Architecture of the sperm cell of Psilotum

Abstract

In this correlated SEM (scanning electron microscope) and TEM (transmission electron microscope) investigation, we describe architectural details of the multiflagellated sperm cell of Psilotum nudum. Comparisons with other pteridophytes are made to (1) assess the placement of Psilotum among pteridophyte taxa and (2) evaluate structural modifications of sperm cells during land plant evolution. The released spermatozoid of Psilotum coils 2.0 revolutions and is outlined by a parallel band of up to 190 microtubules. The elongated nucleus is highly compacted and parallels the cellular coils with numerous mitochondria and starch-laden plastids distributed along its length. Along the anterior coil is an elaborate locomotory apparatus that includes ∼36 flagella that are inserted into the cell by basal bodies. Subtending the basal bodies is the multilayered structure, which consists of a long narrow lamellar strip and an overlying band of microtubules. An elongated anterior mitochondrion underlies the multilayered structure. Additional amyloplasts and mitochondria are aggregated along the anterior coil in association with the locomotory apparatus, while a fibrous band encircles the leading edge of the cell. Salient features of this cell, including details of the locomotory apparatus, structure and position of organelles, and arrangement of the spline, are shared by spermatozoids of Equisetum and ferns (including eusporangiate and leptosporangiate taxa). Thus, this study provides morphological support for the hypothesis that Psilotum nudum is a member of an assemblage that includes ferns and Equisetum. However, the less streamlined architecture of Psilotum gametes and the lack of architectural features shared with any specific taxon examined to date suggest that Psilotum is an early divergent fern, with relatively remote affinities to Ophioglossaceae and Equisetaceae.

Motile Gametes of Land Plants: Diversity, Development, and Evolution

“…The upper row of basal bodies inserts into the striated portion ( Figures 27G, 28B). In Psilotum, the band contains irregular fibers that become less distinct as the sperm cell matures (Renzaglia et al, 2001a). Electron-dense bands and plaques also overlie the MLS in sperm cells of Selaginella and Isoëtes ( Figure 32B) , and they may be composed of the same material that constitutes the granular matrix around the basal bodies in Lycopodiaceae (Maden et al, 1997).…”

“…Most of these have a fibrous substructure and have been referred variously to as osmiophilic ridges, osmiophilic crests (Duckett, 1975a;Kotenko, 1990), flagellar bands Myles and Hepler, 1977), and fibrous bands (Renzaglia et al, , 2001a. Because these bands are electron-opaque even without osmication, we avoid the use of the word osmiophilic in reference to them.…”

“…Flagellar number varies from 36 to 40 in Psilotum, Botrychium, and Angiopteris to 54 to 80 in Equisetum to 60 to 150 in leptosporangiate ferns. Gyres range from two revolutions in Psilotum (Figure 9) to 10 in the water fern Marsilea ( Figure 2F) Renzaglia et al, 2001a). The locomotory apparatus extends around the anterior cellular coil(s) and overlaps to varying degrees with the nucleus.…”

“…In moss and liverwort sperm cells this asymmetry is more or less restricted to the locomotory assemblage where a marked difference between the two basal bodies results in the insertion of one flagellum into the cell anterior and the second flagellum as much as one-half revolution further posterior on the cell (Figures 2E, 4C, D, 5B) (Bernhard and Renzaglia, 1995) (see section on Basal Bodies). Asymmetry in motile gametes of pteridophytes, especially ferns, is evident in virtually every cellular component (Figures 6 to 12) (Renzaglia et al, , 2001a.…”

Tolerance to environmental desiccation in moss sperm

“…The majority of research previously conducted on moss sperm focused on sperm architecture and the composition of the sperm mass (Paolillo, 1977(Paolillo, , 1979(Paolillo, , 1981Bernhard & Renzaglia, 1995;Renzaglia et al, 2001), the mechanism of initial sperm release (Paolillo, 1975), and the behavior of the released sperm mass upon encountering the air-water interface (Muggoch & Walton, 1942;Paolillo, 1981). Working forward from these studies in combination with what we know about the daily stresses of many mosses, it seems pertinent to investigate the effects of stress on the reproductive cycle of mosses.…”