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. 2018 Apr 16;16(1):40.
doi: 10.1186/s12915-018-0509-4.

Madagascar ground gecko genome analysis characterizes asymmetric fates of duplicated genes

Yuichiro Hara  1   2 , Miki Takeuchi  3 , Yuka Kageyama  1   4 , Kaori Tatsumi  1   2 , Masahiko Hibi  3   5 , Hiroshi Kiyonari  6   7   8   9 , Shigehiro Kuraku  10   11
Affiliations

Madagascar ground gecko genome analysis characterizes asymmetric fates of duplicated genes

Yuichiro Hara et al. BMC Biol. .

Abstract

Background: Conventionally, comparison among amniotes - birds, mammals, and reptiles - has often been approached through analyses of mammals and, for comparison, birds. However, birds are morphologically and physiologically derived and, moreover, some parts of their genomes are recognized as difficult to sequence and/or assemble and are thus missing in genome assemblies. Therefore, sequencing the genomes of reptiles would aid comparative studies on amniotes by providing more comprehensive coverage to help understand the molecular mechanisms underpinning evolutionary changes.

Results: Herein, we present the whole genome sequences of the Madagascar ground gecko (Paroedura picta), a promising study system especially in developmental biology, and used it to identify changes in gene repertoire across amniotes. The genome-wide analysis of the Madagascar ground gecko allowed us to reconstruct a comprehensive set of gene phylogenies comprising 13,043 ortholog groups from diverse amniotes. Our study revealed 469 genes retained by some reptiles but absent from available genome-wide sequence data of both mammals and birds. Importantly, these genes, herein collectively designated as 'elusive' genes, exhibited high nucleotide substitution rates and uneven intra-genomic distribution. Furthermore, the genomic regions flanking these elusive genes exhibited distinct characteristics that tended to be associated with increased gene density, repeat element density, and GC content.

Conclusion: This highly continuous and nearly complete genome assembly of the Madagascar ground gecko will facilitate the use of this species as an experimental animal in diverse fields of biology. Gene repertoire comparisons across amniotes further demonstrated that the fate of a duplicated gene can be affected by the intrinsic properties of its genomic location, which can persist for hundreds of millions of years.

Keywords: disparity of genomic fields; gecko; gene duplication; gene loss; gene repertoire evolution; phylome.

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Conflict of interest statement

Ethics approval and consent to participate

All experiments and housing using the Madagascar ground gecko were conducted in accordance with guidelines approved by the RIKEN Animal Experiments Committee (Approval IDs AH25–05-1 and AH24–04–6). The experiments using zebrafish were approved by the Nagoya University animal experiment committee (Approval No. 2016022203).

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
Quality assessment of the P. picta genome assembly. (a) P. picta adult individuals with different color phases. (b) A scatter plot of the assessments of assembly quality: CEGMA completeness scores referring to the CVG and N50 scaffold lengths for available reptile genome assemblies. Each reptile genome assembly is shown with a dot. Detailed statistics of assembly quality are included in Additional file 1: Table S2. These metrics were calculated with the webserver gVolante [90]. (b) Synteny conservation between the longest scaffold of the P. picta genome assembly (scaffold00000001; 33 Mb long) and a part of the green anole chromosome 3 (10–48 Mb in 204 Mb long). Green and gray boxes are protein-coding genes in the gecko and anole genome assembly, respectively, and blue bands indicate orthology between gecko and anole genes
Fig. 2
Fig. 2
Quantification of gene origination, duplication, and loss in amniote evolution. Bars beside inner branches of the amniote species tree denote numbers of origination, duplication, and loss of genes per million years scaled by the numbers at the branch (i). Gene origination, duplication, and loss events in the terminal branches are not counted because they can be largely influenced by rampant misidentifications in gene prediction. Additionally, inferred ancestral gene repertoires are shown at internal nodes of the tree. Branch lengths are proportional to inferred divergence times shown in Additional file 5: Figure S3, and the details of these values are included in Table 2. The gene number at the ancestral nodes of birds shown in italics is likely underestimated due to underrepresentation of certain genomic regions in whole genome sequencing [–5]
Fig. 3
Fig. 3
Asymmetric evolution of FoxG genes. (a) The maximum likelihood tree of the FoxG genes using 243 aligned sites of amino acid sequences with the JTT + I + G4 amino acid substitution model. The ultrafast bootstrap approximation values of 75 or more are indicated at the nodes. FoxG2 and FoxG1 are categorized in the elusive and non-elusive genes defined in this study, respectively. The absence of FoxG2 orthologs in mammals and birds may be attributable to information loss or secondary gene loss (see Discussion). Whole-mount in situ hybridization for FoxG1 (b) and FoxG2 (f) genes using 3 and 4 dpo embryos of the Madagascar ground gecko, respectively. Expression signals of FoxG1 (c–e) and FoxG2 (g) by sections of in situ hybridization using 2 dpo embryos. FoxG1 is expressed in the otocyst, vestibulocochlear ganglion (shown by arrowheads in c), retina (shown by arrowheads in d), and cerebrum (shown by arrowheads in e), whereas FoxG2 is specifically expressed in the vestibulocochlear ganglion (shown by an arrow in g). (h) The levels of the sections for the gecko embryo are indicated by dashed lines. Whole-mount in situ hybridization for foxg1a (i, the FoxG1 ortholog), foxg1c (m, the FoxG2 ortholog), and foxg1d (o) and foxg1b (t) (the FoxG3 orthologs) using 2 dpf zebrafish embryos. Expression signals of foxg1a (j–l), foxg1c (n), and foxg1d (p–s) by sections of in situ hybridization using the 2 dpf embryos. Any expression signals of foxg1b were not observed in the ganglion. (u) The levels of the sections for the zebrafish embryos are indicated by dashed lines. Scale bars in b–f, 1 mm, and those in i, j, m, o, and t, 100 μm. k, l, n, and p–s have the same scale as j
Fig. 4
Fig. 4
Evolutionary rates of elusive genes and non-elusive genes. Scatter plots of the (a) KA, (b) KS, and (c) KA/KS values of the orthologs of the elusive genes and their non-elusive paralogs between Madagascar ground gecko and Japanese gecko, and those of the (d) KA, (e) KS, and (f) KA/KS values of the orthologs between Madagascar ground gecko and green anole. Each dot denotes an ortholog pair of elusive genes and their non-elusive paralogs. All of the statistical tests were conducted with the Wilcoxon signed-rank test
Fig. 5
Fig. 5
Genomic characteristics of elusive genes and their non-elusive paralogs in the P. picta genome. (a) Fractions of the 259 elusive genes flanked by other elusive genes (100 kb on both ends). The expected values, which assumed a random distribution of elusive genes, are shown in a dotted line. The observed and expected values are significantly different (p = 8.27 × 10− 27, the exact test of goodness-of-fit). (b) Frequency distributions of the genes flanking the elusive and non-elusive genes related to the numbers of species retaining the orthologs. The genes that harbored one or more actinopterygians or coelacanth orthologs were used. The two distributions are significantly different from each other (p = 4.18 × 10− 19, Mann–Whitney U test). (c) Comparison of synonymous substitution rates (KS) between the genes flanking the elusive and the non-elusive genes. The distributions are significantly different between the two groups (p = 1.23 × 10− 17, Mann–Whitney U test). The KS values were computed for the individual ortholog pairs of the Madagascar ground gecko and Japanese gecko. (d) Gene densities of the flanking regions of the elusive genes and their non-elusive paralogs, which are significantly different from each other (p = 4.44 × 10− 16, Wilcoxon signed-rank test). Each dot denotes the gene densities of the flanking regions of an elusive gene and its non-elusive paralog. (e) Repeat densities of the genomic regions consisting of the elusive genes or non-elusive paralogs with their flanking regions, which are significantly different between the two groups (p = 1.58 × 10− 4, Wilcoxon signed-rank test). The repeats annotated with RepeatMasker excluding simple repeats and low-complexity regions were used. (f) GC content of the genomic regions consisting of the elusive genes or non-elusive paralogs with their flanking regions, which exhibit a significant difference between the two groups (p = 1.11 × 10− 10, Wilcoxon signed-rank test)
Fig. 6
Fig. 6
Disparity of genomic fields. A permissive field (a brown bar) that includes elusive genes displays elevated GC content, high gene density, high repeat density, and high mutation rate in comparison with other regions (a black bar)
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References

    1. Hedges SB, Marin J, Suleski M, Paymer M, Kumar S. Tree of life reveals clock-like speciation and diversification. Mol Biol Evol. 2015;32(4):835–845. doi: 10.1093/molbev/msv037. - DOI - PMC - PubMed
    1. International Chicken Genome Sequencing Consortium Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature. 2004;432(7018):695–716. doi: 10.1038/nature03154. - DOI - PubMed
    1. Bornelov S, Seroussi E, Yosefi S, Pendavis K, Burgess SC, Grabherr M, et al. Correspondence on Lovell et al.: identification of chicken genes previously assumed to be evolutionarily lost. Genome Biol. 2017;18(1):112. doi: 10.1186/s13059-017-1231-1. - DOI - PMC - PubMed
    1. Botero-Castro F, Figuet E, Tilak MK, Nabholz B, Galtier N. Avian genomes revisited: hidden genes uncovered and the rates vs. traits paradox in birds. Mol Biol Evol. 2017;34(12):3123–3131. doi: 10.1093/molbev/msx236. - DOI - PubMed
    1. Warren WC, Hillier LW, Tomlinson C, Minx P, Kremitzki M, Graves T, et al. A new chicken genome assembly provides insight into avian genome structure. G3 (Bethesda) 2017;7(1):109–117. doi: 10.1534/g3.116.035923. - DOI - PMC - PubMed

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