A new emu genome illuminates the evolution of genome configuration and nuclear architecture of avian chromosomes
- Jing Liu1,2,16,
- Zongji Wang1,2,3,16,
- Jing Li1,
- Luohao Xu2,
- Jiaqi Liu4,
- Shaohong Feng5,
- Chunxue Guo5,
- Shengchan Chen6,
- Zhanjun Ren7,
- Jinpeng Rao8,
- Kai Wei8,
- Yuezhou Chen9,
- Erich D. Jarvis10,11,
- Guojie Zhang12,13,14,15 and
- Qi Zhou1,2,8
- 1MOE Laboratory of Biosystems Homeostasis & Protection and Zhejiang Provincial Key Laboratory for Cancer Molecular Cell Biology, Life Sciences Institute, Zhejiang University, Hangzhou 310058, China;
- 2Department of Neuroscience and Developmental Biology, University of Vienna, Vienna 1090, Austria;
- 3Institute of Animal Sex and Development, Zhejiang Wanli University, Ningbo 315100, China;
- 4Wuhan Gooalgene Technology Company, Wuhan 430070, China;
- 5BGI-Shenzhen, Beishan Industrial Zone, Shenzhen 518083, China;
- 6Longteng Ecological Culture Company, Limited, Zhashui 711400, China;
- 7Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling 712100, China;
- 8Center for Reproductive Medicine, The 2nd Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou 310052, China;
- 9Jianzhou Poultry Industry Company, Limited, Yong'an 366000, China;
- 10Laboratory of Neurogenetics of Language, The Rockefeller University, New York, New York 10065, USA;
- 11Howard Hughes Medical Institute, Chevy Chase, Maryland 20815, USA;
- 12China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China;
- 13State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China;
- 14Section for Ecology and Evolution, Department of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark;
- 15Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming 650223, China
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↵16 These authors contributed equally to this work.
Abstract
Emu and other ratites are more informative than any other birds in reconstructing the evolution of the ancestral avian or vertebrate karyotype because of their much slower rate of genome evolution. Here, we generated a new chromosome-level genome assembly of a female emu, and estimated the tempo of chromosome evolution across major avian phylogenetic branches, by comparing it to chromosome-level genome assemblies of 11 other bird and one turtle species. We found ratites exhibited the lowest numbers of intra- and inter-chromosomal changes among birds since their divergence with turtles. The small-sized and gene-rich emu microchromosomes have frequent inter-chromosomal contacts that are associated with housekeeping genes, which appears to be driven by clustering their centromeres in the nuclear interior, away from the macrochromosomes in the nuclear periphery. Unlike nonratite birds, only less than one-third of the emu W Chromosome regions have lost homologous recombination and diverged between the sexes. The emu W is demarcated into a highly heterochromatic region (WS0) and another recently evolved region (WS1) with only moderate sequence divergence with the Z Chromosome. WS1 has expanded its inactive chromatin compartment, increased chromatin contacts within the region, and decreased contacts with the nearby regions, possibly influenced by the spreading of heterochromatin from WS0. These patterns suggest that alteration of chromatin conformation comprises an important early step of sex chromosome evolution. Overall, our results provide novel insights into the evolution of avian genome structure and sex chromosomes in three-dimensional space.
Footnotes
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[Supplemental material is available for this article.]
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Article published online before print. Article, supplemental material, and publication date are at https://www.genome.org/cgi/doi/10.1101/gr.271569.120.
- Received September 9, 2020.
- Accepted December 30, 2020.
This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see https://genome.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
