Oligopaint DNA FISH reveals telomere-based meiotic pairing dynamics in the silkworm, Bombyx mori.
Accurate chromosome segregation during meiosis is essential for reproductive success. Yet, many fundamental aspects of meiosis remain unclear, including the mechanisms regulating homolog pairing across species. This gap is partially due to our inability to visualize individual chromosomes during mei...
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2021
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oai:doaj.org-article:d3632b0900c4472baf663fca627e5b8a2021-12-02T20:02:54ZOligopaint DNA FISH reveals telomere-based meiotic pairing dynamics in the silkworm, Bombyx mori.1553-73901553-740410.1371/journal.pgen.1009700https://doaj.org/article/d3632b0900c4472baf663fca627e5b8a2021-07-01T00:00:00Zhttps://doi.org/10.1371/journal.pgen.1009700https://doaj.org/toc/1553-7390https://doaj.org/toc/1553-7404Accurate chromosome segregation during meiosis is essential for reproductive success. Yet, many fundamental aspects of meiosis remain unclear, including the mechanisms regulating homolog pairing across species. This gap is partially due to our inability to visualize individual chromosomes during meiosis. Here, we employ Oligopaint FISH to investigate homolog pairing and compaction of meiotic chromosomes and resurrect a classical model system, the silkworm Bombyx mori. Our Oligopaint design combines multiplexed barcoding with secondary oligo labeling for high flexibility and low cost. These studies illustrate that Oligopaints are highly specific in whole-mount gonads and on meiotic squashes. We show that meiotic pairing is robust in both males and females and that pairing can occur through numerous partially paired intermediate structures. We also show that pairing in male meiosis occurs asynchronously and seemingly in a transcription-biased manner. Further, we reveal that meiotic bivalent formation in B. mori males is highly similar to bivalent formation in C. elegans, with both of these pathways ultimately resulting in the pairing of chromosome ends with non-paired ends facing the spindle pole. Additionally, microtubule recruitment in both C. elegans and B. mori is likely dependent on kinetochore proteins but independent of the centromere-specifying histone CENP-A. Finally, using super-resolution microscopy in the female germline, we show that homologous chromosomes remain associated at telomere domains in the absence of chiasma and after breakdown and modification to the synaptonemal complex in pachytene. These studies reveal novel insights into mechanisms of meiotic homolog pairing both with or without recombination.Leah F RosinJose GilInes A DrinnenbergElissa P LeiPublic Library of Science (PLoS)articleGeneticsQH426-470ENPLoS Genetics, Vol 17, Iss 7, p e1009700 (2021) |
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Genetics QH426-470 |
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Genetics QH426-470 Leah F Rosin Jose Gil Ines A Drinnenberg Elissa P Lei Oligopaint DNA FISH reveals telomere-based meiotic pairing dynamics in the silkworm, Bombyx mori. |
description |
Accurate chromosome segregation during meiosis is essential for reproductive success. Yet, many fundamental aspects of meiosis remain unclear, including the mechanisms regulating homolog pairing across species. This gap is partially due to our inability to visualize individual chromosomes during meiosis. Here, we employ Oligopaint FISH to investigate homolog pairing and compaction of meiotic chromosomes and resurrect a classical model system, the silkworm Bombyx mori. Our Oligopaint design combines multiplexed barcoding with secondary oligo labeling for high flexibility and low cost. These studies illustrate that Oligopaints are highly specific in whole-mount gonads and on meiotic squashes. We show that meiotic pairing is robust in both males and females and that pairing can occur through numerous partially paired intermediate structures. We also show that pairing in male meiosis occurs asynchronously and seemingly in a transcription-biased manner. Further, we reveal that meiotic bivalent formation in B. mori males is highly similar to bivalent formation in C. elegans, with both of these pathways ultimately resulting in the pairing of chromosome ends with non-paired ends facing the spindle pole. Additionally, microtubule recruitment in both C. elegans and B. mori is likely dependent on kinetochore proteins but independent of the centromere-specifying histone CENP-A. Finally, using super-resolution microscopy in the female germline, we show that homologous chromosomes remain associated at telomere domains in the absence of chiasma and after breakdown and modification to the synaptonemal complex in pachytene. These studies reveal novel insights into mechanisms of meiotic homolog pairing both with or without recombination. |
format |
article |
author |
Leah F Rosin Jose Gil Ines A Drinnenberg Elissa P Lei |
author_facet |
Leah F Rosin Jose Gil Ines A Drinnenberg Elissa P Lei |
author_sort |
Leah F Rosin |
title |
Oligopaint DNA FISH reveals telomere-based meiotic pairing dynamics in the silkworm, Bombyx mori. |
title_short |
Oligopaint DNA FISH reveals telomere-based meiotic pairing dynamics in the silkworm, Bombyx mori. |
title_full |
Oligopaint DNA FISH reveals telomere-based meiotic pairing dynamics in the silkworm, Bombyx mori. |
title_fullStr |
Oligopaint DNA FISH reveals telomere-based meiotic pairing dynamics in the silkworm, Bombyx mori. |
title_full_unstemmed |
Oligopaint DNA FISH reveals telomere-based meiotic pairing dynamics in the silkworm, Bombyx mori. |
title_sort |
oligopaint dna fish reveals telomere-based meiotic pairing dynamics in the silkworm, bombyx mori. |
publisher |
Public Library of Science (PLoS) |
publishDate |
2021 |
url |
https://doaj.org/article/d3632b0900c4472baf663fca627e5b8a |
work_keys_str_mv |
AT leahfrosin oligopaintdnafishrevealstelomerebasedmeioticpairingdynamicsinthesilkwormbombyxmori AT josegil oligopaintdnafishrevealstelomerebasedmeioticpairingdynamicsinthesilkwormbombyxmori AT inesadrinnenberg oligopaintdnafishrevealstelomerebasedmeioticpairingdynamicsinthesilkwormbombyxmori AT elissaplei oligopaintdnafishrevealstelomerebasedmeioticpairingdynamicsinthesilkwormbombyxmori |
_version_ |
1718375689135063040 |