The Genetics and Cell Biology of Fertilization - Caenorhabditis Elegans: Molecular Genetics and Development - page 352

leaving the distal mitotic zone, germ cells simultaneously enter meiosis and become
committed to spermatogenesis ( Jaramillo-Lambert et al., 2007 ). After homolog
pairing, they then enter an extended period of pachytene. By mid to late pachytene,
sperm-specific proteins begin to accumulate within the developing spermatocytes.
As the most proximal spermatocytes exit pachytene, synaptonemal complexes
between the paired homologs disassemble. Then global transcription ceases as the
chromatin fully condenses and the spermatocytes enter a distinctive karyosome
stage during which the chromosomes come together in a single mass within the
still-intact nuclear envelope ( Shakes et al., 2009 ). Throughout this initial phase of
spermatogenesis, the germ-cell nuclei are only partially encased within cellular
membranes as the individual spermatocytes are syncytially connected to a common
central cytoplasmic core called the rachis. Spermatocytes transition to the meiotic
division stage of spermatogenesis as individual spermatocytes then detach from this
rachis and their microtubule organization switches from a network to a centrosome-
based pattern ( Shakes et al., 2009 ).
During the first meiotic division, 1 spermatocytes undergo a symmetrical, actin-
based (and sometimes incomplete) division to form two 2 spermatocytes. The
second round of meiotic chromosome segregation rapidly follows. Anaphase II is
followed by the transient formation of a shallow cleavage furrow, but this furrow
rapidly regresses. Cellular components unnecessary for subsequent sperm formation
accumulate in a central residual body whereas individual spermatids bud and detach
from this residual body using poorly understood, non-actin-based mechanisms of
division ( Shakes et al., 2009; Ward et al., 1981 ). Once spermatids detach from the
residual body, they undergo a rapid maturation process that includes final compac-
tion of the sperm chromatin, release of MSP from a paracrystalline assembly known
as the fibrous body into the cytosol, and docking of the sperm-specific ''membra-
nous organelles (MOs)'' with the plasma membrane ( Shakes et al., 2009; Ward et al.,
1981 ).
Although some investigators are beginning to include both residual body forma-
tion and initial events of spermatid maturation as part of ''spermiogenesis''
( Wu et al., 2010 ), within the C. elegans literature, spermiogenesis is most frequently
defined as the subsequent dramatic morphogenesis of spherical, sessile spermatids
into amoeboid, motile, fertilization-competent spermatozoa ( Shakes and Ward,
1989 ). Cellular changes include plasma membrane flow to the site of the newly
developing pseudopod, fusion of caveolae-like MOs to the cell body plasma mem-
brane, and the formation of a dynamic MSP pseudopod cytoskeleton. The entire
transition takes less than 10 min, and the formation of filopodia-like spikes precedes
the formation of fully motile pseudopods ( Shakes andWard, 1989; Singaravelu et al.,
2011 ). For male-derived spermatids, spermiogenesis occurs after ejaculation. For
hermaphrodite-derived spermatids, the process begins as they are pushed into the
spermatheca with the passage of the first oocyte ( Singson, 2006 ). In males, prema-
ture spermiogenesis is actively repressed by a protease inhibitor known as SWM-1
( Stanfield and Villeneuve, 2006 ). Unlike many other examples of morphogenetic
change, C. elegans spermiogenesis occurs without actin/tubulin cytoskeleton