Extra Microchromosomes Play Male Determination Role in Polyploid Gibel Carp

Abstract

Sex is generally determined by sex chromosomes in vertebrates, and sex chromosomes exhibit the most rapidly-evolving traits. Sex chromosome evolution has been revealed previously in numerous cases, but the association between sex chromosome origin and the reproduction mode transition from unisexual to sexual reproduction remains unclear. Here, we have isolated a male-specific sequence via analysis of amplified fragment length polymorphism from polyploid gibel carp (Carassius gibelio), a species that not only has the ability to reproduce unisexually but also contains males in wild populations. Subsequently, we have found through FISH analysis that males have several extra microchromosomes with repetitive sequences and transposable elements when compared to females. Moreover, we produced sex-reversed physiological females with a male-specific marker by using estradiol hormone treatment, and two gynogenetic families were established from them. In addition, the male incidence rates of two gynogenetic families were revealed to be closely associated with the extra microchromosome number of the sex-reversed physiological females. These results suggest that the extra microchromosomes in males might resemble a common feature of sex chromosomes and might play a significant role in male determination during the evolutionary trajectory of the reproduction mode transition from unisexual to sexual reproduction in the polyploid fish.KEYWORDS microchromosome; sex determination; sex chromosome; polyploid; gibel carp; genetics of sex S EX is a common phenomenon in nature and also one of the most important topics in life sciences, especially in evolutionary biology and genetics (Graves 2008). Most vertebrates are gonochoristic and reproduce by sexual reproduction. Different sex-determination systems, such as male heterogametic XX/XY sex chromosomes and female heterogametic ZZ/ZW sex chromosomes, as well as their numerous variants, have been revealed (Bachtrog et al. 2014;Mei and Gui 2015). Along with the rapid development of genomics and molecular genetic techniques, labile sex-determination systems and rapid sex chromosome turnovers have been noticed in both animals and plants recently (Bachtrog et al. 2014;Chen et al. 2014;Cortez et al. 2014;Graves 2014;Wei and Barbash 2015). Although how neo-sex chromosomes evolved (Roberts et al. 2009;Cortez et al. 2014;Vicoso and Bachtrog 2015) and how unisexual and sexual reproduction modes transformed (Jokela et al. 2009;Zhang et al. 2015) have been revealed, the association between sex chromosome origin and reproduction mode transition from unisexual to sexual reproduction remains unclear in vertebrates.The gibel carp, Carassius gibelio, has a wide geographic distribution in the Eurasian continent (Hanfling et al. 2005;Li and Gui 2008;Gui and Zhou 2010;Jakovlic and Gui 2011;Jiang et al. 2013) and diverse gynogenetic strains have been identified using biological traits and genetic markers (Zhou et al. 2000a;Yang and Gui 2004;Guo and Gui 2008). As a hexaploid with .150 chromosomes (...

Genetic identification of a newly synthetic allopolyploid strain with 206 chromosomes in polyploid gibel carp

“…Owing to its unique reproduction modes and polyploidy background, some allopolyploid clones or strains are able to be easily synthetized from different clones by incorporating an alien sperm genome (Gui & Zhou, ; Gui et al., a; Gui, Liang, Zhu, & Jiang, b; Li, Zhang et al. (); Li, Liang et al. (); Zhu & Gui, ).…”

“…Five of 70 allopolyploid individuals by ploidy determination were randomly selected to count chromosome number. The preparation of metaphase chromosomes was performed as described (Zhu & Gui, ; Li, Zhang et al., ). A total of the best 100 metaphase spreads were detected and the statistics modal number was characterized as the chromosome number (Li, Liang et al., ; Liu et al., ; Wang et al., ; Zhou & Gui, ).…”

“…The preparation procedures of the 45S rDNA and fluorescence in situ hybridization probes were performed according to the method described by Zhu, Ma and Gui (); Li, Zhang et al. () and Li, Liang et al. ().…”

Induction of meiotic gynogenesis in bagrid catfish (Pseudobagrus ussuriensis) with homologous sperm and its confirmation for female homogamety

“…AFLP analysis was conducted using a male‐specific primer pair (F: 5′‐TGT TGA GCG TGA TGT GAG TGA GC‐3′, R: 5′‐AAA CAA ACA CCA GGG CAG GAC TA‐3′) as per previous description (Pan et al., ). The PCR products were separated using 6% denaturing polyacrylamide gel (Bio‐Rad, Sequi‐Gen GT System) and visualized via silver staining (Li et al., ; Wang, Mao, Chen, Liu & Gui, ).…”

Molecular characterization and expression pattern of a germ cell marker gene dnd in gibel carp (Carassius gibelio)

“…However, unlike most unisexual vertebrates (Avise, 2008), gibel carp has been revealed to have multiple reproduction modes including unisexual gynogenesis and sexual reproduction (Zhou et al, 2000;Gui and Zhou, 2010;Li et al, 2014a;Mei and Gui, 2015;Zhang et al, 2015), and a high male incidence has been also observed in many natural populations (Jiang et al, 2013;Li et al, 2016). Utilizing it as an evolutional development biology model for screening reproduction-related genes, many important genes, such as oocytespecific and ovarian development-associated genes C-type lection (Dong et al, 2004), C1q-like (Mei et al, 2008(Mei et al, , 2014 and spindlin (Sun et al, 2010), oocyte-specific H2A variant h2af1o (Wu et al, 2009;Yue et al, 2013) and stem-loop binding protein-encoded gene slbp2 (Liu et al, 2015a), testis determination-related gene Dmrt1 (Li et al, 2014a), and germ cell marker genes Vasa and Dazl (Xu et al, 2005;Peng et al, 2009), have been identified and functionally characterized in gibel carp.…”