Collenchyma: a versatile mechanical tissue with dynamic cell walls

Abstract

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.

Fig. 1.

General morphology of celery collenchyma (Apium graveolens, eudicot, Apiaceae). (A) Transverse vibratome-cut section of a fresh petiole triple-stained with acridine red, chrysoidine and astra blue showing collenchyma strands in prominent abaxial ribs. Vascular bundles are positioned opposite the collenchyma strands. (B) Detail of a collenchyma strand indicated in A. (C) Transverse section of a resin-embedded petiole stained with toluidine blue showing that collenchyma accompanies the vascular bundles at the phloem side. Note that dehydration, which is required for resin embedding, resulted in a decreased thickness of the collenchyma cell walls. (D) Longitudinal resin section stained with toluidine blue showing elongated collenchyma cells and isodiametric ground parenchyma and epidermis cells. Note that most collenchyma cells are septate with thin cross-walls (inset, arrowhead). Abbreviations: c, collenchyma; p, parenchyma; e, epidermis; ph, phloem; x, xylem. Scale bars: (A) = 500 µm; B–D, D inset) = 100 µm.

Fig. 2.

Collenchyma diversity: position in the stem (A–C) and histological types (D–F). Vibratome sections triple-stained with acridine red, chrysoidine and astra blue. (A) Coprosma repens (Rubiaceae, eudicots) with a continuous peripheral layer of collenchyma. (B, C) Levisticum officinale (Apiaceae, eudicots) with collenchyma in the ribs (B) and at the phloem side of the vascular bundles (C). (D) Angular collenchyma in Plectranthus fruticosus (Lamiaceae, eudicots). Note the sub-epidermal periderm tissue. (E) Intermediate type between tangential and lacunar collenchyma in Geranium sobolifolium (Geraniaceae, eudicots). Note the many intercellular spaces (arrows). (F) Peperomia sp. (Piperaceae, basal angiosperms) with annular collenchyma. Abbreviations: c, collenchyma; p, parenchyma; pe, periderm; ph, phloem. Scale bars = 50 µm.

Fig. 3.

Schematic drawings of the most common types of collenchyma. (A) Angular collenchyma. (B) Tangential collenchyma. (C) Annular collenchyma. (D) Lacunar collenchyma. This type often occurs as an intermediate type with angular and lamellar collenchyma, in which the size of the intercellular spaces can vary from minute spaces (1) to large cavities surrounded by collenchymatous walls (2).

Fig. 4.

Structure of celery collenchyma cell walls revealed by transmission electron microscopy. (A) Transverse section of collenchyma tissue treated with dimethylsulfoxide (DMSO) to extract matrix polysaccharides showing unevenly thickened cell walls. (B) Detail of a thickened cell wall showing its lamellated structure. While the helicoidal pattern is obvious near the plasma membrane, it is dispersed in the outward direction (arrow). Note the lateral thinning of the lamellae (squared area). Abbreviations: ct, collenchyma thickenings; n, nucleus; pm: plasma membrane; pp, periplasmatic space. Reproduced with minor modifications from Vian et al. (1993) with permission from The University of Chicago Press.

Fig. 5.

Indirect immunolabelling of cell wall polysaccharides in collenchyma of elderberry (Sambucus nigra, Adoxaceae, eudicots) and tobacco (Nicotiana tabacum, Solanaceae, eudicots) with monoclonal antibodies and carbohydrate-binding modules (CBMs). (A) CBM3a, targeting crystalline cellulose, binds strongly to the collenchyma cell walls. (B) Equivalent section to (A) stained with Calcofluor White to show the full extent of cell walls. (C) Binding of the pectic homogalacturonan antibody JIM5 to all cell walls. Note stronger labelling of the inner cell wall layers of the collenchyma tissue (arrow). (D) Equivalent section to (C) stained with Calcofluor White to show the full extent of cell walls. (E) LM5, directed against pectic galactan, labels the inner layer of the collenchyma cell walls (arrow). (F) Equivalent section to (E) stained with Calcofluor White to show the full extent of cell walls. (G) Section immunolabelled with the pectic homogalacturonan-directed probe JIM5. (H, I) Weak recognition of the xyloglucan LM15 epitope (H) and its increased detection after pectate lyase pre-treatment (I). (J) Section immunolabelled with the pectic arabinan probe LM6 after pectate lyase pre-treatment. (K) Calcofluor White staining of equivalent section to (G–J) showing the full extent of cell walls. (L, M) The anti-xylan monoclonal antibodies LM10 and LM11 bind to the inner regions (arrow) of cell wall thickenings and to the outer regions (arrow) of the cell wall near the cell junctions, respectively (combined with Calcofluor White fluorescence in the insets). Abbreviations: e, epidermis; c, collenchyma; p, parenchyma. Scale bars: (A–K) = 100 µm; (L, M) = 10 µm. (A–F) are reproduced from unpublished results with kind permission of P. Knox (University of Leeds, UK); (G–K) are reproduced from Marcus et al. (2008), and (L, M) are reproduced from Hervé et al. (2009) with permission from John Wiley and Sons.

Fig. 6.

Sclerified collenchyma tissue in the petiole of Eryngium campestre (Apiaceae, eudicots). (A) Vibratome section triple-stained with acridine red, chrysoidine and astra blue showing gross anatomy. (B) Detail of (A) showing sub-epidermal sclerified collenchyma (sc) and sclerenchyma (s). (C) Unstained vibratome section. (D) Vibratome section stained with phloroglucinol/HCl to indicate lignins (red). Only the inner layer of the collenchyma cell walls is lignified. Note the glistening nature of the non-lignified collenchyma cell walls under the epidermis (arrowheads). Abbreviations: s, sclerenchyma; sc, sclerified collenchyma. Scale bars = 50 µm.