Species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila.

Postzygotic reproductive barriers such as sterility and lethality of hybrids are important for establishing and maintaining reproductive isolation between species. Identifying the causal loci and discerning how they interfere with the development of hybrids is essential for understanding how hybrid...

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Autores principales:	Patrick M Ferree, Daniel A Barbash
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2009
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/da8acf571b4a45b6a6256893758d94d8
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spelling	oai:doaj.org-article:da8acf571b4a45b6a6256893758d94d82021-11-25T05:34:31ZSpecies-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila.1544-91731545-788510.1371/journal.pbio.1000234https://doaj.org/article/da8acf571b4a45b6a6256893758d94d82009-10-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/19859525/?tool=EBIhttps://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885Postzygotic reproductive barriers such as sterility and lethality of hybrids are important for establishing and maintaining reproductive isolation between species. Identifying the causal loci and discerning how they interfere with the development of hybrids is essential for understanding how hybrid incompatibilities (HIs) evolve, but little is known about the mechanisms of how HI genes cause hybrid dysfunctions. A previously discovered Drosophila melanogaster locus called Zhr causes lethality in F1 daughters from crosses between Drosophila simulans females and D. melanogaster males. Zhr maps to a heterochromatic region of the D. melanogaster X that contains 359-bp satellite repeats, suggesting either that Zhr is a rare protein-coding gene embedded within heterochromatin, or is a locus consisting of the noncoding repetitive DNA that forms heterochromatin. The latter possibility raises the question of how heterochromatic DNA can induce lethality in hybrids. Here we show that hybrid females die because of widespread mitotic defects induced by lagging chromatin at the time during early embryogenesis when heterochromatin is first established. The lagging chromatin is confined solely to the paternally inherited D. melanogaster X chromatids, and consists predominantly of DNA from the 359-bp satellite block. We further found that a rearranged X chromosome carrying a deletion of the entire 359-bp satellite block segregated normally, while a translocation of the 359-bp satellite block to the Y chromosome resulted in defective Y segregation in males, strongly suggesting that the 359-bp satellite block specifically and directly inhibits chromatid separation. In hybrids produced from wild-type parents, the 359-bp satellite block was highly stretched and abnormally enriched with Topoisomerase II throughout mitosis. The 359-bp satellite block is not present in D. simulans, suggesting that lethality is caused by the absence or divergence of factors in the D. simulans maternal cytoplasm that are required for heterochromatin formation of this species-specific satellite block. These findings demonstrate how divergence of noncoding repetitive sequences between species can directly cause reproductive isolation by altering chromosome segregation.Patrick M FerreeDaniel A BarbashPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 7, Iss 10, p e1000234 (2009)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Patrick M Ferree Daniel A Barbash Species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila.
description	Postzygotic reproductive barriers such as sterility and lethality of hybrids are important for establishing and maintaining reproductive isolation between species. Identifying the causal loci and discerning how they interfere with the development of hybrids is essential for understanding how hybrid incompatibilities (HIs) evolve, but little is known about the mechanisms of how HI genes cause hybrid dysfunctions. A previously discovered Drosophila melanogaster locus called Zhr causes lethality in F1 daughters from crosses between Drosophila simulans females and D. melanogaster males. Zhr maps to a heterochromatic region of the D. melanogaster X that contains 359-bp satellite repeats, suggesting either that Zhr is a rare protein-coding gene embedded within heterochromatin, or is a locus consisting of the noncoding repetitive DNA that forms heterochromatin. The latter possibility raises the question of how heterochromatic DNA can induce lethality in hybrids. Here we show that hybrid females die because of widespread mitotic defects induced by lagging chromatin at the time during early embryogenesis when heterochromatin is first established. The lagging chromatin is confined solely to the paternally inherited D. melanogaster X chromatids, and consists predominantly of DNA from the 359-bp satellite block. We further found that a rearranged X chromosome carrying a deletion of the entire 359-bp satellite block segregated normally, while a translocation of the 359-bp satellite block to the Y chromosome resulted in defective Y segregation in males, strongly suggesting that the 359-bp satellite block specifically and directly inhibits chromatid separation. In hybrids produced from wild-type parents, the 359-bp satellite block was highly stretched and abnormally enriched with Topoisomerase II throughout mitosis. The 359-bp satellite block is not present in D. simulans, suggesting that lethality is caused by the absence or divergence of factors in the D. simulans maternal cytoplasm that are required for heterochromatin formation of this species-specific satellite block. These findings demonstrate how divergence of noncoding repetitive sequences between species can directly cause reproductive isolation by altering chromosome segregation.
format	article
author	Patrick M Ferree Daniel A Barbash
author_facet	Patrick M Ferree Daniel A Barbash
author_sort	Patrick M Ferree
title	Species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila.
title_short	Species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila.
title_full	Species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila.
title_fullStr	Species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila.
title_full_unstemmed	Species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila.
title_sort	species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in drosophila.
publisher	Public Library of Science (PLoS)
publishDate	2009
url	https://doaj.org/article/da8acf571b4a45b6a6256893758d94d8
work_keys_str_mv	AT patrickmferree speciesspecificheterochromatinpreventsmitoticchromosomesegregationtocausehybridlethalityindrosophila AT danielabarbash speciesspecificheterochromatinpreventsmitoticchromosomesegregationtocausehybridlethalityindrosophila
_version_	1718414607798763520

Species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila.

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