Kinetochore proteins and microtubule-destabilizing factors are fast evolving in eutherian mammals.
development and evolution
genomics
life history evolution
mammals
molecular evolution
proteomics
sexual selection
Journal
Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478
Informations de publication
Date de publication:
03 2021
03 2021
Historique:
received:
16
06
2020
accepted:
14
01
2021
pubmed:
22
1
2021
medline:
22
6
2021
entrez:
21
1
2021
Statut:
ppublish
Résumé
Centromeres have central functions in chromosome segregation, but centromeric DNA and centromere-binding proteins evolve rapidly in most eukaryotes. The selective pressure(s) underlying the fast evolution of centromere-binding proteins are presently unknown. An attractive possibility is that selfish centromeres promote their preferential inclusion in the oocyte and centromeric proteins evolve to suppress meiotic drive (centromere drive hypothesis). We analysed the selective patterns of mammalian genes that encode kinetochore proteins and microtubule (MT)-destabilizing factors. We show that several of these proteins evolve at the same rate or faster than proteins with a role in centromere specification. Elements of the kinetochore that bind MTs or that bridge the interaction between MTs and the centromere represented the major targets of positive selection. These data are in line with the possibility that the genetic conflict fuelled by meiotic drive extends beyond genes involved in centromere specification. However, we cannot exclude that different selective pressures underlie the rapid evolution of MT-destabilizing factors and kinetochore components. Whatever the nature of such pressures, they must have been constant during the evolution of eutherian mammals, as we found a surprisingly good correlation in dN/dS (ratio of the rate of nonsynonymous and synonymous substitutions) across orders/clades. Finally, when phylogenetic relationships were accounted for, we found little evidence that the evolutionary rates of these genes change with testes size, a proxy for sperm competition. Our data indicate that, in analogy to centromeric proteins, kinetochore components are fast evolving in mammals. This observation may imply that centromere drive plays out at multiple levels or that these proteins adapt to lineage-specific centromeric features.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1505-1515Informations de copyright
© 2021 John Wiley & Sons Ltd.
Références
Akera, T., Trimm, E., & Lampson, M. A. (2019). Molecular strategies of meiotic cheating by selfish centromeres. Cell, 178, 1132-1144.e10.
Anisimova, M., Nielsen, R., & Yang, Z. (2003). Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites. Genetics, 164, 1229-1236.
Arslan, A., & Zima, J. (2015). Heterochromatin distribution and localization of nucleolar organizing regions in the 2n=56 cytotypes of Nannospalax xanthodon and N. ehrenbergi from Turkey. Zoological Studies, 54, 6.
Ávila Robledillo, L., Neumann, P., Koblížková, A., Novák, P., Vrbová, I., & Macas, J. (2020). Extraordinary sequence diversity and promiscuity of centromeric satellites in the legume tribe fabeae. Molecular Biology and Evolution, 37, 2341-2356.
Baker, R. R., & Shackelford, T. K. (2018). A comparison of paternity data and relative testes size as measures of level of sperm competition in the Hominoidea. American Journal of Physical Anthropology, 165, 421-443.
Ben Faleh, A., Ben Othmen, A., Said, K., & Granjon, L. (2010). Karyotypic variation in two species of jerboas Jaculus jaculus and Jaculus orientalis (Rodentia, Dipodidae) from Tunisia. Folia Biologica, 58, 229-236.
Bensasson, D., Zarowiecki, M., Burt, A., & Koufopanou, V. (2008). Rapid evolution of yeast centromeres in the absence of drive. Genetics, 178, 2161-2167.
Caldas, G. V., & DeLuca, J. G. (2014). KNL1: Bringing order to the kinetochore. Chromosoma, 123, 169-181.
Cheeseman, I. M. (2014). The kinetochore. Cold Spring Harbor Perspectives in Biology, 6, a015826.
Cheeseman, I. M., & Desai, A. (2008). Molecular architecture of the kinetochore-microtubule interface. Nature Reviews. Molecular Cell Biology, 9, 33-46.
Chmátal, L., Gabriel, S. I., Mitsainas, G. P., Martínez-Vargas, J., Ventura, J., Searle, J. B., Schultz, R. M., & Lampson, M. A. (2014). Centromere strength provides the cell biological basis for meiotic drive and karyotype evolution in mice. Current Biology, 24, 2295-2300.
Daniel, A. (2002). Distortion of female meiotic segregation and reduced male fertility in human Robertsonian translocations: Consistent with the centromere model of co-evolving centromere DNA/centromeric histone (CENP-A). American Journal of Medical Genetics, 111, 450-452.
Dixson, A. F., & Anderson, M. J. (2004). Sexual behavior, reproductive physiology and sperm competition in male mammals. Physiology & Behavior, 83, 361-371.
Dumont, M., Gamba, R., Gestraud, P., Klaasen, S., Worrall, J. T., De Vries, S. G., Boudreau, V., Salinas-Luypaert, C., Maddox, P. S., Lens, S. M., Kops, G. J., McClelland, S. E., Miga, K. H., & Fachinetti, D. (2020). Human chromosome-specific aneuploidy is influenced by DNA-dependent centromeric features. The EMBO Journal, 39, e102924.
Eaker, S., Pyle, A., Cobb, J., & Handel, M. A. (2001). Evidence for meiotic spindle checkpoint from analysis of spermatocytes from Robertsonian-chromosome heterozygous mice. Journal of Cell Science, 114, 2953-2965.
Elde, N. C., Roach, K. C., Yao, M. C., & Malik, H. S. (2011). Absence of positive selection on centromeric histones in Tetrahymena suggests unsuppressed centromere: Drive in lineages lacking male meiosis. Journal of Molecular Evolution, 72, 510-520.
Elowe, S. (2011). Bub1 and BubR1: At the interface between chromosome attachment and the spindle checkpoint. Molecular and Cellular Biology, 31, 3085-3093.
Emlen, S. T., & Oring, L. W. (1977). Ecology, sexual selection, and the evolution of mating systems. Science, 197, 215-223.
Fishman, L., & Kelly, J. K. (2015). Centromere-associated meiotic drive and female fitness variation in Mimulus. Evolution; International Journal of Organic Evolution, 69, 1208-1218.
Guindon, S., Delsuc, F., Dufayard, J. F., & Gascuel, O. (2009). Estimating maximum likelihood phylogenies with PhyML. Methods in Molecular Biology, 537, 113-137.
Hartley, G., & O’Neill, R. J. (2019). Centromere repeats: Hidden gems of the genome. Genes, 10, 223. https://doi.org/10.3390/genes10030223
Hatanaka, F., Matsubara, C., Myung, J., Yoritaka, T., Kamimura, N., Tsutsumi, S., Kanai, A., Suzuki, Y., Sassone-Corsi, P., Aburatani, H., Sugano, S., & Takumi, T. (2010). Genome-wide profiling of the core clock protein BMAL1 targets reveals a strict relationship with metabolism. Molecular and Cellular Biology, 30, 5636-5648.
Hauffe, H. C., & Searle, J. B. (1998). Chromosomal heterozygosity and fertility in house mice (Mus musculus domesticus) from Northern Italy. Genetics, 150, 1143-1154.
Henikoff, S., Ahmad, K., & Malik, H. S. (2001). The centromere paradox: Stable inheritance with rapidly evolving DNA. Science, 293, 1098-1102.
Henikoff, S., & Malik, H. S. (2002). Centromeres: Selfish drivers. Nature, 417, 227.
Holman, L., Price, T. A., Wedell, N., & Kokko, H. (2015). Coevolutionary dynamics of polyandry and sex-linked meiotic drive. Evolution; International Journal of Organic Evolution, 69, 709-720.
Huang, Y. C., Lee, C. C., Kao, C. Y., Chang, N. C., Lin, C. C., Shoemaker, D., & Wang, J. (2016). Evolution of long centromeres in fire ants. BMC Evolutionary Biology, 16, 189.
Iwata-Otsubo, A., Dawicki-McKenna, J. M., Akera, T., Falk, S. J., Chmátal, L., Yang, K., Sullivan, B. A., Schultz, R. M., Lampson, M. A., & Black, B. E. (2017). Expanded satellite repeats amplify a discrete CENP-A nucleosome assembly site on chromosomes that drive in female meiosis. Current Biology, 27, 2365-2373.e8.
Johnson, M. K., & Wise, D. A. (2009). The kinetochore moves ahead: Contributions of molecular and genetic techniques to our understanding of mitosis. BioScience, 59, 933-943.
Kenagy, G. J., & Trombulak, S. C. (1986). Size and function of mammalian testes in relation to body size. Journal of Mammalogy, 67, 1-22.
Kim, J., Ishiguro, K., Nambu, A., Akiyoshi, B., Yokobayashi, S., Kagami, A., Ishiguro, T., Pendas, A. M., Takeda, N., Sakakibara, Y., Kitajima, T. S., Tanno, Y., Sakuno, T., & Watanabe, Y. (2015). Meikin is a conserved regulator of meiosis-I-specific kinetochore function. Nature, 517, 466-471.
Kosakovsky Pond, S. L., & Frost, S. D. (2005). Not so different after all: A comparison of methods for detecting amino acid sites under selection. Molecular Biology and Evolution, 22, 1208-1222.
Kosakovsky Pond, S. L., Posada, D., Gravenor, M. B., Woelk, C. H., & Frost, S. D. (2006). Automated phylogenetic detection of recombination using a genetic algorithm. Molecular Biology and Evolution, 23, 1891-1901.
Krenn, V., Overlack, K., Primorac, I., van Gerwen, S., & Musacchio, A. (2014). KI motifs of human Knl1 enhance assembly of comprehensive spindle checkpoint complexes around MELT repeats. Current Biology, 24, 29-39.
Kuchta-Gładysz, M., Grabowska-Joachimiak, A., Szeleszczuk, O., Szczerbal, I., Kociucka, B., & Niedbała, P. (2015). Karyotyping of Chinchilla lanigera Mol. (Rodentia, Chinchillidae). Caryologia, 68, 138-146.
Kursel, L. E., & Malik, H. S. (2018). The cellular mechanisms and consequences of centromere drive. Current Opinion in Cell Biology, 52, 58-65.
Lampson, M. A., & Cheeseman, I. M. (2011). Sensing centromere tension: Aurora B and the regulation of kinetochore function. Trends in Cell Biology, 21, 133-140.
Lartillot, N., & Poujol, R. (2011). A phylogenetic model for investigating correlated evolution of substitution rates and continuous phenotypic characters. Molecular Biology and Evolution, 28, 729-744.
Llano, E., Gómez, R., Gutiérrez-Caballero, C., Herrán, Y., Sánchez-Martín, M., Vázquez-Quiñones, L., Hernández, T., de Alava, E., Cuadrado, A., Barbero, J. L., Suja, J. A., & Pendás, A. M. (2008). Shugoshin-2 is essential for the completion of meiosis but not for mitotic cell division in mice. Genes & Development, 22, 2400-2413.
Maheshwari, S., Tan, E. H., West, A., Franklin, F. C., Comai, L., & Chan, S. W. (2015). Naturally occurring differences in CENH3 affect chromosome segregation in zygotic mitosis of hybrids. PLoS Genetics, 11, e1004970.
Malik, H. S. (2009). The centromere-drive hypothesis: A simple basis for centromere complexity. Progress in Molecular and Subcellular Biology, 48, 33-52.
Malik, H. S., & Bayes, J. J. (2006). Genetic conflicts during meiosis and the evolutionary origins of centromere complexity. Biochemical Society Transactions, 34, 569-573.
Malik, H. S., & Henikoff, S. (2009). Major evolutionary transitions in centromere complexity. Cell, 138, 1067-1082.
Manser, A., Lindholm, A. K., Simmons, L. W., & Firman, R. C. (2017). Sperm competition suppresses gene drive among experimentally evolving populations of house mice. Molecular Ecology, 26, 5784-5792.
McKinley, K. L., & Cheeseman, I. M. (2016). The molecular basis for centromere identity and function. Nature reviews.Molecular Cell Biology, 17, 16-29.
Miyazaki, S., Kim, J., Yamagishi, Y., Ishiguro, T., Okada, Y., Tanno, Y., Sakuno, T., & Watanabe, Y. (2017). Meikin-associated polo-like kinase specifies Bub1 distribution in meiosis I. Genes to Cells : Devoted to Molecular & Cellular Mechanisms, 22, 552-567.
Modi, W. S. (1987). Phylogenetic analyses of chromosomal banding patterns among the Nearctic Arvicolidae (Mammalia: Rodentia). Systematic Zoology, 36, 109-136.
Muro, Y., Masumoto, H., Yoda, K., Nozaki, N., Ohashi, M., & Okazaki, T. (1992). Centromere protein B assembles human centromeric alpha-satellite DNA at the 17-bp sequence, CENP-B box. The Journal of Cell Biology, 116, 585-596.
Murrell, B., Moola, S., Mabona, A., Weighill, T., Sheward, D., Pond, S. L. K., & Scheffler, K. (2013). FUBAR: A fast, unconstrained Bayesian approximation for inferring selection. Molecular Biology and Evolution, 30, 1196-1205.
Musacchio, A., & Desai, A. (2017). A molecular view of kinetochore assembly and function. Biology, 6, 5. https://doi.org/10.3390/biology6010005
Okada, M., Cheeseman, I. M., Hori, T., Okawa, K., McLeod, I. X., Yates, J. R. III, Desai, A., & Fukagawa, T. (2006). The CENP-H-I complex is required for the efficient incorporation of newly synthesized CENP-A into centromeres. Nature Cell Biology, 8, 446-457.
Pardo-Manuel de Villena, F., & Sapienza, C. (2001). Female meiosis drives karyotypic evolution in mammals. Genetics, 159, 1179-1189.
Pesenti, M. E., Prumbaum, D., Auckland, P., Smith, C. M., Faesen, A. C., Petrovic, A., Erent, M., Maffini, S., Pentakota, S., Weir, J. R., Lin, Y. C., Raunser, S., McAinsh, A. D., & Musacchio, A. (2018). Reconstitution of a 26-subunit human kinetochore reveals cooperative microtubule binding by CENP-OPQUR and NDC80. Molecular Cell, 71, 923-939.e10.
Pond, S. L., Frost, S. D., & Muse, S. V. (2005). HyPhy: Hypothesis testing using phylogenies. Bioinformatics, 21, 676-679.
Pontremoli, C., Forni, D., Cagliani, R., Pozzoli, U., Clerici, M., & Sironi, M. (2018). Evolutionary rates of mammalian telomere-stability genes correlate with karyotype features and female germline expression. Nucleic Acids Research, 46, 7153-7168.
Rosin, L. F., & Mellone, B. G. (2017). Centromeres drive a hard bargain. Trends in Genetics, 33, 101-117.
Schalch, T., & Steiner, F. A. (2017). Structure of centromere chromatin: From nucleosome to chromosomal architecture. Chromosoma, 126, 443-455.
Schueler, M. G., Swanson, W., Thomas, P. J., NISC Comparative Sequencing Program, & Green, E. D. (2010). Adaptive evolution of foundation kinetochore proteins in primates. Molecular Biology and Evolution, 27, 1585-1597.
Sironi, M., Cagliani, R., Forni, D., & Clerici, M. (2015). Evolutionary insights into host-pathogen interactions from mammalian sequence data. Nature reviews.Genetics, 16, 224-236.
Sotero-Caio, C., Baker, R. J., & Volleth, M. (2017). Chromosomal evolution in Chiroptera. Genes, 8, 272.
Talbert, P. B., Bryson, T. D., & Henikoff, S. (2004). Adaptive evolution of centromere proteins in plants and animals. Journal of Biology, 3, 18.
Tanaka, K., Chang, H. L., Kagami, A., & Watanabe, Y. (2009). CENP-C functions as a scaffold for effectors with essential kinetochore functions in mitosis and meiosis. Developmental Cell, 17, 334-343.
Tromer, E., Snel, B., & Kops, G. J. (2015). Widespread recurrent patterns of rapid repeat evolution in the kinetochore scaffold KNL1. Genome Biology and Evolution, 7, 2383-2393.
van Hooff, J. J., Tromer, E., van Wijk, L. M., Snel, B., & Kops, G. J. (2017). Evolutionary dynamics of the kinetochore network in eukaryotes as revealed by comparative genomics. EMBO Reports, 18, 1559-1571.
Varma, D., & Salmon, E. D. (2012). The KMN protein network-chief conductors of the kinetochore orchestra. Journal of Cell Science, 125, 5927-5936.
Vilella, A. J., Severin, J., Ureta-Vidal, A., Heng, L., Durbin, R., & Birney, E. (2009). EnsemblCompara GeneTrees: Complete, duplication-aware phylogenetic trees in vertebrates. Genome Research, 19, 327-335.
Vujošević, M., Rajičić, M., & Blagojević, J. (2018). B chromosomes in populations of mammals revisited. Genes, 9, 487. https://doi.org/10.3390/genes9100487
Wallace, B. M., Searle, J. B., & Everett, C. A. (2002). The effect of multiple simple Robertsonian heterozygosity on chromosome pairing and fertility of wild-stock house mice (Mus musculus domesticus). Cytogenetic and Genome Research, 96, 276-286.
Wernersson, R., & Pedersen, A. G. (2003). RevTrans: Multiple alignment of coding DNA from aligned amino acid sequences. Nucleic Acids Research, 31, 3537-3539.
Wong, A. (2014). Covariance between testes size and substitution rates in primates. Molecular Biology and Evolution, 31, 1432-1436.
Wu, T., Lane, S. I. R., Morgan, S. L., & Jones, K. T. (2018). Spindle tubulin and MTOC asymmetries may explain meiotic drive in oocytes. Nature Communications, 9. https://doi.org/10.1038/s41467-018-05338-7
Xia, X. (2013). DAMBE5: A comprehensive software package for data analysis in molecular biology and evolution. Molecular Biology and Evolution, 30, 1720-1728.
Xia, X., Xie, Z., Salemi, M., Chen, L., & Wang, Y. (2003). An index of substitution saturation and its application. Molecular Phylogenetics and Evolution, 26, 1-7.
Yang, Z. (1997). PAML: A program package for phylogenetic analysis by maximum likelihood. Computer Applications in the Biosciences, 13, 555-556.
Yang, Z. (2007). PAML 4: Phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution, 24, 1586-1591.
Yang, Z., & Nielsen, R. (1998). Synonymous and nonsynonymous rate variation in nuclear genes of mammals. Journal of Molecular Evolution, 46, 409-418.
Yang, Z., Wong, W. S., & Nielsen, R. (2005). Bayes empirical bayes inference of amino acid sites under positive selection. Molecular Biology and Evolution, 22, 1107-1118.