Testes-specific hemoglobins in Drosophilaevolved by a combination of sub- and neofunctionalization after gene duplication

Abstract

BackgroundFor 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.ResultsHere 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.ConclusionsPhylogenetic 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.

The Globin Gene Family in Arthropods: Evolution and Functional Diversity

“…In fact, we have previously reported that the HbL variants in D. melanogaster , with Glob1 on the one hand and a duplicated gene pair named Glob2 and 3 on the other, display completely different structural characteristics and gene expression profiles. While Glob1 is currently thought to fulfill a role associated with oxidative metabolism in tracheoles and fat body cells of embryonal larval and adult flies ( Hankeln et al, 2002 ; Gleixner et al, 2008 , 2016 ), Glob2 and 3 are exclusively expressed during spermatogenesis and may be important for male fertility ( Gleixner et al, 2012 ). In conclusion, the multiple gene duplication events observed within the HbL class may have provided the basis for neo-functionalization events in the different arthropod lineages, which of course has to be proven experimentally.…”

“…Data from knockdown experiments indicate that Glob1 may play a role in O 2 metabolism of insects ( Gleixner et al, 2016 ), although a different role for Glob1 in maintenance of the cytoskeleton was recently proposed ( Yadav and Sarkar, 2016 ; Yadav et al, 2018 ). Drosophila has two additional globins, Glob2 and 3, which are structurally derived and specifically expressed in the testis ( Burmester et al, 2006 ; Gleixner et al, 2012 ). It is unlikely that they play a role in O 2 supply.…”

Transcriptomes reveal expression of hemoglobins throughout insects and other Hexapoda

“…Particularly if androglobins [53] have been lost in many insect groups, as has been hypothesized for D. melanogaster [27], then globin-2/3 functions may have been independently acquired in several insect groups in compensation. As Gleixner et al [51] demonstrated, the D. melanogaster globin-2/3 genes are quite divergent and have evolved at faster rates following duplication. Congruent with their findings, a small clade of dipterans (including D. melanogaster) apparently possessing globins-2/3 appear distant from the larger globin-1 clade in the cladogram (Figs 3 and S1) and may be a result of long-branch attraction.…”

“…To address the lack of hemoglobins in the remaining 89 transcriptomes, sample data submitted with each transcriptome's entry in NCBI was reviewed. Hemoglobin is not universally expressed across all tissue types and developmental stages, so targeted sampling used in many studies, such as specific tissues or developmental stages, could affect the presence or absence of hemoglobin transcripts (e.g., [16,27,51]). For example, hemoglobin expression in chironomids is known to be primarily in larval stages, and certain hemoglobins in Chironomus thummi are expressed during particular larval instars.…”

Analysis of Mitochondrial haemoglobin in Parkinson's disease brain

“…This is particularly relevant to brain ageing and neurodegeneration, as the brain is most sensitive to reduced oxygen levels. Hypoxia affects mitochondrial structure and function as well as intracellular haemoglobin expression ( Gleixner et al, 2012 ). Haemoglobin (HBA2) expression changes are now also implicated in preclinical prion disease, and Hbb has been found to interact with subunits of ATP synthase in a study of Multiple Sclerosis ( Xerxa et al, 2016 , Brown et al, 2016 ).…”