和螺纹加厚缺如。射线主要为单列射线,2～3列射线较多;射线细胞多为方形,射线组织主要为异型,边缘直立细胞常1行;射线组织稀为同型;鞘细胞和瓦形细胞缺如。轴向薄壁组织傍管和离管型,主要为带状。晶体丰富,主要在射线、纤维和薄壁组织中。研究的4个种可以通过枝条木材解剖特征加以区分。     

WOOD ANATOMY OF ILLICIUM (ILLICIACEAE): PHYLOGENETIC,ECOLOGICAL, AND FUNCTIONAL INTERPRETATIONS

Quantitative and qualitative features are reported for 23 collections of ten species of Illicium, sole genus of Illiciaceae. Vessel elements are long, thin-walled, and angular; perforation plates are scalariform and range from long to moderately long; vessel-ray pitting is scalariform to opposite. Tracheids bear fully bordered pits. Axial parenchyma is sparse, abaxial to vessels with some diffuse cells also present. Rays are both multiseriate and uniseriate; the former are lacking near the pith in some species. No erect sheathing cells are present on multiseriate rays, and procumbent cells become more abundant as stems increase in size. Four species from montane subequatorial highlands lack growth rings and helical sculpture in vessels; the remainder of Illicium species have these features. Notably narrow vessels and large numbers of vessels per sq. mm characterize the temperate species from northern limits for the genus, I. anisatum, I. floridanum, and I. parviflorum. Greater vessel density offers redundancy and greater safety and is correlated with greater frost and possibly greater fluctuation in moisture availability. These two ecological features are probably also related to the narrow vessel diameter, which may retard entry of air embolisms (lowered air entry values) in accord with the physiological considerations of Slatyer. Reduction of number of bars per perforation plate within Illicium is also correlated with the more northerly climates. An additional hypothesis for evolution of shorter vessel elements in dicotyledons is introduced: if, as claimed by Slatyer, air embolisms in vessels tend to stop at ends of vessel elements and thus do not disable entire vessels, shorter vessel elements would maximally localize air embolisms. Presence of helical sculpture and other forms of relief within vessels has been difficult to explain in conifers and dicotyledons; such features might help resist cavitations by increasing adhesion of water molecules to cell walls (hydration).     

Structural analysis of K<Superscript>+</Superscript> dependence in <Emphasis Type="SmallCaps">l</Emphasis>-asparaginases from <Emphasis Type="Italic">Lotus japonicus</Emphasis>

Wood is composed of various types of cells and each type of cell has different structural and functional properties. However, the temporal and spatial diversities of cell wall components in the cell wall between different cell types are rarely understood. To extend our understanding of distributional diversities of cell wall components among cells, we investigated the immunolabeling of mannans (O-acetyl-galactoglucomannans, GGMs) and xylans (arabino-4-O-methylglucuronoxylans, AGXs) in ray cells and pits. The labeling of GGMs and AGXs was temporally different in ray cells. GGM labeling began to be detected in ray cells at early stages of S₁ formation in tracheids, whereas AGX labeling began to be detected in ray cells at the S₂ formation stage in tracheids. The occurrence of GGM and AGX labeling in ray cells was also temporally different from that of tracheids. AGX labeling began to be detected much later in ray cells than in tracheids. GGM labeling also began to be detected in ray cells either slightly earlier or later than in tracheids. In pits, GGM labeling was detected in bordered and cross-field pit membranes at early stages of pit formation, but not observed in mature pits, indicating that enzymes capable of GGM degradation may be involved in pit membrane formation. In contrast to GGMs, AGXs were not detected in pit membranes during the entire developmental process of bordered and cross-field pits. AGXs showed structural and depositional variations in pit borders depending on the developmental stage of bordered and cross-field pits.     

What is disjunctive xylem parenchyma? A case study of the African tropical hardwood Okoubaka aubrevillei (Santalaceae)

The morphological variation and structure-function relationships of xylem parenchyma still remain open to discussion. We analyzed the three-dimensional structure of a poorly known type of xylem parenchyma with disjunctive walls in the tropical hardwood Okoubaka aubrevillei (Santalaceae). Disjunctive cells occurred among the apotracheal parenchyma cells and at connections between axial and ray parenchyma cells. The disjunctive cells were partly detached one from another, but their tubular structures connected them into a continuous network of axial and ray parenchyma. The connecting tubules had thick secondary walls and simple pits with plasmodesmata at the points where one cell contacted a tubule of another cell. The imperforate tracheary elements of the ground tissue were seven times longer than the axial parenchyma strands, a fact that supports a hypothesis that parenchyma cells develop disjunctive walls because they are pulled apart and partly separated during the intrusive growth of fibers. We discuss unresolved details of the formation of disjunctive cell walls and the possible biomechanical advantage of the wood with disjunctive parenchyma: the proportion of tissue that improves mechanical strength is increased by the intrusive elongation of fibers (thick-walled tracheids), whereas the symplastic continuum of the parenchyma is maintained through formation of disjunctive cells.     

圆籽荷属木材构造的研究

山茶科圆籽荷属(Apterospefma)木材为散孔材至半环孔材,管孔细,射线细,薄壁组织肉眼下不见,密度中偏大,纹理直,结构细。微观构造:在导管相互间纹孔式对列夏导管分子穿孔梯状的横栅24—77条,射线异形Ⅰ型。射线与导管问纹孔为较大不规则形单纹孔,对列,薄壁组织星散.1—2个细胞。     

Observations on the vegetative anatomy of Austrobaileya: habital, organographic and phylogenetic conclusions

For the single species of Austmbaileya (Austrobaileyaceae), quantitative and qualitative data are offered on the basis of a mature stem and a root of moderate diameter. Data available hitherto have been based on stems of small to moderate diameter, and roots have not previously been studied. Scanning electron microscope (SEM) photographs are utilized for roots, and show compound starch grains. Roots lack sclerenchyma but have relatively narrow vessels and abundant ray tissue. Recent phylogenies group Austrobaileyaceae with the woody families Illiciaceae, Schisandraceae, and Trimeniaceae (these four may be considered Illiciales), and somewhat less closely with the vesselless families Amborellaceae and Winteraceae and the aquatic families Cambombaceae and Nymphaeaceae. The vessel-bearing woody families above share vessels with scalariform perforation plates; bordered bars on plates; pit membrane remnants present in perforations; lateral wall pitting of vessels mostly alternate and opposite; tracheids and/or septate fibre-tracheids present; axial parenchyma vasicentric (sometimes abaxial); rays Heterogeneous Type I; ethereal oil cells present; stomata paracytic or variants of paracytic. Although comparisons between vessel-bearing and vesselless families must depend on fewer features, Amborellaceae and Winteraceae have no features incompatible with their inclusion in an expanded Illiciales.     

薏苡种子胚芽鞘细胞的结构

观察了薏苡浸泡种子胚芽鞘的结构。胚芽 外,内表皮薄壁组织及２个侧位的维管束组成。在外表皮两处,观察到径向壁不边原细胞群,它们实际是合胞体。薄壁细胞含丰富的核糖体,内质网小泡和线粒体,说明代谢活动已经活跃。初生纹孔场内有胞间连丝,显示胞间已存在物质的共质运转。     

Xylem of early angiosperms: Nuphar (Nymphaeaceae) has novel tracheid microstructure1

SEM studies of xylem of stems of Nuphar reveal a novel feature, not previously reported for any angiosperm. Pit membranes of tracheid end walls are composed of coarse fibrils, densest on the distal (outside surface, facing the pit of an adjacent cell) surface of the pit membrane of a tracheid, thinner, and disposed at various levels on the lumen side of a pit membrane. The fibrils tend to be randomly oriented on the distal face of the pit membrane; the innermost fibrils facing the lumen take the form of longitudinally oriented strands. Where most abundantly present, the fibrils tend to be disposed in a spongiform, three-dimensional pattern. Pores that interconnect tracheids are present within the fibrillar meshwork. Pit membranes on lateral walls of stem tracheids bear variously diminished versions of this pattern. Pits of root tracheids are unlike those of stems in that the lumen side of pit membranes bears a reticulum revealed on the outer surface of the tracheid after most of the thickness of a pit membrane is shaved away by the sectioning process. No fibrillar texturing is visible on the root tracheid pits when they are viewed from the inside of a tracheid. Tracheid end walls of roots do contain pores of various sizes in pit membranes. These root and stem patterns were seen in six species representing the two sections of Nuphar, plus one intersectional hybrid, as well as in one collection of Nymphaea, included for purposes of comparison. Differences between root and stem tracheids with respect to microstructure are consistent in all species studied. Microstructural patterns reported here for stem tracheid pits of Nymphaeaceae are not like those of Chloranthaceae, Illiciaceae, or other basal angiosperms. They are not referable to any of the patterns reported for early vascular plants. The adaptational nature of the pit membrane structure in these tracheids is not apparent; microstructure of pit membranes in basal angiosperms is more diverse than thought prior to study with SEM.