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      Comparative genomics and transcriptomics of Chrysolophus provide insights into the evolution of complex plumage coloration

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          Abstract

          Background

          As one of the most recognizable characteristics in birds, plumage color has a high impact on understanding the evolution and mechanisms of coloration. Feather and skin are ideal tissues to explore the genomics and complexity of color patterns in vertebrates. Two species of the genus Chrysolophus, golden pheasant ( Chrysolophus pictus) and Lady Amherst's pheasant ( Chrysolophus amherstiae), exhibit brilliant colors in their plumage, but with extreme phenotypic differences, making these two species great models to investigate plumage coloration mechanisms in birds.

          Results

          We sequenced and assembled a genome of golden pheasant with high coverage and annotated 15,552 protein-coding genes. The genome of Lady Amherst's pheasant is sequenced with low coverage. Based on the feather pigment identification, a series of genomic and transcriptomic comparisons were conducted to investigate the complex features of plumage coloration. By identifying the lineage-specific sequence variations in Chrysolophus and golden pheasant against different backgrounds, we found that four melanogenesis biosynthesis genes and some lipid-related genes might be candidate genomic factors for the evolution of melanin and carotenoid pigmentation, respectively. In addition, a study among 47 birds showed some candidate genes related to carotenoid coloration in a broad range of birds. The transcriptome data further reveal important regulators of the two colorations, particularly one splicing transcript of the microphthalmia-associated transcription factor gene for pheomelanin synthesis.

          Conclusions

          Analysis of the golden pheasant and its sister pheasant genomes, as well as comparison with other avian genomes, are helpful to reveal the underlying regulation of their plumage coloration. The present study provides important genomic information and insights for further studies of avian plumage evolution and diversity.

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          Most cited references50

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          Using RepeatMasker to identify repetitive elements in genomic sequences.

          Nansheng Chen (2004)
          The RepeatMasker program is used for identifying repetitive elements in nucleotide sequences for further detailed analyses. Users can run RepeatMasker remotely via a Web site, or, for larger input sequences, the program and its dependent programs may be downloaded and run locally on Unix/Linux computers. The protocols in this chapter detail how to use RepeatMasker both remotely and locally to extract repetitive elements data and mask these repetitive elements in nucleotide sequences.
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            Good genes, oxidative stress and condition-dependent sexual signals.

            T von Schantz, S Bensch, M Grahn … (1999)
            The immune and the detoxication systems of animals are characterized by allelic polymorphisms, which underlie individual differences in ability to combat assaults from pathogens and toxic compounds. Previous studies have shown that females may improve offspring survival by selecting mates on the basis of sexual ornaments and signals that honestly reveal health. In many cases the expression of these ornaments appears to be particularly sensitive to oxidative stress. Activated immune and detoxication systems often generate oxidative stress by an extensive production of reactive metabolites and free radicals. Given that tolerance or resistance to toxic compounds and pathogens can be inherited, female choice should promote the evolution of male ornaments that reliably reveal the status of the bearers' level of oxidative stress. Hence, oxidative stress may be one important agent linking the expression of sexual ornaments to genetic variation in fitness-related traits, thus promoting the evolution of female mate choice and male sexual ornamentation, a controversial issue in evolutionary biology ever since Darwin.
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              Unexpected consequences of a sudden and massive transposon amplification on rice gene expression.

              Ken Naito, Feng Zhang, Takuji Tsukiyama … (2009)
              High-copy-number transposable elements comprise the majority of eukaryotic genomes where they are major contributors to gene and genome evolution. However, it remains unclear how a host genome can survive a rapid burst of hundreds or thousands of insertions because such bursts are exceedingly rare in nature and therefore difficult to observe in real time. In a previous study we reported that in a few rice strains the DNA transposon mPing was increasing its copy number by approximately 40 per plant per generation. Here we exploit the completely sequenced rice genome to determine 1,664 insertion sites using high-throughput sequencing of 24 individual rice plants and assess the impact of insertion on the expression of 710 genes by comparative microarray analysis. We find that the vast majority of transposable element insertions either upregulate or have no detectable effect on gene transcription. This modest impact reflects a surprising avoidance of exon insertions by mPing and a preference for insertion into 5' flanking sequences of genes. Furthermore, we document the generation of new regulatory networks by a subset of mPing insertions that render adjacent genes stress inducible. As such, this study provides evidence for models first proposed previously for the involvement of transposable elements and other repetitive sequences in genome restructuring and gene regulation.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Gigascience
                Journal ID (iso-abbrev): Gigascience
                Journal ID (publisher-id): gigascience
                Title: GigaScience
                Publisher: Oxford University Press
                ISSN (Electronic): 2047-217X
                Publication date Collection: October 2018
                Publication date (Electronic): 06 September 2018
                Publication date PMC-release: 06 September 2018
                Volume: 7
                Issue: 10
                Electronic Location Identifier: giy113
                Affiliations
                [1 ]The State key Laboratory of Reproductive Regulation and Breeding of Grassland Livestock, Inner Mongolia University, No.235, University West Road, Saihan District,Hohhot, Inner Mongolia, 010021, China
                [2 ]College of Life Science, Inner Mongolia University, Hohhot, 010070, China
                [3 ]BGI Genomics, Co., Ltd. Buiding No.7, BGI Park, No.21 Hongan 3rd Street, Yantian District, Shenzhen, 518083, China
                [4 ]College of Life Science, Inner Mongolia Agricultural University, No.306, Zhaowuda Road, Saihan District, Hohhot, Inner Mongolia, 010018
                [5 ]Department of Pathology, Keck School of Medicine, Universit of Southern California, 2011 Zonal Avenue, HMR315B, Los Angeles, CA90033, USA
                Author notes
                Correspondence address. Jun Yin; College of Life Science, Inner Mongolia Agricultural University, No.306, Zhaowuda Road, Saihan District, Hohhot, Inner Mongolia, 010018, China, E-mail: yinjun@ 123456imau.edu.cn
                Correspondence address. Yongchun Zuo, The State key Laboratory of Reproductive Regulation and Breeding of Grassland Livestock, Inner Mongolia University, No.235, University West Road, Saihan District, Hohhot, Inner Mongolia, 010021, China, E-mail: yczuo@ 123456imu.edu.cn

                Co-first author.

                Author information
                http://orcid.org/0000-0003-4747-7319
                Article
                Publisher ID: giy113
                DOI: 10.1093/gigascience/giy113
                PMC ID: 6204425
                PubMed ID: 30192940
                SO-VID: 1e9c3fd5-c161-44b0-a8ac-f0340f58e9cd
                Copyright © © The Author(s) 2018. Published by Oxford University Press.
                License:

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                Date received : 05 January 2018
                Date revision received : 30 June 2018
                Date accepted : 29 August 2018
                Page count
                Pages: 14
                Funding
                Funded by: State Key Development Program for Basic Research of China
                Award ID: 2012CB22306
                Funded by: National Natural Science Foundation of China 10.13039/501100001809
                Award ID: 31660301
                Funded by: Natural Science Foundation of Inner Mongolia 10.13039/501100004763
                Award ID: 2013ZD06
                Funded by: State Key Laboratory of Agricultural Genomics
                Award ID: 2011DQ782025
                Categories
                Subject: Research

                Keywords: genome,transcriptome,chrysolophus,plumage,coloration
                Data availability:
                Keywords: genome, transcriptome, chrysolophus, plumage, coloration

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