Pit Plugs Research Articles

AN EXPANDED SURVEY OF THE ULTRASTRUCTURE OF RED ALGAL PIT PLUGS1

ABSTRACTThe fine structure of pit plugs in 90 species of red algae was examined, bringing the total number of species in the continuing survey to 153. The organization of plug caps was confirmed to be a stable, predictable trait within thalli, between generations in heteromorphic life histories, and within the presently recognized orders, with one exception—the Acrochaetiales. Two forms of the outer cap were found in this group, a thin plate, as in the Nemaliales and Palmariales, and a dome, as in Batrachospermales and Corallinales. Variation of pit plug structure indicates that the Acrochaetiales are a heterogeneous assemblage and that pit plugs will be useful in reappraising their systematics. The systematic affinities of several species of uncertain affinities are clarified. Schmitziella endophloea Bornet et Batters is excluded from both orders, Corallinales and Acrochaetiales, with which it previously was allied. Although other ordinal attributions are not precluded by pit plug structure alone, pit plug structure is consistent with placement of Apophlaea sinclairii Harvey and Hildenbrandia rivularis (Liebman) J. Agardh in the Hildenbrandiales, Plagiospora gracilis Kuckuck, Schmitziella endophloea, and Wurdemannia miniata (Duby) J. Feldmann et Hamel in the Gigartinales, and Pseudorhododiscus nipponicus Masuda in the Palmariales.

MORPHOLOGY AND DEVELOPMENT OF AHNFELTIA PLICATA (RHODOPHYTA): PROPOSAL OF AHNFELTIALES ORD. NOV.1

ABSTRACTAhnfeltia plicata (Hudson) Fries, the type species of Ahnfeltia Fries, is currently assigned to the Phyllophoraceae (Gigartinales). Several morphological and biochemical characters distance A. plicata from the Phyllophoraceae but, because sexual reproduction has never been demonstrated, an alternative placement has not been possible. A. plicata now is shown to have a heteromorphic sexual life history. Erect branched gametophytes are dioecious. In male sori, spermatangia are cut off transversely from spermatangial mother cells. Female sori form numerous terminal sessile carpogonia. Following fertilization, several zygotes in each sorus fuse facultatively with undifferentiated intercalary cells of the female sorus and cut off gonimoblast initials obliquely outwards. These initials give rise to branching gonimoblast filaments that fuse with apical and intercalary female sorus cells and with each other, then grow radially outward in the compound external carposporophyte and terminate in carposporangia. Carpospores develop in culture into crustose tetrasporophytes identical to Porphyrodiscus simulans Batters. Field‐collected P. simulans tetraspores grew into erect A. plicata axes. Tetrasporangia are formed by division and enlargement of crust apical cells followed by sequential enlargement and maturation of tetrasporocytes in an erosive process. Monosporangia are formed in sori on male gametophytes. Pit plugs of both gametophyte and tetrasporophyte phases consist of naked plug cores without cap layers of membranes. Gametophytes exhibit both cell fusions and secondary pit connections whereas tetrasporophytes form cell fusions but lack secondary pit connections. On the basis of the unique female and postfertilization reproductive development and in conjunction with the pit plug structure which is unique among florideophytes, the order Ahnfeltiales, containing the family Ahnfeltiaceae, is proposed.

Primary pit connections in Compsopogon coeruleus (Balbis) Montagne (Compsopogonales, Rhodophyta)

Abstract Primary pit connections are diagnostic features of all red algae in subclass Florideophycidae but also have been reported in earlier light microscopic studies of four bangiophycidean genera (Porphyra, Bangia, Rhodochaete, and Compsopogon). Electron microscopic (EM) studies so far have confirmed the prescence of pit connections in Rhodochaete and the conchocelis stages of Porphyra and Bangia but an EM examination conducted on Compsopogon prior to this study concluded that pit connections were absent. To the contrary, we have found that pit connections are consistently located between axial cells, between axial and cortical cells and between cortical cells in Compsopogon coeruleus. The pit connections are very similar to those seen in Rhodochaete in that they are extremely small (less than 0.2 μm in diameter) and possess pit plugs which appear to lack both plug caps and cap membranes. These results indicate that the pit connections in Compsopogon and Rhodochaete are the simplest known among the red...

An investigation of cystocarp development in Gelidium pteridifolium with a revised description of the Gelidiales (Rhodophyta)

The Gelidiales possess a unique combination of characters that set them apart from all other orders of red algae. Our observations have revealed features in the development of the female reproductive system that differ from reports of previous workers. We find that in Gelidium pteridifolium nutritive filaments are initiated prior to carpogonial elongation; functional carpogonia are intercalary; a fertilized carpogonium becomes multinucleate as it cuts off gonimoblast initials; nuclei in the cortical filaments borne on the carpogonium divide and enlarge following fertilization and pit plugs break down forming channels between the carpogonium and adjoining cortical filaments; terminal gonimoblast cells first fuse with the terminal cells of nutritive filaments and later unite with the fusion cells themselves; unfused, uninucleate gonimoblast cells cut off the first carposporangia, and multinucleate fusion cells produce a second series of carposporangia later on. The auxiliary cell concept is reviewed as it has been applied to Gelidiales. We have provided a revised description of the order Gelidiales and discuss its status and possible taxonomic affinities.

ABSENCE OF CAP MEMBRANES AS A CHARACTERISTIC OF PIT PLUGS OF SOME RED ALGAL ORDERS1

ABSTRACTThe current general model of the organization of a fully developed rhodophycean pit plug includes a cap membrane associated with each end of the plug. Continuity of the plasmalemma and cap membrane results in the plug core being extracellular. However, routine ultrastructural methods have not convincingly demonstrated cap membranes in the Bangiales or the Corallinales. In this study, a variety of fixation regimes that enhance membrane contrast were used in an attempt to detect cap membranes in representatives of these two orders. Although cap membranes were readily and clearly demonstrable by these methods in a representative of an order previously known to have cap membranes, they could not be detected in members of the Bangiales or Corallinales. Should the absence of cap membranes prove to be an invariant feature of these two orders, presence or absence of cap membranes will constitute a new character for phylogenetic analysis.It is proposed that the ancestral character state of red algal pit plugs was a homogeneous plug without caps and without cap membranes.

ABSENCE OF CAP MEMBRANES AS A CHARACTERISTIC OF PIT PLUGS OF SOME RED ALGAL ORDERS1

ABSTRACTThe current general model of the organization of a fully developed rhodophycean pit plug includes a cap membrane associated with each end of the plug. Continuity of the plasmalemma and cap membrane results in the plug core being extracellular. However, routine ultrastructural methods have not convincingly demonstrated cap membranes in the Bangiales or the Corallinales. In this study, a variety of fixation regimes that enhance membrane contrast were used in an attempt to detect cap membranes in representatives of these two orders. Although cap membranes were readily and clearly demonstrable by these methods in a representative of an order previously known to have cap membranes, they could not be detected in members of the Bangiales or Corallinales. Should the absence of cap membranes prove to be an invariant feature of these two orders, presence or absence of cap membranes will constitute a new character for phylogenetic analysis.It is proposed that the ancestral character state of red algal pit plugs was a homogeneous plug without caps and without cap membranes.

Ultrastructure of the fungus Petersenia palmariae (Oomycetes) parasitic on the alga Palmaria mollis (Rhodophyceae)

Invasion of Palmaria mollis by the marine oomycete Petersenia palmariae begins with penetration of the cell wall and then the lumen of an outer cortex cell. The fungus in its vegetative phase lacks a wall but is separated from the host cytoplasm by the invaginated plasmalemmaof the host cell. By promoting fusion of host cells or by the dissolution of the host cells' pit plugs, the fungus is able to use a symplastic route to invade cells deep in the cortex and medulla of the host. In the process, a compound confluent host cell lumen is created. The deposition of a thick wall around the lobed fungal cell marks the beginning of holocarpic sporangium formation and is followed by great proliferation of the parasite's nuclei and concomitant diminution of nuclear and nucleolar size. The cytoplasm becomes parietal when a large central vacuole develops. Mastigonemes are formed in dilated endoplasmic reticulum, mitochondria become associated with nuclei, and cleavage begins. Flagella begin to form on paired basal bodies before cleavage is complete. Following a period of motility, zoospores retract and then resorb their flagella. The naked spores develop walls and the basal bodies persist as centrioles.

THE MORPHOLOGY AND DEVELOPMENT OF SOME PROMINENTLY STALKED SOUTHERN AUSTRALIAN HALYMENIACEAE (CRYPTONEMIALES, RHODOPHYTA). II. THE SPONGE‐ASSOCIATED GENERA THAMNOCLONIUM KUETZING AND CODIOPHYLLUM GRAY1

ABSTRACTThree members of the red algal family Halymeniaceae (Thamnoclonium dichotomum (J. Ag.) J. Ag., Codiophyllum flabelliforme (Sond.) Schmitz, and C. decipiens (J. Ag.) Schmitz) are investigated. All are endemic to southern and southwestern Australia, possess basal stalks of substantial size and firmness, and are consistently associated with specific sponge taxa. In each case, the sponges are bonded by collagen‐like fibrils to the host cuticle without modifying the algal tissue at the ultrastructural level. Secondary cortication and prominent growth rings occur in the stalks of all three species, and in each the pit plugs between cells become wider, more convoluted and less electron dense with increasing distance from the surface. Such pit plugs are apparently a unique attribute of the stalked Halymeniaceae. The three species share pit plug, sponge association and stalk morphological features but are not otherwise closely related, as they actually represent three distinct genera.

The structure and formation of host-parasite pit connections between the red algal alloparasiteHarveyella mirabilis and its red algal hostOdonthalia floccosa

Harveyella mirabilis is a colourless red algal alloparasite which grows on and within its photosynthetic hostOdonthalia floccosa. Cells ofHarveyella establish secondary pit connections (PCs) with other parasite cells and with cells of the host. Small, uninucleate conjunctor cells are produced by parasite cells and remain connected to them by PCs. Conjunctor cells may fuse with either an adjacent host or parasite cell, with the parasite-conjunctor cell PC becoming either a host-parasite or parasite-parasite secondary PC. Occasionally the conjunctor cell does not fuse with an adjacent cell (either host or parasite) and degenerates. The secondary pit plug which forms between a parasite cell and its conjunctor cell always develops with two structurally distinct surfaces characteristic of a host-parasite pit plug. Only if the conjunctor cell fuses with another parasite cell will the structure of the pit plug be altered to that of a parasite-parasite pit plug. Fungal hyphae also invade the region of infection, andHarveyella cells respond by producing nonfunctional conjunctor cells that grow towards adjacent hyphae. Evidence suggests that secondary PCs may be induced to form mechanically, by the physical presence of another cell, rather than in direct response to a message received from an adjacent cell. The mechanism of secondary PC formation described here is similar to that reported for the closely related alloparasiteHolmsella and may be common to a number of red algal parasitic associations.

ULTRASTRUCTURE OF EARLY DEVELOPMENT IN THE FEMALE REPRODUCTIVE SYSTEM OF POLYSIPHONIA HARVEYI BAILEY (CERAMIALES, RHODOPHYTA)1

ABSTRACTPrefertilization and immediate postfertilization development in the female reproductive branch of Polysiphonia harveyi (Bailey) was studied with the electron microscope. Results pertaining to prefertilization morphology and development are consistent with those established in earlier light microscopic studies, but several unexpected ultrastructural characteristics were discovered. The mature carpogonium was found to have double membrane‐bound vacuoles of nuclear origin and the carpogonial nucleus contained a nucleolus with a distinctive crystalline lattice. Trichogynes lacked a nucleus. Of particular interest was the discovery of a highly structured channel of smooth endoplasmic reticulum (SER) which extended uninterrupted, except for pit connections, through the carpogonial branch. It is suggested that the message of fertilization is conducted through the SER channel from the carpogonium to the support cell. Few observations were made on postfertilization branches, but evidence of direct fusion between the carpogonium and auxiliary cell was fairly conclusive. Pit plugs in the female branch were found to be of three morphological types differing by the presence and number of pit membranes. We have designated these plugs Type I–III since differential functioning was not fully ascertained. Our data suggest that pit membranes may serve to stabilize the plug and that those plugs without membranes are more readily dismantled to allow cytoplasmic continuity between cells.

RHODOPHYCEAN PIT PLUGS: AN ULTRASTRUCTURAL SURVEY WITH TAXONOMIC IMPLICATIONS

The fine structure of pit plugs was examined in 63 species of red algae representing 34 families. The number of plug cap layers was found to be a taxonomically reliable character when tested against a recent revision of the Rhodymeniales which established the order Palmariales. In a broader survey involving all the orders of red algae possessing pit plugs, three basic plug cap configurations were detected. These differ in having one, two, or no plug cap layers. Some taxa have plug caps in which the outer cap layer is greatly elaborated, however, this layer was shown to be positionally and cytochemically identical, thus probably homologous, to the outer cap layer of the typical two‐layered plug cap. The pit plug character confirms the validity of the order Palmariales and indicates that the Nemaliales and Cryptonemiales are heterogeneous assemblages. Revision of these groups along lines indicated by the plug character is supported by significant features of morphology and reproduction. These correlations lead us to propose that Rhodophysema and Coriophyllum be transferred to the Palmariales, that the Gelidiales be resurrected, that the Bonnemaisoniales (including the Naccariaceae) is deserving of recognition, that the Batrachospermaceae be raised to a higher rank which will also receive the Lemaneaceae and the Thoreaceae, and that the Corallinaceae and Hildenbrandiaceae both be raised to ordinal status.

Rhodophycean Pit Plugs: An Ultrastructural Survey with Taxonomic Implications

Rhodophycean Pit Plugs: An Ultrastructural Survey with Taxonomic Implications

A reappraisal of the cytochemical properties of rhodophycean pit plugs

The cytochemical properties of pit plugs of hoth bangiophycean and florideophycean red algae were studied using light and electron microscopic techniques. The two major structural components of the...

THE BIOLOGY OFHARVEYELLA MIRABILIS(CRYPTONEMIALES, RHODOPHYCEAE). VI. TRANSLOCATION OF PHOTOASSIMILATED14C122

ABSTRACTPulse‐chase labelling experiments demonstrate that photoassimilated14C‐bicarbonate is translocated from the host red algaOdonthalia floccosa (Esper)Falkenberg to the parasiteHarveyella mirabilis(Reinsch) Schmitz & Reinke. The primary path of translocation is from host cortical cells (the site of photoassimilation) to the erumpent parasite pustule via the zone of interdigitation. The latter is a tissue region in which rhizoidal cells ofHarveyellagrow between, and establish secondary pit plugs with medullary cells ofOdonthalia.A secondary translocation pathway occurs from isolated host cells dispersed in the pustule ofHarveyellato adjacent parasite cells.

The fine structure of the pit connections ofBatrachospermum sirodotii skuja

A new type of pit connection is described in the fresh water red algaBatrachospermum sirodotii and reported inTuomeya sp. consisting of a doughnut-shaped pit ring with a central pore that is occluded by a rivet-shaped pit plug. This structure occurs in pit connections between cells of the indeterminant axes and also cells of whorled assimilatory branches of limited growth, the pleuridia, but not between axial cells and the basal cells of the pleuridia, the periaxial cells. The pit plug and pit ring ultimately break down in pit connections of the main axis reopening the septal pore to intercellular cytoplasmic connection between vegetative axial cells. A similar breakdown of pit connections may also occur in the pleuridia. The functioning of a truncated cone-shaped network of endoplasmic reticulum in the development of the pit connection is described.

A freeze-etch study of the ultrastructure of red algal pit plugs

Freeze-etch studies indicate that the fully-formed pit plug ofPalmaria palmata consists of a homogeneous plug core, a pair of plug caps, and associated membranes. A single cap membrane separates the two layers of each plug cap and is the only membrane found between the cytoplasm and the plug core. Due to the apparent junction of the plasmalemma and cap membranes, the plug core, along with the adjacent plug cap layer on either face of the core, is entirely membrane-bounded and essentially extracellular. Fracture faces of the cap membrane bear large populations of particles which are inconspicuous due to their low profile. The plasmalemma lining the plug core from cell to cell has numerous, very obvious particles on its fracture faces, more even than does the cytoplasmic plasmalemma.

THE ULTRASTRUCTURE OF CARPOSPOROGENESIS IN THE MARINE HEMIPARASITIC RED ALGAERYTHROCYSTIS SACCATA1

SUMMARYThe ultrastructure of carposporogenesis forErythrocystis saccatais described. The fusion and gonimoblast cells contain few organelles, and chloroplasts are in a proplastid state, with pit plugs between gonimoblast cells dissolving early in development. Carpospore development may be separated into 3 stages, the first stage being characterized by the appearance of straight‐profiled dictyosomes, fibrous vesicles, and an increase of discoid thylakoids within the chloroplasts. During the second, stage the dictyosomes assume a curved profile and striped vesicles are formed by the endoplasmic reticulum. The third stage is initiated by the disappearance of striped vesicles and the appearance of straight‐profiled dictyosomes secreting vesicles with cores. Mature carpospores consist of many cored vesicles, fibrous vesicles, and floridean starch grains. A single wall layer surrounds each carpospore since the carposporangial wall becomes incorporated into a mucilaginous matrix surrounding the spores.