Academic journal article Genetics

Functional Evolution of the Vertebrate Myb Gene Family: B-Myb, but Neither A-Myb nor C-Myb, Complements Drosophila Myb in Hemocytes

Academic journal article Genetics

Functional Evolution of the Vertebrate Myb Gene Family: B-Myb, but Neither A-Myb nor C-Myb, Complements Drosophila Myb in Hemocytes

Article excerpt

ABSTRACT

The duplication of genes and genomes is believed to be a major force in the evolution of eukaryotic organisms. However, different models have been presented about how duplicated genes are preserved from elimination by purifying selection. Preservation of one of the gene copies due to rare mutational events that result in a new gene function (neofunctionalization) necessitates that the other gene copy retain its ancestral function. Alternatively, preservation of both gene copies due to rapid divergence of coding and noncoding regions such that neither retains the complete function of the ancestral gene (subfunctionalization) may result in a requirement for both gene copies for organismal survival. The duplication and divergence of the tandemly arrayed homeotic clusters have been studied in considerable detail and have provided evidence in support of the subfunctionalization model. However, the vast majority of duplicated genes are not clustered tandemly, but instead are dispersed in syntenic regions on different chromosomes, most likely as a result of genome-wide duplications and rearrangements. The Myb oncogene family provides an interesting opportunity to study a dispersed multigene family because invertebrates possess a single Myb gene, whereas all vertebrate genomes examined thus far contain three different Myb genes (A-Myb, B-Myb, and c-Myb). A-Myb and c-Myb appear to have arisen by a second round of gene duplication, which was preceded by the acquisition of a transcriptional activation domain in the ancestral A-Myb/ c-Myb gene generated from the initial duplication of an ancestral B-Myb-like gene. B-Myb appears to be essential in all dividing cells, whereas A-Myb and c-Myb display tissue-specific requirements during spermatogenesis and hematopoiesis, respectively. We now report that the absence of Drosophila Myb (Dm-Myb) causes a failure of larval hemocyte proliferation and lymph gland development, while Dm-Myb^sup -/-^ hemocytes from mosaic larvae reveal a phagocytosis defect. In addition, we show that vertebrate B-Myb, but neither vertebrate A-Myb nor c-Myb, can complement these hemocyte proliferation defects in Drosophila. Indeed, vertebrate A-Myb and c-Myb cause lethality in the presence or absence of endogenous Dm-Myb. These results are consistent with aneomorphic origin of an ancestral A-Myb/c-Myb gene from a duplicated B-Myb-like gene. In addition, our results suggest that B-Myb and Dm-Myb share essential conserved functions that are required for cell proliferation. Finally, these experiments demonstrate the utility of genetic complementation in Drosophila to explore the functional evolution of duplicated genes in vertebrates.

IT has been extensively reported that genome or large chromosomal regional duplications may be responsible for the structure and evolution of vertebrate genomes from preduplication invertebrate genomes (ABI-RACHED et al. 2002; MCLYSAGHT et al. 2002; PANOPOULOU et al. 2003). For example, at least 15% of the known human genes are recognizable as duplicates (LI et al. 2001). While controversial, it has been proposed that vertebrate genome evolution has occurred through two whole-genome duplication events that are thought to have occurred early in vertebrate evolution ~500 million years ago (OHNO 1999). Consistent with this model, many vertebrate multigene families are represented by a single homolog in modern invertebrate species such as the sea urchin, Drosophila, and Caenorhabditis elegans (HOLLAND 1999; MEYER and SCHARTL 1999). Conclusive support for whole-genome duplication as a source for duplicate gene innovation has recently been shown for the yeast Saccharomyces cerevisiae. Analysis of the complete genome of a related yeast species, Kluyveromyces walti, has demonstrated that the genome of S. cerevisiae is a degenerate tetraploid that arose from an ancient whole-genome duplication after the divergence of the two species from a common ancestor (WOLFE and SHIELDS 1997; KELLIS et al. …

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