Spermiogenesis in the fern Marsilea: Microtubules, nuclear shaping, and cytomorphogenesis

Abstract

Spermiogenesis in Marsilea is a complex series of events, including the formation of a helically wound organelle coil. The coil begins to appear in early development when a multilayered structure (MLS) is formed de novo in association with a mitochondrion. The outermost layer of the MLS is a ribbon of microtubules. As the microtubules grow out from the MLS, they grow along the nuclear envelope. The nucleus elongates parallel to the longitudinal axis of the microtubule ribbon until it makes 4‐5 gyres. The coil mitochondrion associated with the MLS grows until it completes approximately 9 gyres, following the path of the nucleus in its posterior gyres. The microtubule ribbon is associated with both of these organelles along their exterior edge and separates them from the developing flagellar band. This band arises from dense material that is associated with the basal bodies from early development, increases in volume, and finally condenses into a solid band, interconnecting the 100‐120 basal bodies of the sperm. The flagella are distributed along the entire organelle coil. Besides the microtubules of the ribbon, a set of cytoplasmic tubules is seen during spermiogenesis. These microtubules radiate in bundles from a region of dense nodules located near the MLS. Late in development there is a gross rearrangement of the cytoplasm. This rearrangement begins as the outgrowth of a ring of cytoplasm from the posterior end of the sperm, and continues to grow down around the organelle coil in the anterior end, and fuses to form a bridge, enclosing the anterior end and all the flagella. This bridge fills with cytoplasm that migrates from the posterior region, including many mitochondria and ribosomes, and is finally shed by the sperm when it is released from the microspore and becomes motile. The possible involvement of chromatin condensation and/or microtubules in nuclear morphogenesis is considered. Because much of the shaping of the nucleus occurs before bulk chromatin condensation, the possibility that it is the cause of shaping is ruled out. We postulate that microtubules are involved, not in providing the mechanical force, but as a guide along which shape formation occurs. Furthermore, microtubules of the ribbon were observed to have a close structural relationship to the condensing chromatin.