Collenchyma: a versatile mechanical tissue with dynamic cell walls

Background

Collenchyma has remained in the shadow of commercially exploited mechanical tissues such as wood and fibres, and therefore has received little attention since it was first described. However, collenchyma is highly dynamic, especially compared with sclerenchyma. It is the main supporting tissue of growing organs with walls thickening during and after elongation. In older organs, collenchyma may become more rigid due to changes in cell wall composition or may undergo sclerification through lignification of newly deposited cell wall material. While much is known about the systematic and organographic distribution of collenchyma, there is rather less information regarding the molecular architecture and properties of its cell walls.

Scope and conclusions

This review summarizes several aspects that have not previously been extensively discussed including the origin of the term ‘collenchyma’ and the history of its typology. As the cell walls of collenchyma largely determine the dynamic characteristics of this tissue, I summarize the current state of knowledge regarding their structure and molecular composition. Unfortunately, to date, detailed studies specifically focusing on collenchyma cell walls have not been undertaken. However, generating a more detailed understanding of the structural and compositional modifications associated with the transition from plastic to elastic collenchyma cell wall properties is likely to provide significant insights into how specific configurations of cell wall polymers result in specific functional properties. This approach, focusing on architecture and functional properties, is likely to provide improved clarity on the controversial definition of collenchyma.     

Immunolocalization of a plant glutathione peroxidase-like protein

We report on the localization of GPXle-1, a plant glutathione peroxidase (GPX)-like protein, in the internode of Lycopersicon esculentum Mill. GPXle-1 was detected in the cytoplasm near to the plasma membrane of trichomes, in the wall of collenchyma and in both the cytoplasm and wall of vascular tissues. GPXle-1 was not found in the epidermis or parenchyma. After mechanical stimulation, a change in its cell distribution was recorded. In stimulated plants, GPXle-1 was detected throughout the cytoplasm in the epidermis, collenchyma and cortical parenchyma.Abbreviations GPX Glutathione peroxidase - ROS Reactive oxygen species     

Detection of hemicelluloses specific to the cell wall of tracheary elements and phloem cells by fluorescein-conjugated lectins

Summary Binding of fluorescein-conjugated wheat-germ agglutinin (F-WGA) and some other lectins to tissues from various plants were examined by epifluorescence microscopy. F-WGA bound specifically to the walls of tracheary elements (TEs) and phloem cells of pea roots. The binding sites in TEs were localized only in the secondary thickening and became evident at very early stages of differentiation. Fluorescein-conjugated derivatives ofSolanum tuberosum lectin,Lycopersicon esculentum lectin, andDatura stramonium lectin, which bind N-acetylglucosamine residues as WGA, also bound to the secondary thickening of TEs of pea roots. The binding sites for F-WGA were not removed by extraction with hot EDTA and proteinase K, but removed by extraction with an alkali solution. The alkali-extracted binding sites from the roots were precipitated together with hemicelluloses by 80% ethanol. These results indicate that the binding sites are not present on pectins, proteins, or cellulose, but hemicelluloses. Localized distribution of the binding sites for F-WGA in TEs was found also in a variety of angiosperm plants.Abbreviations BSL-II Bandeiraea simplicifolia lectin II - DSL Datura stramonium lectin - F fluorescein-conjugated - LEL Lycopersicon esculentum lectin - MT microtubule - STL Solanum tuberosum lectin - TE tracheary element - WGA wheat-germ agglutinin     

Interaction between 2,4-Dichlorophenoxyacetic Acid and Vitamin K in Datura stramonium

Plants of the cross Datura stramonium L. var. stramonium×Datura stramonium L. var. inermis (Juss. ex Jacq.) Timm. were sprayed either with a water solution of the sodium salt of 2,4-dichlorophenoxyacetic acid (2,4-D) or with a combination of 2,4-D (sodium salt) and the vitamin K compound menadione sodium bisulfite in water solution. The plants were found to differ in one of their responses to the treatments, namely the development of necrotic spots on the leaf blades. Many necroses appeared on the plants treated with 2,4-D plus menadione sodium bisulfite while only a few necroses or none at all developed on the plants treated with 2,4-D alone. Furthermore, 2,4-D in combination with menadione sodium bisulfite induced much larger necrotic spots than did 2,4-D by itself. Spraying with menadione sodium bisulfite in water solution did not produce any observable effects upon Datura plants. The great increase in necrotic lesion formation was probably due to an interaction between 2,4-D and menadione sodium bisulfite (or a metabolite of this compound) within leaf cells.     

DETERMINANTS OF OUTCROSSING RATE IN A PREDOMINANTLY SELF-FERTILIZING WEED,DATURA STRAMONIUM (SOLANACEAE)

We measured outcrossing rates of several North Carolina populations of the annual weed Datura stramonium including both natural populations and experimental populations in which we manipulated plant spatial arrangement. Because capsules of D. stramonium typically produce hundreds of seeds and we used an easily scored genetic marker for flower and hypocotyl color, we could measure outcrossing rates accurately for both individual plants and single flowers. The population-wide estimates of outcrossing rates were surprisingly low for a species with showy, entomophilous flowers and ranged from 1.9% in an experimental population with a “clumped” spatial arrangement to 8.5% in an experimental population with a “dispersed” arrangement. These low values were not produced by pollinator discrimination among flower color morphs, as determined by outcrossing measurements on test plants of different colors and by direct observations of pollinator behavior. For individual plants and single flowers in the experimental populations, variation in outcrossing rates was significantly affected by such population-wide characteristics as plant spatial arrangement and nightly fluctuations in total floral abundance. However, by far the most important factor was stigma position. Flowers with stigmas above the anthers had significantly higher outcrossing rates than did flowers with overlapping stigma and anthers. The strong effect of floral morphology suggests that the very low population-wide levels of outcrossing in D. stramonium may represent a persistent mixing mating system rather than a transition to complete selfing.     

STRUCTURAL SPECIALIZATION OF THE SITE OF RESPONSE TO VECTORIAL PHOTO-EXCITATION IN THE SOLAR-TRACKING LEAF OF LAVATERA CRETICA

Structural features of the pulvinus of the solar-tracking leaf of Lavatera cretica L. that are involved in its capacity for omnidirectional and fully reversible bending in response to vectorial excitation of the lamina were studied by light- and scanning electron microscopy. Pulvini that had bent in the plane at right angles to the midvein were bisected along that plane and the symmetrical tissues of the expanded and contracted flanks were compared. The pulvinus contains a central vascular core and exhibits a transversely furrowed exterior. These specialized features enable the fully mature tissue of this region of the petiole to bend reversibly. The epidermis, chlorenchyma, peripheral collenchyma, and cortical parenchyma in the pulvinus form concentric, radially symmetric sheaths around the vascular core and exhibit structural features in their cell walls that would allow considerable changes in cell volume and consequently enable the omnidirectional bending of this pulvinus. Thickened wall portions of the pulvinar epidermis and peripheral collenchyma exhibit a highly specialized architecture, consisting of alternating thick and thin strips, that enhances their flexibility, while maintaining mechanical support. Cell walls of the chlorenchyma and the cortical parenchyma are thin and capable of reversible infolding. Those of the cortical parenchyma also exhibit numerous prominent transverse pit fields, indicative of anisotropic orientation of their microfibrillar lattice transverse to the pulvinar axis. This orientation is compatible with elastic deformation of the cortical parenchyma cells along the pulvinar axis. Filament-like cytoplasmic strands were observed along the walls of pulvinar motor cells, predominantly transverse to the pulvinar axis, but their function (if any) in volume changes of these cells is unknown.     

Primary effects of allelochemicals ofDatura stramonium L.

Summary Alkaloids leached from seed ofDatura stramonium were identified as scopolamine and hyoscyamine and levels leached from seed over a seven day period were quantified. Scopolamine is known to inhibit early seedling growth of some crop plants. The hypothesis that such inhibition results from interference with gibberellin-stimulated food reserve metabolism in germinating seedlings was tested, using barley and wheat in bioassays. Seedling growth of both cereals was inhibited by scopolamine but no evidence of interference with responses to gibberellins was obtained.     

空心莲子草茎的解剖结构对不同水湿生境的适应研究

研究了空心莲子草茎的解剖结构对水分变化的适应,这些空心莲子草生活在因水分差异而形成的3种生境类型中。对茎表蜡质层厚度、髓腔面积/髓部面积、厚角细胞层数、厚角细胞壁厚、韧皮纤维束数、韧皮纤维壁厚、导管束数、导管腔大小8个结构参数的分析结果表明:茎的全部结构参数随水分条件的变化都有显著或极显著的差异,其趋异程度的大小顺序是,导管腔大小>厚角细胞壁厚>蜡质层厚度>髓腔面积/髓面积>韧皮纤维细胞壁厚>韧皮纤维束数>厚角细胞层数>导管束数;水分变化对机械组织细胞壁结构影响较大,而对细胞数量的影响较小;茎的结构在旱生生境中变异较大,保证了它对不均一环境的适应;空心莲子草茎的结构既具有旱生性特点又具有水生性特点,其结构究竟朝哪个方向发展,取决于环境水分条件。从茎的结构上看,治理该种应以限制其导管腔和髓腔分化为主要手段。     

Activité néformatrice d'acides ribonucléiques extraits de tumeurs végétales

RNAs extracted from crown-gall tumors, induced by Agrobacterium tumefaciens (strain B6) on stems of Datura stramonium L., have been isolated by the phenol method and purified through Biogel P 60 columns. These RNAs have been transformed into complexes with l -amino acids by incubation in a medium containing: Tris HCI buffer, pH 7.6, ATP, MgCl₂, a mixture of l -amino acids and a polypeptide synthetase purified from Alcaligenes faecalis. The inoculation of stems of Datura plants with these complexes induces the development of nodular outgrowths, whereas other complexes made from RNAs isolated from healthy Datura plants, from Agrobacterium tumefaciens, Escherichia coli and Alcaligenes faecalis do not cause any hyperplasia under our experimental conditions. The analysis of the results obtained, supported by histological studies of the outgrowths, suggests that these neoformations should be of tumoral nature.     

Immunolocalization of LeAGP-1, a modular arabinogalactan-protein, reveals its developmentally regulated expression in tomato

 Arabinogalactan-proteins (AGPs) are highly glycosylated cell surface proteins that are thought to function in plant growth and development. The developmentally regulated expression of LeAGP-1, a novel and major AGP in tomato, was examined in different organs and tissues of tomato (Lycopersicon esculentum Mill. cv. UC82B) plants with an anti-peptide antibody (i.e. the PAP antibody) directed specifically against the lysine-rich subdomain of the LeAGP-1 core protein. During cell differentiation in tomato plants, LeAGP-1 was associated with cell wall thickening and lignification of particular cell types. Specifically, LeAGP-1 was detected in secondary wall thickenings of maturing metaxylem and secondary xylem tracheary elements in roots and stems, and in thickened cell walls of phloem sieve elements. However, LeAGP-1 was also present in thin-walled, cortical parenchyma cells of seedling roots as well as thick-walled collenchyma cells in young stems, both of which are not lignified. Based on these observed patterns, possible roles for LeAGP-1 in plant growth and development are discussed. Received: 17 August 1999 / Accepted: 7 October 1999     

Mycorrhizal colonization does not affect tolerance to defoliation of an annual herb in different light availability and soil fertility treatments but increases flower size in light-rich environments

Heterogeneous distribution of resources in most plant populations results in a mosaic of plant physiological responses tending to maximize plant fitness. This includes plant responses to trophic interactions such as herbivory and mycorrhizal symbiosis which are concurrent in most plants. We explored fitness costs of 50% manual defoliation and mycorrhizal inoculation in Datura stramonium at different light availability and soil fertility environments in a greenhouse experiment. Overall, we showed that non-inoculated and mycorrhiza-inoculated plants did not suffer from 50% manual defoliation in all the tested combinations of light availability and soil fertility treatments, while soil nutrients and light availability predominately affected plant responses to the mycorrhizal inoculation. Fifty percent defoliation had a direct negative effect on reproductive traits whereas mycorrhiza-inoculated plants produced larger flowers than non-inoculated plants when light was not a limiting factor. Although D. stramonium is a facultative selfing species, other investigations had shown clear advantages of cross-pollination in this species; therefore, the effects of mycorrhizal inoculation on flower size observed in this study open new lines of inquiry for our understanding of plant responses to trophic interactions. Also in this study, we detected shifts in the limiting resources affecting plant responses to trophic interactions.     

Isolation and characterization of three new PGPR and their effects on the growth of Arabidopsis and Datura plants

This study characterizes three bacterial strains isolated from plant rhizospheres and evaluates their performance as plant-growth-promoting rhizobacteria. Pseudomonas plecoglossicida strain Pp20 was isolated from the rhizosphere of a date palm in Bechar (Algerian Sahara), Bacillus spec. strain Bt04 isolated from the rhizosphere of pear in Ghardaia (Algerian Sahara) and Lysinibacillus fusiformis strain Lf89 was isolated from the rhizosphere of tomato in Ain Defla (northern Algeria). Their effects on plant growth and development were analyzed in different in vitro cultures: an Arabidopsis thaliana plate assay and two hydroponic systems for Datura stramonium and Datura tatula. Our results show that all strains significantly improve plant growth of the plant species tested and some strains produce a shift in the C/N ratio in A. thaliana. Inoculation had no effect on alkaloid production per gram leaf dry weight in D. stramonium, but specific plant-growth-promoting rhizobacteria interactions may alter the alkaloid composition in the shoot.     

DEVELOPMENTAL ANATOMY OF THE STEM OF WELFIA GEORGII,IRIARTEA GIGANTEA,AND OTHER ARBORESCENT PALMS: IMPLICATIONS FOR MECHANICAL SUPPORT

Changes in stem anatomy with radial position and height were studied for the arborescent palms Welfia georgii, Iriartea gigantea, Socratea durissima, Euterpe macrospadix, Prestoea decurrens, and Cryosophila albida. Vascular bundles are concentrated toward the stem periphery and peripheral bundles contain more fibers than central bundles. Expansion and cell wall thickening of fibers within vascular bundles continues throughout the life of a palm, even in the oldest tissue. Within individual vascular bundles, the fibers nearest the phloem expand first and fiber cell walls become heavily thickened. A front of expanding fibers moves outward from the phloem until all fibers within a vascular bundle are fully expanded and have thick cell walls. Peripheral vascular bundles differentiate first and inner bundles later. In the stem beneath the crown, vascular bundles and ground tissue cells show little or no size increase, but marked cell wall thickening during development for Welfia georgii. Beneath the crown, diameters of peripheral vascular bundles increase more than twofold for Iriartea gigantea, while diameters of central bundles do not increase. In Iriartea stems, ground tissue cells at the periphery elongate to accommodate expanding vascular bundles and cell walls become thickened to a lesser degree than in fibers; central ground tissue cells elongate markedly, but cell walls do not become thickened; and large lacunae form between central parenchyma cells. For Iriartea, Socratea, and Euterpe, sustained cell expansion results in limited, but significant increases in stem diameter. For all species, sustained cell wall thickening results in dramatic increases in stem stiffness and strength.     

Somatic hybrids of Datura innoxia Mill.+Datura discolor Bernh. and of Datura innoxia Mill.+Datura stramonium L. var tatula L.

Summary Following fusion of protoplasts from a chlorophyll-deficient diploid mutant of Datura innoxia Mill. which can be regenerated to shoots, with green wild-type protoplasts of Datura stramonium L. var. tatula L. which can not, it was possible to isolate 49 green hybrid calli on agar medium. Most of these somatic hybrid calli gave rise to leaves and shoots. The chromosome numbers of the somatic hybrids were determined: 15 were tetraploid (amphidiploid), 24 hexaploid, and the other showed an aneuploid chromosome number.In a similar experiment protoplasts of the Datura innoxia mutant were fused with green wild-type protoplasts of Datura discolor Bernh. which are also not able to be regenerated, four green calli were obtained from which leaves and shoots developed after some transfers on agar medium. Three of them showed the amphidiploid (48) chromosome number, whereas one possessed an aneuploid number of 46 chromosomes.After transfer of rooted shoots to soil flowering plants could be obtained in both combinations. The habits of the somatic hybrids in both combinations were intermediate between the habits of the respective parental plants.Dedicated to my father, Prof. Dr. Theodor Schieder, on the occasion of his 70th birthday.     

STEM ABSCISSION IN TUMBLEWEEDS OF THE CHENOPODIACEAE: KOCHIA

Anatomical, histochemical, and mechanical studies indicated the presence of a highly modified and weakened stem base in Kochia scoparia L. Schrader. This base, the abscission zone, is the site for stem abscission. In autumn progressive desiccation of the plant is accompanied by the gradual loss of stem flexibility and concomitant increase in rigidity. The tissues of the stem remain relatively tough, but abscission zone tissues become very brash or brittle. When conditioned plants are stressed by winds, the stem acts as a moment arm, and large stresses are generated in the abscission zone. Rupture then occurs across the stem base, often abruptly. Strength tests indicated that breakage occurred with 40% less stress if a soil-inhabiting fungus (Rhizoctonia sp.) had degraded the nonlignified cell wall components of the abscission zone. Abscission, therefore, is caused by the wind, an external driving variable, but tissue desiccation, changes in anatomy, and decay are internal, preparatory variables.     

THE ULTRASTRUCTURAL CYTOLOGY OF THE DIFFERENTIATING GUARD CELLS OF VIGNA SINENSIS

Structural differentiation of the guard cells of Vigna sinensis results from the integration of the following interrelated processes: a) intense activity of ribosomes, dictyosomes, endoplasmic reticulum (ER) membranes and mitochondria and patterned organization of microtubules; b) unequal thickening and ordered micellation of their walls and opening of the stomatal pore; and c) the divergent differentiation of the plastids. In differentiating guard cells, microtubules appear anticlinally oriented and more or less evenly distributed along the unthickened part of the dorsal wall and in the middle part of the ventral wall where thickening of the future pore occurs. In periclinal walls, microtubules fan away from the margins of the increasing thickening of the ventral wall and, later, from the rims of the stomatal pore towards the dorsal walls, parallel to the depositing radial microfibrils. Microtubules may be the cytoplasmic elements underlying guard-cell morphogenesis. Although cell-plate organization in guard-cell mother cells does not seem to differ from that of other protodermal cells, the middle lamella of the ventral wall becomes electron-translucent. The stomatal pore develops schizogenously from the internal and/or external ends of the ventral wall and proceeds inwards, remaining incomplete in most of the stomata of plants grown for 30 days in darkness and in some malformed ones which were developed after a prolonged action of colchicine. The guard cell, when approaching maturity, loses its organelle complexity and plasmodesmata, but it keeps a significant portion of its cytoplasm and organelles. Perigenous stomata generally exceed the size of mesoperigenous and mesogenous ones, develop large vacuoles and appear able to induce oriented divisions in their vicinity.     

Activity of allelochemicals ofDatura stramonium L. (Thorn-apple) in contrasting soil types

Summary Alkaloids washed from the seeds ofDatura stramonium inhibited the early gowth ofHelianthus annuus in Black Earth and Lateritic Podzolic soils. Under laboratory conditions, the magnitude of the inhibition was greater in the Lateritic Podzolic than the Black Earth soil. Phytotoxicity ofD. stramonium alkaloids persisted for 20 weeks in Lateritic Podzolic soil under controlled conditions, and for eight months in aD. stramonium-infested Black Earth soil in the field.     

THE FINE STRUCTURE OF DIFFERENTIATING XYLEM ELEMENTS

Differentiating xylem elements of Avena coleoptiles have been examined by light and electron microscopy. Fixation in 2 per cent phosphate-buffered osmium tetroxide and in 6 per cent glutaraldehyde, followed by 2 per cent osmium tetroxide, revealed details of the cell wall and cytoplasmic fine structure. The localized secondary wall thickening identified the xylem elements and indicated their state of differentiation. These differentiating xylem elements have dense cytoplasmic contents in which the dictyosomes and elements of rough endoplasmic reticulum are especially numerous. Vesicles are associated with the dictyosomes and are found throughout the cytoplasm. In many cases, these vesicles have electron-opaque contents. "Microtubules" are abundant in the peripheral cytoplasm and are always associated with the secondary wall thickenings. These microtubules are oriented in a direction parallel to the microfibrillar direction of the thickenings. Other tubules are frequently found between the cell wall and the plasma membrane. Our results support the view that the morphological association of the "microtubules" with developing cell wall thickenings may have a functional significance, especially with respect to the orientation of the microfibrils. Dictyosomes and endoplasmic reticulum may have a function in some way connected with the synthetic mechanism of cell wall deposition.     

The effect of inbreeding on defence against multiple enemies in Datura stramonium

The ability of plants to respond to natural enemies might depend on the availability of genetic variation for the optimal phenotypic expression of defence. Selfing can affect the distribution of genetic variability of plant fitness, resistance and tolerance to herbivores and pathogens. The hypothesis of inbreeding depression influencing plant defence predicts that inbreeding would reduce resistance and tolerance to damage by natural enemies relative to outcrossing. In a field experiment entailing experimentally produced inbred and outcrossed progenies, we assessed the effects of one generation of selfing on Datura stramonium resistance and tolerance to three types of natural enemies, herbivores, weevils and a virus. We also examined the effect of damage on relative growth rate (RGR), flower, fruit, and seed production in inbred and outcrossed plants. Inbreeding significantly reduced plant defence to natural enemies with an increase of 4% in herbivore damage and 8% in viral infection. These results indicate inbreeding depression in total resistance. Herbivory increased 10% inbreeding depression in seed number, but viral damage caused inbred and outcrossed plants to have similar seed production. Inbreeding and outcrossing effects on fitness components were highly variable among families, implying that different types or numbers of recessive deleterious alleles segregate following inbreeding in D. stramonium. Although inbreeding did not equally alter all the interactions, our findings indicate that inbreeding reduced plant defence to herbivores and pathogens in D. stramonium.     

THE TRANSITION FROM FILAMENTOUS TO TWO-DIMENSIONAL GROWTH IN FERN GAMETOPHYTES. I. THE REQUIREMENT FOR PROTEIN SYNTHESIS IN GAMETOPHYTES OF PTERIDIUM AQUILINUM

Two-dimensional (2-D) development of gametophytes of Pteridium aquilinum was estimated by the percentage of plants with at least one cell wall at an oblique angle, relative to the long axis. Inhibition of cell division per se was assayed by counting the cell number per filamentous (1-D) gametophyte. Specific concentrations of 8-azaguanine, 5-fluorouracil, p-fluorophenylalanine, actinomycin D, streptomycin, and cycloheximide were found to selectively inhibit 2-D development. A reduction in the percentage of 2-D gametophytes was accompanied by a reduction in the relative protein content (protein per dry weight). A comparable association was found only during the initial stages of 2-D development; after 5 days the relative protein content decreased as the percentage of 2-D gametophytes increased. Different intensities of white light resulted in a 10-fold difference in the percentage of 2-D plants with no alteration of the relative protein content. These results demonstrate that no strict relationship between 2-D development and relative protein content occurred in these gametophytes.