Sex- and Gamete-Specific Patterns of X Chromosome Segregation in a Trioecious Nematode

• DOI: 10.1016/j.cub.2017.11.037
• Publication Date: 2017-12-21T16:34:13Z
• Authors: Sophie Tandonnet; Maureen C. Farrell; Georgios D. Kouts...; Mark L. Blaxter; Manish Parihar; Penny L. Sadler; Diane C. Shakes; Andre Pires-daSilva
• Keywords: SB347; Male; 570; QL; X Chromosome; [SDV]Life Sciences [q-bio]; non-disjunction; Chromatids; Article; 576; father-to-son X transmission; X chromosome; lack of recombination; Meiosis; Oogenesis; Chromosome Segregation; C. elegans; meiosis; Animals; Female; Hermaphroditic Organisms; Auanema rhodensis; Rhabditoidea; Spermatogenesis

Three key steps in meiosis allow diploid organisms to produce haploid gametes: (1) homologous chromosomes (homologs) pair and undergo crossovers; (2) homologs segregate to opposite poles; and (3) sister chromatids segregate to opposite poles. The XX/XO sex determination system found in many nematodes [1] facilitates the study of meiosis because variation is easily recognized [2-4]. Here we show that meiotic segregation of X chromosomes in the trioecious nematode Auanema rhodensis [5] varies according to sex (hermaphrodite, female, or male) and type of gametogenesis (oogenesis or spermatogenesis). In this species, XO males exclusively produce X-bearing sperm [6, 7]. The unpaired X precociously separates into sister chromatids, which co-segregate with the autosome set to generate a functional haplo-X sperm. The other set of autosomes is discarded into a residual body. Here we explore the X chromosome behavior in female and hermaphrodite meioses. Whereas X chromosomes segregate following the canonical pattern during XX female oogenesis to yield haplo-X oocytes, during XX hermaphrodite oogenesis they segregate to the first polar body to yield nullo-X oocytes. Thus, crosses between XX hermaphrodites and males yield exclusively male progeny. During hermaphrodite spermatogenesis, the sister chromatids of the X chromosomes separate during meiosis I, and homologous X chromatids segregate to the functional sperm to create diplo-X sperm. Given these intra-species, intra-individual, and intra-gametogenesis variations in the meiotic program, A. rhodensis is an ideal model for studying the plasticity of meiosis and how it can be modulated.