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Testes-specific hemoglobins in Drosophila evolved by a combination of sub- and neofunctionalization after gene duplication.

Gleixner E, Herlyn H, Zimmerling S, Burmester T, Hankeln T - BMC Evol. Biol. (2012)

Bottom Line: Therefore, flies of the Drosophila subgenus harbor only one glob2/3-like gene.Phylogenetic and sequence analyses indicate an evolution of the glob2 and glob3 duplicates by a combination of sub- and neofunctionalization.Considering their restricted, testes-specific expression, an involvement of both globins in alleviating oxidative stress during spermatogenesis is conceivable.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Molecular Genetics, University of Mainz, 55099 Mainz, Germany.

ABSTRACT

Background: For a long time the presence of respiratory proteins in most insects has been considered unnecessary. However, in recent years it has become evident that globins belong to the standard repertoire of the insect genome. Like most other insect globins, the glob1 gene of Drosophila melanogaster displays a conserved expression pattern in the tracheae, the fat body and the Malpighian tubules.

Results: Here we show that the recently discovered D. melanogaster globin genes glob2 and glob3 both display an unusual male-specific expression in the reproductive tract during spermatogenesis. Both paralogs are transcribed at equivalent mRNA levels and largely overlap in their cellular expression patterns during spermatogenesis. Phylogenetic analyses showed that glob2 and glob3 reflect a gene duplication event that occurred in the ancestor of the Sophophora subgenus at least 40 million years ago. Therefore, flies of the Drosophila subgenus harbor only one glob2/3-like gene.

Conclusions: Phylogenetic and sequence analyses indicate an evolution of the glob2 and glob3 duplicates by a combination of sub- and neofunctionalization. Considering their restricted, testes-specific expression, an involvement of both globins in alleviating oxidative stress during spermatogenesis is conceivable.

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Dmeglob2, dmeglob3 and dviglob2/3 mRNA expression pattern. Quantification of mRNA expression of glob2 and glob3 in D. melanogaster and glob2/3 in D. virilis in sexed 3rd instar larvae, pupae and adults. mRNA levels (bars) are shown relative to glob-expression in adult males. (A) glob2 expression in D. melanogaster. (B) glob3 expression in D. melanogaster. (C) glob2/3 expression in D. virilis.
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Figure 3: Dmeglob2, dmeglob3 and dviglob2/3 mRNA expression pattern. Quantification of mRNA expression of glob2 and glob3 in D. melanogaster and glob2/3 in D. virilis in sexed 3rd instar larvae, pupae and adults. mRNA levels (bars) are shown relative to glob-expression in adult males. (A) glob2 expression in D. melanogaster. (B) glob3 expression in D. melanogaster. (C) glob2/3 expression in D. virilis.

Mentions: In embryos, the mRNA expression of D. melanogaster glob2 was minimal (not shown). Dmeglob2 turned out to be maximally expressed in male adult flies (Figure 3A). Expression levels in male larvae and pupae were at 43% and 78% relative to male adults. In female larvae, pupae and adults dmeglob2 expression was always beyond the detection limit. The developmental expression pattern of dmeglob3 showed a high similarity to dmeglob2. Dmeglob3 mRNA expression in embryos (not shown) as well as in female larvae, pupae and adult flies was not detectable. The amounts of dmeglob3 mRNA in male larvae and pupae were about 16% and 50% of the maximal mRNA expression level obtained in male adult flies (Figure 3B). Thus, for both, dmeglob2 and glob3, we could experimentally confirm the expression pattern derived from the modENCODE project implemented in FlyBase http://flybase.org/reports/FBgn0037385.html; http://flybase.org/reports/FBgn0250846.html. The developmental expression pattern of the single-copy glob2/3 gene in D. virilis was generally matching those of the D. melanogaster paralogs. In embryos, no expression of dviglob2/3 expression could be measured (not shown), while adult males showed maximum expression (Figure 3C). Male and female larvae expressed 5%, male pupae 38%, and female pupae and adults 2% and 6% of the male adult level (Figure 3C).


Testes-specific hemoglobins in Drosophila evolved by a combination of sub- and neofunctionalization after gene duplication.

Gleixner E, Herlyn H, Zimmerling S, Burmester T, Hankeln T - BMC Evol. Biol. (2012)

Dmeglob2, dmeglob3 and dviglob2/3 mRNA expression pattern. Quantification of mRNA expression of glob2 and glob3 in D. melanogaster and glob2/3 in D. virilis in sexed 3rd instar larvae, pupae and adults. mRNA levels (bars) are shown relative to glob-expression in adult males. (A) glob2 expression in D. melanogaster. (B) glob3 expression in D. melanogaster. (C) glob2/3 expression in D. virilis.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3361466&req=5

Figure 3: Dmeglob2, dmeglob3 and dviglob2/3 mRNA expression pattern. Quantification of mRNA expression of glob2 and glob3 in D. melanogaster and glob2/3 in D. virilis in sexed 3rd instar larvae, pupae and adults. mRNA levels (bars) are shown relative to glob-expression in adult males. (A) glob2 expression in D. melanogaster. (B) glob3 expression in D. melanogaster. (C) glob2/3 expression in D. virilis.
Mentions: In embryos, the mRNA expression of D. melanogaster glob2 was minimal (not shown). Dmeglob2 turned out to be maximally expressed in male adult flies (Figure 3A). Expression levels in male larvae and pupae were at 43% and 78% relative to male adults. In female larvae, pupae and adults dmeglob2 expression was always beyond the detection limit. The developmental expression pattern of dmeglob3 showed a high similarity to dmeglob2. Dmeglob3 mRNA expression in embryos (not shown) as well as in female larvae, pupae and adult flies was not detectable. The amounts of dmeglob3 mRNA in male larvae and pupae were about 16% and 50% of the maximal mRNA expression level obtained in male adult flies (Figure 3B). Thus, for both, dmeglob2 and glob3, we could experimentally confirm the expression pattern derived from the modENCODE project implemented in FlyBase http://flybase.org/reports/FBgn0037385.html; http://flybase.org/reports/FBgn0250846.html. The developmental expression pattern of the single-copy glob2/3 gene in D. virilis was generally matching those of the D. melanogaster paralogs. In embryos, no expression of dviglob2/3 expression could be measured (not shown), while adult males showed maximum expression (Figure 3C). Male and female larvae expressed 5%, male pupae 38%, and female pupae and adults 2% and 6% of the male adult level (Figure 3C).

Bottom Line: Therefore, flies of the Drosophila subgenus harbor only one glob2/3-like gene.Phylogenetic and sequence analyses indicate an evolution of the glob2 and glob3 duplicates by a combination of sub- and neofunctionalization.Considering their restricted, testes-specific expression, an involvement of both globins in alleviating oxidative stress during spermatogenesis is conceivable.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Molecular Genetics, University of Mainz, 55099 Mainz, Germany.

ABSTRACT

Background: For a long time the presence of respiratory proteins in most insects has been considered unnecessary. However, in recent years it has become evident that globins belong to the standard repertoire of the insect genome. Like most other insect globins, the glob1 gene of Drosophila melanogaster displays a conserved expression pattern in the tracheae, the fat body and the Malpighian tubules.

Results: Here we show that the recently discovered D. melanogaster globin genes glob2 and glob3 both display an unusual male-specific expression in the reproductive tract during spermatogenesis. Both paralogs are transcribed at equivalent mRNA levels and largely overlap in their cellular expression patterns during spermatogenesis. Phylogenetic analyses showed that glob2 and glob3 reflect a gene duplication event that occurred in the ancestor of the Sophophora subgenus at least 40 million years ago. Therefore, flies of the Drosophila subgenus harbor only one glob2/3-like gene.

Conclusions: Phylogenetic and sequence analyses indicate an evolution of the glob2 and glob3 duplicates by a combination of sub- and neofunctionalization. Considering their restricted, testes-specific expression, an involvement of both globins in alleviating oxidative stress during spermatogenesis is conceivable.

Show MeSH
Related in: MedlinePlus