Structures of Bordered Pits Potentially Contributing to Isolation of a Refilled Vessel from Negative Xylem Pressure in Stems ofMorus australisPoir.: Testing of the Pit Membrane Osmosis and Pit Valve Hypotheses

ABSTRACTPit membranes in bordered pits of tracheary elements of angiosperm xylem represent primary cell walls that undergo structural and chemical modifications, not only during cell death but also during and after their role as safety valves for water transport between conduits. Cellulose microfibrils, which are typically grouped in aggregates with a diameter between 20 to 30 nm, make up their main component. While it is clear that pectins and hemicellulose are removed from immature pit membranes during hydrolysis, recent observations of amphiphilic lipids and proteins associated with pit membranes raise important questions about drought-induced embolism formation and spread via air-seeding from gas-filled conduits. Indeed, mechanisms behind air-seeding remain poorly understood, which is due in part to little attention paid to the three-dimensional structure of pit membranes in earlier studies. Based on perfusion experiments and modelling, pore constrictions in fibrous pit membranes are estimated to be well below 50 nm, and typically smaller than 20 nm. Together with the low dynamic surface tensions of amphiphilic lipids at air-water interfaces in pit membranes, 5 to 20 nm pore constrictions are in line with the observed xylem water potentials values that generally induce spread of embolism. Moreover, pit membranes appear to show ideal porous medium properties for sap flow to promote hydraulic efficiency and safety due to their very high porosity (pore volume fraction), with highly interconnected, non-tortuous pore pathways, and the occurrence of multiple pore constrictions within a single pore. This three-dimensional view of pit membranes as mesoporous media may explain the relationship between pit membrane thickness and embolism resistance, but is largely incompatible with earlier, two-dimensional views on air-seeding. It is hypothesised that pit membranes enable water transport under negative pressure by producing stable, surfactant coated nanobubbles while preventing the entry of large bubbles that would cause embolism.

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Conifer tracheids resolve conflicting structural requirements: Data, hypotheses, questions

Journal of the Botanical Research Institute of Texas ◽

10.17348/jbrit.v11.i1.1144 ◽

2017 ◽

Vol 11 (1) ◽

pp. 123-141

Author(s):

Sherwin Carlquist

Keyword(s):

Mechanical Strength ◽

Cell Walls ◽

Surface Relief ◽

Anatomical Structure ◽

Structural Requirements ◽

Wall Strength ◽

Pit Membrane ◽

Bordered Pits ◽

Cool Temperate ◽

Solid Cell

The nature of conduction involves movement of a liquid (under tension or pressure) through a solid (cell walls necessary to direct the liquid and provide mechanical strength). The numerous consequences of the liquid/solid nature of the conductive interface in plants can be viewed as a series of conflicting requirements that are resolved by various mechanisms. For example, the types of mechanical strength conferred by thicker cell walls (latewood) run counter to optimal conduction (earlywood). Conflict resolution situations are examined with light microscopy and SEM to show in detail not merely conflicting requirements but the various types of resolution in various conifers. Abies is presented as exemplary of a cool temperate conifer with numerous aspects to earlywood/latewood structure. Tropical conifers (Araucaria) present different compromises; the riparian conifer Dacrydium guillauminii has only earlywood; the parasitic conifer Parasitaxus has only latewood. Particular conifers have only some of the features by which latewood differs from earlywood. Cell dimorphism is only one aspect of resolution of conflicting requirements; others include modifications in pit size, shape, and density; the nature of the pit membrane; the nature of the pit cavity, pit border and pit aperture; and surface relief (warty layer) of the tracheid wall. The invention of coniferous bordered pits involves a circular shape, so that tension on the margo strands is equal, and thus the pit can be closed. These factors and margo pore maximization necessitate expending a large amount of space to pits in earlywood, the strength of which is thereby lessened and must be compensated by greater wall strength in latewood. The paper concludes with a series of twenty features which represent resolutions of conflicting requirements in terms of anatomical structure. Wood physiological literature is integrated with the anatomical observations.

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STUDIES OF WOOD: I. THE CELL WALL

Canadian Journal of Research ◽

10.1139/cjr35-062 ◽

1935 ◽

Vol 12 (6) ◽

pp. 715-726 ◽

Cited By ~ 3

Author(s):

R. Darnley Gibbs

Keyword(s):

Cell Wall ◽

Enzymatic Analysis ◽

Review Of Literature ◽

Pit Membrane ◽

Bordered Pits

A brief review of literature relating to the nature of the cell wall is presented. The difficulty of separating lignin from cellulose is stressed, and attempts to effect separation by the use of mild solvents are described. The torus, pit membrane and border of bordered pits are more resistant to solution than the rest of the wall. The possibility of enzymatic analysis of the wall is noted.

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DISTRIBUTION OF PHENOLIC COMPOUNDS, PECTINS AND HEMICELLULOSES IN MATURE PIT MEMBRANES AND ITS VARIATION BETWEEN PIT TYPES IN ENGLISH OAK XYLEM (QUERCUS ROBUR)

IAWA Journal ◽

10.1163/22941932-20160143 ◽

2016 ◽

Vol 37 (3) ◽

pp. 402-419

Author(s):

Jong Sik Kim ◽

Geoffrey Daniel

Keyword(s):

Electron Microscopy ◽

Transmission Electron Microscopy ◽

Phenolic Compounds ◽

Quercus Robur ◽

Transmission Electron ◽

Pit Membrane ◽

Bordered Pits ◽

English Oak ◽

Pectin Epitopes

Although there is considerable information on the chemistry of bordered intervessel pit membranes, little is known on the pit membrane chemistry of other pit types in hardwoods. This study investigated distribution of phenolic compounds, pectins and hemicelluloses in different mature pit membranes of English oak xylem using transmission electron microscopy coupled with cytochemistry and immunocytochemistry. Mature bordered intertracheid (vasicentric)- and tracheid-vessel pits showed presence of xyloglucan and heteromannan (hemicelluloses) epitopes across the pit membrane (except for the annulus regions) with differences in amounts of epitopes between earlywood (EW) and latewood (LW). In contrast, pectin epitopes were detected only in the annulus regions of pit membranes. Unlike bordered pits, half-bordered (tracheary-parenchyma pits) and simple (parenchyma pits) pit membranes were rich in pectin epitopes but lacked heteromannan epitopes, indicating difference in pit membrane chemistry between pit types. Distribution of phenolic compounds also differed between pit types and between EW and LW. LW also showed great variations in distribution of phenolic compounds between vessels. Together, this study demonstrates that there are great variations in pit membrane chemistry between pit types and between EW and LW in English oak xylem.

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Ultrastructural observations on pit membrane alterations and associated effects in elm xylem tissues infected by Ceratocystis ulmi

Canadian Journal of Botany ◽

10.1139/b78-310 ◽

1978 ◽

Vol 56 (20) ◽

pp. 2567-2588 ◽

Cited By ~ 8

Author(s):

G. B. Ouellette

Keyword(s):

Protective Layer ◽

Cavity Formation ◽

Bordered Pit ◽

Fibrillar Material ◽

Host Cytoplasm ◽

Pit Membrane ◽

Bordered Pits ◽

Parenchyma Cells

Gradations in the degree of pit membrane alteration in tissues infected by Ceratocystis ulmi (Buism.) C. Moreau and collected at various intervals after inoculation are described. Membranes of bordered pit pairs are coated and apparently impregnated with bands or masses of osmiophilic material; this coating may be thick and stratified and the pit cavities completely occluded. Similar osmiophilic material also occurs in decreasing amounts over and within membranes of simple or half-bordered pits and within the adjacent protective layer. Various degrees of distention and cavity formation in these pit membranes are associated with the osmiophilic material. Products released into vessels from disintegrating pit membranes seem to be sparse. Host cytoplasm in contiguous parenchyma cells can have diverse reactions.Examination of specimens at various angles established the interrelationship between osmiophilic material and remnants of pit membranes. Variously oriented lamellar-like structures and a fibrillar material intermixed with a more amorphous one characterize the osmiophilic material. The significance of these observations is discussed.

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The aspiration of bordered pits in conifer wood

Proceedings of the Royal Society of London Series B Biological Sciences ◽

10.1098/rspb.1972.0057 ◽

1972 ◽

Vol 181 (1065) ◽

pp. 395-406 ◽

Cited By ~ 35

Keyword(s):

Surface Tension ◽

Hydrogen Bonding ◽

Pinus Sylvestris ◽

Growth Ring ◽

Surface Tension Force ◽

The Other ◽

Liquid Meniscus ◽

Pit Membrane ◽

Bordered Pits ◽

Conifer Wood

The variation of tension in a radial strand of a bordered pit membrane during drying has been derived theoretically from two approaches. One considers the mechanical extension of the strand, while the other considers the surface tension force caused by an annular liquid meniscus in the pit chamber. The tension has been calculated for pits in earlywood, in latewood and in regions near the earlywood-latewood boundary of a single growth ring in Pinus sylvestris L., using experimentally observed typical values for pit dimensions. The occurrence of aspiration of earlywood but not of latewood pits in air-seasoned wood is correctly predicted by the analysis, which also predicts that, contrary to accepted theory, earlywood pit membranes should be displaced and brought into contact with the pit border irrespective of the liquid present during drying. It is shown that this must involve considerable creep in the radial strands. Permanent aspiration must only occur when the liquid promotes bonding between the membrane and the border, and the probability that this is hydrogen bonding is discussed.

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Bordered Pit Aspiration in the Wood of Cryptomeria Japonica in Relation to Air Permeability

IAWA Journal ◽

10.1163/22941932-90001462 ◽

1997 ◽

Vol 18 (1) ◽

pp. 69-76 ◽

Cited By ~ 13

Author(s):

Tomoyuki Fujii ◽

Youki Suzuki ◽

Naohiro Kuroda

Keyword(s):

Moisture Content ◽

Cryptomeria Japonica ◽

Initial Moisture Content ◽

Air Permeability ◽

Heartwood Formation ◽

Permeability Measurement ◽

Air Drying ◽

Freeze Dried ◽

Pit Membrane ◽

Bordered Pits

Aspiration of bordered pits in Cryptomeria japonica (L. f.) D. Don was studied in relation to the air permeability in sapwood, transition zone wood, and heartwood. The percentage of aspirated pits relative to the total number of bordered pits with observable tori was determined in samples that were epoxy-embedded and thin sectioned. Air permeability of air-dried and freeze-dried wood samples was measured following the method described by Siau (1984). Pit membrane structure of air-dried and freeze-dried samples was investigated by scanning electron microscopy on split radial surfaces. It is proposed that pit aspiration progresses during heartwood formation as already reported, but the pit aspiration was frequently incomplete and the percentage varied between individuals. The pit aspiration percentage was not obviously related to the sample's initial green moisture content or heartwood color. The results from permeability measurement and SEM observation on air- and freeze-dried samples suggest that pit aspiration occurred in sapwood samples (the initial moisture content of which ranged from 200 to 300%) during air-drying and caused a significant decrease in permeability confirming the pit aspiration mechanism proposed by Hart and Thomas (1967). In the heartwood, encrustation of pit membranes prevented aspiration during air-drying.

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Comparative culm anatomy of metaxylem vessel pits in three different types of bamboo rhizome

IAWA Journal ◽

10.1163/22941932-00002110 ◽

2020 ◽

Vol 41 (2) ◽

pp. 141-158 ◽

Cited By ~ 1

Author(s):

Junji Luo ◽

Rong Liu ◽

Shuqin Zhang ◽

Caiping Lian ◽

Feng Yang ◽

...

Keyword(s):

Structural Parameters ◽

Bamboo Species ◽

Qualitative And Quantitative ◽

Horizontal Diameter ◽

Pit Membrane ◽

Bordered Pits ◽

Different Types ◽

Quantitative Characteristics ◽

Distribution Frequency ◽

Qualitative And Quantitative Characteristics

Abstract Not only are vessel pits vital for the passage of sap into adjacent cells, but their anatomical morphology is also used as a tool to identify bamboo species. However, detailed studies comparing the pits’ structural parameters in culms of species with three rhizome types: sympodial bamboo, amphipodial bamboo, and monopodial bamboo, are lacking. Scanning electron microscopy (SEM) observations were conducted to obtain the qualitative and quantitative characteristics of vessel pits in sympodial, amphipodial and monopodial bamboos, from twelve bamboo species in eight genera. Sympodial bamboos possess small and ovoid bordered pits, whereas amphipodial bamboos contain an abundance of slit-like pits, with the greatest pit membrane length occurring in the vessel wall. Both minute and large pit sizes can be found in monopodial bamboos. This study identified the first compound pits ever to be found in a bamboo species and these were found to occur more frequently in amphipodial and monopodial bamboos than in sympodial bamboos. Using the distribution frequency of the pit chamber’s horizontal diameter, we were able to determine pit size as being either small, medium or large. The striking differences in the vessel pits’ qualitative and quantitative characteristics could be the result of different climate and environmental factors.

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An “Ultrafilter” in the Margo of Mature Bordered Pits?

Proceedings, annual meeting, Electron Microscopy Society of America ◽

10.1017/s0424820100094280 ◽

1972 ◽

Vol 30 ◽

pp. 206-207

Author(s):

I. B. Sachs ◽

R. E. Kinney

Keyword(s):

Surface Tension ◽

Electron Microscope ◽

Molecular Sieve ◽

Pinus Strobus ◽

Postmortem Changes ◽

Sodium Chlorite ◽

Bordered Pit ◽

Pit Membrane ◽

Bordered Pits ◽

Surface Tension Forces

The micrographs illustrating this paper were obtained from never-dried springwood bordered pit-pairs of Pinus strobus L. Specimens were treated with acidified sodium chlorite in order to remove incrusting materials from the pit membrane. To prevent or reduce interfacial and surface tension forces and provide a view of bordered pit structure without postmortem changes, the specimens were further treated either by the critical point method of Weatherwax and Caulfield, a version of Anderson's method, or by a low temperature evaporation method using molecular sieve material at -40° C. to gently remove the alcohol, Arenberg, et al. For studying the pit membrane of bordered pit-pairs, neither technique seems to have an advantage, giving similar results.Light and electron microscope studies have established that structurally the bordered pit-pair membrane consists of a torus and a margo.

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Permeability and structure of the wood of Sitka spruce

Proceedings of the Royal Society of London Series B Biological Sciences ◽

10.1098/rspb.1970.0016 ◽

1970 ◽

Vol 175 (1039) ◽

pp. 149-166 ◽

Cited By ~ 31

Keyword(s):

Sitka Spruce ◽

Basic Fuchsin ◽

Flow Paths ◽

Membrane Pores ◽

Pit Membrane ◽

Bordered Pits ◽

In Series ◽

Flow Through ◽

Conifer Wood ◽

Tangential Directions

The gaseous permeability of dry Sitka spruce sapwood in the longitudinal and tangential directions has been measured at various mean pressures between 1 and 700 mmHg. From these measurements it has been shown that both the tracheid lumina and the pores in the membranes of the bordered pits make significant contributions to the total resistance to longitudinal fluid flow through the wood, and the number and equivalent radii of the conducting tracheid lumina and the pit membrane pores have been derived. The conducting tracheids have been observed directly by examination of transverse wood sections, after staining the flow -paths with reduced basic fuchsin solution. The conducting tracheids were found mainly in the latewood and their radii and number were in agreement with the values derived from permeability measurements. Direct carbon replicas of bordered pit membranes have been examined in the electron microscope. Unaspirated, i. e. conducting bordered pits were found only in the latewood region and the size and number of the pores in the latewood pit membranes were in agreement with values derived from permeability measurements, which predicted about 250 pit membrane pores of radius 0.14 μ m in series with each conducting tracheid lumen. The effect of a possible distribution of pore size on the results is considered, and the significance of this work in relation to previous work on the gaseous permeability of conifer wood is discussed.

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