View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Springer - Publisher Connector J Plant Res (2015) 128:7–15 DOI 10.1007/s10265-014-0677-4 JPR SYMPOSIUM Plasmodesmata: Function and Diversity in Plant Intercellular Communication Plasmodesmata of brown algae Makoto Terauchi · Chikako Nagasato · Taizo Motomura Received: 27 August 2014 / Accepted: 14 October 2014 / Published online: 17 December 2014 © The Botanical Society of Japan and Springer Japan 2014 Abstract Plasmodesmata (PD) are intercellular connec- Keywords Brown algae · Multicellularity · Pit field · tions in plants which play roles in various developmental Plasmodesmata · Primary plasmodesmata · Secondary processes. They are also found in brown algae, a group of plasmodesmata 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 Introduction algae are commonly straight plasma membrane-lined chan- nels with a diameter of 10–20 nm and they lack desmotu- Brown algae are multicellular photosynthetic eukaryotes bule in contrast to green plants. Moreover, branched PD that are found in marine environments. They include spe- could not be observed in brown algae. In the brown alga, cies of various sizes from microscopic to large exceeding Dictyota dichotoma, PD are produced during cytokinesis tens of meters, namely, giant kelps. In many cases, brown through the formation of their precursor structures (pre- algae have complex life cycles that include sexual dimor- plasmodesmata, PPD). Clustering of PD in a structure phism, and the alternation occurs between the sporophyte termed “pit field” was recognized in several species having and gametophyte generations (Luthringer et al. 2014; Sil- a complex multicellular thallus structure but not in those berfeld et al. 2010; Wynne and Loiseaux 1976). The two having uniseriate filamentous or multiseriate one. The pit generations are connected by asexual and sexual reproduc- fields might control cell-to-cell communication and con- tions with diverse modes. Brown algae have evolved unique tribute to the establishment of the complex multicellular systems such as a complex life cycle, during adaptation to thallus. In this review, we discuss fundamental morphologi- coastal environments. cal aspects of brown algal PD and present questions that Brown algae, together with diatoms, belong to the het- remain open. erokontophyta and to the phylum of “Stramenopiles” with other heterotrophic organisms including Oomycetes. Stra- menopiles are phylogenetically distant from the Opis- tokonts (animals and fungi) and the Archaeplastida (green plants and red algae) (Yoon et al. 2004). Brown algae M. Terauchi Graduate School of Environmental Science, Hokkaido University, evolved complex multicellularity independently of animals, Sapporo 060-0810, Japan fungi, green plants and red algae. These five multicellular e-mail: [email protected] groups have developed intercellular connections, namely gap junctions in animals (Caspar et al. 1977; Hervé and M. Terauchi Research Center for Inland Seas, Kobe University, Derangeon 2013; Kumar and Gilula 1996), septal pores Kobe 657-8501, Japan in fungi (Bauer et al. 2006; Marchant 1976; Reichle and Alexander 1965), pit plugs in red algae (Pueschel 1977; * C. Nagasato ( ) · T. Motomura Pueschel and Cole 1982) and plasmodesmata (PD) in green Muroran Marine Station, Field Science Center for Northern Biosphere, Hokkaido University, Muroran 051-0003, Japan plants (Burch-Smith et al. 2011) and brown algae (Schmitz e-mail: [email protected] and Srivastava 1974; Schmitz 1981, 1990; Terauchi et al. 1 3 8 J Plant Res (2015) 128:7–15 2012). Intercellular connections allow cell-to-cell com- evolved PD independently (Raven 2008). The similarity of munication through the transport of various molecules and molecular components between brown algal PD and those contribute to the elaboration of the complex multicellular- of green plants might be low (Cock et al. 2010; Salmon and ity (Bloemendal and Kück 2013). Bayer 2013). Structural and functional analyses of PD will In land plants, PD are plasma membrane-lined tubular give insights into how brown algae established indepen- channels with a diameter of 30–50 nm, creating symplastic dently complex multicellularity. Recently, we carried out continuity across the cell wall. Endoplasmic reticulum (ER, ultrastructural observations of PD in the brown alga Dic- desmotubule), characteristically passes through the PD tyota dichotoma (Terauchi et al. 2012). We characterized lumen. PD of land plants are categorized into two types: their detail structure and formation during cytokinesis. In unbranched “simple PD” and branched “complex PD”. this review, we summarize our current knowledge on the Molecules transported via PD include ions, small com- structure of brown algal PD and compare them with green pounds, proteins and RNA (Kim 2005). Transport of these plants. materials via PD is highly regulated and is involved in a number of developmental processes in land plants (Burch- Ultrastructure of brown algal PD and its relationship to the Smith et al. 2011). The structure of PD is much different molecular traffic from that of gap junctions of animals; these 2–4 nm wide proteinous channels facilitate the transport of small mol- All brown algae are multicellular species organized in ecules up to about 1 kDa such as ions, secondary signal- branching uniseriate and multiseriate filamentous, and ing messengers, nucleotides and metabolites (Hervé and complex multicellular thalli. For example, Dictyota dicho- Derangeon 2013; Maeda and Tsukihara 2011). Septal pores toma forms a macroscopic complex multiseriate thal- of fungi are 50–500 nm wide plasma membrane-lined lus (Fig. 1a), Sphacelaria rigidula forms a filamentous pores co-localized with peroxisome-derived vesicles or multiseriate thallus (Fig. 1b), and Ectocarpus siliculosus ER-derived septal pore caps. They contribute to the cellular forms a filamentous uniseriate thallus (Fig. 1c). Transmis- differentiation (Bauer et al. 2006; Reichle and Alexander sion electron microscopic (TEM) observations showed 1965; van Peer et al. 2010). Pit plugs of red algae consist of that vegetative cells of all species examined had ER a proteinaceous plug core occluding a pore lined by plasma (desmotubule)-free PD with an inner diameter ranging membrane in the cell wall and cap membrane covering from 10 to 20 nm and a length from 1 to several 100 nm both sides of the plug core (Pueschel and Cole 1982). The (Fig. 1d–f). Branched complex PD were never observed structure of pit plug provides significant taxonomical infor- in brown algae, in contrast to land plants. Although in one mation (Pueschel and Cole 1982). of the published figures of pores in the sieve element from In brown algae, studies on intercellular transport have Laminaria groenlandica (Fig. 18 of Schmitz and Srivas- focused on sieve elements in kelps. In some laminarialean tava 1974) it has been reported that they contain ER, the algae, the differentiation of tissues consisting of epidermal, existence of desmotubule in brown algal PD has never been cortex and medullary cells is conspicuous, and medullary described elsewhere. The occurrence of complex PD and cells (sieve elements) are functionally analogous to those desmotubule has been described in some members of bryo- of land plants. The sieve elements of brown algae are con- phytes and charophycean algae (Cook et al. 1997; Franc- tinuous to cortex cells via the complex filamentous cell net- eschi et al. 1994) but not in other green algae (Fraster and work (Schmitz 1984). The monitoring of transport of iso- Gunning 1969). It was argued that those specializations of topes (14C, 32P, 125I) showed that the long-distance transport PD occurred during the evolution toward land plants in the of photosynthetic products and iodine occurred through the green lineage (Cook et al. 1997). Ultrastructural observa- sieve elements (Amat and Srivastava 1985; Schmitz and tions of brown algal PD in vegetative cells showed that Srivastava 1975, 1979). The cross walls of sieve elements PD have similar form from simple uniseriate to complex are perforated by numerous pores, linking adjacent sieve multicellular species, while PD (diameter 10–20 nm) and elements. The diameter of the pores ranges from 37.5 nm pores of sieve elements (diameter 37.5 nm–2.6 µm) sig- to 2.6 µm (Schmitz 1990). Although smaller pores can be nificantly differ in their diameter. In Fucales and Laminari- regarded as PD, larger pores are predicted to be specialized ales, the number and size of the pores are variable among structures of PD that are formed by the enzymatic digestion species and among sieve elements from different parts or of the cross wall (Schmitz and Srivastava 1974; March- ages of the thallus, and even within one cross wall (Moss ant 1976; Schmitz 1981, 1990). The detail of the structure 1983; Schmitz and Srivastava 1974, 1976). Although struc- and the function of PD in other cell types and algal species ture may differ depending on tissue fixation method used remain obscure. (chemical fixation or cryofixation), regulation of the diam- Considering the distant evolutionary relationship eter of PD and pores may be the main determinant for between brown algae and green plants, they must have molecular transport conductance in brown algae as well as 1 3 J Plant Res (2015) 128:7–15 9 Fig. 1 General view of