Population Scale Analysis of Centromeric Satellite DNA Reveals Highly Dynamic Evolutionary Patterns and Genomic Organization in Long-Tailed and Rhesus Macaques
Abstract
:1. Introduction
2. Materials and Methods
2.1. Specimen Collection and DNA Extraction
2.2. Fosmid DNA Library and Isolation of Satellite DNA Sequences
2.3. Cell Culture and Chromosome Preparation
2.4. C-Banding
2.5. Fluorescence In Situ Hybridization Mapping of Cen-satDNA
2.6. Centromeric Satellite DNA Sequencing in Macaques
2.7. Identification of Putative Satellite DNA in Long-Tailed and Rhesus Macaque Populations
2.8. Genomic Organization and Comparative Genomics of Satellite DNA Sequences
2.9. Tests of Genetic Diversity within and between Macaque Populations
3. Results
3.1. Karyotype and C-Positive Heterochromatin of Long-Tailed Macaque
3.2. Isolation of Highly Repetitive DNA Sequences and Their Nucleotide Sequences
3.3. Striking Sequence Variability of Cen-satDNA in Macaque Populations
3.4. Genomic Organization of Cen-satDNA Sequences
3.5. Genetic Diversity within and between Macaque Populations
4. Discussion
4.1. Turnover of Cen-satDNA Sequences with Multiple Subfamilies in Long-Tailed and Rhesus Macaque Populations
4.2. Nonrandom Cen-satDNA Sequences in Long-Tailed and Rhesus Macaque Chromosomes
4.3. Cen-satDNA in Long-Tailed and Rhesus Macaque Populations
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Sequence Lengths (bp) | GC Content | Motif Sequences |
---|---|---|
170–174 | 36.8–41.5%, (average of 39.5%) | Motif 1: CTCACAGAGTTAC Motif 2: CTTTCTGAGAAACT |
Population | Tajima’s D Statistic | Fu and Li’s D Test | Fu and Li’s F Test |
---|---|---|---|
BPN | 1.34 ns | 0.343 ns | 0.872 ns |
BSS | 2.69 ns | 0.450 ns | 1.547 ns |
KN | 1.17 ns | −0.603 ns | 0.200 ns |
KNG | 3.52 ns | −0.842 ns | 0.918 ns |
KNKTK | 2.72 ns | 0.085 ns | 1.218 ns |
KSP | 1.15 ns | −0.397 ns | 0.284 ns |
MFRC | −1.01 ns | 0.398 ns | 0.519 ns |
SSD | 3.87 ns | -0.549 ns | 1.221 ns |
SY | 2.36 ns | 0.885 ns | 1.580 ns |
WHM | 1.57 ns | 0.235 ns | 0.948 ns |
WKH | 0.82 ns | −0.289 ns | 0.228 ns |
WKT | 4.04 ns | 0.214 ns | 1.468 ns |
WPN | N/A | N/A | N/A |
WPT | 1.98 ns | 0.113 ns | 0.942 ns |
WSK | 0.88 ns | −0.285 ns | 0.284 ns |
WTM | 1.05 ns | −0.153 ns | 0.494 ns |
WTPMH | 3.03 ns | 0.350 ns | 1.629 ns |
WTT | 1.45 ns | −0.024 ns | 0.672 ns |
Population | N | Na | Ne | I | Ho | He | uHe | F | |
---|---|---|---|---|---|---|---|---|---|
BPN | Mean | 17 | 0.836 | 0.778 | 0.128 | 0.149 | 0.088 | 0.111 | −0.597 |
S.E. | 0.067 | 0.061 | 0.022 | 0.028 | 0.016 | 0.021 | 0.031 | ||
BSS | Mean | 40 | 1.008 | 0.921 | 0.197 | 0.198 | 0.136 | 0.170 | −0.383 |
S.E. | 0.072 | 0.065 | 0.026 | 0.031 | 0.018 | 0.024 | 0.058 | ||
KN | Mean | 18 | 0.820 | 0.714 | 0.134 | 0.139 | 0.089 | 0.105 | −0.445 |
S.E. | 0.072 | 0.061 | 0.021 | 0.025 | 0.015 | 0.018 | 0.032 | ||
KNG | Mean | 19 | 0.758 | 0.691 | 0.120 | 0.133 | 0.081 | 0.099 | −0.535 |
S.E. | 0.069 | 0.061 | 0.021 | 0.026 | 0.015 | 0.019 | 0.031 | ||
KNKTK | Mean | 20 | 0.875 | 0.847 | 0.162 | 0.213 | 0.115 | 0.162 | −0.801 |
S.E. | 0.069 | 0.067 | 0.025 | 0.034 | 0.018 | 0.027 | 0.026 | ||
KSP | Mean | 21 | 1.063 | 0.915 | 0.188 | 0.190 | 0.125 | 0.152 | −0.417 |
S.E. | 0.072 | 0.059 | 0.024 | 0.027 | 0.016 | 0.021 | 0.028 | ||
MFRC | Mean | 10 | 0.523 | 0.512 | 0.126 | 0.172 | 0.090 | 0.122 | −0.891 |
S.E. | 0.070 | 0.068 | 0.023 | 0.033 | 0.017 | 0.023 | 0.021 | ||
SSD | Mean | 20 | 0.852 | 0.788 | 0.174 | 0.217 | 0.121 | 0.189 | −0.693 |
S.E. | 0.074 | 0.068 | 0.025 | 0.034 | 0.018 | 0.030 | 0.033 | ||
SY | Mean | 14 | 0.883 | 0.804 | 0.123 | 0.137 | 0.083 | 0.106 | −0.521 |
S.E. | 0.066 | 0.058 | 0.021 | 0.027 | 0.015 | 0.020 | 0.033 | ||
WHM | Mean | 20 | 0.914 | 0.824 | 0.150 | 0.138 | 0.102 | 0.130 | −0.293 |
S.E. | 0.070 | 0.062 | 0.023 | 0.027 | 0.016 | 0.022 | 0.057 | ||
WKH | Mean | 19 | 0.875 | 0.779 | 0.132 | 0.139 | 0.088 | 0.109 | −0.459 |
S.E. | 0.069 | 0.059 | 0.021 | 0.026 | 0.015 | 0.020 | 0.030 | ||
WKT | Mean | 21 | 0.875 | 0.780 | 0.177 | 0.197 | 0.121 | 0.157 | −0.505 |
S.E. | 0.076 | 0.067 | 0.024 | 0.031 | 0.017 | 0.024 | 0.045 | ||
WPN | Mean | 6 | 0.727 | 0.715 | 0.110 | 0.140 | 0.078 | 0.125 | −0.767 |
S.E. | 0.064 | 0.063 | 0.022 | 0.030 | 0.016 | 0.026 | 0.042 | ||
WPT | Mean | 40 | 1.094 | 0.978 | 0.214 | 0.216 | 0.146 | 0.202 | −0.377 |
S.E. | 0.072 | 0.064 | 0.026 | 0.032 | 0.018 | 0.028 | 0.056 | ||
WSK | Mean | 20 | 1.070 | 1.024 | 0.183 | 0.228 | 0.128 | 0.188 | −0.720 |
S.E. | 0.063 | 0.059 | 0.026 | 0.034 | 0.018 | 0.029 | 0.028 | ||
WTM | Mean | 20 | 0.766 | 0.729 | 0.125 | 0.160 | 0.088 | 0.110 | −0.732 |
S.E. | 0.068 | 0.064 | 0.023 | 0.031 | 0.016 | 0.022 | 0.031 | ||
WTPMH | Mean | 33 | 1.695 | 1.428 | 0.359 | 0.382 | 0.241 | 0.278 | −0.420 |
S.E. | 0.041 | 0.037 | 0.025 | 0.035 | 0.018 | 0.023 | 0.045 | ||
WTT | Mean | 20 | 1.648 | 1.345 | 0.325 | 0.323 | 0.214 | 0.240 | −0.373 |
S.E. | 0.045 | 0.036 | 0.024 | 0.030 | 0.017 | 0.020 | 0.031 | ||
Total | Mean | 377 | 0.960 | 0.865 | 0.174 | 0.193 | 0.119 | 0.153 | −0.510 |
S.E. | 0.017 | 0.015 | 0.006 | 0.007 | 0.004 | 0.006 | 0.010 |
Source | df | Sum of Squares | % Variation | F-Statistics |
---|---|---|---|---|
among populations | 17 | 821.495 | 4% | FST = 0.038 * |
among individuals | 359 | 8864.168 | 67% | FIS = 0.701 * |
within individuals | 377 | 1634.500 | 29% | FIT = 0.713 * |
total | 753 | 11320.163 | 100% |
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Singchat, W.; Ahmad, S.F.; Jaisamut, K.; Panthum, T.; Ariyaraphong, N.; Kraichak, E.; Muangmai, N.; Duengkae, P.; Payungporn, S.; Malaivijitnond, S.; et al. Population Scale Analysis of Centromeric Satellite DNA Reveals Highly Dynamic Evolutionary Patterns and Genomic Organization in Long-Tailed and Rhesus Macaques. Cells 2022, 11, 1953. https://doi.org/10.3390/cells11121953
Singchat W, Ahmad SF, Jaisamut K, Panthum T, Ariyaraphong N, Kraichak E, Muangmai N, Duengkae P, Payungporn S, Malaivijitnond S, et al. Population Scale Analysis of Centromeric Satellite DNA Reveals Highly Dynamic Evolutionary Patterns and Genomic Organization in Long-Tailed and Rhesus Macaques. Cells. 2022; 11(12):1953. https://doi.org/10.3390/cells11121953
Chicago/Turabian StyleSingchat, Worapong, Syed Farhan Ahmad, Kitipong Jaisamut, Thitipong Panthum, Nattakan Ariyaraphong, Ekaphan Kraichak, Narongrit Muangmai, Prateep Duengkae, Sunchai Payungporn, Suchinda Malaivijitnond, and et al. 2022. "Population Scale Analysis of Centromeric Satellite DNA Reveals Highly Dynamic Evolutionary Patterns and Genomic Organization in Long-Tailed and Rhesus Macaques" Cells 11, no. 12: 1953. https://doi.org/10.3390/cells11121953