Microtubule organizing centers and the origin of centrioles during spermatogenesis in the pteridophyte Phylloglossum.

Abstract

Spermatogenesis in the lycophyte Phylloglossum is characterized by profound ultrastructural changes that involve complex microtubule arrays and discrete microtubule organizing centers (MTOCs). The first visible MTOC is an electron-opaque acentriolar centrosome that organizes the mitotic spindles in late spermatogeneous cells. In the spermatid mother cell, centrioles arise de novo within the pericentriolar matrix of the MTOC. Approximately 20 centrioles, which ultimately function as basal bodies, originate in each of two branched "blepharoplasts." Constituent centrioles of each organelle radiate from a central region where they are interconnected by cartwheel cylinders, each with nine-fold symmetry. The development and structure of this novel centriolar-generating organelle suggests a direct evolutionary link with the bicentriole of other lycophytes, and are consistent with the concept that multiflagellated spermatozoids in Phylloglossum evolved independently of those in other pteridophytes. During spermiogenesis, two additional structurally defined MTOCs organize the ton and locomotory apparatus, which comprises 20 staggered flagella over a multilayered structure. An MTOC that overlies the multilayered structure and consists of a cloud of electron-opaque material is involved in repositioning basal bodies and generating flagella. The spline, a band of up to 200 microtubules, provides the architectural framework for development and maintenance of cell shape and is organized by the lamellar strip, a highly structured MTOC. Microtubule arrays during spermatogenesis in Phylloglossum are diverse and include mitotic, cytokinetic, cytoskeletal, and locomotory assemblages. MTOCs responsible for the nucleation and organization of these arrays are among the most elaborate and morphologically distinct of any described in land plants.