Cytoskeletal variations in an asymmetric cell division support diversity in nematode sperm size and sex ratios

Abstract

Asymmetric partitioning is an essential component of many developmental processes. As spermatogenesis concludes, sperm are streamlined by discarding unnecessary cellular components into cellular wastebags called residual bodies (RBs). During nematode spermatogenesis, this asymmetric partitioning event occurs shortly after anaphase II, and both microtubules and actin partition into a central RB. Here, we use fluorescence and transmission electron microscopy to elucidate and compare the intermediate steps of RB formation in , sp. SB347 (recently named ) and related nematodes. In all cases, intact microtubules reorganize and move from centrosomal to non-centrosomal sites at the RB-sperm boundary whereas actin reorganizes through cortical ring expansion and clearance from the poles. However, in species with tiny spermatocytes, these cytoskeletal changes are restricted to one pole. Consequently, partitioning yields one functional sperm with the X-bearing chromosome complement and an RB with the other chromosome set. Unipolar partitioning may not require an unpaired X, as it also occurs in XX spermatocytes. Instead, constraints related to spermatocyte downsizing may have contributed to the evolution of a sperm cell equivalent to female polar bodies.

MIB-1 Is Required for Spermatogenesis and Facilitates LIN-12 and GLP-1 Activity in Caenorhabditis elegans

“…S3, E and J) and MOs that stain brightly with fluorescently tagged WGA (in red; Figure 5A, panel 3), but place nearly all tubulin into the residual body as one discrete array per nucleus (green in Figure 5A, panel 2), as described previously (Winter et al 2017), except for what is in the centriole (arrowhead, Figure 5B, panel 2). The result is spermatids with a single, centrally placed nucleus surrounded by WGA-positive MOs ( Figure 5B).…”

“…Recent work showed that the microtubules become disassociated from both the chromosomes and centrosomes, but retain g2tubulin, as they reorganize into what develops as the residual body. This likely depends on a normally formed meiotic spindle being located in the right place at the proper time prior to residual body formation (Winter et al 2017). Terminal spermatocytes are also observed in spe-4 and spe-5 mutants that have defects in proteins associated with FB-MOs, but these mutant spermatocytes also show abnormal distribution of tubulin (L'Hernault and Arduengo 1992; Machaca and L'Hernault 1997;Arduengo et al 1998; a Also contains dpy-18(e364).…”

Liposome-based transfection enhances RNAi and CRISPR-mediated mutagenesis in non-model nematode systems

“…For example, instead of the usual pattern of X chromosome inheritance from mother-to-son, A. rhodensis sons inherit the X chromosome from the father 10 . Moreover, A. rhodensis males produce haploid cells that are discarded as female polar bodies 11,12 , and sex determination is influenced by the mother’s age 13 . A. rhodensis is unique among hermaphroditic nematodes in that two distinct groups of stem cells in the hermaphrodite germline produce either sperm or oocytes 14 .…”

Impaired chromosome segregation results in sperms with excess centrosomes inemb-27APC6mutantC. elegans

“…The second cell division is unique because each secondary spermatocyte (connected with its sister spermatocyte) forms 2 buds (spermatids) and segregates a haploid set of the genome into each spermatid, which will then become a sperm. The 2 mother cells retract the constriction between each other and become a residual body, which do not contain genomic DNA, but show presence of actin, tubulin, ribosomes, and ER/Golgi (Winter et al, 2017). The 2 pairs of centrioles function as spindle poles in meiosis I and disengage in anaphase I.…”