Van Mike V, Larson Braden J, Engebrecht JoAnne
Department of Molecular and Cellular Biology, University of California, Davis, California 95616.
Department of Molecular and Cellular Biology, University of California, Davis, California 95616
Genetics. 2016 Nov;204(3):999-1013. doi: 10.1534/genetics.116.194308. Epub 2016 Sep 7.
Meiotic recombination establishes connections between homologous chromosomes to promote segregation. Hemizygous regions of sex chromosomes have no homologous chromosome to recombine with, yet must be transmitted through meiosis. An extreme case of hemizygosity exists in the genus Caenorhabditis, where males have a single X chromosome that completely lacks a homologous partner. To determine whether similar strategies have evolved to accommodate hemizygosity of the X during male meiosis in Caenorhabditis with distinct modes of sexual reproduction, we examined induction and processing of meiotic double strand breaks (DSBs) in androdioecious (hermaphrodite/male) Caenorhabditis elegans and C. briggsae, and gonochoristic (female/male) C. remanei and C. brenneri Analysis of the recombinase RAD-51 suggests more meiotic DSBs are induced in gonochoristic vs. androdioecious species. However, in late prophase in all species, chromosome pairs are restructured into bivalents around a single axis, suggesting that the holocentric nature of Caenorhabditis chromosomes dictates a single crossover per bivalent regardless of the number of DSBs induced. Interestingly, RAD-51 foci were readily observed on the X chromosome of androdioecious male germ cells, while very few were detected in gonochoristic male germ cells. As in C. elegans, the X chromosome in C. briggsae male germ cells undergoes transient pseudosynapsis and flexibility in DSB repair pathway choice. In contrast, in C. remanei and C. brenneri male germ cells, the X chromosome does not undergo pseudosynapsis and appears refractory to SPO-11-induced breaks. Together our results suggest that distinct strategies have evolved to accommodate sex chromosome hemizygosity during meiosis in closely related Caenorhabditis species.
减数分裂重组在同源染色体之间建立连接以促进分离。性染色体的半合子区域没有同源染色体可供重组,但必须通过减数分裂进行传递。秀丽隐杆线虫属中存在一种极端的半合子情况,雄性只有一条X染色体,完全没有同源配对染色体。为了确定在具有不同有性生殖模式的秀丽隐杆线虫属中,雄性减数分裂期间是否进化出了类似的策略来适应X染色体的半合子状态,我们研究了雌雄同体/雄性的秀丽隐杆线虫和布里格氏秀丽隐杆线虫以及雌雄异体(雌性/雄性)的雷曼氏秀丽隐杆线虫和布伦纳氏秀丽隐杆线虫中减数分裂双链断裂(DSB)的诱导和处理。对重组酶RAD - 51的分析表明,与雌雄同体物种相比,雌雄异体物种中诱导出的减数分裂DSB更多。然而,在所有物种的减数分裂前期晚期,染色体对围绕单一轴重新构建为二价体,这表明秀丽隐杆线虫染色体的全着丝粒性质决定了每个二价体有一次交叉,而与诱导的DSB数量无关。有趣的是,在雌雄同体雄性生殖细胞的X染色体上很容易观察到RAD - 51焦点,而在雌雄异体雄性生殖细胞中检测到的很少。与秀丽隐杆线虫一样,布里格氏秀丽隐杆线虫雄性生殖细胞中的X染色体经历短暂的假联会以及DSB修复途径选择的灵活性。相比之下,在雷曼氏秀丽隐杆线虫和布伦纳氏秀丽隐杆线虫雄性生殖细胞中,X染色体不经历假联会,并且似乎对SPO - 11诱导的断裂具有抗性。我们的研究结果共同表明,在密切相关的秀丽隐杆线虫物种的减数分裂过程中,已经进化出了不同的策略来适应性染色体的半合子状态。