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Structure and evolution of the filaggrin gene repeated region in primates

Romero, Vanessa, Hosomichi, Kazuyoshi, Nakaoka, Hirofumi, Shibata, Hiroki, Inoue, Ituro·2017·BMC Evolutionary Biology
DOI 10.1186/s12862-016-0851-5PMC PMC5225520
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Abstract

BACKGROUND: The evolutionary dynamics of repeat sequences is quite complex, with some duplicates never having differentiated from each other. Two models can explain the complex evolutionary process for repeated genes-concerted and birth-and-death, of which the latter is driven by duplications maintained by selection. Copy number variations caused by random duplications and losses in repeat regions may modulate molecular pathways and therefore affect phenotypic characteristics in a population, resulting in individuals that are able to adapt to new environments. In this study, we investigated the filaggrin gene (FLG), which codes for filaggrin-an important component of the outer layers of mammalian skin-and contains tandem repeats that exhibit copy number variation between and within species. To examine which model best fits the evolutionary pathway for the complete tandem repeats within a single exon of FLG, we determined the repeat sequences in crab-eating macaque (Macaca fascicularis), orangutan (Pongo abelii), gorilla (Gorilla gorilla), and chimpanzee (Pan troglodytes) and compared these with the sequence in human (Homo sapiens). RESULTS: In this study we compared concerted and birth-and-death evolution models, commonly used for gene copies. We found that there is high nucleotide diversity between filaggrin repeat regions, which fits the birth-and-death model. Phylogenetic analyses also suggested that independent duplication events created the repeat sequences in crab-eating macaques and orangutans, while different duplication and loss events created the repeats in gorillas, chimpanzees, and humans. Comparison of the repeat sequences detected purifying selection within species and lineage-specific duplications across species. We also found variation in the length of the repeated region within species such as chimpanzee and crab-eating macaque. CONCLUSIONS: We conclude that the copy number variation in the repeat sequences of FLG between primates may be a consequence of species-specific divergence and expansion.

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Fig. 1 Partial and complete repeat sequences of FLG in human, chimpanzee, gorilla, orangutan, and crab-eating macaque. Left shows the repeat order of FLG in these primates based on the sequences from the National Center for Biotechnology Information database; the gorilla sequence had an unframed repeat at the end of the sequence, and the orangutan sequence had unframed repeats in the middle. Right shows the repeat order of FLG sequences acquired through the use of both PacBio RSII and MiSeq in this study. Black = partial repeats, white = complete repeats, and gray = regions with gaps. The nucleotide length of each repeat is shown beneath each repeat. The number of repeats varies between species
Fig. 1 Partial and complete repeat sequences of FLG in human, chimpanzee, gorilla, orangutan, and crab-eating macaque. Left shows the repeat order of FLG in these primates based on the sequences from the National Center for Biotechnology Information database; the gorilla sequence had an unframed repeat at the end of the sequence, and the orangutan sequence had unframed repeats in the middle. Right shows the repeat order of FLG sequences acquired through the use of both PacBio RSII and MiSeq in this study. Black = partial repeats, white = complete repeats, and gray = regions with gaps. The nucleotide length of each repeat is shown beneath each repeat. The number of repeats varies between speciesCC BY · PubMed Central
Fig. 2 Maximum likelihood tree reconstruction using all complete repeats in these primates and the following parameters: partial deletion option, Tamura-Nei model with gamma distribution and invariable sites, nearest-neighbor-interchange heuristic method, 1000 bootstrap resampling, and a cutoff value of 50%. Bootstrap values are shown at the beginning of each branch. Crab-eating macaque was used as an outgroup. Crab-eating macaque repeats and orangutan repeats grouped into their own clusters (“crab-eating macaque cluster” and “orangutan cluster,” respectively). By contrast, the gorilla repeats, chimpanzee repeats, and human repeats are scattered across the “gorilla/chimpanzee/human cluster.” We divided the “gorilla/chimpanzee/human cluster” into subclusters in accordance with the reconciled tree reconstruction shown in Fig. 3
Fig. 2 Maximum likelihood tree reconstruction using all complete repeats in these primates and the following parameters: partial deletion option, Tamura-Nei model with gamma distribution and invariable sites, nearest-neighbor-interchange heuristic method, 1000 bootstrap resampling, and a cutoff value of 50%. Bootstrap values are shown at the beginning of each branch. Crab-eating macaque was used as an outgroup. Crab-eating macaque repeats and orangutan repeats grouped into their own clusters (“crab-eating macaque cluster” and “orangutan cluster,” respectively). By contrast, the gorilla repeats, chimpanzee repeats, and human repeats are scattered across the “gorilla/chimpanzee/human cluster.” We divided the “gorilla/chimpanzee/human cluster” into subclusters in accordance with the reconciled tree reconstruction shown in Fig. 3CC BY · PubMed Central
Fig. 3 “Reconciled” trees using complete repeats of FLG in human, chimpanzee, gorilla, orangutan, and crab-eating macaque. a “Reconciled” gene tree indicating duplication (red squares) and loss events (light gray italics) from the most common ancestor of these primates: the crab-eating macaque repeats duplicated 11 times, orangutan repeats duplicated 8 times, and gorilla/chimpanzee/human repeats duplicated 18 times, and in human, the counterpart to chimpanzee-repeat 9 was lost, while in chimpanzee, the counterparts to human-repeats 10 and 8 were lost, and in gorilla, the counterpart to human-repeat 2, 9 and 8 and chimpanzee-repeat 8 was lost. b “Reconciled” species tree indicating duplication and loss events in each species from their most common ancestor: crab-eating macaque repeats duplicated 11 times, orangutan repeats duplicated 8 times, gorilla repeats duplicated 6 times, and chimpanzee repeats duplicated 3 times, while the most common ancestor between human and chimpanzee duplicated 6 times, and the most common ancestor between human, chimpanzee, and gorilla duplicated 4 times; and 1 repeat was lost in gorilla, 2 repeats were lost in chimpanzee, and 1 repeat was lost in human. The number of repeats found in each species is provided in parentheses
Fig. 3 “Reconciled” trees using complete repeats of FLG in human, chimpanzee, gorilla, orangutan, and crab-eating macaque. a “Reconciled” gene tree indicating duplication (red squares) and loss events (light gray italics) from the most common ancestor of these primates: the crab-eating macaque repeats duplicated 11 times, orangutan repeats duplicated 8 times, and gorilla/chimpanzee/human repeats duplicated 18 times, and in human, the counterpart to chimpanzee-repeat 9 was lost, while in chimpanzee, the counterparts to human-repeats 10 and 8 were lost, and in gorilla, the counterpart to human-repeat 2, 9 and 8 and chimpanzee-repeat 8 was lost. b “Reconciled” species tree indicating duplication and loss events in each species from their most common ancestor: crab-eating macaque repeats duplicated 11 times, orangutan repeats duplicated 8 times, gorilla repeats duplicated 6 times, and chimpanzee repeats duplicated 3 times, while the most common ancestor between human and chimpanzee duplicated 6 times, and the most common ancestor between human, chimpanzee, and gorilla duplicated 4 times; and 1 repeat was lost in gorilla, 2 repeats were lost in chimpanzee, and 1 repeat was lost in human. The number of repeats found in each species is provided in parenthesesCC BY · PubMed Central
Fig. 4 “Divergence” tree reconstruction using all complete repeats of FLG in five primate species. The following parameters were used: the site model TN93, a substitution rate with gamma distribution = 4, a log-normal relaxed clock, and the birth-and-death model for all three nucleotide positions. The x-axis scale is time in Mya. The crab-eating macaque ancestor repeat diverged around 28 Mya, while the orangutan ancestor repeat diverged around 21 Mya. The gorilla/chimpanzee/human repeats duplicated during the last 9 Mya, while the crab-eating macaque repeats duplicated in the last 5.5 Mya
Fig. 4 “Divergence” tree reconstruction using all complete repeats of FLG in five primate species. The following parameters were used: the site model TN93, a substitution rate with gamma distribution = 4, a log-normal relaxed clock, and the birth-and-death model for all three nucleotide positions. The x-axis scale is time in Mya. The crab-eating macaque ancestor repeat diverged around 28 Mya, while the orangutan ancestor repeat diverged around 21 Mya. The gorilla/chimpanzee/human repeats duplicated during the last 9 Mya, while the crab-eating macaque repeats duplicated in the last 5.5 MyaCC BY · PubMed Central
Fig. 5 Repeat order of gorilla, chimpanzee, and human FLG repeats, as inferred by phylogenetic and “reconciled” tree. Gorilla duplicated repeats “C,” “D,” and “G,” chimpanzee and human duplicated repeat “A,” and human duplicated repeat “B” are shown. In chimpanzee, the counterpart to human-repeats B-2 has been lost, while in human, the counterpart to chimpanzee-repeat “I” has been lost, and in chimpanzee, the counterparts to human and gorilla-repeat H have been lost. In gorilla, the counterpart to human and chimpanzee repeats B has been lost
Fig. 5 Repeat order of gorilla, chimpanzee, and human FLG repeats, as inferred by phylogenetic and “reconciled” tree. Gorilla duplicated repeats “C,” “D,” and “G,” chimpanzee and human duplicated repeat “A,” and human duplicated repeat “B” are shown. In chimpanzee, the counterpart to human-repeats B-2 has been lost, while in human, the counterpart to chimpanzee-repeat “I” has been lost, and in chimpanzee, the counterparts to human and gorilla-repeat H have been lost. In gorilla, the counterpart to human and chimpanzee repeats B has been lostCC BY · PubMed Central

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Metadata

Authors
Romero, V., Hosomichi, K., Nakaoka, H., Shibata, H., & Inoue, I.
Venue
BMC Evolutionary Biology
Publisher
Springer Science and Business Media LLC
Published
2017-01-11
Volume
17
Issue
1
ISSN
1471-2148
DOI
10.1186/s12862-016-0851-5
PMC
PMC5225520
Cited by
11
References
1
Language
en
Funders
The study was funded by the basal running budget from the National Institute of Genetics-Japan”.

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