Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, IA 50011, USA.
Guangdong Laboratory for Lingnan Modern Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518120, People's Republic of China.
Philos Trans R Soc Lond B Biol Sci. 2021 Sep 13;376(1833):20200101. doi: 10.1098/rstb.2020.0101. Epub 2021 Jul 26.
Sex chromosome dosage compensation (SCDC) overcomes gene-dose imbalances that disturb transcriptional networks, as when ZW females or XY males are hemizygous for Z/X genes. Mounting data from non-model organisms reveal diverse SCDC mechanisms, yet their evolution remains obscure, because most informative lineages with variable sex chromosomes are unstudied. Here, we discovered SCDC in turtles and an unprecedented thermosensitive SCDC in eukaryotes. We contrasted RNA-seq expression of Z-genes, their autosomal orthologues, and control autosomal genes in (ZZ/ZW) and turtles with temperature-dependent sex determination (TSD) (proxy for ancestral expression). This approach disentangled chromosomal context effects on Z-linked and autosomal expression, from lineage effects owing to selection or drift. Embryonic SCDC is tissue- and age-dependent, regulated gene-by-gene, complete in females via Z-upregulation in both sexes (Type IV) but partial and environmentally plastic via Z-downregulation in males (accentuated at colder temperature), present in female hatchlings and a weakly suggestive in adult liver (Type I). Results indicate that embryonic SCDC evolved with/after sex chromosomes in 's family Tryonichidae, while co-opting Z-gene upregulation present in the TSD ancestor. Notably, 's SCDC resembles pygmy snake's, and differs from the full-SCDC of lizards who share homologous sex chromosomes (XY), advancing our understanding of how XX/XY and ZZ/ZW systems compensate gene-dose imbalance. This article is part of the theme issue 'Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)'.
性染色体剂量补偿（SCDC）克服了基因剂量失衡，这些失衡会干扰转录网络，例如当 ZW 雌性或 XY 雄性为 Z/X 基因的半合子时。越来越多的非模式生物的数据揭示了多样化的 SCDC 机制，但它们的进化仍然不清楚，因为大多数具有可变性染色体的信息丰富的谱系尚未被研究。在这里，我们在龟类中发现了 SCDC，并在真核生物中发现了一种前所未有的热敏 SCDC。我们对比了（ZZ/ZW）和具有温度依赖性别决定（TSD）的 龟类中 Z 基因、其常染色体同源物和控制常染色体基因的 RNA-seq 表达，这是祖先表达的代理。这种方法将 Z 连锁和常染色体表达的染色体背景效应，与由于选择或漂变引起的谱系效应区分开来。胚胎 SCDC 是组织和年龄依赖的，基因逐个调控，在雌性中通过两性中 Z 基因的上调（IV 型）完全补偿，但在雄性中部分补偿且具有环境可塑性（在较低温度下更明显），在雌性幼体中存在，在成年肝脏中则存在微弱的暗示（I 型）。结果表明，胚胎 SCDC 是在 Tryonichidae 家族的性染色体上进化而来的，同时利用了 TSD 祖先中存在的 Z 基因上调。值得注意的是， 的 SCDC 与 pygmy snake 的相似，与共享同源性染色体（XY）的蜥蜴的完全 SCDC 不同，这推进了我们对 XX/XY 和 ZZ/ZW 系统如何补偿基因剂量失衡的理解。本文是主题为'挑战性染色体进化的范式：以脊椎动物为重点的实证和理论见解（第二部分）'的特刊的一部分。
