Germline-restricted chromosome (GRC) is widespread among songbirds

Anna A. Torgasheva, Lyubov P. Malinovskaya, Kira S. Zadesenets, Tatyana V. Karamysheva, Elena A. Kizilova, Ekaterina A. Akberdina, Inna E. Pristyazhnyuk, Elena P. Shnaider, Valeria A. Volodkina, Alsu F. Saifitdinova, Svetlana A. Galkina, Denis M. Larkin, Nikolai B. Rubtsov, Pavel M. Borodin

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Abstract

An unusual supernumerary chromosome has been reported for two related avian species, the zebra and Bengalese finches. This large, germline-restricted chromosome (GRC) is eliminated from somatic cells and spermatids and transmitted via oocytes only. Its origin, distribution among avian lineages, and function were mostly unknown so far. Using immunolocalization of key meiotic proteins, we found that GRCs of varying size and genetic content are present in all 16 songbird species investigated and absent from germline genomes of all eight examined bird species from other avian orders. Results of fluorescent in situ hybridization of microdissected GRC probes and their sequencing indicate that GRCs show little homology between songbird species and contain a variety of repetitive elements and unique sequences with paralogs in the somatic genome. Our data suggest that the GRC evolved in the common ancestor of all songbirds and underwent significant changes in the extant descendant lineages.

Original languageEnglish
Pages (from-to)11845-11850
JournalProceedings of the National Academy of Sciences of the United States of America
Volume116
Issue number24
DOIs
Publication statusPublished - 2019

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Songbirds
Chromosomes
Genome
Finches
Spermatids
Equidae
Fluorescence In Situ Hybridization
Oocytes
Birds
Proteins

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Torgasheva, A. A., Malinovskaya, L. P., Zadesenets, K. S., Karamysheva, T. V., Kizilova, E. A., Akberdina, E. A., ... Borodin, P. M. (2019). Germline-restricted chromosome (GRC) is widespread among songbirds. Proceedings of the National Academy of Sciences of the United States of America, 116(24), 11845-11850. https://doi.org/10.1073/pnas.1817373116
Torgasheva, Anna A. ; Malinovskaya, Lyubov P. ; Zadesenets, Kira S. ; Karamysheva, Tatyana V. ; Kizilova, Elena A. ; Akberdina, Ekaterina A. ; Pristyazhnyuk, Inna E. ; Shnaider, Elena P. ; Volodkina, Valeria A. ; Saifitdinova, Alsu F. ; Galkina, Svetlana A. ; Larkin, Denis M. ; Rubtsov, Nikolai B. ; Borodin, Pavel M. / Germline-restricted chromosome (GRC) is widespread among songbirds. In: Proceedings of the National Academy of Sciences of the United States of America. 2019 ; Vol. 116, No. 24. pp. 11845-11850.
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title = "Germline-restricted chromosome (GRC) is widespread among songbirds",
abstract = "An unusual supernumerary chromosome has been reported for two related avian species, the zebra and Bengalese finches. This large, germline-restricted chromosome (GRC) is eliminated from somatic cells and spermatids and transmitted via oocytes only. Its origin, distribution among avian lineages, and function were mostly unknown so far. Using immunolocalization of key meiotic proteins, we found that GRCs of varying size and genetic content are present in all 16 songbird species investigated and absent from germline genomes of all eight examined bird species from other avian orders. Results of fluorescent in situ hybridization of microdissected GRC probes and their sequencing indicate that GRCs show little homology between songbird species and contain a variety of repetitive elements and unique sequences with paralogs in the somatic genome. Our data suggest that the GRC evolved in the common ancestor of all songbirds and underwent significant changes in the extant descendant lineages.",
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author = "Torgasheva, {Anna A.} and Malinovskaya, {Lyubov P.} and Zadesenets, {Kira S.} and Karamysheva, {Tatyana V.} and Kizilova, {Elena A.} and Akberdina, {Ekaterina A.} and Pristyazhnyuk, {Inna E.} and Shnaider, {Elena P.} and Volodkina, {Valeria A.} and Saifitdinova, {Alsu F.} and Galkina, {Svetlana A.} and Larkin, {Denis M.} and Rubtsov, {Nikolai B.} and Borodin, {Pavel M.}",
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Torgasheva, AA, Malinovskaya, LP, Zadesenets, KS, Karamysheva, TV, Kizilova, EA, Akberdina, EA, Pristyazhnyuk, IE, Shnaider, EP, Volodkina, VA, Saifitdinova, AF, Galkina, SA, Larkin, DM, Rubtsov, NB & Borodin, PM 2019, 'Germline-restricted chromosome (GRC) is widespread among songbirds', Proceedings of the National Academy of Sciences of the United States of America, vol. 116, no. 24, pp. 11845-11850. https://doi.org/10.1073/pnas.1817373116

Germline-restricted chromosome (GRC) is widespread among songbirds. / Torgasheva, Anna A.; Malinovskaya, Lyubov P.; Zadesenets, Kira S.; Karamysheva, Tatyana V.; Kizilova, Elena A.; Akberdina, Ekaterina A.; Pristyazhnyuk, Inna E.; Shnaider, Elena P.; Volodkina, Valeria A.; Saifitdinova, Alsu F.; Galkina, Svetlana A.; Larkin, Denis M.; Rubtsov, Nikolai B.; Borodin, Pavel M.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 116, No. 24, 2019, p. 11845-11850.

Research outputpeer-review

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T1 - Germline-restricted chromosome (GRC) is widespread among songbirds

AU - Torgasheva, Anna A.

AU - Malinovskaya, Lyubov P.

AU - Zadesenets, Kira S.

AU - Karamysheva, Tatyana V.

AU - Kizilova, Elena A.

AU - Akberdina, Ekaterina A.

AU - Pristyazhnyuk, Inna E.

AU - Shnaider, Elena P.

AU - Volodkina, Valeria A.

AU - Saifitdinova, Alsu F.

AU - Galkina, Svetlana A.

AU - Larkin, Denis M.

AU - Rubtsov, Nikolai B.

AU - Borodin, Pavel M.

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PY - 2019

Y1 - 2019

N2 - An unusual supernumerary chromosome has been reported for two related avian species, the zebra and Bengalese finches. This large, germline-restricted chromosome (GRC) is eliminated from somatic cells and spermatids and transmitted via oocytes only. Its origin, distribution among avian lineages, and function were mostly unknown so far. Using immunolocalization of key meiotic proteins, we found that GRCs of varying size and genetic content are present in all 16 songbird species investigated and absent from germline genomes of all eight examined bird species from other avian orders. Results of fluorescent in situ hybridization of microdissected GRC probes and their sequencing indicate that GRCs show little homology between songbird species and contain a variety of repetitive elements and unique sequences with paralogs in the somatic genome. Our data suggest that the GRC evolved in the common ancestor of all songbirds and underwent significant changes in the extant descendant lineages.

AB - An unusual supernumerary chromosome has been reported for two related avian species, the zebra and Bengalese finches. This large, germline-restricted chromosome (GRC) is eliminated from somatic cells and spermatids and transmitted via oocytes only. Its origin, distribution among avian lineages, and function were mostly unknown so far. Using immunolocalization of key meiotic proteins, we found that GRCs of varying size and genetic content are present in all 16 songbird species investigated and absent from germline genomes of all eight examined bird species from other avian orders. Results of fluorescent in situ hybridization of microdissected GRC probes and their sequencing indicate that GRCs show little homology between songbird species and contain a variety of repetitive elements and unique sequences with paralogs in the somatic genome. Our data suggest that the GRC evolved in the common ancestor of all songbirds and underwent significant changes in the extant descendant lineages.

KW - Avian genome

KW - chromosome evolution

KW - meiosis

KW - Passeriformes

KW - programmed DNA elimination

KW - avian genome

KW - RECOMBINATION

KW - SEXES

KW - SYNAPTONEMAL COMPLEXES

KW - EVOLUTION

KW - DNA

KW - DIVERSITY

KW - PIGEON

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UR - http://www.pnas.org/lookup/doi/10.1073/pnas.1817373116

UR - http://www.mendeley.com/research/germlinerestricted-chromosome-grc-widespread-among-songbirds

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M3 - Article

VL - 116

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EP - 11850

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 24

ER -

Torgasheva AA, Malinovskaya LP, Zadesenets KS, Karamysheva TV, Kizilova EA, Akberdina EA et al. Germline-restricted chromosome (GRC) is widespread among songbirds. Proceedings of the National Academy of Sciences of the United States of America. 2019;116(24):11845-11850. https://doi.org/10.1073/pnas.1817373116