Štundlová Jana, Hospodářská Monika, Lukšíková Karolína, Voleníková Anna, Pavlica Tomáš, Altmanová Marie, Richter Annekatrin, Reichard Martin, Dalíková Martina, Pelikánová Šárka, Marta Anatolie, Simanovsky Sergey A, Hiřman Matyáš, Jankásek Marek, Dvořák Tomáš, Bohlen Joerg, Ráb Petr, Englert Christoph, Nguyen Petr, Sember Alexandr
Laboratory of Fish Genetics, Institute of Animal Physiology and Genetics, Czech Academy of Sciences, Libechov, Czech Republic.
Faculty of Science, University of South Bohemia, Ceske Budejovice, Czech Republic.
Chromosome Res. 2022 Dec;30(4):309-333. doi: 10.1007/s10577-022-09707-3. Epub 2022 Oct 8.
Homomorphic sex chromosomes and their turnover are common in teleosts. We investigated the evolution of nascent sex chromosomes in several populations of two sister species of African annual killifishes, Nothobranchius furzeri and N. kadleci, focusing on their under-studied repetitive landscape. We combined bioinformatic analyses of the repeatome with molecular cytogenetic techniques, including comparative genomic hybridization, fluorescence in situ hybridization with satellite sequences, ribosomal RNA genes (rDNA) and bacterial artificial chromosomes (BACs), and immunostaining of SYCP3 and MLH1 proteins to mark lateral elements of synaptonemal complexes and recombination sites, respectively. Both species share the same heteromorphic XY sex chromosome system, which thus evolved prior to their divergence. This was corroborated by sequence analysis of a putative master sex determining (MSD) gene gdf6Y in both species. Based on their divergence, differentiation of the XY sex chromosome pair started approximately 2 million years ago. In all populations, the gdf6Y gene mapped within a region rich in satellite DNA on the Y chromosome long arms. Despite their heteromorphism, X and Y chromosomes mostly pair regularly in meiosis, implying synaptic adjustment. In N. kadleci, Y-linked paracentric inversions like those previously reported in N. furzeri were detected. An inversion involving the MSD gene may suppress occasional recombination in the region, which we otherwise evidenced in the N. furzeri population MZCS-121 of the Limpopo clade lacking this inversion. Y chromosome centromeric repeats were reduced compared with the X chromosome and autosomes, which points to a role of relaxed meiotic drive in shaping the Y chromosome repeat landscape. We speculate that the recombination rate between sex chromosomes was reduced due to heterochiasmy. The observed differences between the repeat accumulations on the X and Y chromosomes probably result from high repeat turnover and may not relate closely to the divergence inferred from earlier SNP analyses.
同态性染色体及其更替在硬骨鱼中很常见。我们研究了非洲一年生鳉鱼两个姐妹物种——费氏假鳃鳉（Nothobranchius furzeri）和卡氏假鳃鳉（N. kadleci）——几个种群中新生性染色体的进化，重点关注其研究不足的重复序列景观。我们将重复序列组的生物信息学分析与分子细胞遗传学技术相结合，包括比较基因组杂交、用卫星序列、核糖体RNA基因（rDNA）和细菌人工染色体（BAC）进行荧光原位杂交，以及对SYCP3和MLH1蛋白进行免疫染色，分别标记联会复合体的侧生元件和重组位点。这两个物种共享相同的异型XY性染色体系统，因此该系统在它们分化之前就已经进化出来了。这一点在两个物种中一个假定的主性别决定（MSD）基因gdf6Y的序列分析中得到了证实。根据它们的分歧情况，XY性染色体对的分化大约始于200万年前。在所有种群中，gdf6Y基因定位于Y染色体长臂上富含卫星DNA的区域内。尽管它们异型，但X和Y染色体在减数分裂中大多能正常配对，这意味着存在突触调整。在卡氏假鳃鳉中，检测到了像之前在费氏假鳃鳉中报道的Y连锁臂内倒位。涉及MSD基因的倒位可能会抑制该区域偶尔发生的重组，而在林波波河分支的费氏假鳃鳉种群MZCS - 121中，我们在没有这种倒位的情况下证明了这种重组。与X染色体和常染色体相比，Y染色体着丝粒重复序列减少，这表明减数分裂驱动的放松在塑造Y染色体重复序列景观中发挥了作用。我们推测，由于异交叉现象，性染色体之间的重组率降低了。在X和Y染色体上观察到的重复序列积累差异可能是由于重复序列的高更替率导致的，可能与早期SNP分析推断的分歧没有密切关系。
