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多层调控剂量补偿和 Z 染色体雄性化在木白蝶(Leptidea sinapis)中。

Multilayered Tuning of Dosage Compensation and Z-Chromosome Masculinization in the Wood White (Leptidea sinapis) Butterfly.

机构信息

Evolutionary Biology Program, Department of Ecology and Genetics, Evolutionary Biology Centre (EBC), Uppsala University, Sweden.

Plant Ecology and Evolution, Department of Ecology and Genetics, Evolutionary Biology Centre (EBC), Uppsala University, Sweden.

出版信息

Genome Biol Evol. 2019 Sep 1;11(9):2633-2652. doi: 10.1093/gbe/evz176.

DOI:10.1093/gbe/evz176
PMID:31400207
原文链接:https://pmc.ncbi.nlm.nih.gov/articles/PMC6761951/
Abstract

In species with genetic sex determination, dosage compensation can evolve to equal expression levels of sex-linked and autosomal genes. Current knowledge about dosage compensation has mainly been derived from male-heterogametic (XX/XY) model organisms, whereas less is understood about the process in female-heterogametic systems (ZZ/ZW). In moths and butterflies, downregulation of Z-linked expression in males (ZZ) to match the expression level in females (ZW) is often observed. However, little is known about the underlying regulatory mechanisms, or if dosage compensation patterns vary across ontogenetic stages. In this study, we assessed dynamics of Z-linked and autosomal expression levels across developmental stages in the wood white (Leptidea sinapis). We found that although expression of Z-linked genes in general was reduced compared with autosomal genes, dosage compensation was actually complete for some categories of genes, in particular sex-biased genes, but equalization in females was constrained to a narrower gene set. We also observed a noticeable convergence in Z-linked expression between males and females after correcting for sex-biased genes. Sex-biased expression increased successively across developmental stages, and male-biased genes were enriched on the Z-chromosome. Finally, all five core genes associated with the ribonucleoprotein dosage compensation complex male-specific lethal were detected in adult females, in correspondence with a reduction in the expression difference between autosomes and the single Z-chromosome. We show that tuning of gene dosage is multilayered in Lepidoptera and argue that expression balance across chromosomal classes may predominantly be driven by enrichment of male-biased genes on the Z-chromosome and cooption of available dosage regulators.

摘要

在具有遗传性别决定的物种中,剂量补偿可以进化为使性连锁基因和常染色体基因的表达水平相等。目前关于剂量补偿的知识主要来自于雄性异型(XX/XY)模式生物,而对雌性异型系统(ZZ/ZW)中的这一过程了解较少。在蛾和蝴蝶中,常观察到雄性(ZZ)中 Z 连锁表达的下调,以匹配雌性(ZW)的表达水平。然而,对于潜在的调控机制,或者剂量补偿模式是否在个体发育阶段发生变化,人们知之甚少。在这项研究中,我们评估了在木白蝶(Leptidea sinapis)的发育阶段中 Z 连锁和常染色体表达水平的动态变化。我们发现,尽管 Z 连锁基因的表达总体上比常染色体基因低,但对于某些类别的基因,特别是性别偏向基因,实际上是完全补偿的,但雌性的均等化受到更窄的基因集的限制。我们还观察到,在纠正性别偏向基因后,雄性和雌性之间的 Z 连锁表达明显趋同。性别偏向表达随着发育阶段的推移逐渐增加,并且雄性偏向基因富集在 Z 染色体上。最后,在成年雌性中检测到与核糖核蛋白剂量补偿复合物雄性特异性致死相关的五个核心基因,与常染色体和单一 Z 染色体之间的表达差异减少相对应。我们表明,在鳞翅目昆虫中,基因剂量的调谐是多层次的,并认为跨染色体类别的表达平衡可能主要由 Z 染色体上雄性偏向基因的富集和可用剂量调节剂的共适应驱动。

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A sex-linked supergene with large effects on sperm traits has little impact on reproductive traits in female zebra finches.性连锁超基因对精子特征有很大影响,但对雌性斑胸草雀的繁殖特征影响很小。

本文引用的文献

1
Evolution of Sex-Biased Gene Expression and Dosage Compensation in the Eye and Brain of Heliconius Butterflies.雌雄异形基因表达和剂量补偿在Heliconius 蝴蝶的眼和脑中的演化。
Mol Biol Evol. 2018 Sep 1;35(9):2120-2134. doi: 10.1093/molbev/msy111.
2
Dosage Compensation of the X Chromosome: A Complex Epigenetic Assignment Involving Chromatin Regulators and Long Noncoding RNAs.X 染色体的剂量补偿:一个涉及染色质调节剂和长非编码 RNA 的复杂表观遗传分配。
Annu Rev Biochem. 2018 Jun 20;87:323-350. doi: 10.1146/annurev-biochem-062917-011816. Epub 2018 Apr 18.
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A Comprehensive and Dated Phylogenomic Analysis of Butterflies.
Proc Biol Sci. 2024 Mar 27;291(2019):20232796. doi: 10.1098/rspb.2023.2796.
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Wolbachia: Advancing into a Second Century.沃尔巴克氏体:迈向第二个世纪。
Methods Mol Biol. 2024;2739:1-13. doi: 10.1007/978-1-0716-3553-7_1.
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The genome sequence of the wood white butterfly, (Linnaeus, 1758).白钩蛱蝶(林奈,1758年)的基因组序列。
Wellcome Open Res. 2022 Oct 12;7:254. doi: 10.12688/wellcomeopenres.18118.1. eCollection 2022.
6
High-density linkage maps and chromosome level genome assemblies unveil direction and frequency of extensive structural rearrangements in wood white butterflies (Leptidea spp.).高密度连锁图谱和染色体水平基因组组装揭示了木白蝶(Leptidea 属)中广泛结构重排的方向和频率。
Chromosome Res. 2023 Jan 20;31(1):2. doi: 10.1007/s10577-023-09713-z.
7
Host plant diet affects growth and induces altered gene expression and microbiome composition in the wood white (Leptidea sinapis) butterfly.寄主植物的饮食会影响木白蝶(Leptidea sinapis)的生长,并诱导其基因表达和微生物组组成发生改变。
Mol Ecol. 2021 Jan;30(2):499-516. doi: 10.1111/mec.15745. Epub 2020 Dec 14.
蝴蝶的全面及陈旧的系统基因组分析。
Curr Biol. 2018 Mar 5;28(5):770-778.e5. doi: 10.1016/j.cub.2018.01.061. Epub 2018 Feb 15.
4
Gene expression profiling across ontogenetic stages in the wood white (Leptidea sinapis) reveals pathways linked to butterfly diapause regulation.在木白蝶(Leptidea sinapis)的各个发育阶段进行基因表达谱分析,揭示了与蝴蝶滞育调控相关的途径。
Mol Ecol. 2018 Feb;27(4):935-948. doi: 10.1111/mec.14501. Epub 2018 Feb 26.
5
The deep conservation of the Lepidoptera Z chromosome suggests a non-canonical origin of the W.鳞翅目 Z 染色体的深度保守性表明 W 染色体具有非典型的起源。
Nat Commun. 2017 Nov 14;8(1):1486. doi: 10.1038/s41467-017-01663-5.
6
Rapid Increase in Genome Size as a Consequence of Transposable Element Hyperactivity in Wood-White (Leptidea) Butterflies.转座元件的过度活跃导致木白蝶(Leptidea)基因组大小的快速增加。
Genome Biol Evol. 2017 Oct 1;9(10):2491-2505. doi: 10.1093/gbe/evx163.
7
Evolution of Sex Chromosome Dosage Compensation in Animals: A Beautiful Theory, Undermined by Facts and Bedeviled by Details.动物性染色体剂量补偿的进化:一个美丽的理论,却被事实和细节所破坏。
Genome Biol Evol. 2017 Sep 1;9(9):2461-2476. doi: 10.1093/gbe/evx154.
8
Global Dosage Compensation Is Ubiquitous in Lepidoptera, but Counteracted by the Masculinization of the Z Chromosome.全球剂量补偿在鳞翅目中普遍存在,但受到Z染色体雄性化的抵消。
Mol Biol Evol. 2017 Oct 1;34(10):2637-2649. doi: 10.1093/molbev/msx190.
9
RNA sequencing reveals a complete but an unconventional type of dosage compensation in the domestic silkworm .RNA测序揭示了家蚕中一种完整但非常规的剂量补偿类型。
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Sex chromosome evolution: historical insights and future perspectives.性染色体进化:历史见解与未来展望。
Proc Biol Sci. 2017 May 17;284(1854). doi: 10.1098/rspb.2016.2806.