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Journal of Molecular Evolution

, Volume 86, Issue 6, pp 353–364 | Cite as

Concurrent Duplication of Drosophila Cid and Cenp-C Genes Resulted in Accelerated Evolution and Male Germline-Biased Expression of the New Copies

  • José R. Teixeira
  • Guilherme B. Dias
  • Marta Svartman
  • Alfredo Ruiz
  • Gustavo C. S. Kuhn
Original Article

Abstract

Despite their essential role in the process of chromosome segregation in eukaryotes, kinetochore proteins are highly diverse across species, being lost, duplicated, created, or diversified during evolution. Based on comparative genomics, the duplication of the inner kinetochore proteins CenH3 and Cenp-C, which are interdependent in their roles of establishing centromere identity and function, can be said to be rare in animals. Surprisingly, the Drosophila CenH3 homolog Cid underwent four independent duplication events during evolution. Particularly interesting are the highly diverged Cid1 and Cid5 paralogs of the Drosophila subgenus, which are probably present in over one thousand species. Given that CenH3 and Cenp-C likely co-evolve as a functional unit, we investigated the molecular evolution of Cenp-C in species of Drosophila. We report yet another Cid duplication (leading to Cid6) within the Drosophila subgenus and show that not only Cid, but also Cenp-C is duplicated in the entire subgenus. The Cenp-C paralogs, which we named Cenp-C1 and Cenp-C2, are highly divergent. Both Cenp-C1 and Cenp-C2 retain key motifs involved in centromere localization and function, while some functional motifs are conserved in an alternate manner between the paralogs. Interestingly, both Cid5 and Cenp-C2 are male germline-biased and evolved adaptively. However, it is currently unclear if the paralogs subfunctionalized or if the new copies acquired a new function. Our findings point towards a specific inner kinetochore composition in a specific context (i.e., spermatogenesis), which could prove valuable for the understanding of how the extensive kinetochore diversity is related to essential cellular functions.

Keywords

CenH3 Cenp-C Gene duplication Centromere Kinetochore Drosophila 

Notes

Acknowledgements

We are very grateful to the two reviewers for all comments and insightful suggestions that significantly improved the quality of our work. We are also grateful to Dr. Maura Helena Manfrin (University of São Paulo) for providing us the D. seriema strain. This work was supported by grants from “Fundação de Amparo à Pesquisa do Estado de Minas Gerais” (FAPEMIG) (Grant Number APQ-01563-14) and “Conselho Nacional de Desenvolvimento Científico e Tecnológico” (CNPq) (Grant Number 404620/2016-7) to G.K.

Supplementary material

239_2018_9851_MOESM1_ESM.png (3.1 mb)
Supplementary Figure S1 Some Cenp-C motifs are alternatively conserved between Cenp-C1 and Cenp-C2. (A) Schematic representation of the general motif structure of Drosophila subgenus Cenp-C. (B) Logo representations for each motif of the Drosophila subgenus Cenp-C1 (C1) and Cenp-C2 (C2). Motifs are as follow: R-rich, arginine-rich; DH, drosophilid Cenp-C homology; AT1, AT hook 1; NLS, nuclear localization signal; CenH3 binding, also known as Cenp-C motif; AT2, AT hook 2; Cupin, a dimerization domain near the C-terminal region. The asterisk in the CenH3 binding motif indicates the corresponding R1101 of D. melanogaster, which is essential for the centromere localization of Cenp-C1. (PNG 3201 KB)
239_2018_9851_MOESM2_ESM.docx (1.9 mb)
Supplementary File S1 (DOCX 1919 KB)
239_2018_9851_MOESM3_ESM.docx (54 kb)
Supplementary File S2 (DOCX 53 KB)
239_2018_9851_MOESM4_ESM.docx (16 kb)
Supplementary File S3 (DOCX 15 KB)

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Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • José R. Teixeira
    • 1
  • Guilherme B. Dias
    • 1
  • Marta Svartman
    • 1
  • Alfredo Ruiz
    • 2
  • Gustavo C. S. Kuhn
    • 1
    • 3
  1. 1.Departamento de Biologia GeralUniversidade Federal de Minas GeraisBelo HorizonteBrazil
  2. 2.Departament de Genètica i de MicrobiologiaUniversitat Autònoma de BarcelonaBellaterra (Barcelona)Spain
  3. 3.Laboratório de Citogenômica Evolutiva, Departamento de Biologia Geral, Instituto de Ciências BiológicasUniversidade Federal de Minas GeraisBelo HorizonteBrazil

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