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

Sophie Tandonnet,Maureen C Farrell,Georgios D Koutsovoulos,Mark L Blaxter,Manish Parihar,Penny L Sadler,Diane C Shakes,Andre Pires-Dasilva

doi:10.1016/j.cub.2017.11.037

Sophie Tandonnet, Maureen C Farrell + Show 6 more

Open Access

https://doi.org/10.1016/j.cub.2017.11.037

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Abstract

SummaryThree 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, 3, 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.

Highlights

Cytological Analysis of Meiotic X Chromosome Segregation During Hermaphrodite Oogenesis, Both X Chromosomes Appear to Segregate to the First Polar Body Our crossing results predicted specific cytological consequences
We hypothesized that during oogenesis in A. rhodensis hermaphrodites, unorthodox segregation patterns of the X chromosome would result in anaphase figures with unequal amounts of chromatin and in non-standard numbers of DAPI-stained bodies aligned at the metaphase plate due to potential alterations in X chromosome pairing
We examined meiotically dividing oocytes labeled with a combination of DAPI-staining and anti-tubulin antibodies and compared the patterns in A. rhodensis females

Summary

Graphical Abstract

Tandonnet et al show that the X chromosomes segregate differently between sexes and type of gametogenesis in the three-sexed nematode A. rhodensis: hermaphrodites produce diplo-X sperm and nullo-X oocytes, whereas females produce haplo-X oocytes. It has a unique form of X chromosome heritability, from father to son. Highlights d Crosses between A. rhodensis hermaphrodites and males generate only male progeny d Hermaphrodites generate mostly nullo-X oocytes and diplo-X sperm d Following normal Mendelian genetics, XX females produce haplo-X oocytes d In cross-progeny, sons always inherit the X chromosome from the father.

RESULTS AND DISCUSSION

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