Plasmodesmata of brown algae

Abstract

Plasmodesmata (PD) are intercellular connections in plants which play roles in various developmental processes. They are also found in brown algae, a group of eukaryotes possessing complex multicellularity, as well as green plants. Recently, we conducted an ultrastructural study of PD in several species of brown algae. PD in brown algae are commonly straight plasma membrane-lined channels with a diameter of 10-20 nm and they lack desmotubule in contrast to green plants. Moreover, branched PD could not be observed in brown algae. In the brown alga, Dictyota dichotoma, PD are produced during cytokinesis through the formation of their precursor structures (pre-plasmodesmata, PPD). Clustering of PD in a structure termed "pit field" was recognized in several species having a complex multicellular thallus structure but not in those having uniseriate filamentous or multiseriate one. The pit fields might control cell-to-cell communication and contribute to the establishment of the complex multicellular thallus. In this review, we discuss fundamental morphological aspects of brown algal PD and present questions that remain open.

Fig. 1

General view of thallus and ultrastructure of PD in a, d Dictyota dichotoma (sporophyte, Dictyotales), a complex multicellular thallus; b, e Sphacelaria rigidula (male gametophyte, Sphacelariales), a multiseriate thallus; c, f Ectocarpus siliculosus (male sporophyte, Ectocarpales), a filamentous uniseriate thallus. TEM samples were prepared by rapid freezing/freeze substitution. Insets show the transverse views of plasmodesmata. ER-free PD penetrate the electron-dense cell wall (cw). Abbreviations: chl, chloroplast; cw, cell wall; pd, plasmodema; pm, plasma membrane; py, pyrenoid. Scale bars: 20 µm (a–c), 100 nm (d–f), 20 nm (inset of d–f)

Fig. 2

Formation of PD during cytokinesis in D. dichotoma. a Electron micrograph of cytokinesis of a meristematic epidermal cell. Cytokinesis proceeds by expansion of the membranous sacs arranged on the cytokinetic plane as patches (arrowheads). b Longitudinal view of pre-plasmodesmata (PPD) in the developing cell partition membrane. Arrowhead indicates one PPD. c Transverse view of PPD in the developing cell partition membrane. Arrowhead indicates one PPD. Abbreviations: chl, chloroplast; n, nucleus; pm, plasma membrane. Scale bars: 500 nm (a), 100 nm (b), 200 nm (c)

Fig. 3

Schematic illustration of the formation of PD in D. dichotoma (drawn from Terauchi et al. 2012). a Early stage of cytokinesis. Golgi vesicles and flat cisternae (not shown) fuse to form the membranous sac (MS). Cytokinesis proceeds by the expansion of MS (arrows). PPD formation begins in the restricted region of MS by the protrusion (arrowheads) of MS membrane from either side of MS. b Late stage of cytokinesis before the initial cell wall development. The cell partition membrane contains PPD-rich region (PR). c Mature cell wall. Plasmodesmata (PD) are clustered in the thin cell wall (CW) region as a pit field, and then the PD-free cell wall gets thickened

Fig. 4

PD distribution in several brown algae. TEM samples were prepared by chemical fixation in a, b, and by rapid freezing/freeze substitution in c, d. a Transverse view of PD (pit field) between cortex cells in Fucus distichus (sporophyte, Fucales). Inset: overview of the cell wall. The pit field is located in the center of the cell wall (arrowhead). b Transverse view of PD between cortex cells in Desmarestia ligulata (sporophyte, Desmarestiales). Note that both species show the clustering of PD (pit field) but PD frequency is different. c Transverse view of PD in Halopteris paniculata (sporophyte, Sphacelariales). d Transverse view of PD in E. siliculosus (male sporophyte, Ectocarpales). Note that in both species PD are dispersed in the septum cell wall and their frequency is quite low (arrowheads). Scale bars: 2 µm (inset of a), 200 nm (a, b), 500 nm (c, d)

Fig. 5

PD of Saccharina japonica (Laminariales). a Overview of sporophyte thallus. TEM samples were prepared by chemical fixation. Small epidermal cells (E) are seen in the upper side. Cortex cells (C) in the central part are large and highly vacuolated cells. Medulla (M) with expanded extracellular matrix is visible in the lower part. b Longitudinal view of PD between cortex cells. No desmotubule can be seen in the lumen of the plasmodesma. Membranous structures are present in the vicinity of PD (arrowheads). c, d Transverse view of PD between cortex cells. The image in d is magnified from the dotted rectangle in c. Note that three pit fields are present in the central part of the cell wall (arrowheads in d). e Transverse view of one pit field. Note that the distance between PD is almost constant. f Overview of male gametophyte thallus. TEM samples were prepared by rapid freezing/freeze substitution using culture strains. Gametophyte has uniseriate filamentous thallus. g Transverse view of PD. PD frequency is much lower than that of sporophyte and do not gather as the pit field but PD are often located near to each other (arrowheads). Abbreviations: cw, cell wall. Scale bars: 10 µm (a, f), 2 µm (c, d), 100 nm (b, e, g)