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A test of double interspecific introgression of nucleoporin genes in Drosophila.

Sawamura K, Maehara K, Keira Y, Ishikawa HO, Sasamura T, Yamakawa T, Matsuno K - G3 (Bethesda) (2014)

Bottom Line: It appears that introgression of additional autosomal D. simulans genes is necessary to cause lethality and that the effect of the introgression is dominant to D. melanogaster alleles.Interestingly, the genetic background affected dominance of Nup96(sim), and double introgression carrying homozygous Nup96(sim) and hemizygous Nup160(sim) resulted in lethality.Thus, Nup96(sim) and Nup160(sim) seem to be two components of the same incompatibility.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8572 sawamura@biol.tsukuba.ac.jp.

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Related in: MedlinePlus

Genotypes examined previously and in this study. Pairs of bars represent chromosomes X, 2, 3, and 4 (left to right). Open bars (dashed if the presence is not obligate) indicate chromosomes/regions from D. melanogaster, and gray bars indicate chromosomes/regions from D. simulans. D. simulans alleles of Nup160 and Nup96 and the deficiencies on D. melanogaster chromosomes are also indicated. (A) Flies of this genotype all die according to Tang and Presgraves (2009) and Sawamura et al. (2010). (B) Flies of this genotype all die according to Presgraves et al. (2003). (C, D) These flies are viable according to the present analysis. (E) Flies of this genotype all die according to the present analysis. The genotypes in (A) and (B) are usually males carrying one X chromosome from D. melanogaster, but females carrying two D. melanogaster X chromosomes can also be obtained using the attached-X system (Presgraves et al., 2003; Tang & Presgraves 2009). The genotypes in (C), (D), and (E) are females carrying two D. melanogaster X chromosomes or males carrying one D. melanogaster X chromosome.
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fig1: Genotypes examined previously and in this study. Pairs of bars represent chromosomes X, 2, 3, and 4 (left to right). Open bars (dashed if the presence is not obligate) indicate chromosomes/regions from D. melanogaster, and gray bars indicate chromosomes/regions from D. simulans. D. simulans alleles of Nup160 and Nup96 and the deficiencies on D. melanogaster chromosomes are also indicated. (A) Flies of this genotype all die according to Tang and Presgraves (2009) and Sawamura et al. (2010). (B) Flies of this genotype all die according to Presgraves et al. (2003). (C, D) These flies are viable according to the present analysis. (E) Flies of this genotype all die according to the present analysis. The genotypes in (A) and (B) are usually males carrying one X chromosome from D. melanogaster, but females carrying two D. melanogaster X chromosomes can also be obtained using the attached-X system (Presgraves et al., 2003; Tang & Presgraves 2009). The genotypes in (C), (D), and (E) are females carrying two D. melanogaster X chromosomes or males carrying one D. melanogaster X chromosome.

Mentions: A handful of hybrid incompatibility genes that are responsible for reproductive isolation between species have been identified (Johnson 2010; Presgraves 2010; Maheshwari and Barbash 2011; Ferree and Prasad 2012; Sawamura 2012). Surprisingly, two of these genes in the genus Drosophila encode the nuclear pore proteins (nucleoporins = Nups), which were previously thought to be functionally conserved among diverse organisms. Approximately 30 different Nups assemble to form the nuclear pore complex (NPC) and are essential for nucleocytoplasmic transport, gene regulation, and kinetochore formation (Bapteste et al. 2005; Strambio-De-Castillia et al. 2010; Adams and Wente 2013). Nup96 and Nup160 have been identified as reproductive isolation genes by deficiency mapping in which male hybrids were rescued from the independent lethality by Lethal hybrid rescue (Lhr) mutation of D. simulans. D. melanogaster/D. simulans hybrids carrying the D. simulans Nup96sim and Nup160sim are lethal in hemizygotes (or homozygotes) if they do not inherit the D. simulans X chromosome (Figure 1, A and B), and Nup160sim leads to recessive female sterility in the D. melanogaster genetic background (Presgraves et al. 2003; Tang and Presgraves 2009; Sawamura et al. 2010). Furthermore, positive natural selection and intermolecular coevolution have been demonstrated for several Nup genes including Nup96 and Nup160 in the genus Drosophila (Presgraves and Stephan 2007; Clark and Aquadro 2010; Mensch et al. 2013; Nolte et al. 2013).


A test of double interspecific introgression of nucleoporin genes in Drosophila.

Sawamura K, Maehara K, Keira Y, Ishikawa HO, Sasamura T, Yamakawa T, Matsuno K - G3 (Bethesda) (2014)

Genotypes examined previously and in this study. Pairs of bars represent chromosomes X, 2, 3, and 4 (left to right). Open bars (dashed if the presence is not obligate) indicate chromosomes/regions from D. melanogaster, and gray bars indicate chromosomes/regions from D. simulans. D. simulans alleles of Nup160 and Nup96 and the deficiencies on D. melanogaster chromosomes are also indicated. (A) Flies of this genotype all die according to Tang and Presgraves (2009) and Sawamura et al. (2010). (B) Flies of this genotype all die according to Presgraves et al. (2003). (C, D) These flies are viable according to the present analysis. (E) Flies of this genotype all die according to the present analysis. The genotypes in (A) and (B) are usually males carrying one X chromosome from D. melanogaster, but females carrying two D. melanogaster X chromosomes can also be obtained using the attached-X system (Presgraves et al., 2003; Tang & Presgraves 2009). The genotypes in (C), (D), and (E) are females carrying two D. melanogaster X chromosomes or males carrying one D. melanogaster X chromosome.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4232535&req=5

fig1: Genotypes examined previously and in this study. Pairs of bars represent chromosomes X, 2, 3, and 4 (left to right). Open bars (dashed if the presence is not obligate) indicate chromosomes/regions from D. melanogaster, and gray bars indicate chromosomes/regions from D. simulans. D. simulans alleles of Nup160 and Nup96 and the deficiencies on D. melanogaster chromosomes are also indicated. (A) Flies of this genotype all die according to Tang and Presgraves (2009) and Sawamura et al. (2010). (B) Flies of this genotype all die according to Presgraves et al. (2003). (C, D) These flies are viable according to the present analysis. (E) Flies of this genotype all die according to the present analysis. The genotypes in (A) and (B) are usually males carrying one X chromosome from D. melanogaster, but females carrying two D. melanogaster X chromosomes can also be obtained using the attached-X system (Presgraves et al., 2003; Tang & Presgraves 2009). The genotypes in (C), (D), and (E) are females carrying two D. melanogaster X chromosomes or males carrying one D. melanogaster X chromosome.
Mentions: A handful of hybrid incompatibility genes that are responsible for reproductive isolation between species have been identified (Johnson 2010; Presgraves 2010; Maheshwari and Barbash 2011; Ferree and Prasad 2012; Sawamura 2012). Surprisingly, two of these genes in the genus Drosophila encode the nuclear pore proteins (nucleoporins = Nups), which were previously thought to be functionally conserved among diverse organisms. Approximately 30 different Nups assemble to form the nuclear pore complex (NPC) and are essential for nucleocytoplasmic transport, gene regulation, and kinetochore formation (Bapteste et al. 2005; Strambio-De-Castillia et al. 2010; Adams and Wente 2013). Nup96 and Nup160 have been identified as reproductive isolation genes by deficiency mapping in which male hybrids were rescued from the independent lethality by Lethal hybrid rescue (Lhr) mutation of D. simulans. D. melanogaster/D. simulans hybrids carrying the D. simulans Nup96sim and Nup160sim are lethal in hemizygotes (or homozygotes) if they do not inherit the D. simulans X chromosome (Figure 1, A and B), and Nup160sim leads to recessive female sterility in the D. melanogaster genetic background (Presgraves et al. 2003; Tang and Presgraves 2009; Sawamura et al. 2010). Furthermore, positive natural selection and intermolecular coevolution have been demonstrated for several Nup genes including Nup96 and Nup160 in the genus Drosophila (Presgraves and Stephan 2007; Clark and Aquadro 2010; Mensch et al. 2013; Nolte et al. 2013).

Bottom Line: It appears that introgression of additional autosomal D. simulans genes is necessary to cause lethality and that the effect of the introgression is dominant to D. melanogaster alleles.Interestingly, the genetic background affected dominance of Nup96(sim), and double introgression carrying homozygous Nup96(sim) and hemizygous Nup160(sim) resulted in lethality.Thus, Nup96(sim) and Nup160(sim) seem to be two components of the same incompatibility.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8572 sawamura@biol.tsukuba.ac.jp.

Show MeSH
Related in: MedlinePlus