Gong Gaorui, Xiong Yang, Xiao Shijun, Li Xi-Yin, Huang Peipei, Liao Qian, Han Qingqing, Lin Qiaohong, Dan Cheng, Zhou Li, Ren Fan, Zhou Qi, Gui Jian-Fang, Mei Jie
Hubei Hongshan Laboratory, College of Fisheries, Huazhong Agricultural University, Wuhan 430070, China.
Jiaxing Key Laboratory for New Germplasm Breeding of Economic Mycology, Jiaxing 314000, China.
Natl Sci Rev. 2022 Oct 28;10(2):nwac239. doi: 10.1093/nsr/nwac239. eCollection 2023 Feb.
Assembly of a complete Y chromosome is a significant challenge in animals with an XX/XY sex-determination system. Recently, we created YY-supermale yellow catfish by crossing XY males with sex-reversed XY females, providing a valuable model for Y-chromosome assembly and evolution. Here, we assembled highly homomorphic Y and X chromosomes by sequencing genomes of the YY supermale and XX female in yellow catfish, revealing their nucleotide divergences with only less than 1% and with the same gene compositions. The sex-determining region (SDR) was identified to locate within a physical distance of 0.3 Mb by F scanning. Strikingly, the incipient sex chromosomes were revealed to originate via autosome-autosome fusion and were characterized by a highly rearranged region with an SDR downstream of the fusion site. We found that the Y chromosome was at a very early stage of differentiation, as no clear evidence of evolutionary strata and classical structure features of recombination suppression for a rather late stage of Y-chromosome evolution were observed. Significantly, a number of sex-antagonistic mutations and the accumulation of repetitive elements were discovered in the SDR, which might be the main driver of the initial establishment of recombination suppression between young X and Y chromosomes. Moreover, distinct three-dimensional chromatin organizations of the Y and X chromosomes were identified in the YY supermales and XX females, as the X chromosome exhibited denser chromatin structure than the Y chromosome, while they respectively have significantly spatial interactions with female- and male-related genes compared with other autosomes. The chromatin configuration of the sex chromosomes as well as the nucleus spatial organization of the XX neomale were remodeled after sex reversal and similar to those in YY supermales, and a male-specific loop containing the SDR was found in the open chromatin region. Our results elucidate the origin of young sex chromosomes and the chromatin remodeling configuration in the catfish sexual plasticity.
在具有XX/XY性别决定系统的动物中，完整Y染色体的组装是一项重大挑战。最近，我们通过将XY雄性与性反转的XY雌性杂交，培育出了YY超雄黄颡鱼，为Y染色体的组装和进化提供了一个有价值的模型。在这里，我们通过对YY超雄和XX雌性黄颡鱼的基因组进行测序，组装出了高度同源的Y染色体和X染色体，揭示了它们的核苷酸差异仅不到1%，且基因组成相同。通过F扫描确定性别决定区域（SDR）位于0.3 Mb的物理距离内。令人惊讶的是，初始性染色体是通过常染色体-常染色体融合产生的，其特征是在融合位点下游有一个高度重排的区域，其中包含SDR。我们发现Y染色体正处于分化的非常早期阶段，因为没有观察到Y染色体进化后期明显的进化层证据和重组抑制的经典结构特征。值得注意的是，在SDR中发现了许多性拮抗突变和重复元件的积累，这可能是年轻X和Y染色体之间重组抑制初始建立的主要驱动力。此外，在YY超雄和XX雌性中鉴定出了Y染色体和X染色体不同的三维染色质组织，因为X染色体比Y染色体表现出更致密的染色质结构，而与其他常染色体相比，它们分别与雌性和雄性相关基因有显著的空间相互作用。性反转后性染色体的染色质构型以及XX新雄性的细胞核空间组织发生了重塑，与YY超雄中的相似，并在开放染色质区域发现了一个包含SDR的雄性特异性环。我们的结果阐明了年轻性染色体的起源以及黄颡鱼性别可塑性中的染色质重塑构型。
