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Contributed by Marc Van Montagu, September 3, 2020 (sent for review March 26, 2020; reviewed by Ingo Braasch, Axel Meyer, and Manfred Schartl)
Significance
We assembled one of the most contiguous genomes for the common goldfish and unveiled the genetic architecture of many well-known and anatomically interesting traits, owing to the sequencing of a large collection of goldfish varieties. The datasets that we have generated for candidate genes or genomic regions based on population genomics may help to elucidate the evolution of goldfish and goldfish varieties and may provide a resource for a wide range of studies with important implications for the use of goldfish as a model for vertebrate and fish genetics.
Abstract
Goldfish have been subjected to over 1,000 y of intensive domestication and selective breeding. In this report, we describe a high-quality goldfish genome (2n = 100), anchoring 95.75% of contigs into 50 pseudochromosomes. Comparative genomics enabled us to disentangle the two subgenomes that resulted from an ancient hybridization event. Resequencing 185 representative goldfish variants and 16 wild crucian carp revealed the origin of goldfish and identified genomic regions that have been shaped by selective sweeps linked to its domestication. Our comprehensive collection of goldfish varieties enabled us to associate genetic variations with a number of well-known anatomical features, including features that distinguish traditional goldfish clades. Additionally, we identified a tyrosine-protein kinase receptor as a candidate causal gene for the first well-known case of Mendelian inheritance in goldfish—the transparent mutant. The goldfish genome and diversity data offer unique resources to make goldfish a promising model for functional genomics, as well as domestication.
Footnotes
↵1D.C., Qing Zhang, W.T., Z.H., and G.W. contributed equally to this work.
- ↵2To whom correspondence may be addressed. Email: zhuang{at}fjnu.edu.cn, marc.vanmontagu{at}ugent.be, tanghaibao{at}gmail.com, yves.vandepeer{at}psb.ugent.be, yqchen{at}fjnu.edu.cn, or zjisen{at}fafu.edu.cn.
Author contributions: Y.C. and J.Z. conceived this genome project and coordinated research activities; W.T., Z.H., M.V.M., H.T., Y.V.d.P., Y.C., and J.Z. designed the experiments; D.C., Z.H., J.S., Q.S., W.H., Qiujin Zhang, G.L., W.Z., L.Q., A.W., Q.Y., and J.Z. collected and generated goldfish and crucian carp materials; D.C., Qing Zhang, Z.H., G.W., Yongjun Wang, H.X., L. Lin, X.Z., F.L., and H.T. studied genome evolution; D.C., Qing Zhang, W.T., G.W., J.T., G.Z., M.L., and J.Z. contributed to the population genetic analysis; Qing Zhang, X.Z., X.C., Y.Q., Y. Zhou, and T.X. assembled and annotated the genome; D.C., G.W., J.S., Yongjun Wang, H.X., Z.L., W.C., L.H., J.X., L.G., Yuanyuan Wang, P.M., X.H., B.W., Q.J., J.L., H.W., M.D., L. Liu, and H.P. manually checked the gene annotation; D.C., Qing Zhang, J.C., Y. Zhang, R.M., H.T., Y.V.d.P, Y.C., and J.Z. wrote the manuscript.
Reviewers: I.B., Michigan State University; A.M., University of Konstanz; and M.S., University of Würzburg.
The authors declare no competing interest.
This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2005545117/-/DCSupplemental.
Data Availability.
We have submitted the goldfish genome and annotation to National Center for Biotechnology Information (NCBI). The goldfish genome is available from SAMN12618612. Goldfish RNA-Seq data and quality-filtered Illumina reads for the 185 resequenced goldfish genomes, 16 crucian carp, and 6 Barbinae species were deposited into the NCBI BioProject database under accession number PRJNA561458.
Published under the PNAS license.
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The evolutionary origin and domestication history of goldfish (Carassius auratus)
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